Publications by category
Journal articles
Yvon-Durocher G, Buckling A, Smirnoff N (In Press). Adaptation of phytoplankton to a decade of experimental warming linked to increased photosynthesis. Nature Ecology and Evolution
Padfield D, Buckling A, Yvon-Durocher G, Lowe C, Warfield R (In Press). Linking phytoplankton community metabolism to the individual size distribution. Ecology Letters
Yvon-Durocher G, Padfield D, Buckling A, Lowe C, Ffrench-Constant R, Schaum E (In Press). Metabolic compensation constrains the temperature dependence of gross primary production. Ecology Letters
Abbes S, Duy SV, Munoz G, Dinh QT, Simon DF, Husk B, Baulch HM, Vinçon-Leite B, Fortin N, Greer CW, et al (2022). Occurrence of BMAA Isomers in Bloom-Impacted Lakes and Reservoirs of Brazil, Canada, France, Mexico, and the United Kingdom.
Toxins,
14(4).
Abstract:
Occurrence of BMAA Isomers in Bloom-Impacted Lakes and Reservoirs of Brazil, Canada, France, Mexico, and the United Kingdom
The neurotoxic alkaloid β-N-methyl-amino-l-alanine (BMAA) and related isomers, including N-(2-aminoethyl glycine) (AEG), β-amino-N-methyl alanine (BAMA), and 2,4-diaminobutyric acid (DAB), have been reported previously in cyanobacterial samples. However, there are conflict-ing reports regarding their occurrence in surface waters. In this study, we evaluated the impact of amending lake water samples with trichloroacetic acid (0.1 M TCA) on the detection of BMAA isomers, compared with pre-existing protocols. A sensitive instrumental method was enlisted for the survey, with limits of detection in the range of 5–10 ng L−1. Higher detection rates and significantly greater levels (paired Wilcoxon’s signed-rank tests, p < 0.001) of BMAA isomers were observed in TCA-amended samples (method B) compared to samples without TCA (method A). The overall range of B/A ratios was 0.67–8.25 for AEG (up to +725%) and 0.69–15.5 for DAB (up to +1450%), with absolute concentration increases in TCA-amended samples of up to +15,000 ng L−1 for AEG and +650 ng L−1 for DAB. We also documented the trends in the occurrence of BMAA isomers for a large breadth of field-collected lakes from Brazil, Canada, France, Mexico, and the United Kingdom. Data gathered during this overarching campaign (overall, n = 390 within 45 lake sampling sites) indicated frequent detections of AEG and DAB isomers, with detection rates of 30% and 43% and maximum levels of 19,000 ng L−1 and 1100 ng L−1, respectively. In contrast, BAMA was found in less than 8% of the water samples, and BMAA was not found in any sample. These results support the analyses of free-living cyanobacteria, wherein BMAA was often reported at concentrations of 2–4 orders of magnitude lower than AEG and DAB. Seasonal measurements conducted at two bloom-impacted lakes indicated limited correlations of BMAA isomers with total microcystins or chlorophyll-a, which deserves further investigation.
Abstract.
Sørensen MES, Wood AJ, Minter EJA, Lowe CD, Cameron DD, Brockhurst MA (2020). Comparison of Independent Evolutionary Origins Reveals Both Convergence and Divergence in the Metabolic Mechanisms of Symbiosis.
Current Biology,
30(2), 328-334.e4.
Abstract:
Comparison of Independent Evolutionary Origins Reveals Both Convergence and Divergence in the Metabolic Mechanisms of Symbiosis
© 2019 Elsevier Ltd Through the merger of previously independent lineages, symbiosis promotes the acquisition of new traits and exploitation of inaccessible ecological niches [1, 2], driving evolutionary innovation and important ecosystem functions [3–6]. The transient nature of establishment makes study of symbiotic origins difficult, but experimental comparison of independent origins could reveal the degree of convergence in the underpinning mechanisms [7, 8]. We compared the metabolic mechanisms of two independent origins of Paramecium bursaria-Chlorella photosymbiosis [9–11] using a reciprocal metabolomic pulse-chase method. This showed convergent patterns of nutrient exchange and utilization for host-derived nitrogen in the Chlorella genotypes [12, 13] and symbiont-derived carbon in the P. bursaria genotypes [14, 15]. Consistent with a convergent primary nutrient exchange, partner-switched host-symbiont pairings were functional. Direct competition of hosts containing native or recombined symbionts against isogenic symbiont-free hosts showed that the fitness benefits of symbiosis for hosts increased with irradiance but varied by genotype. Global metabolism varied more between the Chlorella than the P. bursaria genotypes and suggested divergent mechanisms of light management. Specifically, the algal symbiont genotypes either produced photo-protective carotenoid pigments at high irradiance or more chlorophyll, resulting in corresponding differences in photosynthetic efficiency and non-photochemical quenching among host-symbiont pairings. These data suggest that the multiple origins of P. bursaria-Chlorella symbiosis use a convergent nutrient exchange, whereas other photosynthetic traits linked to functioning of photosymbiosis have diverged. Although convergence enables partner switching among diverse strains, phenotypic mismatches resulting from divergence of secondary symbiotic traits could mediate host-symbiont specificity in nature. Sørensen et al. compare multiple independent evolutionary origins of Paramecium-Chlorella symbiosis to reveal the underpinning metabolic mechanisms. Although the independent origins use a convergent nutrient exchange, they have diverged in traits linked to photosynthesis, which could mediate host-symbiont specificity in nature.
Abstract.
Stilwell P, O'Brien S, Hesse E, Lowe C, Gardner A, Buckling A (2020). Resource heterogeneity and the evolution of public goods cooperation.
EVOLUTION LETTERS,
4(2), 155-163.
Author URL.
Brown A, Lowe C, Shutler J, Tyler C, Lilley M (2019). Assessing risks and mitigating impacts of Harmful Algal Blooms on mariculture and marine fisheries. Reviews in Aquaculture, 1-77.
Sørensen MES, Lowe CD, Minter EJA, Wood AJ, Cameron DD, Brockhurst MA (2019). The role of exploitation in the establishment of mutualistic microbial symbioses.
FEMS Microbiol Lett,
366(12).
Abstract:
The role of exploitation in the establishment of mutualistic microbial symbioses.
Evolutionary theory suggests that the conditions required for the establishment of mutualistic symbioses through mutualism alone are highly restrictive, often requiring the evolution of complex stabilising mechanisms. Exploitation, whereby initially the host benefits at the expense of its symbiotic partner and mutual benefits evolve subsequently through trade-offs, offers an arguably simpler route to the establishment of mutualistic symbiosis. In this review, we discuss the theoretical and experimental evidence supporting a role for host exploitation in the establishment and evolution of mutualistic microbial symbioses, including data from both extant and experimentally evolved symbioses. We conclude that exploitation rather than mutualism may often explain the origin of mutualistic microbial symbioses.
Abstract.
Author URL.
Schaum CE, Student Research Team, Ffrench-Constant R, Lowe C, Ólafsson JS, Padfield D, Yvon-Durocher G (2018). Temperature-driven selection on metabolic traits increases the strength of an algal-grazer interaction in naturally warmed streams.
Glob Chang Biol,
24(4), 1793-1803.
Abstract:
Temperature-driven selection on metabolic traits increases the strength of an algal-grazer interaction in naturally warmed streams.
Trophic interactions are important determinants of the structure and functioning of ecosystems. Because the metabolism and consumption rates of ectotherms increase sharply with temperature, there are major concerns that global warming will increase the strength of trophic interactions, destabilizing food webs, and altering ecosystem structure and function. We used geothermally warmed streams that span an 11°C temperature gradient to investigate the interplay between temperature-driven selection on traits related to metabolism and resource acquisition, and the interaction strength between the keystone gastropod grazer, Radix balthica, and a common algal resource. Populations from a warm stream (~28°C) had higher maximal metabolic rates and optimal temperatures than their counterparts from a cold stream (~17°C). We found that metabolic rates of the population originating from the warmer stream were higher across all measurement temperatures. A reciprocal transplant experiment demonstrated that the interaction strengths between the grazer and its algal resource were highest for both populations when transplanted into the warm stream. In line with the thermal dependence of respiration, interaction strengths involving grazers from the warm stream were always higher than those with grazers from the cold stream. These results imply that increases in metabolism and resource consumption mediated by the direct, thermodynamic effects of higher temperatures on physiological rates are not mitigated by metabolic compensation in the long term, and suggest that warming could increase the strength of algal-grazer interactions with likely knock-on effects for the biodiversity and productivity of aquatic ecosystems.
Abstract.
Author URL.
Stilwell P, Lowe C, Buckling A (2018). The effect of cheats on siderophore diversity in Pseudomonas aeruginosa.
