Publications by category
Journal articles
Wood E, Pablo C-L, Cram D, Walker L, York J, Anke L, Hamilton P, Tyler C, Young A (In Press). Social dominance and rainfall predict telomere dynamics in a cooperative arid-zone bird. Molecular Ecology
Łapińska U, Glover G, Capilla-Lasheras P, Young AJ, Pagliara S (2019). Bacterial ageing in the absence of external stressors.
Philosophical Transactions of the Royal Society B: Biological Sciences,
374(1786), 20180442-20180442.
Abstract:
Bacterial ageing in the absence of external stressors
. Evidence of ageing in the bacterium
. Escherichia coli
. was a landmark finding in senescence research, as it suggested that even organisms with morphologically symmetrical fission may have evolved strategies to permit damage accumulation. However, recent work has suggested that ageing is only detectable in this organism in the presence of extrinsic stressors, such as the fluorescent proteins and strong light sources typically used to excite them. Here we combine microfluidics with brightfield microscopy to provide evidence of ageing in
. E. coli
. in the absence of these stressors. We report (i) that the doubling time of the lineage of cells that consistently inherits the ‘maternal old pole’ progressively increases with successive rounds of cell division until it reaches an apparent asymptote, and (ii) that the parental cell divides asymmetrically, with the old pole daughter showing a longer doubling time and slower glucose accumulation than the new pole daughter. Notably, these patterns arise without the progressive accumulation or asymmetric partitioning of observable misfolded-protein aggregates, phenomena previously hypothesized to cause the ageing phenotype. Our findings suggest that ageing is part of the naturally occurring ecologically-relevant phenotype of this bacterium and highlight the importance of alternative mechanisms of damage accumulation in this context.
.
. This article is part of a discussion meeting issue ‘Single cell ecology’.
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York JE, Wells KJ, Young AJ (2019). Dominance-related contributions to collective territory defence are adjusted according to the threat.
Animal Behaviour,
158, 25-34.
Abstract:
Dominance-related contributions to collective territory defence are adjusted according to the threat
Across diverse societies, group members benefit from the cooperative maintenance of a shared territory (a public good). How such public goods are maintained has received extensive interest, yet individual contributions to cooperative territory defence remain poorly understood. Recent theory predicts that, in groups with social hierarchies, privileged individuals will contribute most to competition with rival groups as they benefit most from defence of the territory. Here, we investigated whether dominant individuals contribute more to territory defence in a group-territorial bird in which dominants monopolize within-group reproduction: the white-browed sparrow-weaver, Plocepasser mahali. Using simulated territorial intrusions, we demonstrate that dominants contributed significantly more than subordinates to territory defence. We also found that individual contributions were adjusted according to threat: males of both social classes significantly and similarly increased their contributions to defence in response to a high threat (playback of an unfamiliar pair's duet, rather than that of a neighbouring pair), which was associated with a stronger collective response by the group. Thus, while dominants contributed most as predicted by the asymmetry in benefits, subordinates did increase contributions when they were needed most (in small groups and under greater threat). Contributions by subordinates when needed most also highlights that dominants could still benefit substantially from tolerating the presence of subordinates despite their overall lower contributions. Our results show that public goods can be maintained despite unequal contributions and highlight the potential importance of context-dependent behavioural flexibility in mitigating collective action problems.
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Houslay TM, Earley RL, Young AJ, Wilson AJ (2019). Habituation and individual variation in the endocrine stress response in the Trinidadian guppy (Poecilia reticulata).
General and Comparative Endocrinology,
270, 113-122.
Abstract:
Habituation and individual variation in the endocrine stress response in the Trinidadian guppy (Poecilia reticulata)
The vertebrate stress response enables individuals to react to and cope with environmental challenges. A crucial aspect of the stress response is the elevation of circulating glucocorticoids. However, continued activation of the stress response under repeated exposure to stressors can be damaging to fitness. Under certain circumstances it may therefore be adaptive to habituate to repeated exposures to a particular stressor by reducing the magnitude of any associated release of glucocorticoids. Here, we investigate whether Trinidadian guppies (Poecilia reticulata) habituate to repeated exposure to a mild stressor, using a waterborne hormone sampling approach that has previously been shown to elicit a stress response in small fish. We also test for individual variation in the extent of habituation to this stressor. Concentrating on freely circulating cortisol, we found that the first exposure to the assay induced high cortisol release rates but that guppies tended to habituate quickly to subsequent exposures. There were consistent differences among individuals in their average cortisol release rate (after accounting for effects of variables such as body size) over repeated exposures. Our analyses did not find evidence of individual differences in habituation rate, although limitations in statistical power could account for this finding. We repeated the analysis for free 11-ketotestosterone, which can also respond to stressors, but found no obvious habituation pattern and no among-individual variation. We also present data on conjugated forms of both hormones, which were repeatable but did not show the expected time-lagged habituation effect. We discuss consistent individual differences around the general pattern of habituation in the flexible stress response, and highlight the potential for individual variation in habituation to facilitate selection against the deleterious effects of chronic stress.
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Wood EM, Young AJ (2019). Telomere attrition predicts reduced survival in a wild social bird, but short telomeres do not.
Mol Ecol,
28(16), 3669-3680.
Abstract:
Telomere attrition predicts reduced survival in a wild social bird, but short telomeres do not.
Attempts to understand the causes of variation in senescence trajectories would benefit greatly from biomarkers that reflect the progressive declines in somatic integrity (SI) that lead to senescence. While telomere length has attracted considerable interest in this regard, sources of variation in telomere length potentially unrelated to declines in SI could, in some contexts, leave telomere attrition rates a more effective biomarker than telomere length alone. Here, we investigate whether telomere length and telomere attrition rates predict the survival of wild white-browed sparrow-weaver nestlings (Plocepasser mahali). Our analyses of telomere length reveal counterintuitive patterns: telomere length soon after hatching negatively predicted nestling survival to fledging, a pattern that appears to be driven by differentially high in-nest predation of broods with longer telomeres. Telomere length did not predict survival outside this period: neither hatchling telomere length nor telomere length in the mid-nestling period predicted survival from fledging to adulthood. Our analyses using within-individual telomere attrition rates, by contrast, revealed the expected relationships: nestlings that experienced a higher rate of telomere attrition were less likely to survive to adulthood, regardless of their initial telomere length and independent of effects of body mass. Our findings support the growing use of telomeric traits as biomarkers of SI, but lend strength to the view that longitudinal assessments of within-individual telomere attrition since early life may be a more effective biomarker in some contexts than telomere length alone.
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Benton CH, Delahay RJ, Smith FAP, Robertson A, McDonald RA, Young AJ, Burke TA, Hodgson D (2018). Inbreeding intensifies sex- and age-dependent disease in a wild mammal.
J Anim Ecol,
87(6), 1500-1511.
Abstract:
Inbreeding intensifies sex- and age-dependent disease in a wild mammal.
The mutation accumulation theory of senescence predicts that age-related deterioration of fitness can be exaggerated when inbreeding causes homozygosity for deleterious alleles. A vital component of fitness, in natural populations, is the incidence and progression of disease. Evidence is growing for natural links between inbreeding and ageing; between inbreeding and disease; between sex and ageing; and between sex and disease. However, there is scant evidence, to date, for links among age, disease, inbreeding and sex in a single natural population. Using ecological and epidemiological data from a long-term longitudinal field study, we show that in wild European badgers (Meles meles) exposed naturally to bovine tuberculosis (bTB), inbreeding (measured as multilocus homozygosity) intensifies a positive correlation between age and evidence of progressed infection (measured as an antibody response to bTB), but only among females. Male badgers suffer a steeper relationship between age and progressed infection than females, with no influence of inbred status. We found no link between inbreeding and the incidence of progressed infection during early life in either sex. Our findings highlight an age-related increase in the impact of inbreeding on a fitness-relevant trait (disease state) among females. This relationship is consistent with the predictions of the mutation accumulation theory of senescence, but other mechanisms could also play a role. For example, late-life declines in condition, arising through mechanisms other than mutation accumulation might have increased the magnitude of inbreeding depression in late life. Whichever mechanism causes the observed patterns, we have shown that inbreeding can influence age-dependent patterns of disease and, by extension, is likely to affect the magnitude and timing of the late-life declines in components of fitness that characterise senescence. Better understanding of sex-specific links between inbreeding, disease and ageing provides insights into population-level pathogen dynamics and could influence management strategies for wildlife reservoirs of zoonotic disease.
