Publications by year
In Press
Liebl AL, Browning LE, Russell A (In Press). Carer removal and brood size manipulation: not equivalent to quantify carer impacts on provisioning. Behavioral Ecology
Lynton-Jenkins J, Brundl A, Cauchoix M, Lejeune L, Salle L, Thiney A, Russell A, Chaine A, Bonneaud C (In Press). Contrasting the seasonal and elevational prevalence of generalist avian haemosporidia in co-occurring host species. Ecology and Evolution
Liebl AL, Nomano FY, Browning LE, Russell AF (In Press). Experimental evidence for fully additive care among male carers in the cooperatively breeding chestnut-crowned babbler. Animal Behaviour
2023
Cones AG, Liebl AL, Russell AF (2023). Helpers are associated with increased nest attentiveness and more constant egg temperatures in chestnut-crowned babblers.
Behavioral Ecology and Sociobiology,
77(7).
Abstract:
Helpers are associated with increased nest attentiveness and more constant egg temperatures in chestnut-crowned babblers
Abstract: the impacts that helpers have on offspring in cooperative breeding systems depend on parental responses to help. However, the vast majority of investigations into parental responses to the presence of helpers have considered investment responses during a single phase of breeding—offspring provisioning. Whether or not responses during other phases of breeding complement those during offspring provisioning is therefore unclear. Here, we use temperature probes in model eggs of chestnut-crowned babblers (Pomatostomus ruficeps) to determine: (a) maternal responses to helpers, which (like partners) allofeed incubating females but do not share incubation; and (b) the implications of these responses for egg temperatures. We found that during incubation, increased helper number was associated with longer bouts of incubation interspersed with fewer foraging bouts, which resulted in greater nest attentiveness overall. Further, although helpers had limited effects on average egg temperatures, they were associated with reduced variation in egg temperatures. This reduced variation arose because helpers were associated with higher minimum egg temperatures during off-bouts, presumably because of the negative association between helper number and off-bout number. Together, these results suggest that helpers have additive effects on maternal incubation schedules, which contrasts markedly from the dramatic declines in offspring provisioning shown by mothers with helpers during the nestling phase. Further studies are required to assess the generality of these contrasting patterns and their implications for the quantification of helper effects in cooperative breeders. Significance statement: Maternal responses to the presence of helpers are thought to be species-specific, but most tests are only conducted during offspring provisioning. Using temperature probes in model eggs of cooperative chestnut-crowned babblers (Pomatostomus ruficeps), we show that mothers increase contributions to incubation in the presence of helpers, resulting in more constant egg temperatures. This response contrasts markedly with maternal responses to helper presence during nestling provisioning in this system, suggesting that maternal response rules differ across distinct phases of breeding.
Abstract.
Lynton‐Jenkins JG, Chaine AS, Russell AF, Bonneaud C (2023). Parasite detection and quantification in avian blood is dependent on storage medium and duration.
Ecology and Evolution,
13(2).
Abstract:
Parasite detection and quantification in avian blood is dependent on storage medium and duration
AbstractStudies of parasites in wild animal populations often rely on molecular methods to both detect and quantify infections. However, method accuracy is likely to be influenced by the sampling approach taken prior to nucleic acid extraction. Avian Haemosporidia are studied primarily through the screening of host blood, and a range of storage mediums are available for the short‐ to long‐term preservation of samples. Previous research has suggested that storage medium choice may impact the accuracy of PCR‐based parasite detection, however, this relationship has never been explicitly tested and may be exacerbated by the duration of sample storage. These considerations could also be especially critical for sensitive molecular methods used to quantify infection (qPCR). To test the effect of storage medium and duration on Plasmodium detection and quantification, we split blood samples collected from wild birds across three medium types (filter paper, Queen's lysis buffer, and 96% ethanol) and carried out DNA extractions at five time points (1, 6, 12, 24, and 36 months post‐sampling). First, we found variation in DNA yield obtained from blood samples dependent on their storage medium which had subsequent negative impacts on both detection and estimates of Plasmodium copy number. Second, we found that detection accuracy (incidence of true positives) was highest for filter‐paper‐stored samples (97%), while accuracy for ethanol and Queen's lysis buffer‐stored samples was influenced by either storage duration or extraction yield, respectively. Lastly, longer storage durations were associated with decreased copy number estimates across all storage mediums; equating to a 58% reduction between the first‐ and third‐year post‐sampling for lysis‐stored samples. These results raise questions regarding the utility of standardizing samples by dilution, while also illustrating the critical importance of considering storage approaches in studies of Haemosporidia comparing samples subjected to different storage regimes and/or stored for varying lengths of time.
Abstract.
2021
Lynton-Jenkins JG, Russell AF, Chaves J, Bonneaud C (2021). Avian disease surveillance on the island of San Cristobal, Galapagos.
ECOLOGY AND EVOLUTION,
11(24), 18422-18433.
Author URL.
Culina A, Adriaensen F, Bailey LD, Burgess MD, Charmantier A, Cole EF, Eeva T, Matthysen E, Nater CR, Sheldon BC, et al (2021). Connecting the data landscape of long-term ecological studies: the SPI-Birds data hub.
Journal of Animal Ecology,
90(9), 2147-2160.
Abstract:
Connecting the data landscape of long-term ecological studies: the SPI-Birds data hub
The integration and synthesis of the data in different areas of science is drastically slowed and hindered by a lack of standards and networking programmes. Long-term studies of individually marked animals are not an exception. These studies are especially important as instrumental for understanding evolutionary and ecological processes in the wild. Furthermore, their number and global distribution provides a unique opportunity to assess the generality of patterns and to address broad-scale global issues (e.g. climate change). To solve data integration issues and enable a new scale of ecological and evolutionary research based on long-term studies of birds, we have created the SPI-Birds Network and Database (www.spibirds.org)—a large-scale initiative that connects data from, and researchers working on, studies of wild populations of individually recognizable (usually ringed) birds. Within year and a half since the establishment, SPI-Birds has recruited over 120 members, and currently hosts data on almost 1.5 million individual birds collected in 80 populations over 2,000 cumulative years, and counting. SPI-Birds acts as a data hub and a catalogue of studied populations. It prevents data loss, secures easy data finding, use and integration and thus facilitates collaboration and synthesis. We provide community-derived data and meta-data standards and improve data integrity guided by the principles of Findable, Accessible, Interoperable and Reusable (FAIR), and aligned with the existing metadata languages (e.g. ecological meta-data language). The encouraging community involvement stems from SPI-Bird's decentralized approach: research groups retain full control over data use and their way of data management, while SPI-Birds creates tailored pipelines to convert each unique data format into a standard format. We outline the lessons learned, so that other communities (e.g. those working on other taxa) can adapt our successful model. Creating community-specific hubs (such as ours, COMADRE for animal demography, etc.) will aid much-needed large-scale ecological data integration.
Abstract.
Cones AG, Liebl AL, Houslay TM, Russell AF (2021). Temperature-mediated plasticity in incubation schedules is unlikely to evolve to buffer embryos from climatic challenges in a seasonal songbird.
J Evol Biol,
34(3), 465-476.
Abstract:
Temperature-mediated plasticity in incubation schedules is unlikely to evolve to buffer embryos from climatic challenges in a seasonal songbird.
Phenotypic plasticity is hypothesized to facilitate adaptive responses to challenging conditions, such as those resulting from climate change. However, tests of the key predictions of this 'rescue hypothesis', that variation in plasticity exists and can evolve to buffer unfavourable conditions, remain rare. Here, we investigate among-female variation in temperature-mediated plasticity of incubation schedules and consequences for egg temperatures using the chestnut-crowned babbler (Pomatostomus ruficeps) from temperate regions of inland south-eastern Australia. Given recent phenological advances in this seasonal breeder and thermal requirements of developing embryos (>~25°C, optimally ~38°C), support for evolutionary rescue-perhaps paradoxically-requires that plasticity serves to buffer embryos more from sub-optimally low temperatures. We found significant variation in the duration of incubation bouts (mean ± SD = 27 ± 22 min) and foraging bouts (mean ± SD = 17 ± 11 min) in this maternal-only incubator. However, variation in each arose because of variation in the extent to which mothers increased on- and off-bout durations when temperatures (0-36°C) were more favourable rather than unfavourable as required under rescue. In addition, there was a strong positive intercept-slope correlation in on-bout durations, indicating that those with stronger plastic responses incubated more at average temperatures (~19°C). Combined, these effects reduced the functional significance of plastic responses: an individual's plasticity was neither associated with daily contributions to incubation (i.e. attentiveness) nor average egg temperatures. Our results highlight that despite significant among-individual variation in environmental-sensitivity, plasticity in parental care traits need not evolve to facilitate buffering against unfavourable conditions.
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Author URL.
2019
Nomano FY, Savage JL, Browning LE, Griffith SC, Russell AF (2019). Breeding Phenology and Meteorological Conditions Affect Carer Provisioning Rates and Group-Level Coordination in Cooperative Chestnut-Crowned Babblers.
Frontiers in Ecology and Evolution,
7Abstract:
Breeding Phenology and Meteorological Conditions Affect Carer Provisioning Rates and Group-Level Coordination in Cooperative Chestnut-Crowned Babblers
Recent theoretical and empirical work suggests that coordinating offspring provisioning plays a significant role in stabilizing cooperative care systems, with benefits to developing young. However, a warming and increasingly extreme climate might be expected to make contributions to, and so coordination of, care more challenging, particularly in cooperative breeding systems comprising multiple carers of varying age and pairwise relatedness. Here we investigated the interplay between breeding phenology, meteorological conditions and carer number on the individual rates and group-level coordination of nestling care in the cooperatively breeding chestnut-crowned babbler (Pomatostomus ruficeps) in outback south-eastern Australia. From 3 months since the last meaningful rain event, dominant male breeders and—to a lesser extent—related helpers showed reductions in their provisioning rates and increases in their day-to-day variation. Further, on days with high mean wind speed, dominant males contributed less and helpers were less likely to visit the nest on such days. Helpers also showed reduced visitation rates on days with high mean temperature. Provisioning rates were independent of the number of carers, and increasing numbers of carers failed to mitigate the detrimental effects of challenging environment on patterns of provisioning. Those helpers that were unrelated to broods often failed to help on a given day and tended to help at a low rate when they did contribute, with socio-environmental predictors having limited explanatory power. Given the marked variation in individual contributions to offspring care and the variable explanatory power of the socio-environmental predictors tested, babblers unsurprisingly had low levels of nest visitation synchrony. Large groups visited the nest more asynchronously on days of high mean temperature, suggesting that meteorological impacts on individual provisioning have consequences for group-level coordination. Our study has implications for the consequences of climate change on patterns of provisioning, the minimal role of group size in buffering against these challenges and the stabilization of cooperative care.
Abstract.
Engesser S, Holub JL, O'Neill LG, Russell AF, Townsend SW (2019). Chestnut-crowned babbler calls are composed of meaningless shared building blocks.
Proceedings of the National Academy of Sciences of the United States of America,
116(39), 19579-19584.
Abstract:
Chestnut-crowned babbler calls are composed of meaningless shared building blocks
A core component of human language is its combinatorial sound system: meaningful signals are built from different combinations of meaningless sounds. Investigating whether nonhuman communication systems are also combinatorial is hampered by difficulties in identifying the extent to which vocalizations are constructed from shared, meaningless building blocks. Here we present an approach to circumvent this difficulty and show that a pair of functionally distinct chestnut-crowned babbler (Pomatostomus ruficeps) vocalizations can be decomposed into perceptibly distinct, meaningless entities that are shared across the 2 calls. Specifically, by focusing on the acoustic distinctiveness of sound elements using a habituation-discrimination paradigm on wildcaught babblers under standardized aviary conditions, we show that 2 multielement calls are composed of perceptibly distinct sounds that are reused in different arrangements across the 2 calls. Furthermore, and critically, we show that none of the 5 constituent elements elicits functionally relevant responses in receivers, indicating that the constituent sounds do not carry the meaning of the call and so are contextually meaningless. Our work, which allows combinatorial systems in animals to be more easily identified, suggests that animals can produce functionally distinct calls that are built in a way superficially reminiscent of the way that humans produce morphemes and words. The results reported lend credence to the recent idea that language's combinatorial system may have been preceded by a superficial stage where signalers neither needed to be cognitively aware of the combinatorial strategy in place, nor of its building blocks.
Abstract.
Lejeune L, Savage JL, Bründl AC, Thiney A, Russell AF, Chaine AS (2019). Environmental effects on parental care visitation patterns in blue tits Cyanistes caeruleus.
Frontiers in Ecology and Evolution,
7(SEP).
Abstract:
Environmental effects on parental care visitation patterns in blue tits Cyanistes caeruleus
In bi-parental care systems each parent shares benefits with its unrelated partner from the common investment in offspring, but pays an individual cost of providing that care, leading to sexual conflict. However, several recent empirical studies have shown that coordinating behaviours like synchronisation (e.g. arriving at similar times) and alternation (taking turns in providing care) at the nest lead to increased investment overall, presumably to reduce conflict through policing or synergistic benefits. Ecological conditions should impact the costs and benefits of bi-parental care, yet there exists a gap in research on the relationship between ecological conditions and patterns of parental care behaviour beyond visitation rate. Here we provide an examination of how bi-parental provisioning behaviours, i.e. pair feeding rate and feeding consistency, and the degree to which parents synchronise or take turns, differ under contrasting ecological conditions in populations of blue tits (Cyanistes caeruleus) spanning a 1,000 m altitudinal gradient. We found that blue tit pairs synchronised and alternated more than expected by chance, and that care patterns were modified by ecology. Pairs synchronised more in woodland-pasture edges than in woodland interiors, and alternated more and fed more frequently at lower altitude compared to higher altitude nests. Variation in bi-parental coordination behaviours did not have a significant impact on fledging success but more synchronous nests had heavier chicks in woodland habitats. Taken as a whole, our results show that patterns of care are influenced by ecological conditions and that their interplay may change the outcome of sexual conflict.
Abstract.
Bründl AC, Sorato E, Sallé L, Thiney AC, Kaulbarsch S, Chaine AS, Russell AF (2019). Experimentally induced increases in fecundity lead to greater nestling care in blue tits.
Proc Biol Sci,
286(1905).
Abstract:
Experimentally induced increases in fecundity lead to greater nestling care in blue tits.
Models on the evolution of bi-parental care typically assume that maternal investment in offspring production is fixed and predict subsequent contributions to offspring care by the pair are stabilized by partial compensation. While experimental tests of this prediction are supportive, exceptions are commonplace. Using wild blue tits ( Cyanistes caeruleus), we provide, to our knowledge, the first investigation into the effects of increasing maternal investment in offspring production for subsequent contributions to nestling provisioning by mothers and male partners. Females that were induced to lay two extra eggs provisioned nestlings 43% more frequently than controls, despite clutch size being made comparable between treatment groups at the onset of incubation. Further, experimental males did not significantly reduce provisioning rates as expected by partial compensation, and if anything contributed slightly (9%) more than controls. Finally, nestlings were significantly heavier in experimental nests compared with controls, suggesting that the 22% average increase in provisioning rates by experimental pairs was beneficial. Our results have potential implications for our understanding of provisioning rules, the maintenance of bi-parental care and the timescale over which current-future life-history trade-offs operate. We recommend greater consideration of female investment at the egg stage to more fully understand the evolutionary dynamics of bi-parental care.
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Dell R, Carr R, Phillips E, Russell A (2019). Interactions between glacier dynamics, ice structure, and climate at Fjallsjökul, south-east Iceland.
Austin VI, Higgott C, Viguier A, Grundy L, Russell AF, Griffith SC (2019). Song rate and duetting in the Chirruping Wedgebill (Psophodes cristatus): frequency, form and functions.
Emu,
119(2), 138-146.
Abstract:
Song rate and duetting in the Chirruping Wedgebill (Psophodes cristatus): frequency, form and functions
Much of our current understanding of song originates from studies of species living in seasonal environments, where breeding seasons are short and highly synchronised at the population level. By comparison, the form and function of song are less well understood in aseasonal environments, where breeding cycles are less predictable. We examined song rates of male and female Chirruping Wedgebills (Psophodes cristatus), a passerine endemic to the arid regions of inland, south-eastern Australia, across a 4 month period of breeding activity. Our results show that both males and females sing, and provide evidence of duetting. The song rate of male Wedgebills was highest in the early morning and during breeding and was substantially higher than the song rate of female Wedgebills. Over the course of the day, bouts of male singing were two orders of magnitude longer than females. By contrast, female song rate was independent of the time of day or reproductive phase. Females more often sang in tandem with their partners than expected by chance and duets occurred at a relatively low rate, independently of breeding phase. We discuss the possibility that male and female song and duets serve different functions.