J Evol Biol,
31(9), 1330-1339.
Abstract:
The effect of cheats on siderophore diversity in Pseudomonas aeruginosa.
Cooperation can be maintained if cooperative behaviours are preferentially directed towards other cooperative individuals. Tag-based cooperation (greenbeards) - where cooperation benefits individuals with the same tag as the actor - is one way to achieve this. Tag-based cooperation can be exploited by individuals who maintain the specific tag but do not cooperate, and selection to escape this exploitation can result in the evolution of tag diversity. We tested key predictions crucial for the evolution of cheat-mediated tag diversity using the production of iron-scavenging pyoverdine by the opportunistic pathogen, Pseduomonas aeruginosa as a model system. Using two strains that produce different pyoverdine types and their respective cheats, we show that cheats outcompete their homologous pyoverdine producer, but are outcompeted by the heterologous producer in well-mixed environments. As a consequence, co-inoculating two types of pyoverdine producer and one type of pyoverdine cheat resulted in the pyoverdine type whose cheat was not present having a large fitness advantage. Theory suggests that in such interactions, cheats can maintain tag diversity in spatially structured environments, but that tag-based cooperation will be lost in well-mixed populations, regardless of tag diversity. We saw that when all pyoverdine producers and cheats were co-inoculated in well-mixed environments, both types of pyoverdine producers were outcompeted, whereas spatial structure (agar plates and compost microcosms), rather than maintaining diversity, resulted in the domination of one pyoverdine producer. These results suggest cheats may play a more limited role in the evolution of pyoverdine diversity than predicted.
Abstract.
Author URL.
Minter EJA, Lowe CD, Sørensen MES, Wood AJ, Cameron DD, Brockhurst MA (2018). Variation and asymmetry in host-symbiont dependence in a microbial symbiosis.
BMC Evol Biol,
18(1).
Abstract:
Variation and asymmetry in host-symbiont dependence in a microbial symbiosis.
BACKGROUND: Symbiosis is a major source of evolutionary innovation and, by allowing species to exploit new ecological niches, underpins the functioning of ecosystems. The transition from free-living to obligate symbiosis requires the alignment of the partners' fitness interests and the evolution of mutual dependence. While symbiotic taxa are known to vary widely in the extent of host-symbiont dependence, rather less is known about variation within symbiotic associations. RESULTS: Using experiments with the microbial symbiosis between the protist Paramecium bursaria and the alga Chlorella, we show variation between pairings in host-symbiont dependence, encompassing facultative associations, mutual dependence and host dependence upon the symbiont. Facultative associations, that is where both the host and the symbiont were capable of free-living growth, displayed higher symbiotic growth rates and higher per host symbiont loads than those with greater degrees of dependence. CONCLUSIONS: These data show that the Paramecium-Chlorella interaction exists at the boundary between facultative and obligate symbiosis, and further suggest that the host is more likely to evolve dependence than the algal symbiont.
Abstract.
Author URL.
Lowe CD, Minter EJ, Cameron DD, Brockhurst MA (2016). Shining a Light on Exploitative Host Control in a Photosynthetic Endosymbiosis. Current Biology, 26(2), 207-211.
Minter EJA, Lowe CD, Brockhurst MA, Watts PC (2015). A rapid and cost-effective quantitative microsatellite genotyping protocol to estimate intraspecific competition in protist microcosm experiments.
Methods in Ecology and Evolution,
6(3), 315-323.
Abstract:
A rapid and cost-effective quantitative microsatellite genotyping protocol to estimate intraspecific competition in protist microcosm experiments
High levels of intraspecific variation are commonly observed in natural microbial populations, yet the consequences of this variation for ecological and evolutionary processes remain poorly understood. Protists are excellent experimental models for investigating fundamental and applied questions in ecology and evolution, but studying intraspecific variation remains a challenge due to a lack of molecular resources to aid in quantifying and distinguishing strains during experiments. Here we present a molecular method, quantitative microsatellite genotyping, to accurately quantify strain-specific frequencies from microcosm experiments of the marine flagellate Oxyrrhis marina, both between many pairs of strains and between strains in a multistrain mixture. We find that for pairs of strains, the method is effective for relative frequencies as low as 0·02 and with around 99% accuracy. The method is able to quantify four strains reasonably well, though less accurate than for pairs (range 92-97% accuracy). This makes accessible a cheap and easy-to-implement method for quantifying strain (or allele) frequencies and is suitable for use in a broad range of single-celled eukaryotes (protists) where copy number should correlate well with number of individuals (i.e. cells). This opens up the possibility of examining the role of intraspecific variation using experimental protist microcosms.
Abstract.
Dean A, Minter E, Sorenson M, Lowe C, Cameron D, Brockurst M, Wood AJ (2015). Host control and nutrient trading in a photosynthetic symbiosis.
Abstract:
Host control and nutrient trading in a photosynthetic symbiosis
Photosymbiosis is one of the most important evolutionary trajectories,
resulting in the chloroplast and the subsequent development of all complex
photosynthetic organisms. The ciliate Paramecium bursaria and the alga
Chlorella have a well established and well studied light dependent
endosymbiotic relationship. Despite its prominence there remain many unanswered
questions regarding the exact mechanisms of the photosymbiosis. of particular
interest is how a host maintains and manages its symbiont load in response to
the allocation of nutrients between itself and its symbionts. Here we construct
a detailed mathematical model, parameterised from the literature, that
explicitly incorporates nutrient trading within a deterministic model of both
partners. The model demonstrates how the symbiotic relationship can manifest as
parasitism of the host by the symbionts, mutualism, wherein both partners
benefit, or exploitation of the symbionts by the hosts. We show that the
precise nature of the photosymbiosis is determined by both environmental
conditions (how much light is available for photosynthesis) and the level of
control a host has over its symbiont load. Our model provides a framework
within which it is possible to pose detailed questions regarding the
evolutionary behaviour of this important example of an established light
dependent endosymbiosis; we focus on one question in particular, namely the
evolution of host control, and show using an adaptive dynamics approach that a
moderate level of host control may evolve provided the associated costs are not
prohibitive.
Abstract.
Author URL.
Minter EJA, Watts PC, Lowe CD, Brockhurst MA (2015). Negative frequency-dependent selection is intensified at higher population densities in protist populations.
Biol Lett,
11(6).
Abstract:
Negative frequency-dependent selection is intensified at higher population densities in protist populations.
Natural populations of free-living protists often exhibit high-levels of intraspecific diversity, yet this is puzzling as classic evolutionary theory predicts dominance by genotypes with high fitness, particularly in large populations where selection is efficient. Here, we test whether negative frequency-dependent selection (NFDS) plays a role in the maintenance of diversity in the marine flagellate Oxyrrhis marina using competition experiments between multiple pairs of strains. We observed strain-specific responses to frequency and density, but an overall signature of NFDS that was intensified at higher population densities. Because our strains were not selected a priori on the basis of particular traits expected to exhibit NFDS, these data represent a relatively unbiased estimate of the role for NFDS in maintaining diversity in protist populations. These findings could help to explain how bloom-forming plankton, which periodically achieve exceptionally high population densities, maintain substantial intraspecific diversity.
Abstract.
Author URL.
Lowe CD, Martin LE, Montagnes DJS, Watts PC (2012). A legacy of contrasting spatial genetic structure on either side of the Atlantic – Mediterranean transition zone in a marine protist. Proceedings of the National Academy of Sciences of the United States of America, 1-6.
Yang Z, Lowe CD, Crowther W, Fenton A, Watts PC, Montagnes DJS (2012). Strain-specific functional and numerical responses are required to evaluate impacts on predator–prey dynamics. The ISME Journal, 1-12.
Montagnes D, Roberts E, Lukes J, Lowe CD (2012). The rise of model protozoa.
Trends in microbiology, 1-8.
Abstract:
The rise of model protozoa.
It is timely to evaluate the role of protozoa as model organisms given their diversity, abundance and versatility as well as the economic and ethical pressures placed on animal-based experimentation. We first define the term model organism and then examine through examples why protozoa make good models. Our examples reflect major issues including evolution, ecology, population and community biology, disease, the role of organelles, ageing, space travel, toxicity and teaching. We conclude by recognising that although protozoa may in some cases not completely mimic tissue- or whole-animal-level processes, they are extremely flexible and their use should be embraced. Finally, we offer advice on obtaining emergent model protozoa.
Abstract.
Lowe CD, Montagnes DJS, Watts PC (2011). A TALE OF TWO SEAS: THE ATLANTIC-MEDITERRANEAN TRANSITION IMPOSES a STRONG GENETIC BREAK IN THE PROTIST OXYRRHIS MARINA.
JOURNAL OF PHYCOLOGY,
47, S59-S60.