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Houslay TM, Vierbuchen M, Grimmer AJ, Young AJ, Wilson AJ (2018). Testing the stability of behavioural coping style across stress contexts in the Trinidadian guppy.
Functional Ecology,
32(2), 424-438.
Abstract:
Testing the stability of behavioural coping style across stress contexts in the Trinidadian guppy
Within populations, individuals can vary in stress response, a multivariate phenomenon comprising neuroendocrine, physiological and behavioural traits. Verbal models of individual stress “coping style” have proposed that the behavioural component of this variation can be described as a single axis, with each individual's coping style being consistent across time and stress contexts. Focusing on this behavioural component of stress response and combining repeated measures of multiple traits with a novel multivariate modelling framework, we test for the existence of coping style variation and assess its stability across contexts in the Trinidadian guppy (Poecilia reticulata). Specifically, we test the following hypotheses: (1) there exists repeatable among-individual behavioural (co)variation (“personality”) within a mild stress context consistent with a risk-averse–risk-prone continuum of behavioural coping style, (2) there is population-level plasticity in behaviour as a function of stressor severity, (3) there is among-individual variation in plasticity (i.e. IxE), and (4) the presence of IxE reduces cross-context stability of behavioural coping style. We found significant repeatable among-individual behavioural (co)variation in the mild stress context (open field trial), represented as an I matrix. However, I was not readily described by a simple risk-averse–risk-prone continuum as posited by the original coping style model. We also found strong evidence for population-level changes in mean behaviour with increasing stressor severity (simulated avian and piscine predation risks). Single-trait analyses did show the presence of individual-by-environment interactions (IxE), as among-individual cross-context correlations were significantly less than +1. However, multitrait analysis revealed the consequences of this plasticity variation were minimal. Specifically, we found little evidence for changes in the structure of I between mild and moderate stress contexts overall, and only minor changes between the two moderate contexts (avian vs. piscine predator). We show that a multivariate approach to assessing changes in among-individual (co)variance across contexts can prevent the over-interpretation of statistically significant, but small, individual-by-environment effects. While behavioural flexibility enables populations (and individuals) to respond rapidly to changes in the environment, multivariate personality structure can be conserved strongly across such contexts. A plain language summary is available for this article.
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Young AJ (2018). The role of telomeres in the mechanisms and evolution of life-history trade-offs and ageing.
Philosophical Transactions B: Biological Sciences Full text.
Thompson FJ, Cant MA, Marshall HH, Vitikainen, Sanderson JL, Nichols HJ, Gilchrist JS, Bell MBV, Hodge SJ, Young AJ, et al (2017). Explaining negative kin discrimination in a cooperative mammal society.
Proceedings of the National Academy of Sciences of the USA Full text.
Thompson FJ, Marshall HH, Vitikainen EIK, Young AJ, Cant MA (2017). Individual and demographic consequences of mass eviction in cooperative banded mongooses.
Animal Behaviour,
134, 103-112.
Abstract:
Individual and demographic consequences of mass eviction in cooperative banded mongooses
In animal societies, conflict within groups can result in eviction, where individuals are often permanently expelled from their group. To understand the evolution of eviction and its role in the resolution of within-group conflict requires information on the demographic consequences of eviction for individuals and groups. However, such information is usually difficult to obtain because of the difficulty in tracking and monitoring individuals after they are evicted from their natal groups. Here we used a 15-year data set on life history and demography to investigate the consequences of eviction in a tractable cooperatively breeding mammal, the banded mongoose, Mungos mungo. In this species, groups of individuals are periodically evicted en masse and eviction is a primary mechanism by which new groups form in the study population. Following eviction, we found sex differences in dispersal distance: some females established new groups on the study peninsula but males always dispersed away from the study peninsula. Evicted females suffered reduced reproductive success in the year after eviction. For the evicting group, eviction was associated with increased per capita reproductive success for females, suggesting that eviction is successful in reducing reproductive competition. However, eviction was also associated with increased intergroup conflict for the evicting group. Our results suggest that within-group conflict resolution strategies affect group productivity, group interactions and the structure of the population, and hence have fitness impacts that reach beyond the individual evictors and evictees involved in eviction.
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Beirne C, Waring L, Mcdonald RA, Delahay R, Young AJ (2016). Age-related declines in immune response in a wild mammal are unrelated to immune cell telomere length.
Proceedings of the Royal Society of London. Series B Full text.
York JE, Radford AN, de Vries B, Groothuis TG, Young AJ (2016). Dominance-related seasonal song production is unrelated to circulating testosterone in a subtropical songbird.
General and Comparative Endocrinology,
233, 43-52.
Abstract:
Dominance-related seasonal song production is unrelated to circulating testosterone in a subtropical songbird
Circulating testosterone (T) is widely considered to play a key role in the production of sexual displays by male vertebrates. While numerous studies support a role for circulating T in promoting the production of song in male birds, this understanding is based primarily on evidence from seasonally breeding northern temperate species, leaving it unclear whether this mechanism generalizes to other regions of the world. Here we investigate whether variation in circulating levels of T can explain the marked within- and among-individual variation in male song performance observed in a subtropical population of the year-round territorial white-browed sparrow weaver (Plocepasser mahali mahali). Our findings reveal that both circulating T and male song production peaked at a similar time point, halfway through the population-level breeding season. However, while dominant males were more likely to sing and sang for longer than subordinate males, within-group paired comparisons revealed no dominance-related differences in circulating T. Moreover, comparisons both among and within individual dominant males revealed that song duration, syllable rate and proportion of time spent singing were all unrelated to circulating T. Together, our findings suggest that natural variation in male song production, at least in this population of white-browed sparrow weavers, is achieved principally through mechanisms other than variation in circulating T concentration. More widely, our results are in line with the view that male song production is not exclusively regulated by gonadally synthesized steroids.
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York JE, Radford AN, Groothuis TG, Young AJ (2016). Dominant male song performance reflects current immune state in a cooperatively breeding songbird.
Ecol Evol,
6(4), 1008-1015.
Abstract:
Dominant male song performance reflects current immune state in a cooperatively breeding songbird.
Conspicuous displays are thought to have evolved as signals of individual "quality", though precisely what they encode remains a focus of debate. While high quality signals may be produced by high quality individuals due to "good genes" or favourable early-life conditions, whether current immune state also impacts signalling performance remains poorly understood, particularly in social species. Here, we experimentally demonstrate that male song performance is impaired by immune system activation in the cooperatively breeding white-browed sparrow weaver (Plocepasser mahali). We experimentally activated the immune system of free-living dominant males via subcutaneous injection of phytohemagglutinin (PHA) and contrasted its effects with those of a control (phosphate buffered saline) injection. PHA-challenged males showed significant reductions in both the duration and the rate of their song performance, relative to controls, and this could not be readily attributed to effects of the challenge on body mass, as no such effects were detected. Furthermore, male song performance prior to immune-challenge predicted the scale of the inflammatory response to the challenge. Our findings suggest that song performance characteristics are impacted by current immune state. This link between current state and signal performance might therefore contribute to enforcing the honesty of signal performance characteristics. Impacts of current state on signaling may be of particular importance in social species, where subordinates may benefit from an ability to identify and subsequently challenge same-sex dominants in a weakened state.
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Thornton A, McAuliffe K, Dall SRX, Fernandez-Duque E, Garber PA, Young AJ (2016). Fundamental Problems with the Cooperative Breeding Hypothesis. A reply to Burkart & Van Schaik.
Journal of Zoology,
299(2), 84-88.
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Thompson F, Marshall HH, Sanderson JL, Vitikainen EIK, Nichols HJ, Gilchrist J, Young AJ, Hodge SJ, Cant MA (2016). Reproductive competition triggers mass eviction in cooperative banded mongooses.
Proceedings of the Royal Society of London: Biological Sciences Full text.
Walker L, York JE, Young AJ (2016). Sexually-selected sentinels? Evidence of a role for intra-sexual competition in sentinel behavior. Behavioral Ecology
Sanderson JL, Nichols H, Marshall HH, Vitikainen E, Thompson F, Walker S, Cant MA, Young AJ (2015). Elevated glucocorticoid concentrations during gestation predict reduced reproductive success in subordinate female banded mongooses.
Biology Letters Full text.
Cram DL, Blount JD, York JE, Young AJ (2015). Immune response in a wild bird is predicted by oxidative status but does not cause oxidative stress.
PLoS One Full text.
Cram DL, Blount JD, Young AJ (2015). Oxidative status and social dominance in a wild cooperative breeder.
