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Telomeres have been advocated to be important markers of biological age in evolutionary and ecological studies. Telomeres usually shorten with age, and shortening is frequently associated with environmental stressors and increased subsequent mortality. Telomere lengthening – an apparent increase in telomere length between repeated samples from the same individual – also occurs. However, the exact circumstances, and consequences, of telomere lengthening are poorly understood. Using longitudinal data from the Seychelles warbler (Acrocephalus sechellensis), we tested whether telomere lengthening – which occurs in adults of this species – is associated with specific stressors (reproductive effort, food availability, malarial infection and cooperative breeding) and predicts subsequent survival. In females, telomere shortening was observed under greater stress (i.e. low food availability, malaria infection), while telomere lengthening was observed in females experiencing lower stress (i.e. high food availability, assisted by helpers, without malaria). The telomere dynamics of males were not associated with the key stressors tested. These results indicate that, at least for females, telomere lengthening occurs in circumstances more conducive to self-maintenance. Importantly, both females and males with lengthened telomeres had improved subsequent survival relative to individuals that displayed unchanged, or shortened, telomeres – indicating that telomere lengthening is associated with individual fitness. These results demonstrate that telomere dynamics are bidirectionally responsive to the level of stress that an individual faces, but may poorly reflect the accumulation of stress over the lifetime. This study challenges how we think of telomeres as a marker of biological age.

Individual variation in telomere length is predictive of health and mortality risk across a range of species. However, the relative influence of environmental and genetic variation on individual telomere length in wild populations remains poorly understood. Heritability of telomere length has primarily been calculated using parent-offspring regression which can be confounded by shared environments. To control for confounding variables, quantitative genetic "animal models" can be used, but few studies have applied animal models in wild populations. Furthermore, parental age at conception may also influence offspring telomere length, but most studies have been cross-sectional. We investigated within- and between-parental age at conception effects and heritability of telomere length in the Seychelles warbler using measures from birds caught over 20 years and a multigenerational pedigree. We found a weak negative within-paternal age at conception effect (as fathers aged, their offspring had shorter telomeres) and a weak positive between-maternal age at conception effect (females that survived to older ages had offspring with longer telomeres). Animal models provided evidence that heritability and evolvability of telomere length were low in this population, and that variation in telomere length was not driven by early-life effects of hatch period or parental identities. Quantitative polymerase chain reaction plate had a large influence on telomere length variation and not accounting for it in the models would have underestimated heritability. Our study illustrates the need to include and account for technical variation in order to accurately estimate heritability, as well as other environmental effects, on telomere length in natural populations.

COG-UK is supported by funding from the MRC part of UK Research & Innovation, the National Institute of Health Research (Grant code MC_PC_19027), and Genome Research Limited, operating as the Welcome Sanger Institute. Background The first epidemic wave of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) in Scotland resulted in high case numbers and mortality in care homes. In Lothian, over one-third of care homes reported an outbreak, while there was limited testing of hospital patients discharged to care homes. Aim To investigate patients discharged from hospitals as a source of SARS-CoV-2 introduction into care homes during the first epidemic wave. Methods A clinical review was performed for all patients discharges from hospitals to care homes from 1st March 2020 to 31st May 2020. Episodes were ruled out based on coronavirus disease 2019 (COVID-19) test history, clinical assessment at discharge, whole-genome sequencing (WGS) data and an infectious period of 14 days. Clinical samples were processed for WGS, and consensus genomes generated were used for analysis using Cluster Investigation and Virus Epidemiological Tool software. Patient timelines were obtained using electronic hospital records. Findings In total, 787 patients discharged from hospitals to care homes were identified. Of these, 776 (99%) were ruled out for subsequent introduction of SARS-CoV-2 into care homes. However, for 10 episodes, the results were inconclusive as there was low genomic diversity in consensus genomes or no sequencing data were available. Only one discharge episode had a genomic, time and location link to positive cases during hospital admission, leading to 10 positive cases in their care home. Conclusion The majority of patients discharged from hospitals were ruled out for introduction of SARS-CoV-2 into care homes, highlighting the importance of screening all new admissions when faced with a novel emerging virus and no available vaccine. Publisher PDF