Author URL.
Thompson DJ, Hassall C, Lowe CD, Watts PC (2011). Field estimates of reproductive success in a model insect: behavioural surrogates are poor predictors of fitness.
Ecology letters, 905-913.
Abstract:
Field estimates of reproductive success in a model insect: behavioural surrogates are poor predictors of fitness.
Ecology Letters (2011) ABSTRACT: Understanding, and therefore measuring, factors that determine fitness is a central problem in evolutionary biology. We studied a natural population of Coenagrion puella (Odonata: Zygoptera) over two entire breeding seasons, with over a thousand individuals uniquely marked and genotyped, and all mating events at the rendezvous site recorded. Using a parentage analysis, fitness of individuals in the first generation was quantified as the numbers of offspring that survived to maturity. Although mating behaviour can be predicted by environmental and demographical variables, the numbers of mature offspring produced (fitness) cannot, and crucially, are poorly correlated with behavioural observations of mating. While fitness of both sexes was positively related to mating behaviour and to female’s ectoparasite burden, these behavioural observations explained little more variance in offspring production than environmental and demographical variables. Thus, we demonstrate that behavioural measures of reproductive success are not necessarily reliable estimates of fitness in natural populations.
Abstract.
Lowe CD, Mello LV, Samatar N, Martin LE, Montagnes DJS, Watts PC (2011). The transcriptome of the novel dinoflagellate Oxyrrhis marina (Alveolata: Dinophyceae): response to salinity examined by 454 sequencing. BMC genomics, 12, 519-519.
Montagnes DJS, Lowe CD, Roberts EC, Breckels MN, Boakes DE, Davidson K, Keeling PJ, Slamovits CH, Steinke M, Yang Z, et al (2010). An introduction to the special issue: Oxyrrhis marina, a model organism?. Journal of Plankton Research, 00, 1-6.
Lowe CD, Martin LE, Roberts EC, Watts PC, Wootton EC, Montagnes DJS (2010). Collection, isolation and culturing strategies for Oxyrrhis marina. Journal of Plankton Research, 00
Sherratt TN, Laird RA, Hassall C, Lowe CD, Harvey IF, Watts PC, Cordero-Rivera A, Thompson DJ (2010). Empirical evidence of senescence in adult damselflies (Odonata: Zygoptera).
The Journal of animal ecology, 1034-1044.
Abstract:
Empirical evidence of senescence in adult damselflies (Odonata: Zygoptera).
Summary 1. Age-dependent increases in mortality have been documented in a variety of species of insect under laboratory conditions. However, while strong statistical evidence has been presented for senescence in vertebrate populations in the wild, we know little about the rate and shape of senescence in wild populations of insects. 2. Odonates (damselflies and dragonflies) provide excellent candidate species for evaluating demographic senescence as they are large enough to be marked individually and they are easily re-sighted without recapture. The prevailing opinion - based entirely on qualitative examination of the declines in log numbers alive with time since marking - is that odonates exhibit age-independent daily survivorship. 3. Here, we examine mark-recapture data on the Azure Damselfly Coenagrion puella over two consecutive seasons. For the first time, we evaluate and compare the fit of quantitative models that not only account for weather-dependent daily variation in daily re-sighting rates, but also age-dependent variation in daily survivorship. 4. Models with age-dependent declines in daily survivorship provide a more parsimonious explanation for the data than similar models without these age-dependent effects. In general, models in which mortality increases in an exponential (Gompertz) fashion explain the mark-recapture sequences more efficiently than a range of alternative models, including those in which mortality increases as a power function (Weibull) or reaches a plateau (logistic). These results are indicative of a general senescent decline in physiological functioning, which is particularly marked after 15 days as a mature adult. 5. Weather (temperature, sun and precipitation) and initial mite load influenced the probability of daily re-sighting. Weather and mite load also influenced daily survivorship, but their effects differed between seasons. 6. Overall, fitting models with age as an explicit covariate demonstrates that odonates do indeed senesce. This contradicts previously held assumptions that Odonata do not exhibit age-dependent survivorship in the wild.
Abstract.
Roberts EC, Wootton EC, Davidson K, Jeong HJ, Lowe CD, Montagnes DJS (2010). Feeding in the dinoflagellate Oxyrrhis marina: linking behaviour with mechanisms. Journal of Plankton Research, 33, 603-614.
Lowe CD, Montagnes DJS, Martin LE, Watts PC (2010). High Genetic Diversity and Fine-Scale Spatial Structure in the Marine Flagellate Oxyrrhis marina (Dinophyceae) Uncovered by Microsatellite Loci. PLoS ONE, 5, e15557-e15557.
Montagnes DJS, Lowe CD, Martin L, Watts PC, Downes-Tettmar N, Yang Z, Roberts EC, Davidson K (2010). Oxyrrhis marina growth, sex and reproduction. Journal of Plankton Research, 00
Lowe CD, Montagnes DJS, Martin LE, Watts PC (2010). Patterns of genetic diversity in the marine heterotrophic flagellate Oxyrrhis marina (Alveolata: Dinophyceae).
Protist,
161, 212-21.
Abstract:
Patterns of genetic diversity in the marine heterotrophic flagellate Oxyrrhis marina (Alveolata: Dinophyceae).
Oxyrrhis marina is an important model in ecological studies of free-living protists. Despite this, O. marina has rarely been studied in the environment and no explicit distributional studies exist. Further, phylogenetic data for a small number of isolates indicate that O. marina constitutes two divergent lineages. Here, we quantify phylogenetic variation between 58 globally distributed O. marina isolates using 5.8S - internal transcribed spacer 1 and 2 rDNA (5.8S ITS) and cytochrome c oxidase I (COI) partial sequences. 5.8S ITS and COI phylogenies both partitioned O. marina into four clades, which formed two lineages; mean sequence identity for 5.8S ITS and COI respectively was approximately 40 and 90% between these two lineages. Sequence identities for 5.8S ITS/ COI between clades within lineages were 66.3/99.4% (lineage 1: clade 1 vs 2) and 42.3/99.1% (lineage 2: clade 3 vs 4). rDNA mutation rates in O. marina appear to be abnormally high and were not interpreted in a species delineation context. Based on variation in COI sequence and comparisons with other protists, we suggest that O. marina lineages may constitute two species. In a geographic context, evidence of spatial restriction but also extensive overlap between O. marina clades occurred. Further, clade abundances varied considerably: clades 1 and 2 (belonging to one lineage) were abundant and widespread; in contrast, clades 3 and 4 (belonging to the second lineage) were rare and spatially restricted (occurring only in the Mediterranean or in culture collection). There is need for further phylogenetic and taxonomic studies to assess species delineation in O. marina, and for the application of high resolution genetic markers to resolve processes driving genetic diversity in this important model organism.
Abstract.
Hassall C, Lowe CD, Harvey IF, Watts PC, Thompson DJ (2010). Phenology determines seasonal variation in ectoparasite loads in a natural insect population. Ecological Entomology, no-no.
Hassall C, Lowe CD, Harvey IF, Watts PC, Thompson DJ (2010). Phenology determines seasonal variation in ectoparasite loads in a natural insect population.
Ecological Entomology,
35(4), 514-522.
Abstract:
Phenology determines seasonal variation in ectoparasite loads in a natural insect population
1. The extent to which individuals are parasitised is a function of exposure to parasites and the immune response, which in ectotherms may be associated with temperature. 2. We test the hypothesis that seasonal variation in ectoparasite burden is driven by temperature using an extensive mark-release-recapture study of adult Coenagrion puella (L.) (Zygoptera) as a model system. Mite counts were taken both at capture and on a subset of subsequent recaptures over two entire, consecutive breeding seasons. 3. Emergence date was the most significant factor in determining individual differences in mite burden, and mean counts for individuals emerging on the same days showed strong unimodal relationships with time of season. Subsequent recounting of mites on a subset of individuals showed that patterns of loss of mites were similar between seasons. 4. While temperature did not significantly affect mite burdens within seasons and ectoparasite prevalence was very similar across the two seasons, intensity of infection and rate of mite gain in unparasitised individuals were significantly higher in the cooler season. 5. We demonstrate that, while temperature may modulate the invertebrate immune response, this modulation does not manifest in variations in mite burdens in natural populations. © 2010 the Authors. Journal compilation © 2010 the Royal Entomological Society.
Abstract.
Watts PC, Martin LE, Kimmance SA, Montagnes DJS, Lowe CD (2010). The distribution of Oxyrrhis marina: a global disperser or poorly characterized endemic?. Journal of Plankton Research, 0
Lowe CD, Keeling PJ, Martin LE, Slamovits CH, Watts PC, Montagnes DJS (2010). Who is Oxyrrhis marina? Morphological and phylogenetic studies on an unusual dinoflagellate. Journal of Plankton Research, 00
Lowe CD, Harvey IF, Watts PC, Thompson DJ (2009). Reproductive timing and patterns of development for the damselfly Coenagrion puella in the field.