Functional Ecology,
29(2), 229-238.
Abstract:
Oxidative status and social dominance in a wild cooperative breeder
© 2014 British Ecological Society. Oxidative stress has been proposed as a key mediator of life-history trade-offs, yet the social factors that affect patterns of oxidative status amongst individuals in animal societies remain virtually unexplored. This is important, as rank-related differences in reproductive effort in many social species have the potential to generate, or indeed arise from, differences in oxidative status across dominance classes. Here, we examine rank-related variation in oxidative status before and after a lengthy breeding season in a wild cooperatively breeding bird with high reproductive skew, in the semi-arid zone of Southern Africa; the white-browed sparrow weaver (Plocepasser mahali). Our findings reveal that prior to breeding, neither sex showed rank-related differences in markers of oxidative damage or antioxidant protection, suggesting that dominants' reproductive monopolies do not arise from superior pre-breeding oxidative status. After breeding, however, females (who provision young at higher rates than males) suffered elevated oxidative damage, and dominant females (the only birds to lay and incubate eggs, and the primary nestling provisioners) experienced differential declines in antioxidant protection. While males als o showed reduced antioxidant capacity after breeding, this decline was not dependent on rank and not associated with elevated oxidative damage. Our findings suggest that divisions of labour in animal societies can leave the hardest-working classes differentially exposed to oxidative stress, raising the possibility of hitherto unexplored impacts on health and ageing in social species.
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Beirne C, Delahay R, Young AJ (2015). Sex differences in senescence: the role of intra-sexual competition in early adulthood. Proceedings of the Royal Society of London. Series B
Sanderson JL, Stott I, Young AJ, Vitikainen E, Hodge SJ, Cant MA (2015). The origins of consistent individual differences in cooperation in wild banded mongooses. Animal Behaviour
Cram DL, Blount JD, Young AJ (2015). The oxidative costs of reproduction are group-size dependent in a wild cooperative breeder.
Proceedings of the Royal Society of London. Series B Full text.
Young AJ, Jarvis JUM, Barnaville J, Bennett NC (2015). Workforce effects and the evolution of complex sociality in wild Damaraland mole-rat societies. The American Naturalist
Beirne C, Delahay R, Hares M, Young AJ (2014). Age-related declines and disease-associated variation in immune cell telomere length in a wild mammal.
PLoS One Full text.
Sanderson JL, Young AJ, Hodge SJ, Kyabulima S, Walker S, Cant MA (2014). Hormonal mediation of a carry-over effect in a wild cooperative mammal. Functional Ecology
Harrison XA, York JE, Young AJ (2014). Population genetic structure and direct
observations reveal sex-reversed patterns of dispersal in a cooperative bird.
Molecular Ecology Full text.
York JE, Young AJ, Radford AN (2014). Singing in the moonlight: dawn song performance of a diurnal bird varies with lunar phase. Biology Letters
Mares R, Bateman AW, English S, Clutton-Brock TH, Young AJ (2014). Timing of predispersal prospecting is influenced by environmental, social and state-dependent factors in meerkats. Animal Behaviour
Harrison XA, York JE, Cram DL, Hares MC, Young AJ (2013). Complete reproductive skew within white-browed sparrow weaver groups despite outbreeding opportunities for subordinates of both sexes.
Behavioral Ecology and Sociobiology,
67(12), 1915-1929.
Abstract:
Complete reproductive skew within white-browed sparrow weaver groups despite outbreeding opportunities for subordinates of both sexes
The distribution of reproductive success within societies is a key determinant of the outcomes of social evolution. Attempts to explain social diversity, therefore, require that we quantify reproductive skews and identify the mechanisms that generate them. Here, we address this priority using life history and genotypic data from >600 individuals in 40 wild groups of the cooperatively breeding white-browed sparrow weaver, Plocepasser mahali. We show that groups comprise up to six males and seven females, but within-group reproduction is completely monopolised by a single dominant male and female, while extra-group males sire 12-18 % of offspring. Strong within-group kin structure could frequently explain these monopolies, as subordinates had typically delayed dispersal from their natal groups and so frequently (1) lacked within-group outbreeding partners, and/or (2) stood to gain little from contesting dominant reproduction, being almost as related to the dominant's young as they would have been to their own. Kin structure alone cannot account entirely for these monopolies, however, as they remained complete following the immigration of unrelated males and females. That subordinate females remain reproductively quiescent despite also showing comparable body condition to dominants, overlapping them substantially in age, and showing no evidence of elevated stress hormone levels raises the possibility that they exercise reproductive restraint due instead to a threat of action by dominants and/or deficits in offspring fitness that might arise if subordinates bred. Our findings highlight the complexity of the mechanisms that generate reproductive disparities in animal societies and the challenge of identifying them when skews are complete. © 2013 Springer-Verlag Berlin Heidelberg.
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Harrison XA, York JE, Cram DL, Young AJ (2013). Extra-group mating increases inbreeding risk in a cooperatively breeding bird.
Molecular Ecology,
22(22), 5700-5715.
Abstract:
Extra-group mating increases inbreeding risk in a cooperatively breeding bird
In many cooperatively breeding species, females mate extra-group, the adaptive value of which remains poorly understood. One hypothesis posits that females employ extra-group mating to access mates whose genotypes are more dissimilar to their own than their social mates, so as to increase offspring heterozygosity. We test this hypothesis using life history and genetic data from 36 cooperatively breeding white-browed sparrow weaver (Plocepasser mahali) groups. Contrary to prediction, a dominant female's relatedness to her social mate did not drive extra-group mating decisions and, moreover, extra-group mating females were significantly more related to their extra-group sires than their social mates. Instead, dominant females were substantially more likely to mate extra-group when paired to a dominant male of low heterozygosity, and their extra-group mates (typically dominants themselves) were significantly more heterozygous than the males they cuckolded. The combined effects of mating with extra-group males of closer relatedness, but higher heterozygosity resulted in extra-group-sired offspring that were no more heterozygous than their within-group-sired half-siblings. Our findings are consistent with a role for male-male competition in driving extra-group mating and suggest that the local kin structure typical of cooperative breeders could counter potential benefits to females of mating extra-group by exposing them to a risk of inbreeding. © 2013 John Wiley & Sons Ltd.
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Young AJ, Bennett NC (2013). Intra-sexual selection in cooperative mammals and birds: why aren't females bigger and better armed?. Philosophical Transactions of the Royal Society of London: Biological Sciences
Lutermann H, Young AJ, Bennett NC (2013). Reproductive status and testosterone among females in cooperative mole-rat societies. General and Comparative Endocrinology
Cant MA, Young AJ (2013). Resolving social conflict among females without overt aggression. Philosophical Transactions of the Royal Society of London: Biological Sciences
Mares R, Young AJ, Clutton-Brock TH (2012). Individual contributions to territory defence
in a cooperative breeder: weighing up the benefits and costs. Proceedings of the Royal Society of London: Biological Sciences
Abbot P, Abe J, Alcock J, Alizon S, Alpedrinha JAC, Andersson M, Andre J-B, van Baalen M, Balloux F, Balshine S, et al (2011). Inclusive fitness theory and eusociality.
Nature,
471(7339), E1-E4.
Abstract:
Inclusive fitness theory and eusociality.
Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. We will focus our comments on three general issues.
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Mares R, Young AJ, Levesque DL, Harrison N, Clutton-Brock TH (2011). Responses to intruder scents in the cooperatively breeding meerkat: Sex and social status differences and temporal variation.
Behavioral Ecology,
22(3), 594-600.
Abstract:
Responses to intruder scents in the cooperatively breeding meerkat: Sex and social status differences and temporal variation
Although sex-specific responses to intruder scent marks have been described in many mammal species, less is known about variation in responses in cooperatively breeding species where differential access to breeding opportunities exists within groups. When reproductive skew is high, strong responses to extragroup breeding rivals would be expected mainly from dominant individuals, with levels of investment depending on female receptiveness. However, evidence from controlled experiments on cooperative breeders for sex and social status differences in responses to intruder scent marks is limited. Here, we investigated responses to intruder scent marks in cooperatively breeding meerkats (Suricata suricatta), where a single dominant pair largely monopolizes within-group reproduction. A series of experimental presentations using feces were used to test first, whether meerkats discriminate between resident and extragroup male scent marks; second, whether sex and social status affect the response to intruding male scents; and third, whether dominant males increase their level of response when dominant females are most receptive. Our results suggest that meerkats are able to discriminate between resident and intruding male scent marks and show that dominant males have the strongest overall response to intruder scent marks, which does not increase with female receptiveness. We suggest that, although all group members may be affected by the presence of intruders, reproductive conflict may be the main reason for the stronger response of dominant males to extragroup male scent marks in this cooperatively breeding species with high reproductive skew. © the Author 2011.