Genomes retain evidence of the demographic history and evolutionary forces that have shaped populations and drive speciation. Across island systems, contemporary patterns of genetic diversity reflect population demography, including colonization events, bottlenecks, gene flow and genetic drift. Here, we investigate genome-wide diversity and the distribution of runs of homozygosity (ROH) using whole-genome resequencing of individuals (>22x coverage) from six populations across three archipelagos of Berthelot's pipit (Anthus berthelotii)-a passerine that has recently undergone island speciation. We show the most dramatic reduction in diversity occurs between the mainland sister species (the tawny pipit) and Berthelot's pipit and is lowest in the populations that have experienced sequential bottlenecks (i.e., the Madeiran and Selvagens populations). Pairwise sequential Markovian coalescent (PSMC) analyses estimated that Berthelot's pipit diverged from its sister species similar to 2 million years ago, with the Madeiran archipelago founded 50,000 years ago, and the Selvagens colonized 8000 years ago. We identify many long ROH (>1 Mb) in these most recently colonized populations. Population expansion within the last 100 years may have eroded long ROH in the Madeiran archipelago, resulting in a prevalence of short ROH (250 kb. These findings highlight the importance of demographic history, as well as selection and genetic drift, in shaping contemporary patterns of genomic diversity across diverging populations.

Flour beetles of the genus Tribolium have been utilised as informative study systems for over a century and contributed to major advances across many fields. This review serves to highlight the significant historical contribution that Tribolium study systems have made to the fields of ecology and evolution, and to promote their use as contemporary research models. We review the broad range of studies employing Tribolium to make significant advances in ecology and evolution. We show that research using Tribolium beetles has contributed a substantial amount to evolutionary and ecological understanding, especially in the fields of population dynamics, reproduction and sexual selection, population and quantitative genetics, and behaviour, physiology and life history. We propose a number of future research opportunities using Tribolium, with particular focus on how their amenability to forward and reverse genetic manipulation may provide a valuable complement to other insect models.

Understanding the mechanisms and genes that enable animal populations to adapt to pathogens is important from an evolutionary, health and conservation perspective. Berthelot's pipit (Anthus berthelotii) experiences extensive and consistent spatial heterogeneity in avian pox infection pressure across its range of island populations, thus providing an excellent system with which to examine how pathogen-mediated selection drives spatial variation in immunogenetic diversity. Here, we test for evidence of genetic variation associated with avian pox at both an individual and population-level. At the individual level, we find no evidence that variation in MHC class I and TLR4 (both known to be important in recognising viral infection) was associated with pox infection within two separate populations. However, using genotype-environment association (Bayenv) in conjunction with genome-wide (ddRAD-seq) data, we detected strong associations between population-level avian pox prevalence and allele frequencies of single nucleotide polymorphisms (SNPs) at a number of sites across the genome. These sites were located within genes involved in cellular stress signalling and immune responses, many of which have previously been associated with responses to viral infection in humans and other animals. Consequently, our analyses indicate that pathogen-mediated selection may play a role in shaping genomic variation among relatively recently colonised island bird populations and highlight the utility of genotype-environment associations for identifying candidate genes potentially involved in host-pathogen interactions., We are grateful to the Regional Governments of the Canary Islands (Ref.: 2019/5555), the Cabildo of Lanzarote (Ref.: 101/2019), the Cabildo of Tenerife (Ref.: 2019-01740), and the National Parks of El Teide (Ref.: MDV/amp) and Madeira (Ref.: 06/IFCN/2020) for their permission to sample and ring Berthelot’s pipits for this research, the Regional Governments of the Canary Islands and Madeira for providing accommodation, and the Portuguese Navy for transport to Selvagem Grande and Deserta Grande. The Bayenv analysis and associated bioinformatics performed in this study were carried out on the High Performance Computing Cluster supported by the Research and Specialist Computing Support service at the University of East Anglia. This work was supported by Natural Environment Research Council (NERC) studentships awarded to ECS through the ARIES DTP (NE/S007334/1), and to CAM and CA through the EnvEAST DTP (NE/L002582/1), a PhD grant awarded to CG-Q from COLCIENCIAS (Departamento Administrativo de Ciencia, Tecnología e Innovación, Colombia), and a Heredity Fieldwork Grant from the Genetics Society awarded to CAM.