Ecology,
90, 2202-12.
Abstract:
Reproductive timing and patterns of development for the damselfly Coenagrion puella in the field.
By a combination of detailed behavioral observations and molecular genetic approaches we have assessed development time, timing of first maturity, and the extent of genetic structure through the flying season in a wild population of the damselfly Coenagrion puella in England. This work provides the first estimate of development time (egg to mature adult) in the field based on individual damselflies. Development time was significantly longer for females than males. In contrast to reported laboratory studies, there was no difference in development times between different female color morphs. Development time ranged between 347 and 396 days and was negatively correlated with egg-laying date. As a result eggs laid early in one season reach adult maturity relatively late in the next; concurrently individuals developing from eggs laid late mature relatively early. We speculate that this pattern of development is a direct physiological response to seasonal environmental variation and results in reproductive synchrony within a population. Size, specifically hind wing length, declined with development time in males, but not in females. In one of the two years of the study there was evidence for weak clustering of related individuals during the reproductive season. This appeared to be the result of developmental synchronization within families: variance in timing of maturation was smaller in full-sib families than in half-sib families or randomly assigned unrelated groups.
Abstract.
Fakhar M, Noyes HA, Lowe CD, Motazedian MH, Daly D, Kemp SJ (2008). An integrated pipeline for the development of novel panels of mapped microsatellite markers for Leishmania donovani complex, Leishmania braziliensis and Leishmania major.
Parasitology,
135, 567-74.
Abstract:
An integrated pipeline for the development of novel panels of mapped microsatellite markers for Leishmania donovani complex, Leishmania braziliensis and Leishmania major.
A panel of microsatellites mapped to the Leishmania genome might make it possible to find associations between specific loci and phenotypic traits. To identify such loci, a Perl programme was written that scans the sequence of a genome and writes all loci containing microsatellites to a MySQL database. The programme was applied to the sequences of the L. braziliensis, L. infantum and L. major genomes. The database is publicly available over the internet: http://www.genomics.liv.ac.uk/tryps/resources.html ’Microsatellite Locus Extractor’, and allows the selection of mapped microsatellites that meet user-defined criteria from a specified region of the selected genome. The website also incorporates a primer design pipeline that will design primers to amplify the selected loci. Using this pipeline 12 out of 17 primer sets designed against the L. infantum genome generated polymorphic PCR products. A tailed primer protocol was used to label all microsatellite primers with a single set of labelled primers. To avoid the culture of parasites prior to genotyping, sets of nested PCR primers were developed to amplify parasite DNA eluted from microscope slides. The limit of detection was approximately 1.6 parasite equivalents. However, only 6/56 DNA from slides stored at ambient temperature for over 6 months gave positive PCR results.
Abstract.
Lowe CD, Harvey IF, Thompson DJ, Watts PC (2008). Strong genetic divergence indicates that congeneric damselflies Coenagrion puella and C. pulchellum (Odonata: Zygoptera: Coenagrionidae) do not hybridise. Hydrobiologia, 605, 55-63.
Watts PC, Lowe CD, Montagnes DJS (2007). An ecological perspective on protistan molecular genetics.
JOURNAL OF EUKARYOTIC MICROBIOLOGY,
54(2), 56S-56S.
Author URL.
Lowe CD, Kemp SJ, Harvey IF, Thompson DJ, Watts PC (2007). Variable microsatellite loci isolated from the azure damselfly, Coenagrion puella (L.) (Zygoptera; Coenagrionidae). Molecular Ecology Notes, 7, 880-882.
Lowe CD, Kemp SJ, Díaz-avalos C, Montagnes DJS (2006). How does salinity tolerance influence the distributions of Brachionus plicatilis sibling species?. Marine Biology, 150, 377-386.
Lowe CD, Kemp S, Montagnes D (2005). An interdisciplinary approach to assess the functional diversity of free-living microscopic eukaryotes. Aquatic Microbial Ecology, 41, 67-77.
Lowe CD, Kemp SJ, Bates AD, Montagnes DJS (2005). Evidence that the rotifer Brachionus plicatilis is not an osmoconformer. Marine Biology, 146, 923-929.
Lowe CD, Day A, Kemp SJ, Montagnes DJS (2005). There are high levels of functional and genetic diversity in Oxyrrhis marina.
The Journal of eukaryotic microbiology,
52, 250-7.
Abstract:
There are high levels of functional and genetic diversity in Oxyrrhis marina.
Oxyrrhis marina, a widely distributed marine protist, is used to model heterotrophic flagellate responses in microbial food webs. Although clonal variability occurs in protists, assessments of intraspecific diversity are rare; such assessments are critical, particularly where species are used as models in ecological studies. To address the extent of intraspecific variation within O. marina, we assessed diversity among 11 strains using 5.8S rDNA and ITS sequences. The 5.8S rDNA and ITS regions revealed high divergence between strains: 63.1% between the most diverse. To compare O. marina diversity relative to other alveolates, 18S rDNA sequences for five strains were analysed with sequences from representatives of the major alveolate groups. 18S rDNA also revealed high divergence in O. marina. Additionally, consistent with phylogenies based on protein coding genes, maximum likelihood analysis indicated that O. marina was monophyletic and ancestral to the dinoflagellates. To assess ecophysiological differences, growth rates of seven O. marina strains were measured at 10 salinities (10-55 per thousand). Two salinity responses occurred: one group achieved highest growth rates at high salinities; the other grew best at low salinities. There was no clear correlation between molecular, ecophysiological, or geographical differences. However, salinity tolerance was associated with habitat type: intertidal strains grew best at high salinities; open-water strains grew best at low salinities. These data indicate the need to examine many strains of a species in both phylogenetic and ecological studies, especially where key-species are used to model ecological processes.
Abstract.
Montagnes D, Wilson D, Brooks S, Lowe CD, Campey M (2002). Cyclical behaviour of the tide-pool ciliate Strombidium oculatum. Aquatic Microbial Ecology, 28, 55-68.
Montagnes DJS, Lowe CD, Poultonb A, Jonsson PR (2002). Redescription of Strombidium oculatum Gruber 1884 (Ciliophora, Oligotrichia).
J Eukaryot Microbiol,
49(4), 329-337.
Abstract:
Redescription of Strombidium oculatum Gruber 1884 (Ciliophora, Oligotrichia).
The marine, tide pool-dwelling ciliate Stombidium oculatum was redescribed using live, stained, SEM, and TEM material prepared from samples collected from pools on the Isle of Man (Irish Sea) and Brittany (France). Also, we reviewed the older German and French works that reported on ciliates collected in the Mediterranean and Brittany, respectively. The Brittany and Isle of Man populations of the ciliate were considered identical. Some morphological and behavioural differences exist between the Brittany-Isle of Man populations and the Mediterranean populations, but they were insufficient to distinguish different taxa. Thus, taxa from all three locations were considered to be conspecific. Key features used to describe the ciliate were: morphology and ultrastructure of the free-swimming ciliate; cyst morphology; presence of mixotrophic-chloroplasts; presence of an eye spot composed of stigma obtained from chlorophyte prey; division, morphogenesis, and nuclear structure; live observations and behaviour, including the encystment-excystment cycle. Based on morphological and behavioural characteristics the taxon was distinguished from other similar species, and a neotype has been designated as no type material exists.
Abstract.
Author URL.
Publications by year
In Press
Yvon-Durocher G, Buckling A, Smirnoff N (In Press). Adaptation of phytoplankton to a decade of experimental warming linked to increased photosynthesis. Nature Ecology and Evolution
Padfield D, Buckling A, Yvon-Durocher G, Lowe C, Warfield R (In Press). Linking phytoplankton community metabolism to the individual size distribution. Ecology Letters
Yvon-Durocher G, Padfield D, Buckling A, Lowe C, Ffrench-Constant R, Schaum E (In Press). Metabolic compensation constrains the temperature dependence of gross primary production. Ecology Letters
2022
Abbes S, Duy SV, Munoz G, Dinh QT, Simon DF, Husk B, Baulch HM, Vinçon-Leite B, Fortin N, Greer CW, et al (2022). Occurrence of BMAA Isomers in Bloom-Impacted Lakes and Reservoirs of Brazil, Canada, France, Mexico, and the United Kingdom.
Toxins,
14(4).