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Clutton-Brock TH, Hodge SJ, Flower TP, Spong G, Young AJ (2010). Adaptive suppression of subordinate reproduction in cooperative mammals. American Naturalist, 176, 664-673.
Young AJ, Bennett NC (2010). Morphological divergence of breeders and helpers in Damaraland mole-rat societies. Evolution, 64, 3190-3197.
Young AJ, Oosthuizen MK, Lutermann H, Bennett NC (2010). Physiological suppression eases in Damaraland mole-rat societies when ecological constraints on dispersal are relaxed.
Horm Behav,
57, 177-183.
Abstract:
Physiological suppression eases in Damaraland mole-rat societies when ecological constraints on dispersal are relaxed
In many vertebrate societies, subordinate females exhibit down-regulated reproductive physiologies relative to those of dominants, a condition commonly termed physiological suppression. Research into the causes of physiological suppression has focused principally on the role of the subordinate’s social environment (typically the presence of the dominant female and/or an absence of unrelated males within the group), while few studies have considered the additional role that the physical environment may play. Here we present new evidence from wild Damaraland mole-rats, Fukomys damarensis, revealing that physiological suppression among subordinate females eases markedly during the annual rains (a time when ecological constraints on dispersal are relaxed), despite the continued presence of the dominant female and in groups that contain no new immigrant males. Subordinate females showed substantially higher pituitary sensitivities to GnRH challenge during the wet period than the dry, a contrast that cannot be attributed to between-female differences (as it holds for paired within-female comparisons), associated changes in body mass (as our analyses control for this), or concomitant reductions in physiological stress (as their urinary cortisol concentrations were actually higher in the wet period). We suggest that our findings reflect selection for the maintenance of reproductive readiness among subordinate females during high rainfall periods, given the increased likelihood of encountering dispersal and/or mating opportunities with extra-group males when ecological constraints on dispersal are relaxed. These findings reveal new complexity in the processes that regulate physiological suppression, suggesting a key role in some species for changes in the physical as well as social environment.
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Young AJ, Monfort SL (2009). Stress and the costs of extra-territorial movement in a social carnivore. Biology Letters
Spong GF, Hodge SJ, Young AJ, Clutton-Brock TH (2008). Factors affecting the reproductive success of dominant male meerkats.
Mol Ecol,
17(9), 2287-2299.
Abstract:
Factors affecting the reproductive success of dominant male meerkats.
Identifying traits that affect the reproductive success of individuals is fundamental for our understanding of evolutionary processes. In cooperative breeders, a dominant male typically restricts mating access to the dominant female for extended periods, resulting in pronounced variation in reproductive success among males. This may result in strong selection for traits that increase the likelihood of dominance acquisition, dominance retention and reproductive rates while dominant. However, despite considerable research on reproductive skew, few studies have explored the factors that influence these three processes among males in cooperative species. Here we use genetic, behavioural and demographic data to investigate the factors affecting reproductive success in dominant male meerkats (Suricata suricatta). Our data show that dominant males sire the majority of all offspring surviving to 1 year. A male's likelihood of becoming dominant is strongly influenced by age, but not by weight. Tenure length and reproductive rate, both important components of dominant male reproductive success, are largely affected by group size and composition, rather than individual traits. Dominant males in large groups have longer tenures, but after this effect is controlled, male tenure length also correlates negatively to the number of adult females in the group. Male reproductive rate also declines as the number of intra- and extra-group competitors increases. As the time spent in the dominant position and reproductive rate while dominant explain > 80% of the total variance in reproductive success, group composition thus has major implications for male reproductive success.
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Young AJ, Monfort, S.L. Clutton-Brock, T.H. (2008). The causes of physiological suppression among female meerkats: a role for subordinate restraint due to the threat of infanticide?. Hormones and Behaviour, 53
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
Young AJ, Spong G, Clutton-Brock TH (2007). Subordinate male meerkats prospect for extra-group paternity: alternative reproductive tactics in a cooperative animal. Proceedings of the Royal Society B Biological Sciences, 274(1618), 1603-1609.
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
Young AJ, Clutton-Brock TH (2006). Infanticide by subordinates influences reproductive sharing in cooperatively breeding meerkats. Biology Letters, 2(3), 385-387.
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.
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.
Young AJ, Carlson AA, Clutton-Brock TH (2005). Trade-offs between extra-territorial prospecting and helping in a cooperative mammal. Animal Behaviour, 70(4), 829-837.
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.
Carlson AA, Nicol, L. Young, A.J. Parlow, A.F. McNeilly AS (2003). Radioimmunoassay of prolactin for the meerkat (Suricata suricatta), a cooperatively breeding carnivore. General & Comparative Endocrinology, 130
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).
Chapters
Young AJ (2009). The Causes of Physiological Suppression in Vertebrate Societies: a Synthesis. In Hager R, Jones CB (Eds.) Reproductive Skew in Vertebrates, Cambridge University Press, 397-436.
Publications by year
In Press
Wood E, Pablo C-L, Cram D, Walker L, York J, Anke L, Hamilton P, Tyler C, Young A (In Press). Social dominance and rainfall predict telomere dynamics in a cooperative arid-zone bird. Molecular Ecology
2020
Mathison K (2020). Comparing social dynamics and telomere attrition between high promiscuity and low promiscuity flocks of zebra finches (Taeniopygia guttata).
Abstract:
Comparing social dynamics and telomere attrition between high promiscuity and low promiscuity flocks of zebra finches (Taeniopygia guttata)
Extra-pair paternity (EPP) is now recognised as a widespread phenomenon among socially monogamous avian systems, but the factors driving intraspecific variation in extra-pair mating behaviours are still poorly understood. Here, I quantified EPP in two promiscuity breeding lines of the zebra finch (Taeniopygia guttata), which had been selected to have high or low breeding values of male sex drive. I found that the majority of birds were involved in extra-pair mating behaviour, and the prevalence of EPP did not differ between the two breeding lines. I present evidence that males can benefit from an increased reproductive output by engaging in extra-pair mating strategies. However, I found no evidence that males reproduced with a larger number of different mates as compared to the females in the population. I also tested the hypothesis that extra-pair mating behaviour could be stressful due to its potential to compromise social pair bonds. To do so, I conducted a within-individual repeated-measures study of telomere attrition across an experimentally-controlled breeding season. Telomere dynamics have become widely regarded as a long-term indicator of cumulative stress and biological age. I found no conclusive evidence that receiving infidelity or experiencing weaker pair bonds induces sufficient physiological stress in zebra finches for it to affect telomere dynamics. I present evidence that in this species, some individuals experienced telomere lengthening while others experienced shortening, with the longest telomeres shortening the fastest. I demonstrate that individuals with stronger social associations produced more eggs together, both within and outside the social pairs (i.e. through EPP). For this reason, I suggest that future research investigating extra-pair mating behaviours should consider the role that the social environment plays in extra-pair reproduction. This could help us gain a further understanding of how social associations influence extra-pair mate selection and the prevalence of EPP within socially monogamous species.
Abstract.
Full text.
Capilla-Lasheras P (2020). The evolution of cooperation in an arid-zone bird:. bet-hedging, plasticity and constraints.