Oceanic island archipelagos provide excellent models to understand evolutionary processes. Colonization events and gene flow can interact with selection to shape genetic variation at different spatial scales. Landscape-scale variation in biotic and abiotic factors may drive fine-scale selection within islands, while long-term evolutionary processes may drive divergence between distantly related populations. Here, we examine patterns of population history and selection between recently diverged populations of the Berthelot's pipit (Anthus berthelotii), a passerine endemic to three North Atlantic archipelagos. First, we use demographic trees and f3 statistics to show that genome-wide divergence across the species range is largely shaped by colonization and bottlenecks, with evidence of very weak gene flow between populations. Then, using a genome scan approach, we identify signatures of divergent selection within archipelagos at single nucleotide polymorphisms (SNPs) in genes potentially associated with craniofacial development and DNA repair. We did not detect within-archipelago selection at the same SNPs as were detected previously at broader spatial scales between archipelagos, but did identify signatures of selection at loci associated with similar biological functions. These findings suggest that similar ecological factors may repeatedly drive selection between recently separated populations, as well as at broad spatial scales across varied landscapes., This work was supported by Natural Environment Research Council (NERC) studentships to C.A.M. and C.A. (NE/L002582/1), a Norwich Research Park Science Links grant to D.S.R., M.C. and L.G.S., and a BBSRC fellowship (BB/N011759/1) and British Ecological Society Large Research Grant to L.G.S.We thank two anonymous reviewers whose insight and helpful suggestions have improved this manuscript. We thank Matthew Clark and Lawrence Percival-Alwyn for assistance generating the Berthelot's pipit genome, and Helen Hipperson, Clemens Küpper and Terry Burke (NERC Biomolecular Analysis Facility—Sheffield) for assistance with RAD sequencing. We also thank the Spanish Environment Ministry, the Canary government and the Natural Park of Madeira who gave permission for us to perform the sampling work, local governments in the Canary Islands and Madeira who provided accommodation, and the Portuguese Navy who provided transport. The research presented in this paper was carried out on the High Performance Computing Cluster supported by the Research and Specialist Computing Support service at the University of East Anglia.

Genetic pest management (GPM) methods involve releasing modified versions of a pest species to mate with wild pests in the target area. Proposed for a wide range of applications in public health, agriculture and conservation, most progress has been made with pest insects. Offspring of the released modified insects and wild pests carry the modification—which might be transgenes, artificially introduced Wolbachia or genetic damage from radiation, for example—but they also carry a complete haploid genome from their laboratory-reared parent, as well as one from their wild parent. Unless these F 1 hybrids are completely unable to reproduce, further mating will lead to introgression of DNA sequences from the release strain into the wild population. We discuss issues around strain selection and the potential consequences of such introgression. We conclude that such introgression is probably harmless in almost all circumstances, and could, in theory, provide specific additional benefits to the release programme. We outline population monitoring approaches that could be used, going forward, to determine how background genetics may affect GPM. This article is part of the theme issue ‘Novel control strategies for mosquito-borne diseases’.

Polyandry, when females mate with more than one male, is theorised to play an important role in successful colonisation of new habitats. In addition to possible benefits from sexual selection, even mild polyandry could facilitate colonisation by protecting against inbreeding and reducing the costs of mating with incompatible or infertile males. Here, we measure the importance of mild polyandry for population viability and reproductive fitness following experimental founder events into a higher‐temperature regime. Using colonisation experiments with the model beetle Tribolium castaneum, in which females can produce offspring for up to 140 days following a single mating, we founded more than 100 replicate populations using single females that had been given the opportunity to mate with either one or two males and then tracked their subsequent population dynamics. Following population viability and fitness across 10 generations, we found that extinction rates were significantly lower in populations founded by females given polyandrous opportunities to mate with two males (9%) compared to populations founded by monogamous females (34%). In addition, populations founded by females that had been provided with opportunities to store sperm from two different males showed double the median productivity following colonisation compared to monogamous‐founded populations. Notably, we identified short‐term and longer‐term benefits to post‐colonisation populations from double‐mating, with results suggesting that polyandry acts to both protect against mating with incompatible males through the founder event, and reduce inbreeding depression as the colonisation proceeds for 10 generations. Our results therefore show that even mild polyandry provides both reproductive and genetic benefits for colonising populations., We performed an evolution experiment to test the hypothesis that polyandry can enable populations to successfully colonise new environments. We found that populations founded by polyandrous females were less likely to go extinct and grew larger in size than those founded by monogamous females.