Abstract.
L'Herpiniere KL, O'Neill LG, Russell AF, Duursma DE, Griffith SC (2019). Unscrambling variation in avian eggshell colour and patterning in a continent-wide study.
R Soc Open Sci,
6(1).
Abstract:
Unscrambling variation in avian eggshell colour and patterning in a continent-wide study.
The evolutionary drivers underlying marked variation in the pigmentation of eggs within many avian species remains unclear. The leading hypotheses proposed to explain such variation advocate the roles of genetic differences, signalling and/or structural integrity. One means of testing among these hypotheses is to capitalize on museum collections of eggs obtained throughout a broad geographical range of a species to ensure sufficient variation in predictors pertaining to each hypothesis. Here, we measured coloration and patterning in eggs from 272 clutches of Australian magpies (Cracticus tibicen) collected across most of their geographical range of ca 7 million km2; encompassing eight subspecies, variation in environmental parameters, and the presence/absence of a brood parasite. We found considerable variation in background colour, as well as in the extent and distribution of patterning across eggs. There was little evidence that this variation was explained by subspecies or the contemporary presence of a brood parasite. However, measures of maximum temperature, leaf area index and soil calcium all contributed to variation in egg appearance, although their explanatory power was relatively low. Our results suggest that multiple factors combine to influence egg appearance in this species, and that even in species with highly variable eggs, coloration is not readily explained.
Abstract.
Author URL.
2018
Capp E, Liebl AL, Cones AG, Russell AF (2018). Advancing breeding phenology does not affect incubation schedules in chestnut-crowned babblers: Opposing effects of temperature and wind.
Ecology and Evolution,
8(1), 696-705.
Abstract:
Advancing breeding phenology does not affect incubation schedules in chestnut-crowned babblers: Opposing effects of temperature and wind
Projecting population responses to climate change requires an understanding of climatic impacts on key components of reproduction. Here, we investigate the associations among breeding phenology, climate and incubation schedules in the chestnut-crowned babbler (Pomatostomus ruficeps), a 50 g passerine with female-only, intermittent incubation that typically breeds from late winter (July) to early summer (November). During daylight hours, breeding females spent an average of 33 min on the nest incubating (hereafter on-bouts) followed by 24-min foraging (hereafter off-bouts), leading to an average daytime nest attentiveness of 60%. Nest attentiveness was 25% shorter than expected from allometric calculations, largely because off-bout durations were double the expected value for a species with 16 g clutches (4 eggs × 4 g/egg). On-bout durations and daily attentiveness were both negatively related to ambient temperature, presumably because increasing temperatures allowed more time to be allocated to foraging with reduced detriment to egg cooling. By contrast, on-bout durations were positively associated with wind speed, in this case because increasing wind speed exacerbated egg cooling during off-bouts. Despite an average temperature change of 12°C across the breeding season, breeding phenology had no effect on incubation schedules. This surprising result arose because of a positive relationship between temperature and wind speed across the breeding season: Any benefit of increasing temperatures was canceled by apparently detrimental consequences of increasing wind speed on egg cooling. Our results indicate that a greater appreciation for the associations among climatic variables and their independent effects on reproductive investment are necessary to understand the effects of changing climates on breeding phenology.
Abstract.
Jacob S, Sallé L, Zinger L, Chaine AS, Ducamp C, Boutault L, Russell AF, Heeb P (2018). Chemical regulation of body feather microbiota in a wild bird.
Mol Ecol,
27(7), 1727-1738.
Abstract:
Chemical regulation of body feather microbiota in a wild bird.
The microbiota has a broad range of impacts on host physiology and behaviour, pointing out the need to improve our comprehension of the drivers of host-microbiota composition. of particular interest is whether the microbiota is acquired passively, or whether and to what extent hosts themselves shape the acquisition and maintenance of their microbiota. In birds, the uropygial gland produces oily secretions used to coat feathers that have been suggested to act as an antimicrobial defence mechanism regulating body feather microbiota. However, our comprehension of this process is still limited. In this study, we for the first time coupled high-throughput sequencing of the microbiota of both body feathers and the direct environment (i.e. the nest) in great tits with chemical analyses of the composition of uropygial gland secretions to examine whether host chemicals have either specific effects on some bacteria or nonspecific broad-spectrum effects on the body feather microbiota. Using a network approach investigating the patterns of co-occurrence or co-exclusions between chemicals and bacteria within the body feather microbiota, we found no evidence for specific promicrobial or antimicrobial effects of uropygial gland chemicals. However, we found that one group of chemicals was negatively correlated to bacterial richness on body feathers, and a higher production of these chemicals was associated with a poorer body feather bacterial richness compared to the nest microbiota. Our study provides evidence that chemicals produced by the host might function as a nonspecific broad-spectrum antimicrobial defence mechanism limiting colonization and/or maintenance of bacteria on body feathers, providing new insight about the drivers of the host's microbiota composition in wild organisms.
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Author URL.
2017
Russell AF, Townsend SW (2017). Communication: Animal Steps on the Road to Syntax?.
Curr Biol,
27(15), R753-R755.
Abstract:
Communication: Animal Steps on the Road to Syntax?
From tool use to teaching, proto-forms of 'human traits' are being discovered in animals. But what of language? New evidence suggests that a garden bird has hopped on the long road to syntax, an integral component of language.
Abstract.
Author URL.
Savage JL, Browning LE, Manica A, Russell AF, Johnstone RA (2017). Turn-taking in cooperative offspring care: by-product of individual provisioning behavior or active response rule?.
Behav Ecol Sociobiol,
71(11).
Abstract:
Turn-taking in cooperative offspring care: by-product of individual provisioning behavior or active response rule?
ABSTRACT: for individuals collaborating to rear offspring, effective organization of resource delivery is difficult because each carer benefits when the others provide a greater share of the total investment required. When investment is provided in discrete events, one possible solution is to adopt a turn-taking strategy whereby each individual reduces its contribution rate after investing, only increasing its rate again once another carer contributes. To test whether turn-taking occurs in a natural cooperative care system, here we use a continuous time Markov model to deduce the provisioning behavior of the chestnut-crowned babbler (Pomatostomus ruficeps), a cooperatively breeding Australian bird with variable number of carers. Our analysis suggests that turn-taking occurs across a range of group sizes (2-6), with individual birds being more likely to visit following other individuals than to make repeat visits. We show using a randomization test that some of this apparent turn-taking arises as a by-product of the distribution of individual inter-visit intervals ("passive" turn-taking) but that individuals also respond actively to the investment of others over and above this effect ("active" turn-taking). We conclude that turn-taking in babblers is a consequence of both their individual provisioning behavior and deliberate response rules, with the former effect arising through a minimum interval required to forage and travel to and from the nest. Our results reinforce the importance of considering fine-scale investment dynamics when studying parental care and suggest that behavioral rules such as turn-taking may be more common than previously thought. SIGNIFICANCE STATEMENT: Caring for offspring is a crucial stage in the life histories of many animals and often involves conflict as each carer typically benefits when others contribute a greater share of the work required. One way to resolve this conflict is to monitor when other carers contribute and adopt a simple "turn-taking" rule to ensure fairness, but natural parental care has rarely been studied in sufficient detail to identify such rules. Our study investigates whether cooperatively breeding chestnut-crowned babblers "take turns" delivering food to offspring, and (if so) whether this a deliberate strategy or simply a by-product of independent care behavior. We find that babblers indeed take turns and conclude that part of the observed turn-taking is due to deliberate responsiveness, with the rest arising from the species' breeding ecology.
Abstract.
Author URL.
2016
Russell AF (2016). Chestnut-crowned babblers: Dealing with climatic adversity and uncertainty in the Australian arid zone. In Koenig WD, Dickinson JL (Eds.) Cooperative breeding in vertebrates: studies in ecology, evolution and behavior, MA, USA: Cambridge University Press, 150-164.
Crane JMS, Savage JL, Russell AF (2016). Diversity and function of vocalisations in the cooperatively breeding Chestnut-crowned Babbler. Emu - Austral Ornithology, 116(3), 241-253.
Langmore NE, Bailey LD, Heinsohn RG, Russell AF, Kilner RM (2016). Egg size investment in superb fairy-wrens: helper effects are modulated by climate.
Proc Biol Sci,
283(1843).
Abstract:
Egg size investment in superb fairy-wrens: helper effects are modulated by climate.
Natural populations might exhibit resilience to changing climatic conditions if they already show adaptive flexibility in their reproductive strategies. In cooperative breeders, theory predicts that mothers with helpers should provide less care when environmental conditions are favourable, but maintain high investment when conditions are challenging. Here, we test for evidence of climate-mediated flexibility in maternal investment in the cooperatively breeding superb fairy-wren Malurus cyaneus We focus on egg size because in this species egg size influences offspring size, and females reduce egg investment when there are helpers at the nest. We report that females lay larger eggs during dry, hot conditions. However, the effect of temperature is modulated by the presence of helpers: the average egg size of females with helpers is reduced during cooler conditions but increased during hot conditions relative to females without helpers. This appears to reflect plasticity in egg investment rather than among female differences. Analysis of maternal survival suggests that helped females are better able to withstand the costs of breeding in hot conditions than females without helpers. Our study suggests that females can use multiple, independent cues to modulate egg investment flexibly in a variable environment.
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Author URL.
Chappell MA, Buttemer WA, Russell AF (2016). Energetics of communal roosting in chestnut-crowned babblers: implications for group dynamics and breeding phenology.
J Exp Biol,
219(Pt 21), 3321-3328.
Abstract:
Energetics of communal roosting in chestnut-crowned babblers: implications for group dynamics and breeding phenology.
For many endotherms, communal roosting saves energy in cold conditions, but how this might affect social dynamics or breeding phenology is not well understood. Using chestnut-crowned babblers (Pomatostomus ruficeps), we studied the effects of nest use and group size on roosting energy costs. These 50
g cooperatively breeding passerine birds of outback Australia breed from late winter to early summer and roost in huddles of up to 20 in single-chambered nests. We measured babbler metabolism at three ecologically relevant temperatures: 5°C (similar to minimum nighttime temperatures during early breeding), 15°C (similar to nighttime temperatures during late breeding) and 28°C (thermal neutrality). Nest use alone had modest effects: even for solitary babblers at 5°C, it reduced nighttime energy expenditures by
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Author URL.
Sorato E, Griffith SC, Russell AF (2016). The price of associating with breeders in the cooperatively breeding chestnut-crowned babbler: foraging constraints, survival and sociality.
J Anim Ecol,
85(5), 1340-1351.
Abstract:
The price of associating with breeders in the cooperatively breeding chestnut-crowned babbler: foraging constraints, survival and sociality.
Understanding the costs of living with breeders might offer new insights into the factors that counter evolutionary transitions from selfish individuals to cooperative societies. While selection on early dispersal is well understood, it is less clear whether costs are also associated with remaining with family members during subsequent breeding, a prerequisite to the evolution of kin-based cooperation. We propose and test the hypothesis that living in groups containing breeders is costly and that such costs are exacerbated by increasing group size. For example, in group-living central-place foragers, group members might suffer from resource depletion when foraging in a restricted area during breeding and significant costs of repeatedly travelling between foraging patches and the site of offspring. Using the cooperatively breeding chestnut-crowned babbler (Pomatostomus ruficeps), for which grouping during breeding is obligatory, we show that reproduction is associated with substantially reduced foraging areas and evidence of resource depletion, particularly in larger groups. Such effects largely persisted from the onset of incubation through to offspring independence 4-5 months later. All group members, irrespective of their breeder or helper status, lost significant body mass over this period, and, in males, mass loss was associated with reduced interannual survival. Although babblers are constrained from living outside of breeding groups due to high risks of predation and the poor success of breeding without helpers, we suggest that the effects we describe may generally select against group living during breeding attempts in species where constraints to independent breeding and costs of dispersal are less acute.
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2015
Crane JMS, Pick JL, Tribe AJ, Vincze E, Hatchwell BJ, Russell AF (2015). Chestnut-crowned babblers show affinity for calls of removed group members: a dual playback without expectancy violation.
Animal Behaviour,
104, 51-57.
Abstract:
Chestnut-crowned babblers show affinity for calls of removed group members: a dual playback without expectancy violation
Cooperative breeding typically evolves within discrete, stable groups of individuals, in which group members derive direct and/or indirect fitness benefits from cooperative behaviour. In such systems, strong selection on group discrimination should emerge. Despite this prediction, relatively few studies have investigated the mechanism of group discrimination in cooperative vertebrates, and the results of many may be confounded by 'expectancy violation', since test individuals from which stimuli were derived remained in the group during experimentation. Here, we used a novel experimental protocol that eliminates this confounding effect in a test of group discrimination in cooperatively breeding chestnut-crowned babblers, Pomatostomus ruficeps, using long-distance contact calls. Long-distance contact calls were found to be individually specific, but to lack obvious group level signatures. Using dual playbacks of removed group and nongroup members, we found that these calls allow effective discrimination: groups unanimously approached the speaker broadcasting calls of group members and concomitantly increased their contact call rates. Together, our results suggest that group discrimination emerges from individual recognition. Additionally, the affiliative behaviour of group members towards playbacks of removed members contrasts with the aggressive responses towards nongroup members found in all other studies. One explanation for these differences stems from our elimination of expectancy violation, but further studies are required to verify this.
Abstract.
Engesser S, Crane JMS, Savage JL, Russell AF, Townsend SW (2015). Experimental Evidence for Phonemic Contrasts in a Nonhuman Vocal System.
PLoS Biol,
13(6).
Abstract:
Experimental Evidence for Phonemic Contrasts in a Nonhuman Vocal System.
The ability to generate new meaning by rearranging combinations of meaningless sounds is a fundamental component of language. Although animal vocalizations often comprise combinations of meaningless acoustic elements, evidence that rearranging such combinations generates functionally distinct meaning is lacking. Here, we provide evidence for this basic ability in calls of the chestnut-crowned babbler (Pomatostomus ruficeps), a highly cooperative bird of the Australian arid zone. Using acoustic analyses, natural observations, and a series of controlled playback experiments, we demonstrate that this species uses the same acoustic elements (A and B) in different arrangements (AB or BAB) to create two functionally distinct vocalizations. Specifically, the addition or omission of a contextually meaningless acoustic element at a single position generates a phoneme-like contrast that is sufficient to distinguish the meaning between the two calls. Our results indicate that the capacity to rearrange meaningless sounds in order to create new signals occurs outside of humans. We suggest that phonemic contrasts represent a rudimentary form of phoneme structure and a potential early step towards the generative phonemic system of human language.
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Author URL.
Savage JL, Russell AF, Johnstone RA (2015). Maternal allocation in cooperative breeders: Should mothers match or compensate for expected helper contributions?.
Animal Behaviour,
102, 189-197.
Abstract:
Maternal allocation in cooperative breeders: Should mothers match or compensate for expected helper contributions?
Among species with variable numbers of individuals contributing to offspring care, an individual's investment strategy should depend upon both the size of the breeding group and the relative contributions of each carer. Existing theoretical work on carer investment rules has, however, largely focused on biparental care, and on modelling offspring provisioning in isolation from other stages of investment. Consequently, there has been little exploration of how maternal investment prior to birth might be expected to influence carer provisioning decisions after birth, and how these should be modified by the number of carers present. In particular, it is unclear whether mothers should increase or decrease their investment in each offspring under favourable rearing conditions, and whether this differs under alternative assumptions about the consequences of being 'high quality' at birth. We develop a game-theoretical model of cooperative care that incorporates female control of prebirth investment, and allow increased maternal investment to either substitute for later investment (giving offspring a 'head start') or raise the value of later investment (a 'silver spoon'). We show that mothers reduce prebirth investment under better rearing conditions (more helpers) when investment is substitutable, leading to concealed helper effects. In contrast, when maternal prebirth investment primes offspring to benefit more from postbirth care, mothers should take advantage of good care environments by investing more in offspring both before and after birth. These results provide novel mechanisms to explain contrasting patterns of maternal investment across cooperative breeders.
Abstract.
Sorato E, Gullett PR, Creasey MJS, Griffith SC, Russell AF (2015). Plastic territoriality in group-living chestnut-crowned babblers: Roles of resource value, holding potential and predation risk.
Animal Behaviour,
101, 155-168.