Abstract:
The evolution of cooperation in an arid-zone bird:. bet-hedging, plasticity and constraints
The evolution of cooperation represents a long-standing puzzle in evolutionary biology. From insects to mammals, this behaviour has evolved multiple times in separate lineages. Even though inclusive fitness theory provides a solid theoretical framework to understand the evolution of cooperation, there are still many research challenges in the evolutionary study of cooperation. First, most of the evidence for the effects of cooperation on the reproductive success of beneficiaries in vertebrate societies is based on correlational studies, which can be confounded by several environmental factors. Second, there are recent theoretical formulations to explain the evolution of cooperation that have not been empirically tested yet but could shed new light on the selective pressures that facilitate the evolution of cooperation. Third, we still have a poor understanding of the sources of among individual variation in cooperative behaviours. In particular, few studies have investigated whether the level of cooperation expressed by individuals is heritable and, therefore, could respond to natural selection. In this thesis, I combine nine years of life-history and behavioural information with field experiments and genomics to investigate (i) the routes for non-breeding individuals to acquire indirect fitness benefits and (ii) the sources of among-individual variation in cooperation in white-browed sparrow-weavers (Plocepasser mahali), an arid-zone cooperative breeder. After a general introduction to the subject of cooperative breeding, in Chapter 2 I test a novel hypothesis for the evolution of cooperation, the ‘altruistic bet-hedging’ hypothesis. There, I show that non-breeding helpers reduce variation in the reproductive success of breeders without affecting their arithmetic mean reproductive success. Furthermore, I show that this reproductive variance compression appears to arise because helpers specifically reduce unpredictable rainfall-induced variation in reproductive success, just as hypothesised by global comparative studies of the evolution of cooperative breeding in birds. Then, I investigate alternative routes through which helpers may gain indirect fitness benefits. Specifically, in Chapter 3 I investigate the effects of helpers on pre- and post-natal maternal investment in reproduction. The findings in Chapter 3 provide clear evidence for maternal plasticity in pre-natal investment in reproduction (egg volume) in response to the number of helpers. Moreover, the helper effect of increased pre-natal maternal investment is associated with a decrease in post-natal maternal investment. In Chapter 4, I test the philopatry hypothesis for the evolution of sex differences in cooperation within animal societies and find strong support for this hypothesis in white-browed sparrow-weavers. Furthermore, Chapter 4 highlights the need to consider both sex differences in direct fitness benefits and costs when trying to understand sex differences in cooperation. Finally, in Chapter 5 I investigate among-helper variation in cooperative generosity, finding consistent individual differences and providing evidence for heritable variation in this trait. To conclude, in Chapter 6 I discuss the implications of these results for our general understanding of the evolution of cooperation in animal societies and highlight methodological approaches for future empirical studies of cooperation in the wild.
Abstract.
Full text.
2019
Łapińska U, Glover G, Capilla-Lasheras P, Young AJ, Pagliara S (2019). Bacterial ageing in the absence of external stressors.
Philosophical Transactions of the Royal Society B: Biological Sciences,
374(1786), 20180442-20180442.
Abstract:
Bacterial ageing in the absence of external stressors
. Evidence of ageing in the bacterium
. Escherichia coli
. was a landmark finding in senescence research, as it suggested that even organisms with morphologically symmetrical fission may have evolved strategies to permit damage accumulation. However, recent work has suggested that ageing is only detectable in this organism in the presence of extrinsic stressors, such as the fluorescent proteins and strong light sources typically used to excite them. Here we combine microfluidics with brightfield microscopy to provide evidence of ageing in
. E. coli
. in the absence of these stressors. We report (i) that the doubling time of the lineage of cells that consistently inherits the ‘maternal old pole’ progressively increases with successive rounds of cell division until it reaches an apparent asymptote, and (ii) that the parental cell divides asymmetrically, with the old pole daughter showing a longer doubling time and slower glucose accumulation than the new pole daughter. Notably, these patterns arise without the progressive accumulation or asymmetric partitioning of observable misfolded-protein aggregates, phenomena previously hypothesized to cause the ageing phenotype. Our findings suggest that ageing is part of the naturally occurring ecologically-relevant phenotype of this bacterium and highlight the importance of alternative mechanisms of damage accumulation in this context.
.
. This article is part of a discussion meeting issue ‘Single cell ecology’.
Abstract.
Full text.
York JE, Wells KJ, Young AJ (2019). Dominance-related contributions to collective territory defence are adjusted according to the threat.
Animal Behaviour,
158, 25-34.
Abstract:
Dominance-related contributions to collective territory defence are adjusted according to the threat
Across diverse societies, group members benefit from the cooperative maintenance of a shared territory (a public good). How such public goods are maintained has received extensive interest, yet individual contributions to cooperative territory defence remain poorly understood. Recent theory predicts that, in groups with social hierarchies, privileged individuals will contribute most to competition with rival groups as they benefit most from defence of the territory. Here, we investigated whether dominant individuals contribute more to territory defence in a group-territorial bird in which dominants monopolize within-group reproduction: the white-browed sparrow-weaver, Plocepasser mahali. Using simulated territorial intrusions, we demonstrate that dominants contributed significantly more than subordinates to territory defence. We also found that individual contributions were adjusted according to threat: males of both social classes significantly and similarly increased their contributions to defence in response to a high threat (playback of an unfamiliar pair's duet, rather than that of a neighbouring pair), which was associated with a stronger collective response by the group. Thus, while dominants contributed most as predicted by the asymmetry in benefits, subordinates did increase contributions when they were needed most (in small groups and under greater threat). Contributions by subordinates when needed most also highlights that dominants could still benefit substantially from tolerating the presence of subordinates despite their overall lower contributions. Our results show that public goods can be maintained despite unequal contributions and highlight the potential importance of context-dependent behavioural flexibility in mitigating collective action problems.
Abstract.
Houslay TM, Earley RL, Young AJ, Wilson AJ (2019). Habituation and individual variation in the endocrine stress response in the Trinidadian guppy (Poecilia reticulata).
General and Comparative Endocrinology,
270, 113-122.
Abstract:
Habituation and individual variation in the endocrine stress response in the Trinidadian guppy (Poecilia reticulata)
The vertebrate stress response enables individuals to react to and cope with environmental challenges. A crucial aspect of the stress response is the elevation of circulating glucocorticoids. However, continued activation of the stress response under repeated exposure to stressors can be damaging to fitness. Under certain circumstances it may therefore be adaptive to habituate to repeated exposures to a particular stressor by reducing the magnitude of any associated release of glucocorticoids. Here, we investigate whether Trinidadian guppies (Poecilia reticulata) habituate to repeated exposure to a mild stressor, using a waterborne hormone sampling approach that has previously been shown to elicit a stress response in small fish. We also test for individual variation in the extent of habituation to this stressor. Concentrating on freely circulating cortisol, we found that the first exposure to the assay induced high cortisol release rates but that guppies tended to habituate quickly to subsequent exposures. There were consistent differences among individuals in their average cortisol release rate (after accounting for effects of variables such as body size) over repeated exposures. Our analyses did not find evidence of individual differences in habituation rate, although limitations in statistical power could account for this finding. We repeated the analysis for free 11-ketotestosterone, which can also respond to stressors, but found no obvious habituation pattern and no among-individual variation. We also present data on conjugated forms of both hormones, which were repeatable but did not show the expected time-lagged habituation effect. We discuss consistent individual differences around the general pattern of habituation in the flexible stress response, and highlight the potential for individual variation in habituation to facilitate selection against the deleterious effects of chronic stress.
Abstract.
Full text.
Williams A (2019). Modelling the evolution of socio-political complexity.
Abstract:
Modelling the evolution of socio-political complexity
The level of organisation required to maintain cohesion in the vast societies we live in today is unprecedented in our past. In this thesis I look into why human societies began to shift from the small-scale groups which characterises the vast majority of human past, into the large-scale entities most of us currently live in. Several ideas have been proposed to explain why many different features of social complexity began to coalesce together in some areas of the world before others, each with some level of support from the archaeological record. In this thesis I have taken a different approach. I rigorously test one hypothesis for its logical consistency before applying it to archaeological data by formalising it as an agent-based model. The hypothesis described by Robert Carneiro (1970, 2012a) suggests that the more limited population movement is through environmental, resource, or social circumscription, the more likely complex societies are to form. By constructing agent-based models from this hypothesis I can show the conditions under which this statement is true, and have identified several areas where assumptions were not made explicit in the original hypothesis. By adapting the models to correspond with the conditions of the Valley of Oaxaca in highland Mexico, I show the extent to which the circumscription theory may explain the emergence of social complexity there and where the gaps in our knowledge lie. In creating and testing an agent-based model of the circumscription hypothesis I have shown how agent-based models may be used in archaeology to deepen our understanding of verbal theories and identified conditions which could have intensified the emergence of complex societies around the world.
Abstract.
Full text.
Wood EM, Young AJ (2019). Telomere attrition predicts reduced survival in a wild social bird, but short telomeres do not.
Mol Ecol,
28(16), 3669-3680.
Abstract:
Telomere attrition predicts reduced survival in a wild social bird, but short telomeres do not.