Methylated amines are ubiquitous in the environment and play a role in regulating the earth’s climate via a set of complex biological and chemical reactions. Microbial degradation of these compounds is a major sink. Recently we isolated a facultative methylotroph, Gemmobacter sp. LW-1, an isolate from the unique environment Movile Cave, Romania, which is capable of methylated amine utilisation as a carbon source. Here, using a comparative genomics approach, we investigate how widespread methylated amine utilisation trait is within the members of the bacterial genus Gemmobacter. Five genomes of different Gemmobacter species isolated from diverse environments, such as activated sludge, fresh water, sulphuric cave waters (Movile Cave) and the marine environment were available from public repositories and used for the analysis. Our results indicate that some members of the genus Gemmobacter, namely G. aquatilis, G. caeni and G. sp. LW-1 have the genetic potential of methylated amine utilisation while others (G. megaterium and G. nectariphilus) have not. Ancestral state reconstruction analysis also suggested that methylated amine utilisation trait might not be ancestral to members of the genus Gemmobacter and has been gained. Based on our analysis, we suggest that the trait of methylated amine utilisation within the members of the genus Gemmobacter might be independent of their habitat and more randomly distributed.

Case isolation and contact tracing can contribute to the control of COVID-19 outbreaks1,2. However, it remains unclear how real-world networks could influence the effectiveness and efficiency of such approaches. To address this issue, we simulated control strategies for SARS-CoV-2 in a real-world social network generated from high resolution GPS data3,4. We found that tracing contacts-of-contacts reduced the size of simulated outbreaks more than tracing of only contacts, but resulted in almost half of the local population being quarantined at a single point in time. Testing and releasing non-infectious individuals led to increases in outbreak size, suggesting that contact tracing and quarantine may be most effective when it acts as a ‘local lockdown’ when contact rates are high. Finally, we estimated that combining physical distancing with contact tracing could enable epidemic control while reducing the number of quarantined individuals. Our approach highlights the importance of network structure and social dynamics in evaluating the potential impact of SARS-CoV-2 control.

In the version of this Letter originally published, the Methods incorrectly stated that all phytoplankton cultures were sampled in mid-exponential phase. The low-nitrogen cultures were sampled in early stationary phase and at the point at which Fv/Fm values decreased, to indicate that cultures were experiencing low-nitrogen conditions. All other phytoplankton cultures were sampled in exponential phase. Growth and Fv/Fm data are provided here on high- and low-nitrogen cultures (Figs 1, 2 and 3) to clarify and support this correction. The Methods also stated that cell counting was done using a Beckman Multisizer 3 Coulter Counter, but a CASY Model TT Cell Counter was used.

Lay Summary Offspring raised with siblings often have to compete for access to limited parental resources; but in adulthood, this prior exposure to competition may be beneficial rather than costly. In Seychelles warblers, nestlings raised with competitors suffered more than those raised alone; but during adulthood, those raised with competition appeared to outperform those raised singly. These results suggest a more multifaceted link between early-life competition and lifetime performance than is currently assumed., Many studies have assessed the costs of sibling rivalry in systems where offspring always have competitors, but conclusions about sibling rivalry in these species are restricted to interpreting the cost of changes in the relative level of competition and are often complicated by the expression of potentially costly rivalry related traits. Additionally, the majority of studies focus on early-life sibling rivalry, but the costs of competition can also affect later-life performance. We test a suite of hypothesized immediate (early-life body mass, telomere length, and survival) and delayed (adult reproductive potential and lifespan) costs of sibling rivalry for offspring of differing competitive ability in Seychelles warblers, where most offspring are raised singly and hence competitor success can be compared to a competition-free scenario. Compared to those raised alone, all competing nestlings had lower body mass and weaker competitors experienced reduced survival. However, the stronger competitors appeared to have longer adult breeding tenures and lifespan than those raised alone. We propose that comparisons with competition-free groups, as well as detailed fitness measures across entire lifetimes, are needed to understand the evolution of sibling rivalry and thus individual reproductive strategy in wild systems.