Abstract:
Occurrence of BMAA Isomers in Bloom-Impacted Lakes and Reservoirs of Brazil, Canada, France, Mexico, and the United Kingdom
The neurotoxic alkaloid β-N-methyl-amino-l-alanine (BMAA) and related isomers, including N-(2-aminoethyl glycine) (AEG), β-amino-N-methyl alanine (BAMA), and 2,4-diaminobutyric acid (DAB), have been reported previously in cyanobacterial samples. However, there are conflict-ing reports regarding their occurrence in surface waters. In this study, we evaluated the impact of amending lake water samples with trichloroacetic acid (0.1 M TCA) on the detection of BMAA isomers, compared with pre-existing protocols. A sensitive instrumental method was enlisted for the survey, with limits of detection in the range of 5–10 ng L−1. Higher detection rates and significantly greater levels (paired Wilcoxon’s signed-rank tests, p < 0.001) of BMAA isomers were observed in TCA-amended samples (method B) compared to samples without TCA (method A). The overall range of B/A ratios was 0.67–8.25 for AEG (up to +725%) and 0.69–15.5 for DAB (up to +1450%), with absolute concentration increases in TCA-amended samples of up to +15,000 ng L−1 for AEG and +650 ng L−1 for DAB. We also documented the trends in the occurrence of BMAA isomers for a large breadth of field-collected lakes from Brazil, Canada, France, Mexico, and the United Kingdom. Data gathered during this overarching campaign (overall, n = 390 within 45 lake sampling sites) indicated frequent detections of AEG and DAB isomers, with detection rates of 30% and 43% and maximum levels of 19,000 ng L−1 and 1100 ng L−1, respectively. In contrast, BAMA was found in less than 8% of the water samples, and BMAA was not found in any sample. These results support the analyses of free-living cyanobacteria, wherein BMAA was often reported at concentrations of 2–4 orders of magnitude lower than AEG and DAB. Seasonal measurements conducted at two bloom-impacted lakes indicated limited correlations of BMAA isomers with total microcystins or chlorophyll-a, which deserves further investigation.
Abstract.
2020
Sørensen MES, Wood AJ, Minter EJA, Lowe CD, Cameron DD, Brockhurst MA (2020). Comparison of Independent Evolutionary Origins Reveals Both Convergence and Divergence in the Metabolic Mechanisms of Symbiosis.
Current Biology,
30(2), 328-334.e4.
Abstract:
Comparison of Independent Evolutionary Origins Reveals Both Convergence and Divergence in the Metabolic Mechanisms of Symbiosis
© 2019 Elsevier Ltd Through the merger of previously independent lineages, symbiosis promotes the acquisition of new traits and exploitation of inaccessible ecological niches [1, 2], driving evolutionary innovation and important ecosystem functions [3–6]. The transient nature of establishment makes study of symbiotic origins difficult, but experimental comparison of independent origins could reveal the degree of convergence in the underpinning mechanisms [7, 8]. We compared the metabolic mechanisms of two independent origins of Paramecium bursaria-Chlorella photosymbiosis [9–11] using a reciprocal metabolomic pulse-chase method. This showed convergent patterns of nutrient exchange and utilization for host-derived nitrogen in the Chlorella genotypes [12, 13] and symbiont-derived carbon in the P. bursaria genotypes [14, 15]. Consistent with a convergent primary nutrient exchange, partner-switched host-symbiont pairings were functional. Direct competition of hosts containing native or recombined symbionts against isogenic symbiont-free hosts showed that the fitness benefits of symbiosis for hosts increased with irradiance but varied by genotype. Global metabolism varied more between the Chlorella than the P. bursaria genotypes and suggested divergent mechanisms of light management. Specifically, the algal symbiont genotypes either produced photo-protective carotenoid pigments at high irradiance or more chlorophyll, resulting in corresponding differences in photosynthetic efficiency and non-photochemical quenching among host-symbiont pairings. These data suggest that the multiple origins of P. bursaria-Chlorella symbiosis use a convergent nutrient exchange, whereas other photosynthetic traits linked to functioning of photosymbiosis have diverged. Although convergence enables partner switching among diverse strains, phenotypic mismatches resulting from divergence of secondary symbiotic traits could mediate host-symbiont specificity in nature. Sørensen et al. compare multiple independent evolutionary origins of Paramecium-Chlorella symbiosis to reveal the underpinning metabolic mechanisms. Although the independent origins use a convergent nutrient exchange, they have diverged in traits linked to photosynthesis, which could mediate host-symbiont specificity in nature.
Abstract.
Stilwell P, O'Brien S, Hesse E, Lowe C, Gardner A, Buckling A (2020). Resource heterogeneity and the evolution of public goods cooperation.
EVOLUTION LETTERS,
4(2), 155-163.
Author URL.
2019
Brown A, Lowe C, Shutler J, Tyler C, Lilley M (2019). Assessing risks and mitigating impacts of Harmful Algal Blooms on mariculture and marine fisheries. Reviews in Aquaculture, 1-77.
Hedges S (2019). Genetic diversity and structure in European bumblebee (Bombus spp.) populations.
Abstract:
Genetic diversity and structure in European bumblebee (Bombus spp.) populations.
In recent years there has been a global trend in declines of pollinator species primarily due to anthropogenic stressors, including habitat fragmentation and land-use change resulting from agricultural intensification. The subsequent loss of foraging plants via this process creates habitat ‘islands’, causing genetic isolation similar to that found on geographic islands. Isolated populations are at a much greater risk of inbreeding and reduced genetic diversity, which in turn increases their susceptibility to disease. To reduce the fragmentation of wildlife populations, the EU introduced Agri-environmental schemes (AES) which provide mitigation methods including offers of financial aid to farmers planting wild flower margins. This thesis compared two wild bumblebee species between island and mainland sites in the UK and France to assess the impact of geographic isolation on populations. This thesis also sampled four bumblebee species in sites with different levels of AES in the UK, to assess the efficacy of the schemes in terms of promoting genetic diversity and analyse relationships between heterozygosity and disease.
By using genetic techniques to estimate the diversity, structuring and population size of each species, comparisons between different environment types were made. Molecular analysis found significant structuring in Bombus pascuorum (θ = 0.122) populations across the UK and French populations. Within B. pascuorum populations, there was found to be a higher prevalence of the gut trypanosome Crithidia bombi in populations with reduced heterozygosity. Molecular analysis of the agri-environmental sites found a positive relationship between floral diversity and the heterozygosity of the population, and a large proportion of genetically similar sister pairs were sampled within these sites.
4
The overall conclusions from the research presented in this thesis are that to sustain wild pollinator numbers, further development of agri-environmental schemes is required with a focus on increasing floral diversity. Even with low intensive sampling effort sister pairs are likely, which can impact the results of epidemiological studies of haplodiploid species. Furthermore, the genetic analysis presented here suggests a strong link between population isolation and disease prevalence, thus isolated populations are at greater risk of extinction unless intervention occurs.
Abstract.
Sørensen MES, Lowe CD, Minter EJA, Wood AJ, Cameron DD, Brockhurst MA (2019). The role of exploitation in the establishment of mutualistic microbial symbioses.
FEMS Microbiol Lett,
366(12).
Abstract:
The role of exploitation in the establishment of mutualistic microbial symbioses.
Evolutionary theory suggests that the conditions required for the establishment of mutualistic symbioses through mutualism alone are highly restrictive, often requiring the evolution of complex stabilising mechanisms. Exploitation, whereby initially the host benefits at the expense of its symbiotic partner and mutual benefits evolve subsequently through trade-offs, offers an arguably simpler route to the establishment of mutualistic symbiosis. In this review, we discuss the theoretical and experimental evidence supporting a role for host exploitation in the establishment and evolution of mutualistic microbial symbioses, including data from both extant and experimentally evolved symbioses. We conclude that exploitation rather than mutualism may often explain the origin of mutualistic microbial symbioses.
Abstract.
Author URL.
2018
Schaum CE, Student Research Team, Ffrench-Constant R, Lowe C, Ólafsson JS, Padfield D, Yvon-Durocher G (2018). Temperature-driven selection on metabolic traits increases the strength of an algal-grazer interaction in naturally warmed streams.
Glob Chang Biol,
24(4), 1793-1803.
Abstract:
Temperature-driven selection on metabolic traits increases the strength of an algal-grazer interaction in naturally warmed streams.