Attempts to understand the causes of variation in senescence trajectories would benefit greatly from biomarkers that reflect the progressive declines in somatic integrity (SI) that lead to senescence. While telomere length has attracted considerable interest in this regard, sources of variation in telomere length potentially unrelated to declines in SI could, in some contexts, leave telomere attrition rates a more effective biomarker than telomere length alone. Here, we investigate whether telomere length and telomere attrition rates predict the survival of wild white-browed sparrow-weaver nestlings (Plocepasser mahali). Our analyses of telomere length reveal counterintuitive patterns: telomere length soon after hatching negatively predicted nestling survival to fledging, a pattern that appears to be driven by differentially high in-nest predation of broods with longer telomeres. Telomere length did not predict survival outside this period: neither hatchling telomere length nor telomere length in the mid-nestling period predicted survival from fledging to adulthood. Our analyses using within-individual telomere attrition rates, by contrast, revealed the expected relationships: nestlings that experienced a higher rate of telomere attrition were less likely to survive to adulthood, regardless of their initial telomere length and independent of effects of body mass. Our findings support the growing use of telomeric traits as biomarkers of SI, but lend strength to the view that longitudinal assessments of within-individual telomere attrition since early life may be a more effective biomarker in some contexts than telomere length alone.
Abstract.
Author URL.
2018
Benton CH, Delahay RJ, Smith FAP, Robertson A, McDonald RA, Young AJ, Burke TA, Hodgson D (2018). Inbreeding intensifies sex- and age-dependent disease in a wild mammal.
J Anim Ecol,
87(6), 1500-1511.
Abstract:
Inbreeding intensifies sex- and age-dependent disease in a wild mammal.
The mutation accumulation theory of senescence predicts that age-related deterioration of fitness can be exaggerated when inbreeding causes homozygosity for deleterious alleles. A vital component of fitness, in natural populations, is the incidence and progression of disease. Evidence is growing for natural links between inbreeding and ageing; between inbreeding and disease; between sex and ageing; and between sex and disease. However, there is scant evidence, to date, for links among age, disease, inbreeding and sex in a single natural population. Using ecological and epidemiological data from a long-term longitudinal field study, we show that in wild European badgers (Meles meles) exposed naturally to bovine tuberculosis (bTB), inbreeding (measured as multilocus homozygosity) intensifies a positive correlation between age and evidence of progressed infection (measured as an antibody response to bTB), but only among females. Male badgers suffer a steeper relationship between age and progressed infection than females, with no influence of inbred status. We found no link between inbreeding and the incidence of progressed infection during early life in either sex. Our findings highlight an age-related increase in the impact of inbreeding on a fitness-relevant trait (disease state) among females. This relationship is consistent with the predictions of the mutation accumulation theory of senescence, but other mechanisms could also play a role. For example, late-life declines in condition, arising through mechanisms other than mutation accumulation might have increased the magnitude of inbreeding depression in late life. Whichever mechanism causes the observed patterns, we have shown that inbreeding can influence age-dependent patterns of disease and, by extension, is likely to affect the magnitude and timing of the late-life declines in components of fitness that characterise senescence. Better understanding of sex-specific links between inbreeding, disease and ageing provides insights into population-level pathogen dynamics and could influence management strategies for wildlife reservoirs of zoonotic disease.
Abstract.
Author URL.
Full text.
Houslay TM, Vierbuchen M, Grimmer AJ, Young AJ, Wilson AJ (2018). Testing the stability of behavioural coping style across stress contexts in the Trinidadian guppy.
Functional Ecology,
32(2), 424-438.
Abstract:
Testing the stability of behavioural coping style across stress contexts in the Trinidadian guppy
Within populations, individuals can vary in stress response, a multivariate phenomenon comprising neuroendocrine, physiological and behavioural traits. Verbal models of individual stress “coping style” have proposed that the behavioural component of this variation can be described as a single axis, with each individual's coping style being consistent across time and stress contexts. Focusing on this behavioural component of stress response and combining repeated measures of multiple traits with a novel multivariate modelling framework, we test for the existence of coping style variation and assess its stability across contexts in the Trinidadian guppy (Poecilia reticulata). Specifically, we test the following hypotheses: (1) there exists repeatable among-individual behavioural (co)variation (“personality”) within a mild stress context consistent with a risk-averse–risk-prone continuum of behavioural coping style, (2) there is population-level plasticity in behaviour as a function of stressor severity, (3) there is among-individual variation in plasticity (i.e. IxE), and (4) the presence of IxE reduces cross-context stability of behavioural coping style. We found significant repeatable among-individual behavioural (co)variation in the mild stress context (open field trial), represented as an I matrix. However, I was not readily described by a simple risk-averse–risk-prone continuum as posited by the original coping style model. We also found strong evidence for population-level changes in mean behaviour with increasing stressor severity (simulated avian and piscine predation risks). Single-trait analyses did show the presence of individual-by-environment interactions (IxE), as among-individual cross-context correlations were significantly less than +1. However, multitrait analysis revealed the consequences of this plasticity variation were minimal. Specifically, we found little evidence for changes in the structure of I between mild and moderate stress contexts overall, and only minor changes between the two moderate contexts (avian vs. piscine predator). We show that a multivariate approach to assessing changes in among-individual (co)variance across contexts can prevent the over-interpretation of statistically significant, but small, individual-by-environment effects. While behavioural flexibility enables populations (and individuals) to respond rapidly to changes in the environment, multivariate personality structure can be conserved strongly across such contexts. A plain language summary is available for this article.
Abstract.
Full text.
Young AJ (2018). The role of telomeres in the mechanisms and evolution of life-history trade-offs and ageing.
Philosophical Transactions B: Biological Sciences Full text.
2017
Thompson FJ, Cant MA, Marshall HH, Vitikainen, Sanderson JL, Nichols HJ, Gilchrist JS, Bell MBV, Hodge SJ, Young AJ, et al (2017). Explaining negative kin discrimination in a cooperative mammal society.
Proceedings of the National Academy of Sciences of the USA Full text.
Thompson FJ, Marshall HH, Vitikainen EIK, Young AJ, Cant MA (2017). Individual and demographic consequences of mass eviction in cooperative banded mongooses.
Animal Behaviour,
134, 103-112.
Abstract:
Individual and demographic consequences of mass eviction in cooperative banded mongooses
In animal societies, conflict within groups can result in eviction, where individuals are often permanently expelled from their group. To understand the evolution of eviction and its role in the resolution of within-group conflict requires information on the demographic consequences of eviction for individuals and groups. However, such information is usually difficult to obtain because of the difficulty in tracking and monitoring individuals after they are evicted from their natal groups. Here we used a 15-year data set on life history and demography to investigate the consequences of eviction in a tractable cooperatively breeding mammal, the banded mongoose, Mungos mungo. In this species, groups of individuals are periodically evicted en masse and eviction is a primary mechanism by which new groups form in the study population. Following eviction, we found sex differences in dispersal distance: some females established new groups on the study peninsula but males always dispersed away from the study peninsula. Evicted females suffered reduced reproductive success in the year after eviction. For the evicting group, eviction was associated with increased per capita reproductive success for females, suggesting that eviction is successful in reducing reproductive competition. However, eviction was also associated with increased intergroup conflict for the evicting group. Our results suggest that within-group conflict resolution strategies affect group productivity, group interactions and the structure of the population, and hence have fitness impacts that reach beyond the individual evictors and evictees involved in eviction.
Abstract.
Full text.
2016
Beirne C, Waring L, Mcdonald RA, Delahay R, Young AJ (2016). Age-related declines in immune response in a wild mammal are unrelated to immune cell telomere length.
Proceedings of the Royal Society of London. Series B Full text.
York JE, Radford AN, de Vries B, Groothuis TG, Young AJ (2016). Dominance-related seasonal song production is unrelated to circulating testosterone in a subtropical songbird.
General and Comparative Endocrinology,
233, 43-52.
Abstract:
Dominance-related seasonal song production is unrelated to circulating testosterone in a subtropical songbird
Circulating testosterone (T) is widely considered to play a key role in the production of sexual displays by male vertebrates. While numerous studies support a role for circulating T in promoting the production of song in male birds, this understanding is based primarily on evidence from seasonally breeding northern temperate species, leaving it unclear whether this mechanism generalizes to other regions of the world. Here we investigate whether variation in circulating levels of T can explain the marked within- and among-individual variation in male song performance observed in a subtropical population of the year-round territorial white-browed sparrow weaver (Plocepasser mahali mahali). Our findings reveal that both circulating T and male song production peaked at a similar time point, halfway through the population-level breeding season. However, while dominant males were more likely to sing and sang for longer than subordinate males, within-group paired comparisons revealed no dominance-related differences in circulating T. Moreover, comparisons both among and within individual dominant males revealed that song duration, syllable rate and proportion of time spent singing were all unrelated to circulating T. Together, our findings suggest that natural variation in male song production, at least in this population of white-browed sparrow weavers, is achieved principally through mechanisms other than variation in circulating T concentration. More widely, our results are in line with the view that male song production is not exclusively regulated by gonadally synthesized steroids.