Abstract:
Plastic territoriality in group-living chestnut-crowned babblers: Roles of resource value, holding potential and predation risk
The factors selecting for territoriality and their relative importance are poorly resolved. Theoretical models predict that territoriality will be selected when resources of intermediate abundance are distributed variably and predictably in time and space, but can be selected against if the resource-holding potential of individuals is low or the risk of predation is high. Here we used a model averaging approach in a mixed modelling framework to analyse 5 years of observational and experimental data collected on group responses to actual and perceived intruders in the cooperatively breeding chestnut-crowned babbler, Pomatostomus ruficeps, in order to provide a rare test of the relative importance of resource value, resource-holding potential and predation risk in territorial behaviour. We found that babblers were highly plastic in their responses to actual and simulated intruders: on average, approaches occurred on 55% of occasions, and aggression ensued in 55% of approaches (observational and experimental results combined). Whether or not babbler groups approached, and if so were aggressive towards, actual or simulated intrusions was explained by time of day, location, group sizes, predator encounter rate and habitat characteristics, but not by reproductive status. Consideration of each of these effects regarding the three hypotheses above suggested comparable roles of group competitive advantage and predation risk on approach probability, whereas ensuing aggression was mostly explained by correlates of resource value. Our study provides compelling evidence to suggest that the risk of predation can affect the incidence of territorial and agonistic behaviour between social groups of animals by moderating the effects of resource value and group competitiveness, and might partly explain the high plasticity in group responses to intrusions.
Abstract.
Warrington MH, Rollins LA, Russell AF, Griffith SC (2015). Sequential polyandry through divorce and re-pairing in a cooperatively breeding bird reduces helper-offspring relatedness.
Behavioral Ecology and Sociobiology,
69(8), 1311-1321.
Abstract:
Sequential polyandry through divorce and re-pairing in a cooperatively breeding bird reduces helper-offspring relatedness
Polyandry is an important component of both sexual selection and kin structuring within cooperatively breeding species. A female may have multiple partners within a single reproductive attempt (simultaneous polyandry) or across multiple broods within and/or across years (sequential polyandry). Both types of polyandry confer a range of costs and benefits to individuals and alter the genetic structure of social groups over time. To date, many molecular studies of cooperative breeders have examined the evolution of cooperative breeding in relation to simultaneous polyandry. However, cooperatively breeding vertebrates are iteroparous, and thus sequential polyandry is also likely, but more rarely considered in this context. We examined sequential polyandry in a cooperatively breeding bird that has a low level of within-brood polyandry. Over a 5-year period (2006–2010), we monitored individual mating relationships using molecular markers in a population of individually marked apostlebirds (Struthidea cinerea). Divorce occurred between reproductive seasons in 17 % (8/48) of pairs and appeared to be female-driven. The level of sequential polyandry was also driven by the disappearance of males after breeding, and over 90 % of females, for whom we had suitable data, bred with multiple males over the period of study. This sequential polyandry significantly altered the relatedness of group members to the offspring in the nest. However, in about half of the cases, the second male was related (first- or second-order relative) to the first male of a sequentially polyandrous female and this alleviated the reduction in relatedness caused by polyandry. Our findings suggest that even in species with high within-brood parentage certainty, helper-offspring relatedness values can quickly erode through sequential polyandry.
Abstract.
Nomano FY, Browning LE, Savage JL, Rollins LA, Griffith SC, Russell AF (2015). Unrelated helpers neither signal contributions nor suffer retribution in chestnut-crowed babblers.
BEHAVIORAL ECOLOGY,
26(4), 986-995.
Author URL.
Kramer KL, Russell AF (2015). Was monogamy a key step on the hominin road? Reevaluating the monogamy hypothesis in the evolution of cooperative breeding.
Evolutionary Anthropology,
24(2), 73-83.
Abstract:
Was monogamy a key step on the hominin road? Reevaluating the monogamy hypothesis in the evolution of cooperative breeding
Because human mothers routinely rely on others to help raise their young, humans have been characterized as cooperative breeders. 1-9 Several large-scale phylogenetic analyses have presented compelling evidence that monogamy preceded the evolution of cooperative breeding in a wide variety of nonhuman animals. 10-14 These studies have suggested that monogamy provides a general rule (the monogamy hypothesis) for explaining evolutionary transitions to cooperative breeding. 15 Given the prevalence of cooperative breeding in contemporary human societies, we evaluate whether this suggests a monogamous hominin past.
Abstract.
McAuliffe K, Wrangham R, Glowacki L, Russell AF (2015). When cooperation begets cooperation: the role of key individuals in galvanizing support.
Philos Trans R Soc Lond B Biol Sci,
370(1683).
Abstract:
When cooperation begets cooperation: the role of key individuals in galvanizing support.
Life abounds with examples of conspecifics actively cooperating to a common end, despite conflicts of interest being expected concerning how much each individual should contribute. Mathematical models typically find that such conflict can be resolved by partial-response strategies, leading investors to contribute relatively equitably. Using a case study approach, we show that such model expectations can be contradicted in at least four disparate contexts: (i) bi-parental care; (ii) cooperative breeding; (iii) cooperative hunting; and (iv) human cooperation. We highlight that: (a) marked variation in contributions is commonplace; and (b) individuals can often respond positively rather than negatively to the contributions of others. Existing models have surprisingly limited power in explaining these phenomena. Here, we propose that, although among-individual variation in cooperative contributions will be influenced by differential costs and benefits, there is likely to be a strong genetic or epigenetic component. We then suggest that selection can maintain high investors (key individuals) when their contributions promote support by increasing the benefits and/or reducing the costs for others. Our intentions are to raise awareness in--and provide testable hypotheses of--two of the most poorly understood, yet integral, questions regarding cooperative ventures: why do individuals vary in their contributions and when does cooperation beget cooperation?
Abstract.
Author URL.
2014
Møller AP, Adriaensen F, Artemyev A, Bańbura J, Barba E, Biard C, Blondel J, Bouslama Z, Bouvier JC, Camprodon J, et al (2014). Clutch-size variation in Western Palaearctic secondary hole-nesting passerine birds in relation to nest box design.
Methods in Ecology and Evolution,
5(4), 353-362.
Abstract:
Clutch-size variation in Western Palaearctic secondary hole-nesting passerine birds in relation to nest box design
Secondary hole-nesting birds that do not construct nest holes themselves and hence regularly breed in nest boxes constitute important model systems for field studies in many biological disciplines with hundreds of scientists and amateurs involved. Those research groups are spread over wide geographic areas that experience considerable variation in environmental conditions, and researchers provide nest boxes of varying designs that may inadvertently introduce spatial and temporal variation in reproductive parameters. We quantified the relationship between mean clutch size and nest box size and material after controlling for a range of environmental variables in four of the most widely used model species in the Western Palaearctic: great tit Parus major, blue tit Cyanistes caeruleus, pied flycatcher Ficedula hypoleuca and collared flycatcher F. albicollis from 365 populations and 79 610 clutches. Nest floor area and nest box material varied non-randomly across latitudes and longitudes, showing that scientists did not adopt a random box design. Clutch size increased with nest floor area in great tits, but not in blue tits and flycatchers. Clutch size of blue tits was larger in wooden than in concrete nest boxes. These findings demonstrate that the size of nest boxes and material used to construct nest boxes can differentially affect clutch size in different species. The findings also suggest that the nest box design may affect not only focal species, but also indirectly other species through the effects of nest box design on productivity and therefore potentially population density and hence interspecific competition. © 2014 the Authors. Methods in Ecology and Evolution © 2014 British Ecological Society.
Abstract.
Kramer KL, Russell AF (2014). Kin-selected cooperation without lifetime monogamy: human insights and animal implications.
Trends Ecol Evol,
29(11), 600-606.
Abstract:
Kin-selected cooperation without lifetime monogamy: human insights and animal implications.
Recent phylogenetic analyses suggest that monogamy precedes the evolution of cooperative breeding involving non-breeding helpers. The rationale: only through monogamy can helper-recipient relatedness coefficients match those of parent-offspring. Given that humans are cooperative breeders, these studies imply a monogamy bottleneck during hominin evolution. However, evidence from multiple sources is not compelling. In reconciliation, we propose that selection against cooperative breeding under alternative mating patterns will be mitigated by: (i) kin discrimination, (ii) reduced birth-intervals, and (iii) constraints on independent breeding, particularly for premature and post-fertile individuals. We suggest that such alternatives require consideration to derive a complete picture of the selection pressures acting on the evolution of cooperative breeding in humans and other animals.
Abstract.
Author URL.
Georgiev AV, Russell AF, Emery Thompson M, Otali E, Muller MN, Wrangham RW (2014). The Foraging Costs of Mating Effort in Male Chimpanzees (Pan troglodytes schweinfurthii).
International Journal of Primatology,
35(3-4), 725-745.
Abstract:
The Foraging Costs of Mating Effort in Male Chimpanzees (Pan troglodytes schweinfurthii)
Costs of mating effort can affect the reproductive strategies and lifetime fitness of male primates, but interspecific and interindividual variation in the magnitude and distribution of costs is poorly understood. Male costs have primarily been recognized in seasonally breeding species that experience concentrated periods of mating competition. Here, we examine foraging costs associated with male mating effort in chimpanzees (Pan troglodytes schweinfurthii), a polygynandrous species, in which mating opportunities occur intermittently throughout the year. To quantify male feeding, aggression, and mating, we conducted focal follows on 12 males in a wild community (Kanyawara, Kibale National Park, Uganda) for 11 mo. Males fed less on days when high-value mating opportunities (estrous parous females) were available than on days without any mating opportunities. Reductions in feeding time were related to increased rates of aggression and copulation, indicating that the proximate cause of changes in male foraging was mating effort. Surprisingly, however, there was no relationship between dominance rank and the extent to which feeding time was reduced. High costs of mating effort may reduce the degree of reproductive skew and limit the use of possessive tactics in chimpanzees. We suggest that male bonding in chimpanzees may be favored not only for its benefits but because intragroup competition is so costly. Our results complement the available data on mammals, and primates in particular, by showing that mating effort can have measurable foraging costs even in species, in which breeding is aseasonal and only moderately skewed. © 2014 Springer Science+Business Media New York.
Abstract.
Royle NJ, Russell AF, Wilson AJ (2014). The evolution of flexible parenting.
Science,
345(6198), 776-781.
Abstract:
The evolution of flexible parenting.
Parenting behaviors, such as the provisioning of food by parents to offspring, are known to be highly responsive to changes in environment. However, we currently know little about how such flexibility affects the ways in which parenting is adapted and evolves in response to environmental variation. This is because few studies quantify how individuals vary in their response to changing environments, especially social environments created by other individuals with which parents interact. Social environmental factors differ from nonsocial factors, such as food availability, because parents and offspring both contribute and respond to the social environment they experience. This interdependence leads to the coevolution of flexible behaviors involved in parenting, which could, paradoxically, constrain the ability of individuals to rapidly adapt to changes in their nonsocial environment.
Abstract.
Author URL.
Nomano FY, Browning LE, Nakagawa S, Griffith SC, Russell AF (2014). Validation of an automated data collection method for quantifying social networks in collective behaviours.
Behavioral Ecology and Sociobiology,
68(8), 1379-1391.
Abstract:
Validation of an automated data collection method for quantifying social networks in collective behaviours
The social network of preferences among group members can affect the distribution and consequences of collective behaviours. However, the behavioural contexts and taxa in which social network structure has been described are still limited because such studies require extensive data. Here, we highlight the use of an automated passive integrated transponder (PIT)-tag monitoring system for social network analyses and do so in a novel context-nestling provisioning in an avian cooperative breeder, for which direct observation of social behaviours is difficult. First, we used observers and cameras to arrive at a suitable metric of nest visit synchrony in the PIT-tag data. Second, we validated the use of this metric for social network analyses using internal nest video cameras. Third, we used hierarchical regression models with 'sociality' parameter to investigate structure of networks collected from multiple groups. Use of PIT tags led to nest visitation duration and frequency being obtained with a high degree of accuracy for all group members, except for the breeding female for whom accurate estimations required the use of a video camera due to her high variability in visitation time. The PIT-tag dataset uncovered significant variability in social network structure. Our results highlight the importance of combining complementary observation methods when conducting social network analyses of wild animals. Our methods can also be generalised to multiple contexts in social systems wherever repeated encounters with other individuals in closed space have ecological implications. © 2014 Springer-Verlag Berlin Heidelberg.
Abstract.
2013
Cheatsazan H, de Almedia APLG, Russell AF, Bonneaud C (2013). Experimental evidence for a cost of resistance to the fungal pathogen, Batrachochytrium dendrobatidis, for the palmate newt, Lissotriton helveticus.
BMC Ecol,
13Abstract:
Experimental evidence for a cost of resistance to the fungal pathogen, Batrachochytrium dendrobatidis, for the palmate newt, Lissotriton helveticus.
BACKGROUND: Batrachochytrium dendrobatidis (Bd), the causative agent of chytridiomycosis, is decimating amphibians worldwide. Unsurprisingly, the majority of studies have therefore concentrated on documenting morbidity and mortality of susceptible species and projecting population consequences as a consequence of this emerging infectious disease. Currently, there is a paucity of studies investigating the sub-lethal costs of Bd in apparently asymptomatic species, particularly in controlled experimental conditions. Here we report the consequences of a single dose of B. dendrobatidis zoospores on captive adult palmate newts (Lissotriton helveticus) for morphological and behavioural traits that associate with reproductive success. RESULTS: a single exposure to ~2000 zoospores induced a subclinical Bd infection. One week after inoculation 84% of newts tested positive for Bd, and of those, 98% had apparently lost the infection by the day 30. However, exposed newts suffered significant mass loss compared with control newts, and those experimental newts removing higher levels of Bd lost most mass. We found no evidence to suggest that three secondary sexual characteristics (areas of dorsal crest and rear foot webbing, and length of tail filament) were reduced between experimental versus control newts; in fact, rear foot webbing was 26% more expansive at the end of the experiment in exposed newts. Finally, compared with unexposed controls, exposure to Bd was associated with a 50% earlier initiation of the non-reproductive terrestrial phase. CONCLUSIONS: Our results suggest that Bd has measureable, but sub-lethal effects, on adult palmate newts, at least under the laboratory conditions presented. We conclude that the effects reported are most likely to be mediated through the initiation of costly immune responses and/or tissue repair mechanisms. Although we found no evidence of hastened secondary sexual trait regression, through reducing individual body condition and potentially, breeding season duration, we predict that Bd exposure might have negative impacts on populations of palmate newts through reducing individual reproductive success and adult recruitment.
Abstract.
Author URL.
Nomano FY, Browning LE, Rollins LA, Nakagawa S, Griffith SC, Russell AF (2013). Feeding nestlings does not function as a signal of social prestige in cooperatively breeding chestnut-crowned babblers. Animal Behaviour
Warrington MH, Rollins LA, Raihani NJ, Russell AF, Griffith SC (2013). Genetic monogamy despite variable ecological conditions and social environment in the cooperatively breeding apostlebird.
Ecology and Evolution,
3(14), 4669-4682.
Abstract:
Genetic monogamy despite variable ecological conditions and social environment in the cooperatively breeding apostlebird
Mating strategies may be context-dependent and may vary across ecological and social contexts, demonstrating the role of these factors in driving the variation in genetic polyandry within and among species. Here, we took a longitudinal approach across 5 years (2006-2010), to study the apostlebird (Struthidea cinerea), an Australian cooperatively breeding bird, whose reproduction is affected by ecological "boom and bust" cycles. Climatic variation drives variation in the social (i.e. group sizes, proportion of males and females) and ecological (i.e. plant and insect abundance) context in which mating occurs. By quantifying variation in both social and ecological factors and characterizing the genetic mating system across multiple years using a molecular parentage analysis, we found that the genetic mating strategy did not vary among years despite significant variation in rainfall, driving primary production, and insect abundance, and corresponding variation in social parameters such as breeding group size. Group sizes in 2010, an ecologically good year, were significantly smaller (mean = 5.8 ± 0.9, n = 16) than in the drought affected years, between 2006 and 2008, (mean = 9.1 ± 0.5, n = 63). Overall, apostlebirds were consistently monogamous with few cases of multiple maternity or paternity (8 of 78 nests) across all years. © 2013 the Authors.
Abstract.
Savage JL, Russell AF, Johnstone RA (2013). Intra-group relatedness affects parental and helper investment rules in offspring care.
Behavioral Ecology and Sociobiology,
67(11), 1855-1865.