Trophic interactions are important determinants of the structure and functioning of ecosystems. Because the metabolism and consumption rates of ectotherms increase sharply with temperature, there are major concerns that global warming will increase the strength of trophic interactions, destabilizing food webs, and altering ecosystem structure and function. We used geothermally warmed streams that span an 11°C temperature gradient to investigate the interplay between temperature-driven selection on traits related to metabolism and resource acquisition, and the interaction strength between the keystone gastropod grazer, Radix balthica, and a common algal resource. Populations from a warm stream (~28°C) had higher maximal metabolic rates and optimal temperatures than their counterparts from a cold stream (~17°C). We found that metabolic rates of the population originating from the warmer stream were higher across all measurement temperatures. A reciprocal transplant experiment demonstrated that the interaction strengths between the grazer and its algal resource were highest for both populations when transplanted into the warm stream. In line with the thermal dependence of respiration, interaction strengths involving grazers from the warm stream were always higher than those with grazers from the cold stream. These results imply that increases in metabolism and resource consumption mediated by the direct, thermodynamic effects of higher temperatures on physiological rates are not mitigated by metabolic compensation in the long term, and suggest that warming could increase the strength of algal-grazer interactions with likely knock-on effects for the biodiversity and productivity of aquatic ecosystems.
Abstract.
Author URL.
Stilwell P, Lowe C, Buckling A (2018). The effect of cheats on siderophore diversity in Pseudomonas aeruginosa.
J Evol Biol,
31(9), 1330-1339.
Abstract:
The effect of cheats on siderophore diversity in Pseudomonas aeruginosa.
Cooperation can be maintained if cooperative behaviours are preferentially directed towards other cooperative individuals. Tag-based cooperation (greenbeards) - where cooperation benefits individuals with the same tag as the actor - is one way to achieve this. Tag-based cooperation can be exploited by individuals who maintain the specific tag but do not cooperate, and selection to escape this exploitation can result in the evolution of tag diversity. We tested key predictions crucial for the evolution of cheat-mediated tag diversity using the production of iron-scavenging pyoverdine by the opportunistic pathogen, Pseduomonas aeruginosa as a model system. Using two strains that produce different pyoverdine types and their respective cheats, we show that cheats outcompete their homologous pyoverdine producer, but are outcompeted by the heterologous producer in well-mixed environments. As a consequence, co-inoculating two types of pyoverdine producer and one type of pyoverdine cheat resulted in the pyoverdine type whose cheat was not present having a large fitness advantage. Theory suggests that in such interactions, cheats can maintain tag diversity in spatially structured environments, but that tag-based cooperation will be lost in well-mixed populations, regardless of tag diversity. We saw that when all pyoverdine producers and cheats were co-inoculated in well-mixed environments, both types of pyoverdine producers were outcompeted, whereas spatial structure (agar plates and compost microcosms), rather than maintaining diversity, resulted in the domination of one pyoverdine producer. These results suggest cheats may play a more limited role in the evolution of pyoverdine diversity than predicted.
Abstract.
Author URL.
Minter EJA, Lowe CD, Sørensen MES, Wood AJ, Cameron DD, Brockhurst MA (2018). Variation and asymmetry in host-symbiont dependence in a microbial symbiosis.
BMC Evol Biol,
18(1).
Abstract:
Variation and asymmetry in host-symbiont dependence in a microbial symbiosis.
BACKGROUND: Symbiosis is a major source of evolutionary innovation and, by allowing species to exploit new ecological niches, underpins the functioning of ecosystems. The transition from free-living to obligate symbiosis requires the alignment of the partners' fitness interests and the evolution of mutual dependence. While symbiotic taxa are known to vary widely in the extent of host-symbiont dependence, rather less is known about variation within symbiotic associations. RESULTS: Using experiments with the microbial symbiosis between the protist Paramecium bursaria and the alga Chlorella, we show variation between pairings in host-symbiont dependence, encompassing facultative associations, mutual dependence and host dependence upon the symbiont. Facultative associations, that is where both the host and the symbiont were capable of free-living growth, displayed higher symbiotic growth rates and higher per host symbiont loads than those with greater degrees of dependence. CONCLUSIONS: These data show that the Paramecium-Chlorella interaction exists at the boundary between facultative and obligate symbiosis, and further suggest that the host is more likely to evolve dependence than the algal symbiont.
Abstract.
Author URL.
2017
Schaum C-E, Students B, ffrench-Constant R, Lowe C, Ólafsson JS, Padfield D, Yvon-Durocher G (2017). Temperature-driven selection on metabolic traits increases the strength of an algal-grazer interaction in naturally warmed streams.
2016
Lowe CD, Minter EJ, Cameron DD, Brockhurst MA (2016). Shining a Light on Exploitative Host Control in a Photosynthetic Endosymbiosis. Current Biology, 26(2), 207-211.
2015
Minter EJA, Lowe CD, Brockhurst MA, Watts PC (2015). A rapid and cost-effective quantitative microsatellite genotyping protocol to estimate intraspecific competition in protist microcosm experiments.
Methods in Ecology and Evolution,
6(3), 315-323.
Abstract:
A rapid and cost-effective quantitative microsatellite genotyping protocol to estimate intraspecific competition in protist microcosm experiments
High levels of intraspecific variation are commonly observed in natural microbial populations, yet the consequences of this variation for ecological and evolutionary processes remain poorly understood. Protists are excellent experimental models for investigating fundamental and applied questions in ecology and evolution, but studying intraspecific variation remains a challenge due to a lack of molecular resources to aid in quantifying and distinguishing strains during experiments. Here we present a molecular method, quantitative microsatellite genotyping, to accurately quantify strain-specific frequencies from microcosm experiments of the marine flagellate Oxyrrhis marina, both between many pairs of strains and between strains in a multistrain mixture. We find that for pairs of strains, the method is effective for relative frequencies as low as 0·02 and with around 99% accuracy. The method is able to quantify four strains reasonably well, though less accurate than for pairs (range 92-97% accuracy). This makes accessible a cheap and easy-to-implement method for quantifying strain (or allele) frequencies and is suitable for use in a broad range of single-celled eukaryotes (protists) where copy number should correlate well with number of individuals (i.e. cells). This opens up the possibility of examining the role of intraspecific variation using experimental protist microcosms.
Abstract.
Dean A, Minter E, Sorenson M, Lowe C, Cameron D, Brockurst M, Wood AJ (2015). Host control and nutrient trading in a photosynthetic symbiosis.
Abstract:
Host control and nutrient trading in a photosynthetic symbiosis
Photosymbiosis is one of the most important evolutionary trajectories,
resulting in the chloroplast and the subsequent development of all complex
photosynthetic organisms. The ciliate Paramecium bursaria and the alga
Chlorella have a well established and well studied light dependent
endosymbiotic relationship. Despite its prominence there remain many unanswered
questions regarding the exact mechanisms of the photosymbiosis. of particular
interest is how a host maintains and manages its symbiont load in response to
the allocation of nutrients between itself and its symbionts. Here we construct
a detailed mathematical model, parameterised from the literature, that
explicitly incorporates nutrient trading within a deterministic model of both
partners. The model demonstrates how the symbiotic relationship can manifest as
parasitism of the host by the symbionts, mutualism, wherein both partners
benefit, or exploitation of the symbionts by the hosts. We show that the
precise nature of the photosymbiosis is determined by both environmental
conditions (how much light is available for photosynthesis) and the level of
control a host has over its symbiont load. Our model provides a framework
within which it is possible to pose detailed questions regarding the
evolutionary behaviour of this important example of an established light
dependent endosymbiosis; we focus on one question in particular, namely the
evolution of host control, and show using an adaptive dynamics approach that a
moderate level of host control may evolve provided the associated costs are not
prohibitive.
Abstract.
Author URL.
Minter EJA, Watts PC, Lowe CD, Brockhurst MA (2015). Negative frequency-dependent selection is intensified at higher population densities in protist populations.
Biol Lett,
11(6).
Abstract:
Negative frequency-dependent selection is intensified at higher population densities in protist populations.
Natural populations of free-living protists often exhibit high-levels of intraspecific diversity, yet this is puzzling as classic evolutionary theory predicts dominance by genotypes with high fitness, particularly in large populations where selection is efficient. Here, we test whether negative frequency-dependent selection (NFDS) plays a role in the maintenance of diversity in the marine flagellate Oxyrrhis marina using competition experiments between multiple pairs of strains. We observed strain-specific responses to frequency and density, but an overall signature of NFDS that was intensified at higher population densities. Because our strains were not selected a priori on the basis of particular traits expected to exhibit NFDS, these data represent a relatively unbiased estimate of the role for NFDS in maintaining diversity in protist populations. These findings could help to explain how bloom-forming plankton, which periodically achieve exceptionally high population densities, maintain substantial intraspecific diversity.
Abstract.
Author URL.
2012
Lowe CD, Martin LE, Montagnes DJS, Watts PC (2012). A legacy of contrasting spatial genetic structure on either side of the Atlantic – Mediterranean transition zone in a marine protist. Proceedings of the National Academy of Sciences of the United States of America, 1-6.
Yang Z, Lowe CD, Crowther W, Fenton A, Watts PC, Montagnes DJS (2012). Strain-specific functional and numerical responses are required to evaluate impacts on predator–prey dynamics. The ISME Journal, 1-12.