Abstract.
Full text.
York JE, Radford AN, Groothuis TG, Young AJ (2016). Dominant male song performance reflects current immune state in a cooperatively breeding songbird.
Ecol Evol,
6(4), 1008-1015.
Abstract:
Dominant male song performance reflects current immune state in a cooperatively breeding songbird.
Conspicuous displays are thought to have evolved as signals of individual "quality", though precisely what they encode remains a focus of debate. While high quality signals may be produced by high quality individuals due to "good genes" or favourable early-life conditions, whether current immune state also impacts signalling performance remains poorly understood, particularly in social species. Here, we experimentally demonstrate that male song performance is impaired by immune system activation in the cooperatively breeding white-browed sparrow weaver (Plocepasser mahali). We experimentally activated the immune system of free-living dominant males via subcutaneous injection of phytohemagglutinin (PHA) and contrasted its effects with those of a control (phosphate buffered saline) injection. PHA-challenged males showed significant reductions in both the duration and the rate of their song performance, relative to controls, and this could not be readily attributed to effects of the challenge on body mass, as no such effects were detected. Furthermore, male song performance prior to immune-challenge predicted the scale of the inflammatory response to the challenge. Our findings suggest that song performance characteristics are impacted by current immune state. This link between current state and signal performance might therefore contribute to enforcing the honesty of signal performance characteristics. Impacts of current state on signaling may be of particular importance in social species, where subordinates may benefit from an ability to identify and subsequently challenge same-sex dominants in a weakened state.
Abstract.
Author URL.
Thornton A, McAuliffe K, Dall SRX, Fernandez-Duque E, Garber PA, Young AJ (2016). Fundamental Problems with the Cooperative Breeding Hypothesis. A reply to Burkart & Van Schaik.
Journal of Zoology,
299(2), 84-88.
Full text.
Thompson F, Marshall HH, Sanderson JL, Vitikainen EIK, Nichols HJ, Gilchrist J, Young AJ, Hodge SJ, Cant MA (2016). Reproductive competition triggers mass eviction in cooperative banded mongooses.
Proceedings of the Royal Society of London: Biological Sciences Full text.
Walker L, York JE, Young AJ (2016). Sexually-selected sentinels? Evidence of a role for intra-sexual competition in sentinel behavior. Behavioral Ecology
2015
Sanderson JL, Nichols H, Marshall HH, Vitikainen E, Thompson F, Walker S, Cant MA, Young AJ (2015). Elevated glucocorticoid concentrations during gestation predict reduced reproductive success in subordinate female banded mongooses.
Biology Letters Full text.
Cram DL, Blount JD, York JE, Young AJ (2015). Immune response in a wild bird is predicted by oxidative status but does not cause oxidative stress.
PLoS One Full text.
Cram DL, Blount JD, Young AJ (2015). Oxidative status and social dominance in a wild cooperative breeder.
Functional Ecology,
29(2), 229-238.
Abstract:
Oxidative status and social dominance in a wild cooperative breeder
© 2014 British Ecological Society. Oxidative stress has been proposed as a key mediator of life-history trade-offs, yet the social factors that affect patterns of oxidative status amongst individuals in animal societies remain virtually unexplored. This is important, as rank-related differences in reproductive effort in many social species have the potential to generate, or indeed arise from, differences in oxidative status across dominance classes. Here, we examine rank-related variation in oxidative status before and after a lengthy breeding season in a wild cooperatively breeding bird with high reproductive skew, in the semi-arid zone of Southern Africa; the white-browed sparrow weaver (Plocepasser mahali). Our findings reveal that prior to breeding, neither sex showed rank-related differences in markers of oxidative damage or antioxidant protection, suggesting that dominants' reproductive monopolies do not arise from superior pre-breeding oxidative status. After breeding, however, females (who provision young at higher rates than males) suffered elevated oxidative damage, and dominant females (the only birds to lay and incubate eggs, and the primary nestling provisioners) experienced differential declines in antioxidant protection. While males als o showed reduced antioxidant capacity after breeding, this decline was not dependent on rank and not associated with elevated oxidative damage. Our findings suggest that divisions of labour in animal societies can leave the hardest-working classes differentially exposed to oxidative stress, raising the possibility of hitherto unexplored impacts on health and ageing in social species.
Abstract.
Beirne C, Delahay R, Young AJ (2015). Sex differences in senescence: the role of intra-sexual competition in early adulthood. Proceedings of the Royal Society of London. Series B
Sanderson JL, Stott I, Young AJ, Vitikainen E, Hodge SJ, Cant MA (2015). The origins of consistent individual differences in cooperation in wild banded mongooses. Animal Behaviour
Cram DL, Blount JD, Young AJ (2015). The oxidative costs of reproduction are group-size dependent in a wild cooperative breeder.
Proceedings of the Royal Society of London. Series B Full text.
Young AJ, Jarvis JUM, Barnaville J, Bennett NC (2015). Workforce effects and the evolution of complex sociality in wild Damaraland mole-rat societies. The American Naturalist
2014
Beirne C, Delahay R, Hares M, Young AJ (2014). Age-related declines and disease-associated variation in immune cell telomere length in a wild mammal.
PLoS One Full text.
Sanderson JL, Young AJ, Hodge SJ, Kyabulima S, Walker S, Cant MA (2014). Hormonal mediation of a carry-over effect in a wild cooperative mammal. Functional Ecology
Harrison XA, York JE, Young AJ (2014). Population genetic structure and direct
observations reveal sex-reversed patterns of dispersal in a cooperative bird.
Molecular Ecology Full text.
York JE, Young AJ, Radford AN (2014). Singing in the moonlight: dawn song performance of a diurnal bird varies with lunar phase. Biology Letters
Mares R, Bateman AW, English S, Clutton-Brock TH, Young AJ (2014). Timing of predispersal prospecting is influenced by environmental, social and state-dependent factors in meerkats. Animal Behaviour
2013
Harrison XA, York JE, Cram DL, Hares MC, Young AJ (2013). Complete reproductive skew within white-browed sparrow weaver groups despite outbreeding opportunities for subordinates of both sexes.
Behavioral Ecology and Sociobiology,
67(12), 1915-1929.
Abstract:
Complete reproductive skew within white-browed sparrow weaver groups despite outbreeding opportunities for subordinates of both sexes
The distribution of reproductive success within societies is a key determinant of the outcomes of social evolution. Attempts to explain social diversity, therefore, require that we quantify reproductive skews and identify the mechanisms that generate them. Here, we address this priority using life history and genotypic data from >600 individuals in 40 wild groups of the cooperatively breeding white-browed sparrow weaver, Plocepasser mahali. We show that groups comprise up to six males and seven females, but within-group reproduction is completely monopolised by a single dominant male and female, while extra-group males sire 12-18 % of offspring. Strong within-group kin structure could frequently explain these monopolies, as subordinates had typically delayed dispersal from their natal groups and so frequently (1) lacked within-group outbreeding partners, and/or (2) stood to gain little from contesting dominant reproduction, being almost as related to the dominant's young as they would have been to their own. Kin structure alone cannot account entirely for these monopolies, however, as they remained complete following the immigration of unrelated males and females. That subordinate females remain reproductively quiescent despite also showing comparable body condition to dominants, overlapping them substantially in age, and showing no evidence of elevated stress hormone levels raises the possibility that they exercise reproductive restraint due instead to a threat of action by dominants and/or deficits in offspring fitness that might arise if subordinates bred. Our findings highlight the complexity of the mechanisms that generate reproductive disparities in animal societies and the challenge of identifying them when skews are complete. © 2013 Springer-Verlag Berlin Heidelberg.
Abstract.
Harrison XA, York JE, Cram DL, Young AJ (2013). Extra-group mating increases inbreeding risk in a cooperatively breeding bird.
Molecular Ecology,
22(22), 5700-5715.