Abstract:
Intra-group relatedness affects parental and helper investment rules in offspring care
In any system where multiple individuals jointly contribute to rearing offspring, conflict is expected to arise over the relative contributions of each carer. Existing theoretical work on the conflict over care has: (a) rarely considered the influence of tactical investment during offspring production on later contributions to offspring rearing; (b) concentrated mainly on biparental care, rather than cooperatively caring groups comprising both parents and helpers; and (c) typically ignored relatedness between carers as a potential influence on investment behavior. We use a game-theoretical approach to explore the effects of female production tactics and differing group relatedness structures on the expected rearing investment contributed by breeding females, breeding males, and helpers in cooperative groups. Our results suggest that the breeding female should pay higher costs overall when helpful helpers are present, as she produces additional offspring to take advantage of the available care. We find that helpers related to offspring through the breeding female rather than the breeding male should contribute less to care, and decrease their contribution as group size increases, because the female refrains from producing additional offspring to exploit them. Finally, within-group variation in helper relatedness also affects individual helper investment rules by inflating the differences between the contributions to care of dissimilar helpers. Our findings underline the importance of considering maternal investment decisions during offspring production to understand investment across the entire breeding attempt, and provide empirically testable predictions concerning the interplay between maternal, paternal and helper investment and how these are modified by different relatedness structures. © 2013 Springer-Verlag Berlin Heidelberg.
Abstract.
Savage JL, Russell AF, Johnstone RA (2013). Maternal costs in offspring production affect investment rules in joint rearing.
Behavioral Ecology,
24(3), 750-758.
Abstract:
Maternal costs in offspring production affect investment rules in joint rearing
When multiple individuals contribute to rearing the same offspring, conflict is expected to occur over the relative amounts invested by each carer. Existing models of biparental care suggest that this conflict should be resolved by partially compensating for changes by coinvestors, but this has yet to be explicitly modeled in cooperative breeders over a range of carer numbers. In addition, existing models of biparental and cooperative care ignore potential variation in both the relative costs of offspring production to mothers and in maternal allocation decisions. If mothers experience particularly high costs during offspring production, this might be expected to affect their investment strategies during later offspring care. Here, we show using a game-theoretical model that a range of investment tactics can result depending on the number of carers and the relative costs to the mother of the different stages within the breeding attempt. Additional carers result in no change in investment by individuals when production costs are low, as mothers can take advantage of the greater potential investment by increasing offspring number; however, this tactic ultimately results in a decrease in care delivered to each offspring. Conversely, when production costs prevent the mother from increasing offspring number, our model predicts that other individuals should partially compensate for additional carers and hence offspring should each receive a greater amount of care. Our results reinforce the importance of considering investment across all stages in a breeding attempt and provide some explanatory power for the variation in investment rules observed across cooperative species. © 2012 the Author.
Abstract.
Young CM, Browning LE, Savage JL, Griffith SC, Russell AF (2013). No evidence for deception over allocation to brood care in a cooperative bird.
Behavioral Ecology,
24(1), 70-81.
Abstract:
No evidence for deception over allocation to brood care in a cooperative bird
The evolutionary route(s) to cooperative breeding, wherein individuals provide care to the offspring of others, remains contentious. Two hypotheses propose that such helping behavior constitutes a signal, either to remain on the current territory (pay-to-stay) or to advertise quality to potential partners (social prestige). As such, both hypotheses predict that helpers gain from perceived, rather than actual, levels of care provided. Using the chestnut-crowned babbler (Pomatostomus ruficeps), we test whether individuals attempt to increase their perceived level of care by visiting the nest without food (nonfeeding [NF]) or with food but fail to deliver it (false-feeding [FF]). We found no evidence that either NF or FF was used as a deceptive tactic, with both being more parsimoniously explained by current levels of brood demand. Most notably, categories of helpers (males, adults, immigrants) expected to be "charged" more for staying or to benefit more from advertising quality, neither nonfed nor false-fed more than other categories (females, yearlings, natals). In addition, there was no evidence that the presence of an audience (the breeding females in their domed nests) influenced the probability of NF or FF in a manner consistent with either hypothesis. Finally, the incidences of both NF and FF were low and insufficient to have significant effects on the perceived levels of care provided, even if they were used in an attempt to deceive other group members over their contributions to rearing young. We conclude that signaling-based hypotheses have, at best, a weak role in selecting for helping behavior in chestnut-crowned babblers. © 2012 the Author.
Abstract.
Gillespie DOS, Russell AF, Lummaa V (2013). The Effect of Maternal Age and Reproductive History on Offspring Survival and Lifetime Reproduction in Preindustrial Humans.
Evolution,
67(7), 1964-1974.
Abstract:
The Effect of Maternal Age and Reproductive History on Offspring Survival and Lifetime Reproduction in Preindustrial Humans
Senescence is one of the least understood aspects of organism life history. In part, this stems from the relatively late advent of complete individual-level datasets and appropriate statistical tools. In addition, selection against senescence should depend on the contribution to population growth arising from physiological investment in offspring at given ages, but offspring are rarely tracked over their entire lives. Here, we use a multigenerational dataset of preindustrial (1732-1860) Finns to describe the association of maternal age at offspring birth with offspring survival and lifetime reproduction. We then conduct longitudinal analyses to understand the drivers of this association. At the population level, offspring lifetime reproductive success (LRS) declined by 22% and individual λ, which falls with delays to reproduction, declined by 45% as maternal age at offspring birth increased from 16 to 50 years. These results were mediated by within-mother declines in offspring survival and lifetime reproduction. We also found evidence for modifying effects of offspring sex and maternal socioeconomic status. We suggest that our results emerge from the interaction of physiological with social drivers of offspring LRS, which further weakens selection on late-age reproduction and potentially molds the rate of senescence in humans. © 2013 the Society for the Study of Evolution.
Abstract.
2012
Rollins LA, Browning LE, Holleley CE, Savage JL, Russell AF, Griffith SC (2012). Building genetic networks using relatedness information: a novel approach for the estimation of dispersal and characterization of group structure in social animals.
Mol Ecol,
21(7), 1727-1740.
Abstract:
Building genetic networks using relatedness information: a novel approach for the estimation of dispersal and characterization of group structure in social animals.
Natal dispersal is an important life history trait driving variation in individual fitness, and therefore, a proper understanding of the factors underlying dispersal behaviour is critical to many fields including population dynamics, behavioural ecology and conservation biology. However, individual dispersal patterns remain difficult to quantify despite many years of research using direct and indirect methods. Here, we quantify dispersal in a single intensively studied population of the cooperatively breeding chestnut-crowned babbler (Pomatostomus ruficeps) using genetic networks created from the combination of pairwise relatedness data and social networking methods and compare this to dispersal estimates from re-sighting data. This novel approach not only identifies movements between social groups within our study sites but also provides an estimation of immigration rates of individuals originating outside the study site. Both genetic and re-sighting data indicated that dispersal was strongly female biased, but the magnitude of dispersal estimates was much greater using genetic data. This suggests that many previous studies relying on mark-recapture data may have significantly underestimated dispersal. An analysis of spatial genetic structure within the sampled population also supports the idea that females are more dispersive, with females having no structure beyond the bounds of their own social group, while male genetic structure expands for 750 m from their social group. Although the genetic network approach we have used is an excellent tool for visualizing the social and genetic microstructure of social animals and identifying dispersers, our results also indicate the importance of applying them in parallel with behavioural and life history data.
Abstract.
Author URL.
Browning LE, Young CM, Savage JL, Russell DJF, Barclay H, Griffith SC, Russell AF (2012). Carer provisioning rules in an obligate cooperative breeder: Prey type, size and delivery rate.
Behavioral Ecology and Sociobiology,
66(12), 1639-1649.
Abstract:
Carer provisioning rules in an obligate cooperative breeder: Prey type, size and delivery rate
Providing food to developing offspring is beneficial for offspring but costly for carers. Understanding patterns of provisioning thus yields important insights into how selection shapes (allo-) parental care strategies. Broadly, offspring development will be influenced by three components of provisioning (prey type, size and delivery rate). However, all three variables are rarely considered simultaneously, leading to suggestions that the results of many studies are misleading. Additionally, few studies have examined the provisioning strategies of breeders and non-breeding helpers in obligate cooperative breeders, wherein reproduction without help is typically unsuccessful. We investigated these components of provisioning in obligately cooperative chestnut-crowned babblers (Pomatostomus ruficeps). Prey type was associated with size, and delivery rate was the best predictor of the overall amount of food provided by carers. As broods aged, breeders and helpers similarly modified the relative proportion of different prey provided and increased both prey size and delivery rate. Breeding females contributed less prey than male breeders and adult helpers, and were the only carers to load-lighten by reducing their provisioning rates in the presence of additional carers. While our results suggest that breeders and helpers follow broadly comparable provisioning rules, they are also consistent with the idea that, in obligately cooperative species, breeding females benefit more from conserving resources for future reproduction than do helpers which have a low probability of breeding independently. © 2012 Springer-Verlag Berlin Heidelberg.
Abstract.
Sorato E, Gullett PR, Griffith SC, Russell AF (2012). Effects of predation risk on foraging behaviour and group size: adaptations in a social cooperative species. Animal Behaviour, 84(4), 823-834.
Bonneaud C, Balenger SL, Hill GE, Russell AF (2012). Experimental evidence for distinct costs of pathogenesis and immunity against a natural pathogen in a wild bird.
Mol Ecol,
21(19), 4787-4796.
Abstract:
Experimental evidence for distinct costs of pathogenesis and immunity against a natural pathogen in a wild bird.
Protective immunity is expected to evolve when the costs of mounting an immune response are less than those of harbouring pathogens. Estimating the costs of immunity vs. pathogenesis in natural systems is challenging, however, because they are typically closely linked. Here we attempt to disentangle the relative cost of each using experimental infections in a natural host-parasite system in which hosts (house finches, Carpodacus mexicanus) differ in resistance to a bacterium (Mycoplasma gallisepticum, MG), depending on whether they originate from co-evolved or unexposed populations. Experimental infection with a 2007-strain of MG caused finches from co-evolved populations to lose significantly more mass relative to controls, than those from unexposed populations. In addition, infected co-evolved finches that lost the most mass harboured the least amounts of MG, whereas the reverse was true in finches from unexposed populations. Finally, within co-evolved populations, individuals that displayed transcriptional evidence of higher protective immune activity, as indicated by changes in the expression of candidate immune and immune-related genes in a direction consistent with increased resistance to MG, showed greater mass loss and lower MG load. Thus, mass loss appeared to reflect the costs of immunity vs. pathogenesis in co-evolved and unexposed populations, respectively. Our results suggest that resistance can evolve even when the short-term energetic costs of protective immunity exceed those of pathogenesis, providing the longer-term fitness costs of infection are sufficiently high.
Abstract.
Browning LE, Patrick SC, Rollins LA, Griffith SC, Russell AF (2012). Kin selection, not group augmentation, predicts helping in an obligate cooperatively breeding bird.
Proceedings of the Royal Society of London: Biological Sciences,
279(1743), 3861-3869.
Abstract:
Kin selection, not group augmentation, predicts helping in an obligate cooperatively breeding bird.
Kin selection theory has been the central model for understanding the evolution of cooperative breeding, where non-breeders help bear the cost of rearing young. Recently, the dominance of this idea has been questioned; particularly in obligate cooperative breeders where breeding without help is uncommon and seldom successful. In such systems, the direct benefits gained through augmenting current group size have been hypothesized to provide a tractable alternative (or addition) to kin selection. However, clear empirical tests of the opposing predictions are lacking. Here, we provide convincing evidence to suggest that kin selection and not group augmentation accounts for decisions of whether, where and how often to help in an obligate cooperative breeder, the chestnut-crowned babbler (Pomatostomus ruficeps). We found no evidence that group members base helping decisions on the size of breeding units available in their social group, despite both correlational and experimental data showing substantial variation in the degree to which helpers affect productivity in units of different size. By contrast, 98 per cent of group members with kin present helped, 100 per cent directed their care towards the most related brood in the social group, and those rearing half/full-sibs helped approximately three times harder than those rearing less/non-related broods. We conclude that kin selection plays a central role in the maintenance of cooperative breeding in this species, despite the apparent importance of living in large groups.
Abstract.
Barrette M-F, Monfort SL, Festa-Bianchet M, Clutton-Brock TH, Russell AF (2012). Reproductive rate, not dominance status, affects fecal glucocorticoid levels in breeding female meerkats. Hormones and Behavior, 61(4), 463-471.
Lahdenperä M, Gillespie DOS, Lummaa V, Russell AF (2012). Severe intergenerational reproductive conflict and the evolution of menopause. Ecology Letters, 15(11), 1283-1293.
2011
Cockburn A, Russell AF (2011). Cooperative breeding: a question of climate?.
Current Biology,
21(5), R195-R197.
Abstract:
Cooperative breeding: a question of climate?
In some species, including humans, parents receive help with offspring care. A new comparative study suggests that birds breed cooperatively when environmental conditions vary. Further empirical and theoretical work will be required to understand the evolutionary significance of this insight. © 2011 Elsevier Ltd.
Abstract.
Njabo KY, Cornel AJ, Bonneaud C, Toffelmier E, Sehgal RNM, Valkiūnas G, Russell AF, Smith TB (2011). Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest.
Mol Ecol,
20(5), 1049-1061.
Abstract:
Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest.
Malaria parasites use vertebrate hosts for asexual multiplication and Culicidae mosquitoes for sexual and asexual development, yet the literature on avian malaria remains biased towards examining the asexual stages of the life cycle in birds. To fully understand parasite evolution and mechanism of malaria transmission, knowledge of all three components of the vector-host-parasite system is essential. Little is known about avian parasite-vector associations in African rainforests where numerous species of birds are infected with avian haemosporidians of the genera Plasmodium and Haemoproteus. Here we applied high resolution melt qPCR-based techniques and nested PCR to examine the occurrence and diversity of mitochondrial cytochrome b gene sequences of haemosporidian parasites in wild-caught mosquitoes sampled across 12 sites in Cameroon. In all, 3134 mosquitoes representing 27 species were screened. Mosquitoes belonging to four genera (Aedes, Coquillettidia, Culex and Mansonia) were infected with twenty-two parasite lineages (18 Plasmodium spp. and 4 Haemoproteus spp.). Presence of Plasmodium sporozoites in salivary glands of Coquillettidia aurites further established these mosquitoes as likely vectors. Occurrence of parasite lineages differed significantly among genera, as well as their probability of being infected with malaria across species and sites. Approximately one-third of these lineages were previously detected in other avian host species from the region, indicating that vertebrate host sharing is a common feature and that avian Plasmodium spp. vector breadth does not always accompany vertebrate-host breadth. This study suggests extensive invertebrate host shifts in mosquito-parasite interactions and that avian Plasmodium species are most likely not tightly coevolved with vector species.
Abstract.
Author URL.
Bonneaud C, Balenger SL, Russell AF, Zhang J, Hill GE, Edwards SV (2011). Rapid evolution of disease resistance is accompanied by functional changes in gene expression in a wild bird.
Proc Natl Acad Sci U S A,
108(19), 7866-7871.
Abstract:
Rapid evolution of disease resistance is accompanied by functional changes in gene expression in a wild bird.
Wild organisms are under increasing pressure to adapt rapidly to environmental changes. Predicting the impact of these changes on natural populations requires an understanding of the speed with which adaptive phenotypes can arise and spread, as well as of the underlying mechanisms. However, our understanding of these parameters is poor in natural populations. Here we use experimental and molecular approaches to investigate the recent emergence of resistance in eastern populations of North American house finches (Carpodacus mexicanus) to Mycoplasma galliseptum (MG), a severe conjunctivitis-causing bacterium. Two weeks following an experimental infection that took place in 2007, finches from eastern US populations with a 12-y history of exposure to MG harbored 33% lower MG loads in their conjunctivae than finches from western US populations with no prior exposure to MG. Using a cDNA microarray, we show that this phenotypic difference in resistance was associated with differences in splenic gene expression, with finches from the exposed populations up-regulating immune genes postinfection and those from the unexposed populations generally down-regulating them. The expression response of western US birds to experimental infection in 2007 was more similar to that of the eastern US birds studied in 2000, 7 y earlier in the epizootic, than to that of eastern birds in 2007. These results support the hypothesis that resistance has evolved by natural selection in the exposed populations over the 12 y of the epizootic. We hypothesize that host resistance arose and spread from standing genetic variation in the eastern US and highlight that natural selection can lead to rapid phenotypic evolution in populations when acting on such variation.
Abstract.
Author URL.
Lahdenperä M, Lummaa V, Russell AF (2011). Selection on male longevity in a monogamous human population: late-life survival brings no additional grandchildren.