Montagnes D, Roberts E, Lukes J, Lowe CD (2012). The rise of model protozoa.
Trends in microbiology, 1-8.
Abstract:
The rise of model protozoa.
It is timely to evaluate the role of protozoa as model organisms given their diversity, abundance and versatility as well as the economic and ethical pressures placed on animal-based experimentation. We first define the term model organism and then examine through examples why protozoa make good models. Our examples reflect major issues including evolution, ecology, population and community biology, disease, the role of organelles, ageing, space travel, toxicity and teaching. We conclude by recognising that although protozoa may in some cases not completely mimic tissue- or whole-animal-level processes, they are extremely flexible and their use should be embraced. Finally, we offer advice on obtaining emergent model protozoa.
Abstract.
2011
Lowe CD, Montagnes DJS, Watts PC (2011). A TALE OF TWO SEAS: THE ATLANTIC-MEDITERRANEAN TRANSITION IMPOSES a STRONG GENETIC BREAK IN THE PROTIST OXYRRHIS MARINA.
JOURNAL OF PHYCOLOGY,
47, S59-S60.
Author URL.
Thompson DJ, Hassall C, Lowe CD, Watts PC (2011). Field estimates of reproductive success in a model insect: behavioural surrogates are poor predictors of fitness.
Ecology letters, 905-913.
Abstract:
Field estimates of reproductive success in a model insect: behavioural surrogates are poor predictors of fitness.
Ecology Letters (2011) ABSTRACT: Understanding, and therefore measuring, factors that determine fitness is a central problem in evolutionary biology. We studied a natural population of Coenagrion puella (Odonata: Zygoptera) over two entire breeding seasons, with over a thousand individuals uniquely marked and genotyped, and all mating events at the rendezvous site recorded. Using a parentage analysis, fitness of individuals in the first generation was quantified as the numbers of offspring that survived to maturity. Although mating behaviour can be predicted by environmental and demographical variables, the numbers of mature offspring produced (fitness) cannot, and crucially, are poorly correlated with behavioural observations of mating. While fitness of both sexes was positively related to mating behaviour and to female’s ectoparasite burden, these behavioural observations explained little more variance in offspring production than environmental and demographical variables. Thus, we demonstrate that behavioural measures of reproductive success are not necessarily reliable estimates of fitness in natural populations.
Abstract.
Lowe CD, Mello LV, Samatar N, Martin LE, Montagnes DJS, Watts PC (2011). The transcriptome of the novel dinoflagellate Oxyrrhis marina (Alveolata: Dinophyceae): response to salinity examined by 454 sequencing. BMC genomics, 12, 519-519.
2010
Montagnes DJS, Lowe CD, Roberts EC, Breckels MN, Boakes DE, Davidson K, Keeling PJ, Slamovits CH, Steinke M, Yang Z, et al (2010). An introduction to the special issue: Oxyrrhis marina, a model organism?. Journal of Plankton Research, 00, 1-6.
Lowe CD, Martin LE, Roberts EC, Watts PC, Wootton EC, Montagnes DJS (2010). Collection, isolation and culturing strategies for Oxyrrhis marina. Journal of Plankton Research, 00
Sherratt TN, Laird RA, Hassall C, Lowe CD, Harvey IF, Watts PC, Cordero-Rivera A, Thompson DJ (2010). Empirical evidence of senescence in adult damselflies (Odonata: Zygoptera).
The Journal of animal ecology, 1034-1044.
Abstract:
Empirical evidence of senescence in adult damselflies (Odonata: Zygoptera).
Summary 1. Age-dependent increases in mortality have been documented in a variety of species of insect under laboratory conditions. However, while strong statistical evidence has been presented for senescence in vertebrate populations in the wild, we know little about the rate and shape of senescence in wild populations of insects. 2. Odonates (damselflies and dragonflies) provide excellent candidate species for evaluating demographic senescence as they are large enough to be marked individually and they are easily re-sighted without recapture. The prevailing opinion - based entirely on qualitative examination of the declines in log numbers alive with time since marking - is that odonates exhibit age-independent daily survivorship. 3. Here, we examine mark-recapture data on the Azure Damselfly Coenagrion puella over two consecutive seasons. For the first time, we evaluate and compare the fit of quantitative models that not only account for weather-dependent daily variation in daily re-sighting rates, but also age-dependent variation in daily survivorship. 4. Models with age-dependent declines in daily survivorship provide a more parsimonious explanation for the data than similar models without these age-dependent effects. In general, models in which mortality increases in an exponential (Gompertz) fashion explain the mark-recapture sequences more efficiently than a range of alternative models, including those in which mortality increases as a power function (Weibull) or reaches a plateau (logistic). These results are indicative of a general senescent decline in physiological functioning, which is particularly marked after 15 days as a mature adult. 5. Weather (temperature, sun and precipitation) and initial mite load influenced the probability of daily re-sighting. Weather and mite load also influenced daily survivorship, but their effects differed between seasons. 6. Overall, fitting models with age as an explicit covariate demonstrates that odonates do indeed senesce. This contradicts previously held assumptions that Odonata do not exhibit age-dependent survivorship in the wild.
Abstract.
Roberts EC, Wootton EC, Davidson K, Jeong HJ, Lowe CD, Montagnes DJS (2010). Feeding in the dinoflagellate Oxyrrhis marina: linking behaviour with mechanisms. Journal of Plankton Research, 33, 603-614.
Lowe CD, Montagnes DJS, Martin LE, Watts PC (2010). High Genetic Diversity and Fine-Scale Spatial Structure in the Marine Flagellate Oxyrrhis marina (Dinophyceae) Uncovered by Microsatellite Loci. PLoS ONE, 5, e15557-e15557.
Montagnes DJS, Lowe CD, Martin L, Watts PC, Downes-Tettmar N, Yang Z, Roberts EC, Davidson K (2010). Oxyrrhis marina growth, sex and reproduction. Journal of Plankton Research, 00
Lowe CD, Montagnes DJS, Martin LE, Watts PC (2010). Patterns of genetic diversity in the marine heterotrophic flagellate Oxyrrhis marina (Alveolata: Dinophyceae).
Protist,
161, 212-21.
Abstract:
Patterns of genetic diversity in the marine heterotrophic flagellate Oxyrrhis marina (Alveolata: Dinophyceae).
Oxyrrhis marina is an important model in ecological studies of free-living protists. Despite this, O. marina has rarely been studied in the environment and no explicit distributional studies exist. Further, phylogenetic data for a small number of isolates indicate that O. marina constitutes two divergent lineages. Here, we quantify phylogenetic variation between 58 globally distributed O. marina isolates using 5.8S - internal transcribed spacer 1 and 2 rDNA (5.8S ITS) and cytochrome c oxidase I (COI) partial sequences. 5.8S ITS and COI phylogenies both partitioned O. marina into four clades, which formed two lineages; mean sequence identity for 5.8S ITS and COI respectively was approximately 40 and 90% between these two lineages. Sequence identities for 5.8S ITS/ COI between clades within lineages were 66.3/99.4% (lineage 1: clade 1 vs 2) and 42.3/99.1% (lineage 2: clade 3 vs 4). rDNA mutation rates in O. marina appear to be abnormally high and were not interpreted in a species delineation context. Based on variation in COI sequence and comparisons with other protists, we suggest that O. marina lineages may constitute two species. In a geographic context, evidence of spatial restriction but also extensive overlap between O. marina clades occurred. Further, clade abundances varied considerably: clades 1 and 2 (belonging to one lineage) were abundant and widespread; in contrast, clades 3 and 4 (belonging to the second lineage) were rare and spatially restricted (occurring only in the Mediterranean or in culture collection). There is need for further phylogenetic and taxonomic studies to assess species delineation in O. marina, and for the application of high resolution genetic markers to resolve processes driving genetic diversity in this important model organism.
Abstract.
Hassall C, Lowe CD, Harvey IF, Watts PC, Thompson DJ (2010). Phenology determines seasonal variation in ectoparasite loads in a natural insect population. Ecological Entomology, no-no.
Hassall C, Lowe CD, Harvey IF, Watts PC, Thompson DJ (2010). Phenology determines seasonal variation in ectoparasite loads in a natural insect population.
Ecological Entomology,
35(4), 514-522.