Abstract:
Extra-group mating increases inbreeding risk in a cooperatively breeding bird
In many cooperatively breeding species, females mate extra-group, the adaptive value of which remains poorly understood. One hypothesis posits that females employ extra-group mating to access mates whose genotypes are more dissimilar to their own than their social mates, so as to increase offspring heterozygosity. We test this hypothesis using life history and genetic data from 36 cooperatively breeding white-browed sparrow weaver (Plocepasser mahali) groups. Contrary to prediction, a dominant female's relatedness to her social mate did not drive extra-group mating decisions and, moreover, extra-group mating females were significantly more related to their extra-group sires than their social mates. Instead, dominant females were substantially more likely to mate extra-group when paired to a dominant male of low heterozygosity, and their extra-group mates (typically dominants themselves) were significantly more heterozygous than the males they cuckolded. The combined effects of mating with extra-group males of closer relatedness, but higher heterozygosity resulted in extra-group-sired offspring that were no more heterozygous than their within-group-sired half-siblings. Our findings are consistent with a role for male-male competition in driving extra-group mating and suggest that the local kin structure typical of cooperative breeders could counter potential benefits to females of mating extra-group by exposing them to a risk of inbreeding. © 2013 John Wiley & Sons Ltd.
Abstract.
Young AJ, Bennett NC (2013). Intra-sexual selection in cooperative mammals and birds: why aren't females bigger and better armed?. Philosophical Transactions of the Royal Society of London: Biological Sciences
Lutermann H, Young AJ, Bennett NC (2013). Reproductive status and testosterone among females in cooperative mole-rat societies. General and Comparative Endocrinology
Cant MA, Young AJ (2013). Resolving social conflict among females without overt aggression. Philosophical Transactions of the Royal Society of London: Biological Sciences
2012
Mares R, Young AJ, Clutton-Brock TH (2012). Individual contributions to territory defence
in a cooperative breeder: weighing up the benefits and costs. Proceedings of the Royal Society of London: Biological Sciences
2011
Abbot P, Abe J, Alcock J, Alizon S, Alpedrinha JAC, Andersson M, Andre J-B, van Baalen M, Balloux F, Balshine S, et al (2011). Inclusive fitness theory and eusociality.
Nature,
471(7339), E1-E4.
Abstract:
Inclusive fitness theory and eusociality.
Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. We will focus our comments on three general issues.
Abstract.
Author URL.
Mares R, Young AJ, Levesque DL, Harrison N, Clutton-Brock TH (2011). Responses to intruder scents in the cooperatively breeding meerkat: Sex and social status differences and temporal variation.
Behavioral Ecology,
22(3), 594-600.
Abstract:
Responses to intruder scents in the cooperatively breeding meerkat: Sex and social status differences and temporal variation
Although sex-specific responses to intruder scent marks have been described in many mammal species, less is known about variation in responses in cooperatively breeding species where differential access to breeding opportunities exists within groups. When reproductive skew is high, strong responses to extragroup breeding rivals would be expected mainly from dominant individuals, with levels of investment depending on female receptiveness. However, evidence from controlled experiments on cooperative breeders for sex and social status differences in responses to intruder scent marks is limited. Here, we investigated responses to intruder scent marks in cooperatively breeding meerkats (Suricata suricatta), where a single dominant pair largely monopolizes within-group reproduction. A series of experimental presentations using feces were used to test first, whether meerkats discriminate between resident and extragroup male scent marks; second, whether sex and social status affect the response to intruding male scents; and third, whether dominant males increase their level of response when dominant females are most receptive. Our results suggest that meerkats are able to discriminate between resident and intruding male scent marks and show that dominant males have the strongest overall response to intruder scent marks, which does not increase with female receptiveness. We suggest that, although all group members may be affected by the presence of intruders, reproductive conflict may be the main reason for the stronger response of dominant males to extragroup male scent marks in this cooperatively breeding species with high reproductive skew. © the Author 2011.
Abstract.
2010
Clutton-Brock TH, Hodge SJ, Flower TP, Spong G, Young AJ (2010). Adaptive suppression of subordinate reproduction in cooperative mammals. American Naturalist, 176, 664-673.
Young AJ, Bennett NC (2010). Morphological divergence of breeders and helpers in Damaraland mole-rat societies. Evolution, 64, 3190-3197.
Young AJ, Oosthuizen MK, Lutermann H, Bennett NC (2010). Physiological suppression eases in Damaraland mole-rat societies when ecological constraints on dispersal are relaxed.
Horm Behav,
57, 177-183.
Abstract:
Physiological suppression eases in Damaraland mole-rat societies when ecological constraints on dispersal are relaxed
In many vertebrate societies, subordinate females exhibit down-regulated reproductive physiologies relative to those of dominants, a condition commonly termed physiological suppression. Research into the causes of physiological suppression has focused principally on the role of the subordinate’s social environment (typically the presence of the dominant female and/or an absence of unrelated males within the group), while few studies have considered the additional role that the physical environment may play. Here we present new evidence from wild Damaraland mole-rats, Fukomys damarensis, revealing that physiological suppression among subordinate females eases markedly during the annual rains (a time when ecological constraints on dispersal are relaxed), despite the continued presence of the dominant female and in groups that contain no new immigrant males. Subordinate females showed substantially higher pituitary sensitivities to GnRH challenge during the wet period than the dry, a contrast that cannot be attributed to between-female differences (as it holds for paired within-female comparisons), associated changes in body mass (as our analyses control for this), or concomitant reductions in physiological stress (as their urinary cortisol concentrations were actually higher in the wet period). We suggest that our findings reflect selection for the maintenance of reproductive readiness among subordinate females during high rainfall periods, given the increased likelihood of encountering dispersal and/or mating opportunities with extra-group males when ecological constraints on dispersal are relaxed. These findings reveal new complexity in the processes that regulate physiological suppression, suggesting a key role in some species for changes in the physical as well as social environment.
Abstract.
2009
Young AJ, Monfort SL (2009). Stress and the costs of extra-territorial movement in a social carnivore. Biology Letters
Young AJ (2009). The Causes of Physiological Suppression in Vertebrate Societies: a Synthesis. In Hager R, Jones CB (Eds.) Reproductive Skew in Vertebrates, Cambridge University Press, 397-436.
2008
Spong GF, Hodge SJ, Young AJ, Clutton-Brock TH (2008). Factors affecting the reproductive success of dominant male meerkats.
Mol Ecol,
17(9), 2287-2299.
Abstract:
Factors affecting the reproductive success of dominant male meerkats.
Identifying traits that affect the reproductive success of individuals is fundamental for our understanding of evolutionary processes. In cooperative breeders, a dominant male typically restricts mating access to the dominant female for extended periods, resulting in pronounced variation in reproductive success among males. This may result in strong selection for traits that increase the likelihood of dominance acquisition, dominance retention and reproductive rates while dominant. However, despite considerable research on reproductive skew, few studies have explored the factors that influence these three processes among males in cooperative species. Here we use genetic, behavioural and demographic data to investigate the factors affecting reproductive success in dominant male meerkats (Suricata suricatta). Our data show that dominant males sire the majority of all offspring surviving to 1 year. A male's likelihood of becoming dominant is strongly influenced by age, but not by weight. Tenure length and reproductive rate, both important components of dominant male reproductive success, are largely affected by group size and composition, rather than individual traits. Dominant males in large groups have longer tenures, but after this effect is controlled, male tenure length also correlates negatively to the number of adult females in the group. Male reproductive rate also declines as the number of intra- and extra-group competitors increases. As the time spent in the dominant position and reproductive rate while dominant explain > 80% of the total variance in reproductive success, group composition thus has major implications for male reproductive success.
Abstract.
Author URL.
Young AJ, Monfort, S.L. Clutton-Brock, T.H. (2008). The causes of physiological suppression among female meerkats: a role for subordinate restraint due to the threat of infanticide?. Hormones and Behaviour, 53
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
Young AJ, Spong G, Clutton-Brock TH (2007). Subordinate male meerkats prospect for extra-group paternity: alternative reproductive tactics in a cooperative animal. Proceedings of the Royal Society B Biological Sciences, 274(1618), 1603-1609.
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
Young AJ, Clutton-Brock TH (2006). Infanticide by subordinates influences reproductive sharing in cooperatively breeding meerkats. Biology Letters, 2(3), 385-387.
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
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.
Young AJ, Carlson AA, Clutton-Brock TH (2005). Trade-offs between extra-territorial prospecting and helping in a cooperative mammal. Animal Behaviour, 70(4), 829-837.
2004
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.
2003
Carlson AA, Nicol, L. Young, A.J. Parlow, A.F. McNeilly AS (2003). Radioimmunoassay of prolactin for the meerkat (Suricata suricatta), a cooperatively breeding carnivore. General & Comparative Endocrinology, 130
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).