J Evol Biol,
24(5), 1053-1063.
Abstract:
Selection on male longevity in a monogamous human population: late-life survival brings no additional grandchildren.
Humans are exceptionally long-lived for mammals of their size. In men, lifespan is hypothesized to evolve from benefits of reproduction throughout adult life. We use multi-generational data from pre-industrial Finland, where remarriage was possible only after spousal death, to test selection pressures on male longevity in four monogamous populations. Men showed several behaviours consistent with attempting to accrue direct fitness throughout adult life and sired more children in their lifetimes if they lost their first wife and remarried. However, remarriage did not increase grandchild production because it compromised the success of motherless first-marriage offspring. Overall, grandchild production was not improved by living beyond 51 years and was reduced by living beyond 65. Our results highlight the importance of using grandchild production to understand selection on human life-history traits. We conclude that selection for (or enforcement of) lifetime monogamy will select for earlier reproductive investment and against increased lifespan in men.
Abstract.
Author URL.
Lahdenperä M, Russell AF, Tremblay M, Lummaa V (2011). Selection on menopause in two premodern human populations: no evidence for the Mother Hypothesis.
Evolution,
65(2), 476-489.
Abstract:
Selection on menopause in two premodern human populations: no evidence for the Mother Hypothesis.
Evolutionary theory suggests that natural selection should synchronize senescence of reproductive and somatic systems. In some species, females show dramatic discordance in senescence rates in these systems, leading to a clear menopause coupled with prolonged postreproductive life span. The Mother Hypothesis proposes that menopause evolved to avoid higher reproductive-mediated mortality risk in late-life and ensure the survival of existing offspring. Despite substantial theoretical interest, the critical predictions of this hypothesis have never been fully tested in populations with natural fertility and mortality. Here, we provide an extensive test, investigating both short- and long-term consequences of mother loss for offspring, using multigenerational demographic datasets of premodern Finns and Canadians. We found no support for the Mother Hypothesis. First, although the risk of maternal death from childbirth increased from middle age, the risk only reached 1-2% at age 50 and was predicted to range between 2% and 8% by 70. Second, offspring were adversely affected by maternal loss only in their first two years (i.e. preweaning), having reduced survival probability in early childhood as well as ultimate life span and fitness. Dependent offspring were not affected by maternal death following weaning, either in the short- or long-term. We suggest that although mothers are required to ensure offspring survival preweaning in humans, maternal loss thereafter can be compensated by other family members. Our results indicate that maternal effects on dependent offspring are unlikely to explain the maintenance of menopause or prolonged postreproductive life span in women.
Abstract.
Author URL.
2010
Russell AF, Portelli DJ, Russell DJF, Barclay H (2010). Breeding ecology of the Chestnut-crowned Babbler: a cooperative breeder in the desert.
Emu,
110(4), 324-331.
Abstract:
Breeding ecology of the Chestnut-crowned Babbler: a cooperative breeder in the desert
Cooperative breeding systems provide a rich testing ground for evolutionary theory because of the apparent paradox posed by individuals caring for the offspring of others. Such breeding systems are unusually common among Australian birds, but most species have been studied within the temperate and tropical zones. Here we provide the first detailed study of the breeding ecology of the Chestnut-crowned Babbler (Pomatostomus ruficeps), which was conducted in an arid-zone setting. Chestnut-crowned Babblers bred in groups of 2-13. Breeding occurred between late winter and early summer, 81% of 16 groups fledged offspring and 38% of groups fledged two broods. Clutch-size ranged from two to five, and one to five chicks fledged from successful nests after 21-25 days of provisioning. The size of the breeding unit had a significant effect on breeding success, with an extra chick fledged in the season for every three helpers in the group. These helper effects are among the strongest reported for pomatostomid babblers, perhaps reflecting the extreme environment in which this study was conducted. This study will form a basis for future research into the cooperative breeding system of Chestnut-crowned Babblers and aid with our understanding of variation in the breeding ecology of Australian babblers. © Royal Australasian Ornithologists Union 2010.
Abstract.
Rickard IJ, Holopainen J, Helama S, Helle S, Russell AF, Lummaa V (2010). Food availability at birth limited reproductive success in historical humans.
Ecology,
91(12), 3515-3525.
Abstract:
Food availability at birth limited reproductive success in historical humans.
Environmental conditions in early life can profoundly affect individual development and have consequences for reproductive success. Limited food availability may be one of the reasons for this, but direct evidence linking variation in early-life nutrition to reproductive performance in adulthood in natural populations is sparse. We combined historical agricultural data with detailed demographic church records to investigate the effect of food availability around the time of birth on the reproductive success of 927 men and women born in 18th-century Finland. Our study population exhibits natural mortality and fertility rates typical of many preindustrial societies, and individuals experienced differing access to resources due to social stratification. We found that among both men and women born into landless families (i.e. with low access to resources), marital prospects, probability of reproduction, and offspring viability were all positively related to local crop yield during the birth year. Such effects were generally absent among those born into landowning families. Among landless individuals born when yields of the two main crops, rye and barley, were both below median, only 50% of adult males and 55% of adult females gained any reproductive success in their lifetime, whereas 97% and 95% of those born when both yields were above the median did so. Our results suggest that maternal investment in offspring in prenatal or early postnatal life may have profound implications for the evolutionary fitness of human offspring, particularly among those for which resources are more limiting. Our study adds support to the idea that early nutrition can limit reproductive success in natural animal populations, and provides the most direct evidence to date that this process applies to humans.
Abstract.
Author URL.
Rollins LA, Holleley CE, Wright J, Russell AF, Griffith SC (2010). Isolation and characterization of 12 polymorphic tetranucleotide microsatellite loci in the apostlebird (Struthidea cinerea).
Conservation Genetics Resources,
2(SUPPL.1), 229-231.
Abstract:
Isolation and characterization of 12 polymorphic tetranucleotide microsatellite loci in the apostlebird (Struthidea cinerea)
The apostlebird (Struthidea cinerea) is an Australian endemic passerine belonging to the Corcoracidae family. The species is highly gregarious throughout the year and the name of the species refers to the apparent prevalence of social groups of around 12 birds. The species is becoming a model system for the study of sociality in vertebrates, which will require the analysis of relatedness, paternity and maternity. We characterize 12 microsatellite loci tested for polymorphism on 25 individuals from a population in western New South Wales, Australia. The number of alleles ranged from 4 to 9 per locus. Expected heterozygosities ranged from 0.69 to 0.88. This microsatellite panel will facilitate future studies that will advance our understanding of dispersal processes, inbreeding avoidance and reproductive skew in social animals. © Springer Science+Business Media B.V. 2009.
Abstract.
Gillespie DOS, Lahdenperä M, Russell AF, Lummaa V (2010). Pair-bonding modifies the age-specific intensities of natural selection on human female fecundity.
Am Nat,
176(2), 159-169.
Abstract:
Pair-bonding modifies the age-specific intensities of natural selection on human female fecundity.
In many animals, including humans, the ability of females to reproduce depends not only on their survival to each age but also on being pair-bonded to a mate. Exposure of the genetic variation underlying fecundity to natural selection should therefore depend on the proportion of females both alive and pair-bonded. In spite of this, female "marital" status is seldom considered to impact the strength of selection on age-specific fecundity. We used marriage-history data of preindustrial Finns who experienced conditions of natural mortality and fertility to investigate how assortative mating by age and socioeconomic status affected female fitness and underlay age-specific female marriage patterns. The probability that a female was married peaked at age 30-40 years; females who married in their early 20s to high-socioeconomic-status husbands had the highest levels of lifetime reproductive success. Greater age difference between the pair, which is typical for females who are married to high-socioeconomic-status husbands, increased the likelihood of widowhood occurring premenopause, adding to declines in the proportion of genetic variation exposed to selection with age. Using the age schedule of female marriage, we present an indicator of selection intensity on within-pair-bond fecundity. Our results suggest that the decline in selection intensity after age 30 years is a factor in the evolutionary maintenance of female reproductive senescence and menopause.
Abstract.
Author URL.
Fleisher PJ, Bailey PK, Natel EM, Muller EH, Cadwell DH, Russell A (2010). The 1993–1995 surge and foreland modification, Bering Glacier, Alaska. In (Ed) Bering Glacier: Interdisciplinary Studies of Earth's Largest Temperate Surging Glacier, Geological Society of America.
2009
Russell AF, Wright J (2009). Avian mobbing: byproduct mutualism not reciprocal altruism. Trends in Ecology and Evolution, 24(1), 3-5.
Rickard IJ, Lummaa V, Russell AF (2009). Elder brothers affect the life history of younger siblings in preindustrial humans: social consequence or biological cost?.
Evolution and Human Behavior,
30(1), 49-57.
Abstract:
Elder brothers affect the life history of younger siblings in preindustrial humans: social consequence or biological cost?
Sex-specific sibling interactions are potentially important in human ecology. It is well established that in patrilineal societies that sons suffer from the presence of brothers because of competition for inheritance. However, offspring (of both sexes) might also suffer from being born after an elder brother because of the greater costs sons may entail for their mother. Evidence that the cost of producing sons is higher has been gained from studies of ungulates and humans, with some of this cost being manifested as lower birthweight or reproductive performance of offspring born following a male. Using church record data from preindustrial Finland, we shed light on this process by investigating the demographic 'mechanisms' by which offspring born following an elder brother are compromised. First, we show that, for both men and women in this population, being born after an elder male sibling is associated with reduced probability of reproducing, a later age at first reproduction, and longer interbirth intervals. Second, we show that the primary effect of interest is a reduced probability of reproducing in those born after an elder brother (even among only those who married). Finally, we show that the total number of elder brothers who survived to adulthood has a negative effect on male offspring only, and this effect is independent of the elder brother effect above. We highlight that differences in the success of human offspring are not always social in origin as is often perceived but can also be biological, resulting from differential costs for mothers of producing male versus female offspring. © 2009 Elsevier Inc. All rights reserved.
Abstract.
Langmore NE, Cockburn A, Russell AF, Kilner RM (2009). Flexible cuckoo chick-rejection rules in the superb fairy-wren.
Behavioral Ecology,
20(5), 978-984.
Abstract:
Flexible cuckoo chick-rejection rules in the superb fairy-wren
Recognition of brood parasitic cuckoo nestlings poses a challenge to hosts because cues expressed by cuckoos and host young may be very similar. In theory, hosts should use flexible recognition rules that maximize the likelihood of rejecting cuckoo nestlings while minimizing the risk of rejecting their own young. Our previous work revealed that female superb fairy-wrens Malurus cyaneus often abandoned nestling cuckoos and that the presence of a single chick in the nest was 1 trigger for abandonment because fairy-wrens also sometimes abandoned a single fairy-wren chick. Here we use a combination of 20 years of observational data, a cross-fostering experiment, and a brood size reduction experiment to determine the basis for individual variability in the chick-rejection rules of superb fairy-wrens in response to parasitism by Horsfield's bronze-cuckoos Chalcites basalis. We show that the decision to abandon a single chick is based on integration of learned recognition cues and external cues. Experienced females were relatively more likely to abandon a single cuckoo chick and accept a single fairy-wren chick than naive females. Breeding experience therefore facilitates the ability to make an accurate rejection decision, perhaps through learned refinement of the recognition template. In addition, fairy-wrens modified their rejection threshold in relation to the presence of adult cuckoos in the population, becoming more likely to abandon single nestlings with increasing risk of parasitism. By using these flexible rejection rules, female superb fairy-wrens are more likely to defend themselves successfully against exploitation by the cuckoo and are less prone to mistakenly reject their own offspring.
Abstract.
Griesser M, Barnaby J, Schneider NA, Figenschau N, Kazem A, Wright J, Griffith SC, Russell AF (2009). Influence of winter ranging behaviour on the social organization of a cooperatively breeding bird species, the apostlebird.
Ethology,
115(9), 888-896.
Abstract:
Influence of winter ranging behaviour on the social organization of a cooperatively breeding bird species, the apostlebird
Most cooperative breeding bird species live in family groups that are formed through the prolonged association of offspring with their parents. Research into cooperative families has in particular investigated the balance between cooperation and conflict over reproductive decisions. As a consequence of this research focus, social interactions among group members outside the breeding season are rarely studied, despite the fact that they are likely to be crucial for social decisions. We investigated the social dynamics and ranging behaviour of the family group living cooperatively breeding apostlebird (Struthidea cinerea) outside the breeding season. Group size changed between, but not within, the seasons, being smaller during the breeding season than in the winter season. This change in group size was a consequence of breeding groups merging after breeding, then splitting again before the next breeding season. While breeding groups used small, non-overlapping home ranges (= 113 ha) around the nesting site, during winter groups moved up to 1200 ha (= 598 ha), and interacted frequently with up to four other winter groups. In particular large groups often joined together during winter and spent up to 50% of their time associating with other large winter groups. This apparent fission-fusion system facilitated the exchange of group members, offering the possibility to form new breeding coalitions and new groups. The results of this study suggest that behaviour outside the breeding season can be of considerable importance to the social dynamics of both families and cooperative breeding in such systems. © 2009 Blackwell Verlag GmbH.
Abstract.
Holleley CE, Russell AF, Griffith SC (2009). Isolation and characterization of polymorphic tetranucleotide microsatellite loci in the chestnut-crowned babbler (<i>Pomatostomus ruficeps</i>).
MOLECULAR ECOLOGY RESOURCES,
9(3), 993-995.
Author URL.
Holleley CE, Russell AF, Griffith SC (2009). Isolation and characterization of tetranucleotide loci in the chestnut-crowned babbler Pomatostomus ruficeps. Molecular Ecology Resources, 9, 993-995.
Russell AF, Lummaa V (2009). Maternal effects in cooperative breeders: from hymenopterans to humans.
Philos Trans R Soc Lond B Biol Sci,
364(1520), 1143-1167.
Abstract:
Maternal effects in cooperative breeders: from hymenopterans to humans.
The environment that an offspring experiences during its development can have lifelong consequences for its morphology, anatomy, physiology and behaviour that are strong enough to span generations. One aspect of an offspring's environment that can have particularly pronounced and long-lasting effects is that provided by its parent(s) (maternal effects). Some disciplines in biology have been quicker to appreciate maternal effects than others, and some organisms provide better model systems for understanding the causes and consequences of the maternal environment for ecology and evolution than others. One field in which maternal effects has been poorly represented, and yet is likely to represent a particularly fruitful area for research, is the field of cooperative breeding (i.e. systems where offspring are reared by carers in addition to parent(s)). Here, we attempt to illustrate the scope of cooperative breeding systems for maternal effects research and, conversely, highlight the importance of maternal effects research for understanding cooperative breeding systems. To this end, we first outline why mothers will commonly benefit from affecting the phenotype of their offspring in cooperative breeding systems, present potential strategies that mothers could employ in order to do so and offer predictions regarding the circumstances under which different types of maternal effects might be expected. Second, we highlight why a neglect of maternal strategies and the effects that they have on their offspring could lead to miscalculations of helper/worker fitness gains and a misunderstanding of the factors selecting for the evolution and maintenance of cooperative breeding. Finally, we introduce the possibility that maternal effects could have significant consequences for our understanding of both the evolutionary origins of cooperative breeding and the rise of social complexity in cooperative systems.
Abstract.
Author URL.
Hodge SJ, Bell MBV, Mwanguhya F, Kyabulima S, Waldick RC, Russell AF (2009). Maternal weight, offspring competitive ability, and the evolution of communal breeding.
Behavioral Ecology,
20(4), 729-735.
Abstract:
Maternal weight, offspring competitive ability, and the evolution of communal breeding
Despite the widespread occurrence of communal breeding in animal societies, the fitness consequences for mothers are poorly understood. One factor that may have an important influence on the net benefits mothers gain from breeding communally is the competitive ability of their offspring, as mothers are likely to gain substantial advantages from producing young who can outcompete the offspring of other females for access to resources. Here, we investigate the factors that influence offspring competition in the communally breeding banded mongoose (Mungos mungo). We show that heavy offspring are more likely to win competitive interactions with their littermates. Heavy offspring also receive more care and are more likely to survive to independence in large communal litters where competition is most intense. Our results also indicate that offspring weight at emergence is positively correlated with the weight of the mother at conception. As a consequence, the offspring of heavy mothers are likely to enjoy marked competitive advantages during early life. Together, our findings strongly suggest that the competitive ability of offspring will influence the costs and benefits that females experience while breeding communally and highlights the need for closer examination of the factors that influence offspring competitive ability and the influence this may have on the evolution of communal breeding.
Abstract.