Abstract:
Phenology determines seasonal variation in ectoparasite loads in a natural insect population
1. The extent to which individuals are parasitised is a function of exposure to parasites and the immune response, which in ectotherms may be associated with temperature. 2. We test the hypothesis that seasonal variation in ectoparasite burden is driven by temperature using an extensive mark-release-recapture study of adult Coenagrion puella (L.) (Zygoptera) as a model system. Mite counts were taken both at capture and on a subset of subsequent recaptures over two entire, consecutive breeding seasons. 3. Emergence date was the most significant factor in determining individual differences in mite burden, and mean counts for individuals emerging on the same days showed strong unimodal relationships with time of season. Subsequent recounting of mites on a subset of individuals showed that patterns of loss of mites were similar between seasons. 4. While temperature did not significantly affect mite burdens within seasons and ectoparasite prevalence was very similar across the two seasons, intensity of infection and rate of mite gain in unparasitised individuals were significantly higher in the cooler season. 5. We demonstrate that, while temperature may modulate the invertebrate immune response, this modulation does not manifest in variations in mite burdens in natural populations. © 2010 the Authors. Journal compilation © 2010 the Royal Entomological Society.
Abstract.
Watts PC, Martin LE, Kimmance SA, Montagnes DJS, Lowe CD (2010). The distribution of Oxyrrhis marina: a global disperser or poorly characterized endemic?. Journal of Plankton Research, 0
Lowe CD, Keeling PJ, Martin LE, Slamovits CH, Watts PC, Montagnes DJS (2010). Who is Oxyrrhis marina? Morphological and phylogenetic studies on an unusual dinoflagellate. Journal of Plankton Research, 00
2009
Lowe CD, Harvey IF, Watts PC, Thompson DJ (2009). Reproductive timing and patterns of development for the damselfly Coenagrion puella in the field.
Ecology,
90, 2202-12.
Abstract:
Reproductive timing and patterns of development for the damselfly Coenagrion puella in the field.
By a combination of detailed behavioral observations and molecular genetic approaches we have assessed development time, timing of first maturity, and the extent of genetic structure through the flying season in a wild population of the damselfly Coenagrion puella in England. This work provides the first estimate of development time (egg to mature adult) in the field based on individual damselflies. Development time was significantly longer for females than males. In contrast to reported laboratory studies, there was no difference in development times between different female color morphs. Development time ranged between 347 and 396 days and was negatively correlated with egg-laying date. As a result eggs laid early in one season reach adult maturity relatively late in the next; concurrently individuals developing from eggs laid late mature relatively early. We speculate that this pattern of development is a direct physiological response to seasonal environmental variation and results in reproductive synchrony within a population. Size, specifically hind wing length, declined with development time in males, but not in females. In one of the two years of the study there was evidence for weak clustering of related individuals during the reproductive season. This appeared to be the result of developmental synchronization within families: variance in timing of maturation was smaller in full-sib families than in half-sib families or randomly assigned unrelated groups.
Abstract.
2008
Fakhar M, Noyes HA, Lowe CD, Motazedian MH, Daly D, Kemp SJ (2008). An integrated pipeline for the development of novel panels of mapped microsatellite markers for Leishmania donovani complex, Leishmania braziliensis and Leishmania major.
Parasitology,
135, 567-74.
Abstract:
An integrated pipeline for the development of novel panels of mapped microsatellite markers for Leishmania donovani complex, Leishmania braziliensis and Leishmania major.
A panel of microsatellites mapped to the Leishmania genome might make it possible to find associations between specific loci and phenotypic traits. To identify such loci, a Perl programme was written that scans the sequence of a genome and writes all loci containing microsatellites to a MySQL database. The programme was applied to the sequences of the L. braziliensis, L. infantum and L. major genomes. The database is publicly available over the internet: http://www.genomics.liv.ac.uk/tryps/resources.html ’Microsatellite Locus Extractor’, and allows the selection of mapped microsatellites that meet user-defined criteria from a specified region of the selected genome. The website also incorporates a primer design pipeline that will design primers to amplify the selected loci. Using this pipeline 12 out of 17 primer sets designed against the L. infantum genome generated polymorphic PCR products. A tailed primer protocol was used to label all microsatellite primers with a single set of labelled primers. To avoid the culture of parasites prior to genotyping, sets of nested PCR primers were developed to amplify parasite DNA eluted from microscope slides. The limit of detection was approximately 1.6 parasite equivalents. However, only 6/56 DNA from slides stored at ambient temperature for over 6 months gave positive PCR results.
Abstract.
Lowe CD, Harvey IF, Thompson DJ, Watts PC (2008). Strong genetic divergence indicates that congeneric damselflies Coenagrion puella and C. pulchellum (Odonata: Zygoptera: Coenagrionidae) do not hybridise. Hydrobiologia, 605, 55-63.
2007
Watts PC, Lowe CD, Montagnes DJS (2007). An ecological perspective on protistan molecular genetics.
JOURNAL OF EUKARYOTIC MICROBIOLOGY,
54(2), 56S-56S.
Author URL.
Lowe CD, Kemp SJ, Harvey IF, Thompson DJ, Watts PC (2007). Variable microsatellite loci isolated from the azure damselfly, Coenagrion puella (L.) (Zygoptera; Coenagrionidae). Molecular Ecology Notes, 7, 880-882.
2006
Lowe CD, Kemp SJ, Díaz-avalos C, Montagnes DJS (2006). How does salinity tolerance influence the distributions of Brachionus plicatilis sibling species?. Marine Biology, 150, 377-386.
2005
Lowe CD, Kemp S, Montagnes D (2005). An interdisciplinary approach to assess the functional diversity of free-living microscopic eukaryotes. Aquatic Microbial Ecology, 41, 67-77.
Lowe CD, Kemp SJ, Bates AD, Montagnes DJS (2005). Evidence that the rotifer Brachionus plicatilis is not an osmoconformer. Marine Biology, 146, 923-929.
Lowe CD, Day A, Kemp SJ, Montagnes DJS (2005). There are high levels of functional and genetic diversity in Oxyrrhis marina.
The Journal of eukaryotic microbiology,
52, 250-7.
Abstract:
There are high levels of functional and genetic diversity in Oxyrrhis marina.
Oxyrrhis marina, a widely distributed marine protist, is used to model heterotrophic flagellate responses in microbial food webs. Although clonal variability occurs in protists, assessments of intraspecific diversity are rare; such assessments are critical, particularly where species are used as models in ecological studies. To address the extent of intraspecific variation within O. marina, we assessed diversity among 11 strains using 5.8S rDNA and ITS sequences. The 5.8S rDNA and ITS regions revealed high divergence between strains: 63.1% between the most diverse. To compare O. marina diversity relative to other alveolates, 18S rDNA sequences for five strains were analysed with sequences from representatives of the major alveolate groups. 18S rDNA also revealed high divergence in O. marina. Additionally, consistent with phylogenies based on protein coding genes, maximum likelihood analysis indicated that O. marina was monophyletic and ancestral to the dinoflagellates. To assess ecophysiological differences, growth rates of seven O. marina strains were measured at 10 salinities (10-55 per thousand). Two salinity responses occurred: one group achieved highest growth rates at high salinities; the other grew best at low salinities. There was no clear correlation between molecular, ecophysiological, or geographical differences. However, salinity tolerance was associated with habitat type: intertidal strains grew best at high salinities; open-water strains grew best at low salinities. These data indicate the need to examine many strains of a species in both phylogenetic and ecological studies, especially where key-species are used to model ecological processes.
Abstract.
2002
Montagnes D, Wilson D, Brooks S, Lowe CD, Campey M (2002). Cyclical behaviour of the tide-pool ciliate Strombidium oculatum. Aquatic Microbial Ecology, 28, 55-68.
Montagnes DJS, Lowe CD, Poultonb A, Jonsson PR (2002). Redescription of Strombidium oculatum Gruber 1884 (Ciliophora, Oligotrichia).
J Eukaryot Microbiol,
49(4), 329-337.
Abstract:
Redescription of Strombidium oculatum Gruber 1884 (Ciliophora, Oligotrichia).
The marine, tide pool-dwelling ciliate Stombidium oculatum was redescribed using live, stained, SEM, and TEM material prepared from samples collected from pools on the Isle of Man (Irish Sea) and Brittany (France). Also, we reviewed the older German and French works that reported on ciliates collected in the Mediterranean and Brittany, respectively. The Brittany and Isle of Man populations of the ciliate were considered identical. Some morphological and behavioural differences exist between the Brittany-Isle of Man populations and the Mediterranean populations, but they were insufficient to distinguish different taxa. Thus, taxa from all three locations were considered to be conspecific. Key features used to describe the ciliate were: morphology and ultrastructure of the free-swimming ciliate; cyst morphology; presence of mixotrophic-chloroplasts; presence of an eye spot composed of stigma obtained from chlorophyte prey; division, morphogenesis, and nuclear structure; live observations and behaviour, including the encystment-excystment cycle. Based on morphological and behavioural characteristics the taxon was distinguished from other similar species, and a neotype has been designated as no type material exists.
Abstract.
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