Faurie C, Russell AF, Lummaa V (2009). Middleborns disadvantaged? Testing birth-order effects on fitness in pre-industrial Finns.
PLoS One,
4(5).
Abstract:
Middleborns disadvantaged? Testing birth-order effects on fitness in pre-industrial Finns.
Parental investment is a limited resource for which offspring compete in order to increase their own survival and reproductive success. However, parents might be selected to influence the outcome of sibling competition through differential investment. While evidence for this is widespread in egg-laying species, whether or not this may also be the case in viviparous species is more difficult to determine. We use pre-industrial Finns as our model system and an equal investment model as our null hypothesis, which predicts that (all else being equal) middleborns should be disadvantaged through competition. We found no overall evidence to suggest that middleborns in a family are disadvantaged in terms of their survival, age at first reproduction or lifetime reproductive success. However, when considering birth-order only among same-sexed siblings, first-, middle- and lastborn sons significantly differed in the number of offspring they were able to rear to adulthood, although there was no similar effect among females. Middleborn sons appeared to produce significantly less offspring than first- or lastborn sons, but they did not significantly differ from lastborn sons in the number of offspring reared to adulthood. Our results thus show that taking sex differences into account is important when modelling birth-order effects. We found clear evidence of firstborn sons being advantaged over other sons in the family, and over firstborn daughters. Therefore, our results suggest that parents invest differentially in their offspring in order to both preferentially favour particular offspring or reduce offspring inequalities arising from sibling competition.
Abstract.
Author URL.
Cant MA, Johnstone RA, Russell AF (2009). Reproductive skew and the evolution of menopause. In Hager R, Jones CB (Eds.) Reproductive Skew in vertebrates: proximate and ultimate causes, Cambridge University Press, 24-50.
Berg EC, Eadie JM, Langen TA, Russell AF (2009). Reverse sex-biased philopatry in a cooperative bird: Genetic consequences and a social cause.
Molecular Ecology,
18(16), 3486-3499.
Abstract:
Reverse sex-biased philopatry in a cooperative bird: Genetic consequences and a social cause
The genetic structure of a group or population of organisms can profoundly influence the potential for inbreeding and, through this, can affect both dispersal strategies and mating systems. We used estimates of genetic relatedness as well as likelihood-based methods to reconstruct social group composition and examine sex biases in dispersal in a Costa Rican population of white-throated magpie-jays (Calocitta formosa, Swainson 1827), one of the few birds suggested to have female-biased natal philopatry. We found that females within groups were more closely related than males, which is consistent with observational data indicating that males disperse upon maturity, whereas females tend to remain in their natal territories and act as helpers. In addition, males were generally unrelated to one another within groups, suggesting that males do not disperse with or towards relatives. Finally, within social groups, female helpers were less related to male than female breeders, suggesting greater male turnover within groups. This last result indicates that within the natal group, female offspring have more opportunities than males to mate with nonrelatives, which might help to explain the unusual pattern of female-biased philopatry and male-biased dispersal in this system. We suggest that the novel approach adopted here is likely to be particularly useful for short-term studies or those conducted on rare or difficult-to-observe species, as it allows one to establish general patterns of philopatry and genetic structure without the need for long-term monitoring of identifiable individuals. © 2009 Blackwell Publishing Ltd.
Abstract.
Portelli DJ, Barclay H, Russell DJF, Griffith SC, Russell AF (2009). Social organisation and foraging ecology of the cooperatively breeding Chestnut-crowned Babbler (pomatostomus ruficeps).
Emu,
109(2), 153-162.
Abstract:
Social organisation and foraging ecology of the cooperatively breeding Chestnut-crowned Babbler (pomatostomus ruficeps)
An individual's fitness is assumed to be maximised through early dispersal and independent breeding. However, offspring across a diversity of taxonomic groups delay dispersal and remain with at least one of their parents after reaching sexual maturity. Delayed dispersal and resulting family living are expected to arise when constraints exist on independent reproduction and where offspring benefit by remaining philopatric. A first step to elucidating the nature of such constraints and benefits for a given species is to have an understanding of the social organisation and habitat preferences of a species. The present study examined the social organisation, foraging preferences and characteristics of preferred foraging areas during a breeding season in the cooperatively breeding Chestnut-crowned Babbler (Pomatostomus ruficeps). During the study, groups of Babblers bred plurally in breeding units of two to 13 adults that occupied non-exclusive home-ranges averaging 38ha, with larger groups occupying larger ranges. Babblers spent most of the day foraging, mostly on the ground, and preferred to forage within drainage zones. The preference for such zones probably arose because they offered both greater vegetative cover from aerial predators and biomasses of potential prey. These findings lead to the prediction that the availability of drainage zones within a group's range will influence offspring dispersal decisions in Chestnut-crowned Babblers at the site studied. © 2009 Royal Australasian Ornithologists Union.
Abstract.
2008
Wright J, Russell AF (2008). How helpers help: Disentangling ecological confounds from the benefits of cooperative breeding.
Journal of Animal Ecology,
77(3), 427-429.
Abstract:
How helpers help: Disentangling ecological confounds from the benefits of cooperative breeding
Evolutionary explanations for helping in cooperative breeding systems usually require a positive effect of helping on the fitness of the breeders being assisted. However, such helper effects have proven surprisingly difficult to quantify. Cockburn et al. (this issue) apply detailed statistical analyses to long-term field data on the enigmatic superb fairy-wren. They show that it is possible to disentangle the complex web of ecological and evolutionary interactions that confound so many studies. Whilst fairy-wren helpers may not increase nest productivity, they do increase future survival of breeding females. This study points the way for future statistical explorations of long-term data in other cooperative birds and mammals. © 2008 the Authors.
Abstract.
Russell AF, Langmore NE, Gardner JL, Kilner RM (2008). Maternal investment tactics in superb fairy-wrens.
Proc Biol Sci,
275(1630), 29-36.
Abstract:
Maternal investment tactics in superb fairy-wrens.
In cooperatively breeding species, parents often use helper contributions to offspring care to cut their own costs of investment (i.e. load-lightening). Understanding the process of load-lightening is essential to understanding both the rules governing parental investment and the adaptive value of helping behaviour, but little experimental work has been conducted. Here we report the results of field experiments to determine maternal provisioning rules in cooperatively breeding superb fairy-wrens (Malurus cyaneus). By manipulating carer: offspring ratios, we demonstrate that helpers allow females to reduce the rate at which they provision their brood. Female reductions, however, were less than that provided by helpers, so that chicks still received food at a faster rate in the presence of helpers. Despite this, chicks fed by parents and helpers were not heavier than those provisioned by parents alone. This is because maternal load-lightening not only occurs during the chick provisioning stage, but also at the egg investment stage. Theoretically, complete load-lightening is predicted when parents value themselves more highly than their offspring. We tested this idea by 'presenting' mothers with a 'choice' between reducing their own levels of care and increasing investment in their offspring. We found that mothers preferred to cut their contributions to brood care, just as predicted. Our experiments help to explain why helper effects on offspring success have been difficult to detect in superb fairy-wrens, and suggest that the accuracy with which theoretical predictions of parental provisioning rules are matched in cooperative birds depends on measuring maternal responses to helper presence at both the egg and chick stages.
Abstract.
Author URL.
Gillespie DOS, Russell AF, Lummaa V (2008). When fecundity does not equal fitness: evidence of an offspring quantity versus quality trade-off in pre-industrial humans.
Proc Biol Sci,
275(1635), 713-722.
Abstract:
When fecundity does not equal fitness: evidence of an offspring quantity versus quality trade-off in pre-industrial humans.
Maternal fitness should be maximized by the optimal division of reproductive investment between offspring number and offspring quality. While evidence for this is abundant in many taxa, there have been fewer tests in mammals, and in particular, humans. We used a dataset of humans spanning three generations from pre-industrial Finland to test how increases in maternal fecundity affect offspring quality and maternal fitness in contrasting socio-economic conditions. For 'resource-poor' landless families, but not 'resource-rich' landowning families, maternal fitness returns diminished with increased maternal fecundity. This was because the average offspring contribution to maternal fitness declined with increased maternal fecundity for landless but not landowning families. This decline was due to reduced offspring recruitment with increased maternal fecundity. However, in landowning families, recruited offspring fecundity increased with increased maternal fecundity. This suggests that despite decreased offspring recruitment, maternal fitness is not reduced in favourable socio-economic conditions due to an increase in subsequent offspring fecundity. These results provide evidence consistent with an offspring quantity-quality trade-off in the lifetime reproduction of humans from poor socio-economic conditions. The results also highlight the importance of measuring offspring quality across their whole lifespan to estimate reliably the fitness consequences of increased maternal fecundity.
Abstract.
Author URL.
2007
Russell AF, Young AJ, Spong G, Jordan NR, Clutton-Brock TH (2007). Helpers increase the reproductive potential of offspring in cooperative meerkats. Proceedings of the Royal Society B: Biological Sciences, 274
Bergmüller R, Johnstone RA, Russell AF, Bshary R (2007). Integrating cooperative breeding into theoretical concepts of cooperation.
Behavioural Processes,
76(2), 61-72.
Abstract:
Integrating cooperative breeding into theoretical concepts of cooperation
In cooperative breeding systems, some individuals help to raise offspring that are not their own. While early explanations for such altruistic behaviour were predominantly based on kin selection, recent evidence suggests that direct benefits may be important in the maintenance of cooperation. To date, however, discussions of cooperative breeding have made little reference to more general theories of cooperation between unrelated individuals (while these theories rarely address cooperative breeding). Here, we attempt to integrate the two fields. We identify four key questions that can be used to categorise different mechanisms for the maintenance of cooperative behaviour: (1) whether or not individuals invest in others; (2) whether or not this initial investment elicits a return investment by the beneficiary; (3) whether the interaction is direct, i.e. between two partners, or indirect (involving third parties) and (4) whether only actions that increase the fitness of the partner or also fitness reducing actions (punishment) are involved in the interaction. Asking these questions with regards to concepts in the literature on cooperative breeding, we found that (a) it is often straightforward to relate these concepts to general mechanisms of cooperation, but that (b) a single term (such as 'pay-to-stay', 'group augmentation' or 'prestige') may sometimes subsume two or more distinct mechanisms, and that (c) at least some mechanisms that are thought to be important in cooperative breeding systems have remained largely unexplored in the theoretical literature on the evolution of cooperation. Future theoretical models should incorporate asymmetries in power and pay off structure caused for instance by dominance hierarchies or partner choice, and the use of N-player games. The key challenges for both theoreticians and empiricists will be to integrate the hitherto disparate fields and to disentangle the parallel effects of kin and non-kin based mechanisms of cooperation. © 2007.
Abstract.
Lummaa V, Pettay JE, Russell AF (2007). Male twins reduce fitness of female co-twins in humans.
Proc Natl Acad Sci U S A,
104(26), 10915-10920.
Abstract:
Male twins reduce fitness of female co-twins in humans.
In mammals, including humans, female fetuses that are exposed to testosterone from adjacent male fetuses in utero can have masculinized anatomy and behavior. However, the reproductive consequences of such prebirth sex-ratio effects for offspring and their implications for maternal fitness remain unexplored. Here we investigate the effects of being gestated with a male co-twin for daughter lifetime reproductive success, and the fitness consequences for mothers of producing mixed-sex twins in preindustrial (1734-1888) Finns. We show that daughters born with a male co-twin have reduced lifetime reproductive success compared to those born with a female co-twin. This reduction arises because such daughters have decreased probabilities of marrying as well as reduced fecundity. Mothers who produce opposite-sex twins consequently have fewer grandchildren (and hence lower fitness) than mothers who produce same-sex twins. Our results are unlikely to be a consequence of females born with male co-twins receiving less nutrition because such females do not have reduced survival and increases in food availability fail to improve their reproductive success. Nor are our results explained by after-birth social factors (females growing up with similarly aged brothers) because females born with a male co-twin have reduced success even when their co-twin dies shortly after birth and are raised as singletons after birth. Our findings suggest that hormonal interactions between opposite-sex fetuses known to influence female morphology and behavior can also have negative effects on daughter fecundity and, hence, maternal fitness, and bear significant implications for adaptive sex allocation in mammals.
Abstract.
Author URL.
Bergmüller R, Russell AF, Johnstone RA, Bshary R (2007). On the further integration of cooperative breeding and cooperation theory.
Behavioural Processes,
76(2), 170-181.
Abstract:
On the further integration of cooperative breeding and cooperation theory
We present a synopsis about the commentaries to the target article "Integrating cooperative breeding into theoretical concepts of cooperation", in which we attempted to integrate general mechanisms to explain cooperative behaviour among unrelated individuals with classic concepts to explain helping behaviour in cooperative breeders that do not invoke kin-based benefits. Here we (1) summarize the positions of the commentators concerning the main issues we raised in the target article and discuss important criticisms and extensions. (2) We relate our target article to some recent reviews on the evolution of cooperation and, (3) clarify how we use terminology with regard to cooperation and cooperative behaviour. (4) We discuss several aspects that were raised with respect to cooperative interactions including by-product mutualism, generalised reciprocity and multi-level selection and, (5) examine the alternatives to our classification scheme as proposed by some commentaries. (6) Finally, we highlight several aspects that might hinder the application of game theoretical mechanisms of cooperation in cooperatively breeding systems. Although there is broad agreement that cooperative breeding theory should be integrated within the more general concepts of cooperation, there is some debate about how this may be achieved. We conclude that the contributions in this special issue provide a fruitful first step and ample suggestions for future directions with regard to a more unified framework of cooperation in cooperative breeders. © 2007.
Abstract.
Rickard IJ, Russell AF, Lummaa V (2007). Producing sons reduces lifetime reproductive success of subsequent offspring in pre-industrial Finns.
Proc Biol Sci,
274(1628), 2981-2988.
Abstract:
Producing sons reduces lifetime reproductive success of subsequent offspring in pre-industrial Finns.
Life-history theory states that reproductive events confer costs upon mothers. Many studies have shown that reproduction causes a decline in maternal condition, survival or success in subsequent reproductive events. However, little attention has been given to the prospect of reproductive costs being passed onto subsequent offspring, despite the fact that parental fitness is a function of the reproductive success of progeny. Here we use pedigree data from a pre-industrial human population to compare offspring life-history traits and lifetime reproductive success (LRS) according to the cost incurred by each individual's mother in the previous reproductive event. Because producing a son versus a daughter has been associated with greater maternal reproductive cost, we hypothesize that individuals born to mothers who previously produced sons will display compromised survival and/or LRS, when compared with those produced following daughters. Controlling for confounding factors such as socio-economic status and ecological conditions, we show that those offspring born after elder brothers have similar survival but lower LRS compared with those born after elder sisters. Our results demonstrate a maternal cost of reproduction manifested in reduced LRS of subsequent offspring. To our knowledge, this is the first time such a long-term intergenerational cost has been shown in a mammal species.
Abstract.
Author URL.
Russell AF, Langmore NE, Cockburn A, Astheimer LB, Kilner RM (2007). Reduced egg investment can conceal helper effects in cooperatively breeding birds.
Science,
317(5840), 941-944.
Abstract:
Reduced egg investment can conceal helper effects in cooperatively breeding birds.
Cooperative breeding systems are characterized by nonbreeding helpers that assist breeders in offspring care. However, the benefits to offspring of being fed by parents and helpers in cooperatively breeding birds can be difficult to detect. We offer experimental evidence that helper effects can be obscured by an undocumented maternal tactic. In superb fairy-wrens (Malurus cyaneus), mothers breeding in the presence of helpers lay smaller eggs of lower nutritional content that produce lighter chicks, as compared with those laying eggs in the absence of helpers. Helpers compensate fully for such reductions in investment and allow mothers to benefit through increased survival to the next breeding season. We suggest that failure to consider maternal egg-investment strategies can lead to underestimation of the force of selection acting on helping in avian cooperative breeders.
Abstract.
Author URL.
Lahdenperä M, Russell AF, Lummaa V (2007). Selection for long lifespan in men: Benefits of grandfathering?.
Proceedings of the Royal Society B: Biological Sciences,
274(1624), 2437-2444.
Abstract:
Selection for long lifespan in men: Benefits of grandfathering?
Life-history theory suggests that individuals should live until their reproductive potential declines, and the lifespan of human men is consistent with this idea. However, because women can live long after menopause and this prolonged post-reproductive life can be explained, in part, by the fitness enhancing effects of grandmothering, an alternative hypothesis is that male lifespan is influenced by the potential to gain fitness through grandfathering. Here we investigate whether men, who could not gain fitness through reproduction after their wife's menopause (i.e. married only once), enhanced their fitness through grandfathering in historical Finns. Father presence was associated with reductions in offspring age at first reproduction and birth intervals, but generally not increases in reproductive tenure lengths. Father presence had little influence on offspring lifetime fecundity and no influence on offspring lifetime reproductive success. Overall, in contrast to our results for women in the same population, men do not gain extra fitness (i.e. more grandchildren) through grandfathering. Our results suggest that if evidence for a 'grandfather' hypothesis is lacking in a monogamous society, then its general importance in shaping male lifespan during our more promiscuous evolutionary past is likely to be negligible. © 2007 the Royal Society.
Abstract.
Gilchrist JS, Russell AF (2007). Who cares? Individual contributions to pup care by breeders vs non-breeders in the cooperatively breeding banded mongoose (Mungos mungo).
Behavioral Ecology and Sociobiology,
61(7), 1053-1060.
Abstract:
Who cares? Individual contributions to pup care by breeders vs non-breeders in the cooperatively breeding banded mongoose (Mungos mungo)
Knowledge of the investment rules adopted by breeders and non-breeders, and the factors that affect them, is essential to understanding cooperative breeding as part of a life-history tactic. Although the factors that affect relative contributions to care of young have been studied in some cooperative bird species, there is little data on mammals, making coherent generalisations within mammals and across taxa difficult. In this study, we investigate individual contributions to pup escorting, a strong predictor of offspring provisioning, in the banded mongoose (Mungos mungo), a cooperatively breeding mammal in which reproductive skew is low. Contributions by those under a year old (which virtually never breed) increased with age and body weight but were generally low. Among older age classes (yearlings and adults), individuals that had not bred in the current litter generally contributed less to escorting than those that had bred (with the exception of yearling males). In addition, females that did not breed reduced their investment if they were heavy presumably because such females are more likely to breed in the following event and benefit from saving resources for this. The generally greater contributions by breeders in banded mongooses contrast with the recent findings in meerkats (Suricata suricatta), another obligatorily cooperative mongoose with similar group size but wherein reproductive skew is high. Our results suggest that relative contributions by breeders vs non-breeders are not dependent on group size but on the ratio of breeders to carers and the probability that non-breeders will breed in the near future. © 2007 Springer-Verlag.
Abstract.
2006
Carlson AA, Manser, M.B. Young, A.J. Russell, A.F. Jordan N, McNeilly AS, Clutton-Brock TH (2006). Cortisol levels are positively associated with pup-feeding rates in male meerkats. Proceedings of the Royal Society B: Biological Sciences, 273
Carlson AA, Russell, A.F. Young, A.J. Jordan, N. McNeilly AS, Clutton-Brock TH (2006). Elevated prolactin levels immediately precede decisions to babysit by male meerkat helpers. Hormones and Behaviour, 50
Clutton-Brock TH, Hodge SJ, Spong G, Russell AF, Jordan NR, Bennett NC, Sharpe LL, Manser MB (2006). Intrasexual competition and sexual selection in cooperative mammals.
Nature,
444(7122), 1065-1068.
Abstract:
Intrasexual competition and sexual selection in cooperative mammals.
In most animals, the sex that invests least in its offspring competes more intensely for access to the opposite sex and shows greater development of secondary sexual characters than the sex that invests most. However, in some mammals where females are the primary care-givers, females compete more frequently or intensely with each other than males. A possible explanation is that, in these species, the resources necessary for successful female reproduction are heavily concentrated and intrasexual competition for breeding opportunities is more intense among females than among males. Intrasexual competition between females is likely to be particularly intense in cooperative breeders where a single female monopolizes reproduction in each group. Here, we use data from a twelve-year study of wild meerkats (Suricata suricatta), where females show high levels of reproductive skew, to show that females gain greater benefits from acquiring dominant status than males and traits that increase competitive ability exert a stronger influence on their breeding success. Females that acquire dominant status also develop a suite of morphological, physiological and behavioural characteristics that help them to control other group members. Our results show that sex differences in parental investment are not the only mechanism capable of generating sex differences in reproductive competition and emphasize the extent to which competition for breeding opportunities between females can affect the evolution of sex differences and the operation of sexual selection.
Abstract.
Author URL.
Young AJ, Carlson AA, Russell AF, Bennett NC, Monfort SL, Clutton-Brock TH (2006). Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proceedings of the National Academy of Sciences, 103(32), 12005-12010.
2005
Clutton-Brock TH, Russell AF, Sharpe LL, Jordan NR (2005). 'False feeding' and aggression in meerkat societies.
Animal Behaviour,
69(6), 1273-1284.
Abstract:
'False feeding' and aggression in meerkat societies
In cooperative societies, group members are expected to be punished for being lazy and so behaviours that exaggerate an individual's contribution to cooperation may be favoured by selection. In cooperative meerkats, Suricata suricatta, helpers vary in their level of care and, within breeding attempts, helpers can be categorized as 'generous' or 'lazy'. Lazy helpers were more likely to carry food to pups and then eat it themselves and lazy males received more aggression, supporting the idea that 'false feeding' could be an adaptive tactic used to exaggerate individual contributions to care. However, our results are also consistent with the more parsimonious idea that 'false feeding' occurs when individuals decide not to deliver food items after assessing the needs of pups relative to their own. Group members were not obviously deceived by 'false feeders' nor was 'false feeding' associated with any obvious benefit. In general, the frequency of 'false feeding' increased when the net benefits of feeding pups were likely to be low. The frequency of 'false feeding' increased with rising food item value and with decreasing pup dependency on food provided by helpers. Female helpers (which feed pups more than male helpers and preferentially feed female pups) 'false fed' less than male helpers and 'false fed' male pups more than female pups. We suggest that there is little unequivocal evidence of deception by helpers over contributions to care in cooperative vertebrates and that 'false feeding' may occur where helpers adjust their decisions immediately before feeding young or where they are subject to conflicting motivations. © 2005 the Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Abstract.
Stephens PA, Russell AF, Young AJ, Sutherland WJ, Clutton-Brock TH (2005). Dispersal, eviction, and conflict in meerkats (Suricata suricatta): an evolutionarily stable strategy model.
American Naturalist,
165(1), 120-135.
Abstract:
Dispersal, eviction, and conflict in meerkats (Suricata suricatta): an evolutionarily stable strategy model
Decisions regarding immigration and emigration are crucial to understanding group dynamics in social animals, but dispersal is rarely treated in models of optimal behavior. We developed a model of evolutionarily stable dispersal and eviction strategies for a cooperative mammal, the meerkat Suricata suricatta. Using rank and group size as state variables, we determined state-specific probabilities that subordinate females would disperse and contrasted these with probabilities of eviction by the dominant female, based on the long-term fitness consequences of these behaviors but incorporating the potential for error. We examined whether long-term fitness considerations explain group size regulation in meerkats; whether long-term fitness considerations can lead to conflict between dominant and subordinate female group members; and under what circumstances those conflicts were likely to lead to stability, dispersal, or eviction. Our results indicated that long-term fitness considerations can explain group size regulation in meerkats. Group size distributions expected from predicted dispersal and eviction strategies matched empirical distributions most closely when emigrant survival was approximately that determined from the field study. Long-term fitness considerations may lead to conflicts between dominant and subordinate female meerkats, and eviction is the most likely result of these conflicts. Our model is computationally intensive but provides a general framework for incorporating future changes in the size of multimember cooperative breeding groups.
Abstract.
Caseldine C, Russell A, Harðardóttir J, Knudsen Ó (2005). Preface. In (Ed) Iceland — Modern Processes and Past Environments, Elsevier, ix-x.
2004
Russell AF, Carlson AA, McIlrath GM, Jordan NR, Clutton-Brock T (2004). Adaptive size modification by dominant female meerkats.
Evolution,
58(7), 1600-1607.
Abstract:
Adaptive size modification by dominant female meerkats.
In species of cooperative insects that live in large groups, selection for increased fecundity has led to the evolution of an increased body size among female reproductives, but whether this is also true of cooperative vertebrates is unknown. Among vertebrates, morphological modification of female breeders has only been documented in a single species; in naked mole rats (Heterocephalus glaber), acquisition of alpha status is associated with a significant increase in body size through an elongation of the lumbar vertebrae. Here we provide evidence of morphological modification among breeding females of a cooperative carnivore, the meerkat (Suricata suricatta), and demonstrate that this modification is likely to be adaptive. The same female meerkats were significantly larger when they were dominant than when they were subordinate. This increased body size was not explained by differences in age, foraging efficiency, or investment in offspring care, but may have arisen, in part, through increased levels of hormone that govern bone growth. Increases in body size are likely to result in fitness benefits, for large females delivered larger litters and had heavier offspring, both of which are known to correlate positively with measures of breeding success in meerkats. Our results suggest that the acquisition of alpha status in female meerkats is associated with an adaptive increase in body size and hence that morphological modification of female vertebrates may be more widespread than has been previously supposed.
Abstract.
Author URL.
Clutton-Brock TH, Russell AF, Sharpe LL (2004). Behavioural tactics of breeders in cooperative meerkats.
Animal Behaviour,
68(5), 1029-1040.
Abstract:
Behavioural tactics of breeders in cooperative meerkats
In eusocial invertebrates, queens commonly show morphological and behavioural modifications to their role as the principal breeders in their colonies. With the exception of naked mole-rats, Heterocephalus glaber, morphological modification of breeders has yet to be shown in cooperative vertebrates, but the behaviour of dominant individuals may be modified so as to maximize reproductive success. We studied the cooperative behaviour of dominant and subordinate adults in meerkats, Suricata suricatta, and found that the decision rules governing the contributions of dominant breeders differed from those of subordinate helpers. Dominant breeders contributed less than adult helpers to babysitting and pup feeding, but raised their individual contributions to pup care to a greater extent when helper:pup ratios were low. In contrast to subordinates, dominant breeders did not increase their contributions when they foraged successfully. Finally, while subordinates of both sexes assisted in rearing the young when dominants bred, dominant females contributed little when subordinates attempted to breed, and male helpers (but not females) reduced their contributions to the care of pups. Our results suggest that the division of labour between breeders and helpers in meerkats is intermediate between that of facultatively cooperative species, where parents are principally responsible for rearing young, and that of specialized eusocial species, which show a well-defined division of labour between breeders and workers. © 2004 the Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Abstract.
Lahdenperä M, Lummaa V, Tremblay M, Helle S, Russell AF (2004). Fitness benefits of prolonged post-reproductive lifespan in women.
Nature,
428(6979), 178-181.
Abstract:
Fitness benefits of prolonged post-reproductive lifespan in women
Most animals reproduce until they die, but in humans, females can survive long after ceasing reproduction. In theory, a prolonged post-reproductive lifespan will evolve when females can gain greater fitness by increasing the success of their offspring than by continuing to breed themselves. Although reproductive success is known to decline in old age, it is unknown whether women gain fitness by prolonging lifespan post-reproduction. Using complete multi-generational demographic records, we show that women with a prolonged post-reproductive lifespan have more grandchildren, and hence greater fitness, in pre-modern populations of both Finns and Canadians. This fitness benefit arises because post-reproductive mothers enhance the lifetime reproductive success of their offspring by allowing them to breed earlier, more frequently and more successfully. Finally, the fitness benefits of prolonged lifespan diminish as the reproductive output of offspring declines. This suggests that in female humans, selection for deferred ageing should wane when one's own offspring become post-reproductive and, correspondingly, we show that rates of female mortality accelerate as their offspring terminate reproduction.
Abstract.
Hatchwell BJ, Russell AF, MacColl ADC, Ross DJ, Fowlie MK, McGowan A (2004). Helpers increase long-term but not short-term productivity in cooperatively breeding long-tailed tits. Behavioral Ecology, 15, 1-10.
Carlson AA, Young AJ, Russell AF, Bennett NC, McNeilly AS, Clutton-Brock T (2004). Hormonal correlates of dominance in meerkats (Suricata suricatta).
Horm Behav,
46(2), 141-150.
Abstract:
Hormonal correlates of dominance in meerkats (Suricata suricatta).
In cooperatively breeding meerkats (Suricata suricatta), individuals typically live in extended family groups in which the dominant male and female are the primary reproductives, while their offspring delay dispersal, seldom breed, and contribute to the care of subsequent litters. Here we investigate hormonal differences between dominants and subordinates by comparing plasma levels of luteinizing hormone (LH), estradiol and cortisol in females, and testosterone and cortisol in males, while controlling for potential confounding factors. In both sexes, hormone levels are correlated with age. In females, levels of sex hormone also vary with body weight and access to unrelated breeding partners in the same group: subordinates in groups containing unrelated males have higher levels of LH and estradiol than those in groups containing related males only. When these effects are controlled, there are no rank-related differences in circulating levels of LH among females or testosterone among males. However, dominant females show higher levels of circulating estradiol than subordinates. Dominant males and females also have significantly higher cortisol levels than subordinates. Hence, we found no evidence that the lower levels of plasma estradiol in subordinate females were associated with high levels of glucocorticoids. These results indicate that future studies need to control for the potentially confounding effects of age, body weight, and access to unrelated breeding partners before concluding that there are fundamental physiological differences between dominant and subordinate group members.
Abstract.
Author URL.
Russell AF (2004). Mammals: comparisons & contrasts. In Koenig WD, Dickinson JL (Eds.) Ecology of Cooperative breeding in birds, vol II, MA, USA: Cambridge University Press, 210-227.
Lahdenperä M, Lummaa V, Russell AF (2004). Menopause: Why does fertility end before life?.
Climacteric,
7(4), 327-331.
Abstract:
Menopause: Why does fertility end before life?
Menopause is associated with an ultimate cessation of child-bearing potential. Medical research on menopause focuses mostly on the underlying physiological changes associated with menopause. By contrast, evolutionary biologists are interested in understanding why women lose their potential to reproduce before the end of their lives. Evolution by natural selection predicts that the behaviors that we observe today are products of generations of selection on the genes that govern those behaviors. Since one would expect an individual reproducing throughout its life to produce more offspring than an individual stopping early, one would seldom expect genes for menopause to be selected for during our evolutionary past. This article discusses how menopause and prolonged lifespan might be explained by evolutionary theory, and highlights some angles for future research.
Abstract.
2003
Russell AF, Brotherton PNM, McIlrath GM, Sharpe LL, Clutton-Brock TH (2003). Breeding success in cooperative meerkats: Effects of helper number and maternal state.
Behavioral Ecology,
14(4), 486-492.
Abstract:
Breeding success in cooperative meerkats: Effects of helper number and maternal state
Studies of cooperatively breeding birds and mammals generally concentrate on the effects that helpers have on the number of reproductive attempts females have per year or on the number and size of offspring that survive from hatching/weaning to independence. However, helpers may also influence breeding success before hatching or weaning. In the present study, we used an ultrasound imager to determine litter sizes close to birth, and multivariate statistics to investigate whether helpers influence female fecundity, offspring survival to weaning, and offspring size at weaning in cooperative meerkats, Suricata suricatta. We found that the number of helpers in a group was correlated with the number of litters that females delivered each year, probably because females in large groups gave birth earlier and had shorter interbirth intervals. In addition, although pup survival between birth and weaning was primarily influenced by maternal dominance status, helper number may also have a significant positive effect. By contrast, we found no evidence to suggest that helpers have a direct effect on either litter sizes at birth or pup weights at weaning, which were both significantly influenced by maternal weight at conception. However, because differences in maternal weight were associated with differences in helper number, helpers have the potential to influence maternal fecundity and offspring size within reproductive attempts indirectly. These results suggest that future studies may need to consider direct and indirect helper effects on female fecundity and investment before assessing helper effects on reproductive success in societies of cooperatively breeding vertebrates.
Abstract.
Griffith SC, Örnborg J, Russell AF, Andersson S, Sheldon BC (2003). Correlations between ultraviolet coloration, overwinter survival and offspring sex ratio in the blue tit.
Journal of Evolutionary Biology,
16(5), 1045-1054.
Abstract:
Correlations between ultraviolet coloration, overwinter survival and offspring sex ratio in the blue tit
We studied the correlations between offspring sex ratio, UV coloration and overwinter survival in a population of blue tits, breeding in Gotland, Sweden, over three consecutive breeding seasons. In 2 of 3 years, we found that females paired to males with relatively brighter UV-coloration produced a greater proportion of sons in their broods, and that this effect was significant with all 3 years combined, despite a significant year by male UV interaction. In addition, we found other correlates of sex ratio (breeding time, female age and clutch size) in some, but not all years, and some of these showed significantly different relationships with sex ratio between years. In both years for which data were available, there were indications that males with relatively brighter UV coloration, and that paired with females that produced male-biased clutches, were more likely to survive to the next year. In addition, we also found that in both males and females, individuals produced similar sex ratios in consecutive years. Because correlations with the sex ratio may be expected to be weak, variation in results between years within the same population may be explained by low statistical power or genuine biological differences. Our results suggest that conclusions about sex ratio variation in birds should be based on multiple years. The correlations that we found in some years of this study are consistent with models of adaptive sex ratio adjustment in response to mate quality. However, careful experimental work is required to provide tests of the assumptions of these models, and should be a priority for future work.
Abstract.
Russell AF, Sharpe LL, Brotherton PNM, Clutton-Brock TH (2003). Cost minimization by helpers in cooperative vertebrates.
Proc Natl Acad Sci U S A,
100(6), 3333-3338.
Abstract:
Cost minimization by helpers in cooperative vertebrates.
When parents invest heavily in reproduction they commonly suffer significant energetic costs. Parents reduce the long-term fitness implications of these costs through increased foraging and reduced reproductive investment in the future. Similar behavioral modifications might be expected among helpers in societies of cooperative vertebrates, in which helping is associated with energetic costs. By using multivariate analyses and experiments, we show that in cooperative meerkats, Suricata suricatta, helping is associated with substantial short-term growth costs but limited long-term fitness costs. This association forms because individual contributions to cooperation are initially condition dependent, and, because when helpers invest heavily in cooperation, they increase their foraging rate during the subsequent nonbreeding period and reduce their level of cooperative investment in the subsequent reproductive period. These results provide a unique demonstration that despite significant short-term costs, helpers, like breeders, are able to reduce the fitness consequences of these costs through behavioral modifications.
Abstract.
Author URL.
Clutton-Brock TH, Russell AF, Sharpe LL (2003). Meerkat helpers do not specialize in particular activities.
Animal Behaviour,
66(3), 531-540.
Abstract:
Meerkat helpers do not specialize in particular activities
Differences in the relative contributions of individual helpers to cooperative activities in vertebrate societies are sometimes interpreted as evidence of functional specialization and have been compared with the incipient subcaste systems found in some social insects. However, it is not yet clear whether some helpers specialize in particular tasks throughout their life span or whether variation in cooperative behaviour represents a temporary, age-related polyethism. We describe the development of cooperative behaviour in female helpers in meerkats, Suricata suricatta, an obligately cooperative mammal where young produced by the dominant female are reared by up to 30 helpers. Using a combination of field experiments and long-term records of the development of individuals, we investigated whether particular helpers specialize in particular activities. In the first year of life, variation in body weight affected overall levels of involvement in cooperative behaviour as well as relative contributions to different activities, generating contrasting activity profiles between light and heavy helpers. However, the effects of body weight disappeared by the second year of life, and individual differences in foraging success became the principal factor affecting contributions to cooperative behaviour. Contributions to different cooperative activities were positively correlated across individuals, with some helpers consistently contributing more than others to all cooperative activities. Our study provides no evidence that meerkat helpers specialize in particular cooperative activities. © 2003 Published by Elsevier Ltd on behalf of the Association for the Study of Animal Behaviour.
Abstract.
2002
Clutton-Brock TH, Russell, A.F. Sharpe, L.L. Young, A.J. Balmforth Z, McIlrath GM (2002). Evolution and development of sex differences in cooperative behaviour in meerkats. Science, 297(5579).
Russell AF, Clutton-Brock TH, Brotherton PNM, Sharpe LL, Mcilrath GM, Dalerum FD, Cameron EZ, Barnard JA (2002). Factors affecting pup growth and survival in co-operatively breeding meerkats Suricata suricatta.
Journal of Animal Ecology,
71(4), 700-709.
Abstract:
Factors affecting pup growth and survival in co-operatively breeding meerkats Suricata suricatta
1. We examined the relative importance of maternal, environmental and social factors for post-weaning pup growth and survival in a co-operatively breeding mammal, the meerkat Suricata suricatta. 2. Pup daily weight gain was primarily influenced by the number of carers per pup and the daily weight gain of those carers. Rainfall and daily temperatures had additional positive and negative effects, respectively, on weight gain of pups born to subordinates. 3. Pup overnight weight loss was primarily influenced by the amount of weight pups gained during the day, and their age. However, pups also lost considerably more weight overnight when temperatures were cold, although such effects were less in large groups. 4. Pup growth rates were positively influenced by the number of carers per pup and carer condition, and negatively influenced by high daytime temperatures. 5. Pup weight at independence was positively associated with weight at emergence and pup weight gain during provisioning, but negatively associated with the extent of overnight weight loss. 6. Pup survival between emergence and independence was related to maternal status, pup sex and overnight weight loss, as well as to group size, daytime temperature and monthly rainfall. 7. Thus, in meerkats, social factors largely, but not wholly, replace the importance of maternal factors that are commonly found to govern reproductive success in non-co-operatively breeding social vertebrates.
Abstract.
Scantlebury M, Russell AF, McIlrath GM, Speakman JR, Clutton-Brock TH (2002). The energetics of lactation in cooperatively breeding meerkats <i>Suricata suricatta</i>.
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES,
269(1505), 2147-2153.
Author URL.
2001
Clutton-Brock TH, Brotherton PN, Russell AF, O'Riain MJ, Gaynor D, Kansky R, Griffin A, Manser M, Sharpe L, McIlrath GM, et al (2001). Cooperation, control, and concession in meerkat groups.
Science,
291(5503), 478-481.
Abstract:
Cooperation, control, and concession in meerkat groups.
"Limited control" models of reproductive skew in cooperative societies suggest that the frequency of breeding by subordinates is determined by the outcome of power struggles with dominants. In contrast, "optimal skew" models suggest that dominants have full control of subordinate reproduction and allow subordinates to breed only when this serves to retain subordinates' assistance with rearing dominants' own litters. The results of our 7-year field study of cooperative meerkats, Suricata suricatta, support the predictions of limited control models and provide no indication that dominant females grant reproductive concessions to subordinates to retain their assistance with future breeding attempts.
Abstract.
Author URL.
Cunningham EJA, Russell AF (2001). Differential allocation and 'good genes' - Comment from Cunningham & Russell.
TRENDS IN ECOLOGY & EVOLUTION,
16(1), 21-21.
Author URL.
Russell AF (2001). Dispersal costs set the scene for helping in an atypical avian cooperative breeder.
Proc Biol Sci,
268(1462), 95-99.
Abstract:
Dispersal costs set the scene for helping in an atypical avian cooperative breeder.
The ecological constraints hypothesis is suggested to explain the evolution of cooperative breeding in birds. This hypothesis predicts that the scene for cooperative breeding is set when ecological factors constrain offspring from dispersal. This prediction was tested in the atypical cooperative breeding system of the long-tailed tit, Aegithalos caudatus, by comparing the degree of philopatry and cooperation in an isolated and a contiguous site whilst experimentally controlling for confounding aspects of reproduction. No difference was found between the two sites in the survival of offspring but a greater proportion were found to remain philopatric in the isolated site. This difference was caused by greater philopatry of normally dispersive females suggesting, as predicted, that dispersal costs were greater from this site. Furthermore, a greater proportion of males and females cooperated following breeding failure in the isolated site than in the contiguous site. Thus, as has been suggested for typical avian cooperative breeders, dispersal costs, relative to philopatric benefits, appear to set the scene for cooperative breeding in long-tailed tits.
Abstract.
Author URL.
Clutton-Brock TH, Russell AF, Sharpe LL, Brotherton PN, McIlrath GM, White S, Cameron EZ (2001). Effects of helpers on juvenile development and survival in meerkats.
Science,
293(5539), 2446-2449.
Abstract:
Effects of helpers on juvenile development and survival in meerkats.
Although breeding success is known to increase with group size in several cooperative mammals, the mechanisms underlying these relationships are uncertain. We show that in wild groups of cooperative meerkats, Suricata suricatta, reductions in the ratio of helpers to pups depress the daily weight gain and growth of pups and the daily weight gain of helpers. Increases in the daily weight gain of pups are associated with heavier weights at independence and at 1 year of age, as well as with improved foraging success as juveniles and higher survival rates through the first year of life. These results suggest that the effects of helpers on the fitness of pups extend beyond weaning and that helpers may gain direct as well as indirect benefits by feeding pups.
Abstract.
Author URL.
Russell AF, Hatchwell BJ (2001). Experimental evidence for kin-biased helping in a cooperatively breeding vertebrate.
Proc Biol Sci,
268(1481), 2169-2174.
Abstract:
Experimental evidence for kin-biased helping in a cooperatively breeding vertebrate.
The widespread belief that kin selection is necessary for the evolution of cooperative breeding in vertebrates has recently been questioned. These doubts have primarily arisen because of the paucity of unequivocal evidence for kin preferences in cooperative behaviour. Using the cooperative breeding system of long-tailed tits (Aegithalos caudatus) in which kin and non-kin breed within each social unit and helpers are failed breeders, we investigated whether helpers preferentially direct their care towards kin following breeding failure. First, using observational data, we show that not all failed breeders actually become helpers, but that those that do help usually do so at the nest of a close relative. Second, we confirm the importance of kinship for helping in this species by conducting a choice experiment. We show that potential helpers do not become helpers in the absence of close kin and, when given a choice between helping equidistant broods belonging to kin and non-kin within the same social unit, virtually all helped at the nest of kin. This study provides strong evidence that kinship plays an essential role in the maintenance of cooperative breeding in this species.
Abstract.
Author URL.
Petrie M, Schwabl H, Brande-Lavridsen N, Burke T (2001). Maternal investment - Sex differences in avian yolk hormone levels.
NATURE,
412(6846), 498-498.
Author URL.
Cunningham EJA, Russell AF (2001). Maternal investment - Sex differences in avian yolk hormone levels - Reply.
NATURE,
412(6846), 498-499.
Author URL.
2000
Hatchwell BJ, Russell AF, Ross DJ, Fowlie MK (2000). Divorce in cooperatively breeding long-tailed tits: a consequence of inbreeding avoidance?.
Proc Biol Sci,
267(1445), 813-819.
Abstract:
Divorce in cooperatively breeding long-tailed tits: a consequence of inbreeding avoidance?
The decision of whether to divorce a breeding partner between reproductive attempts can significantly affect individual fitness. In this paper, we report that 63% of surviving pairs of long-tailed tits Aegithalos caudatus divorced between years. We examine three likely explanations for the high divorce rate in this cooperative breeder. The 'better option' hypothesis predicts that divorce and re-pairing increases an individual's reproductive success. However, divorcees did not secure better partners or more helpers and there was no improvement in their reproductive success following divorce. The 'inbreeding avoidance' hypothesis predicts that females should disperse from their family group to avoid breeding with philopatric sons. The observed pattern of divorce was consistent with this hypothesis because, in contrast to the usual avian pattern, divorce was typical for successful pairs (81%) and less frequent in unsuccessful pairs (36-43%). The 'forced divorce' hypothesis predicts that divorce increases as the number of competitors increases. The pattern of divorce among failed breeders was consistent with this hypothesis, but it fails to explain the overall occurrence of divorce because divorcees rarely re-paired with their partners' closest competitors. We discuss long-tailed tits' unique association between divorce and reproductive success in the context of dispersal strategies for inbreeding avoidance.
Abstract.
Author URL.
Cunningham EJ, Russell AF (2000). Egg investment is influenced by male attractiveness in the mallard.
Nature,
404(6773), 74-77.
Abstract:
Egg investment is influenced by male attractiveness in the mallard.
Why females prefer to copulate with particular males is a contentious issue. Attention is currently focused on whether females choose males on the basis of their genetic quality, in order to produce more viable offspring. Support for this hypothesis in birds has come from studies showing that preferred males tend to father offspring of better condition or with increased survivorship. Before attributing greater offspring viability to a male's heritable genetic quality, however, it is important to discount effects arising from confounding sources, including maternal effects. This has generally been addressed by comparing offspring viability from two different breeding attempts by the same female: one when offspring are sired by a preferred male, and one when offspring are sired by a less preferred male. However, here we show that individual female mallard (Anas platyrhynchos) lay larger eggs after copulating with preferred males and smaller eggs after copulating with less preferred males. As a result, females produced offspring of better body condition when paired with preferred males. After controlling for these differences in maternal investment, we found no effect of paternity on offspring condition. This shows that differences between half-sibs cannot always be attributed to paternal or maternal genetic effects.
Abstract.
Author URL.
1999
Hatchwell BJ, Fowlie MK, Ross DJ, Russell AF (1999). Incubation behavior of Long-tailed Tits: Why do males provision incubating females.
Condor,
101(3), 681-686.
Abstract:
Incubation behavior of Long-tailed Tits: Why do males provision incubating females
The incubation period of Long-tailed Tits Aegithalos caudatus is highly variable, ranging from 14 to 21 days. Females alone incubate the eggs, but males provide females with some food during the incubation period, although females must also forage for themselves. Our aim was to investigate whether male provisioning of incubating females influenced female incubation behavior and the length of the incubation period. Provisioning rates varied between males, and female nest attentiveness was negatively related to short-term variation in the rate at which their partner fed them. However, the provisioning rate of individual males also varied significantly through time, and there was no significant effect of male care on female incubation across the whole incubation period. There was no evidence that variation in the behavior of either males or females influenced the length of the incubation period.
Abstract.
Hatchwell BJ, Russell AF, Fowlie MK, Ross DJ (1999). Reproductive success and nest-site selection in a cooperative breeder: Effect of experience and a direct benefit of helping.
Auk,
116(2), 355-363.
Abstract:
Reproductive success and nest-site selection in a cooperative breeder: Effect of experience and a direct benefit of helping
We determined whether nest-site characteristics influence reproductive success and whether experience influences nest-site selection in a population of cooperatively breeding Long-tailed Tits (Aegithalos caudatus). Nest predation was high; only 17% of breeding attempts resulted in fledged young. The height of nests was an important determinant of success; low nests were significantly more successful than high nests. A breeder's age, natal nest site, and breeding experience had no significant effect on nest-site selection. However, failed breeders who helped at the successful nests of conspecifics built subsequent nests lower than nests built prior to their helping experience. Failed breeders who did not help showed no reduction in the height of subsequent nests. Moreover, the subsequent reproductive success of failed breeders who helped was significantly higher than that of failed breeders who did not help. We conclude that helpers gain information on nest-site quality through their helping experience and thus gain a direct fitness benefit from their cooperative behavior. We suggest that experience as a helper offers a more reliable cue to nest-site quality than breeding experience because helpers are associated with nests only during the nestling phase when few nests are depredated. In contrast, although successful breeders may experience success with a low nest, they are even more likely to have experienced the failure of low nests because of the high rate of nest predation.
Abstract.
1996
Hatchwell BJ, Russell AF (1996). Provisioning rules in cooperatively breeding long-tailed tits Aegithalos caudatus: an experimental study.
Proceedings of the Royal Society B: Biological Sciences,
263(1366), 83-88.
Abstract:
Provisioning rules in cooperatively breeding long-tailed tits Aegithalos caudatus: an experimental study
In a population of long-tailed tits Aegithalos caudatus all birds attempted to breed monogamously, but some helped to provision the nestlings of another pair if their own breeding attempt failed. An individual's investment rules will determine the fitness consequences of helping for breeders and helpers, and the aim of this study was to examine how individual investment varied with the number of carers. Provisioning behaviour was investigated in two ways. First, observations of natural variation showed that males and females reduced their provisioning effort when aided by one helper, but showed no further reduction with additional helpers. By contrast, helpers did not adjust their provisioning effort in relation to the number of helpers at a nest. Secondly, the reaction of parents to the presence of helpers was tested experimentally by the temporary removal of helpers. Both parents significantly increased their provisioning rate when helpers were absent, and the total provisioning rate was unaffected by the manipulation. The reactions of breeders and helpers to the number of carers, and the fitness benefits for breeders and helpers are discussed.
Abstract.
1995
Russell AF, Wanless S, Harris MP (1995). Factors affecting the production of
pellets by Shags Phalacrocorax aristotelis. Seabird, 17, 44-49.
1993
Wanless S, Harris MP, Russell AF (1993). Factors influencing food load sizes
brought in by Shags Phalacrocorax aristotelis during chick rearing. Ibis, 135, 19-24.
1990
Harris MP, Towll H, Russell AF, Wanless S (1990). Maximum dive depths attained by auks feeding young on the Isle of May, Scotland. Scottish Birds, 16, 25-28.