Recent work indicates that social structure has extensive implications for patterns of sexual selection and sexual conflict. However, little is known about the individual variation in social behaviours linking social structure to sexual interactions. Here, we use network analysis of replicate polygynandrous groups of red junglefowl ( Gallus gallus ) to show that the association between social structure and sexual interactions is underpinned by differential female sociality. Sexual dynamics are largely explained by a core group of highly social, younger females, which are more fecund and more polyandrous, and thus associated with more intense postcopulatory competition for males. By contrast, less fecund females from older cohorts, which tend to be socially dominant, avoid male sexual attention by clustering together and perching on branches, and preferentially reproduce with dominant males by more exclusively associating and mating with them. Collectively, these results indicate that individual females occupy subtly different social niches and demonstrate that female sociality can be an important factor underpinning the landscape of intrasexual competition and the emergent structure of animal societies.

Endangered species face a huge array of challenges, including the negative consequences of individuals having to breed with close genetic relatives. But just how costly is inbreeding in small populations? New research from an endangered bird species suggests that considering inbreeding could be crucial for conservation programmes.

Environmental conditions play a major role in shaping the spatial distributions of pathogens, which in turn can drive local adaptation and divergence in host genetic diversity. Haemosporidians, such as Plasmodium (malaria), are a strong selective force, impacting survival and fitness of hosts, with geographic distributions largely determined by habitat suitability for their insect vectors. Here, we have tested whether patterns of fine‐scale local adaptation to malaria are replicated across discrete, ecologically differing island populations of Berthelot's pipits Anthus berthelotii. We sequenced TLR4, an innate immunity gene that is potentially under positive selection in Berthelot's pipits, and two SNPs previously identified as being associated with malaria infection in a genome‐wide association study (GWAS) in Berthelot's pipits in the Canary Islands. We determined the environmental predictors of malaria infection, using these to estimate variation in malaria risk on Porto Santo, and found some congruence with previously identified environmental risk factors on Tenerife. We also found a negative association between malaria infection and a TLR4 variant in Tenerife. In contrast, one of the GWAS SNPs showed an association with malaria risk in Porto Santo, but in the opposite direction to that found in the Canary Islands GWAS. Together, these findings suggest that disease‐driven local adaptation may be an important factor in shaping variation among island populations., We have investigated patterns of fine‐scale local adaptation to malaria between two ecologically divergent populations of an island bird. Our results found contrasting associations with malaria infection at candidate immune loci between the islands, suggesting that disease‐driven local adaptation may be an important factor in shaping variation among island populations.

A major aim of evolutionary biology is to understand why patterns of genomic variation vary among populations and species. Large-scale genomic studies of widespread species are useful for studying how the environment and demographic history shape patterns of genomic divergence, and with the continually decreasing cost of sequencing, such studies are now becoming feasible. Here, we carry out one of the most comprehensive surveys of genomic variation in a wild vertebrate to date; the great tit ( Parus major ) HapMap project. We screened ca 500,000 SNP markers across 647 individuals from 29 populations, spanning almost the entire geographic range of the European great tit subspecies. We found that genome-wide variation was consistent with a recent colonisation across Europe from a single refugium in the Balkans and/or Turkey, with bottlenecks and reduced genetic diversity in island populations. Differentiation across the genome was highly heterogeneous, with clear “islands of differentiation” even among populations which are ostensibly panmictic. These islands of differentiation were consistently found in regions of low recombination, suggesting that background selection can rapidly promote population differentiation among even the most recently colonised populations. We also detected genomic outlier regions that were unique to peripheral great tit populations, most likely as a result of recent directional selection at the range edges of this species. These “unique” outlier regions contained candidate genes for morphology, thermal adaptation and colouration, supporting previous research in this species, and providing avenues for future investigation. Our study suggests that comprehensive screens of genomic variation in wild organisms can provide unique insights into evolution. Author summary Studying patterns of genetic variation is a useful way of determining why populations and species differ in nature. Genetic variation is shaped by natural selection, but also by the present and past size of populations, the amount of migration, and by features of the genome, such as variation in recombination rate, of the organism being studied. Teasing apart the effects of these different processes on genomic diversity is difficult, but one way that this can be achieved is by studying genomic variation across the entire range of a species. We performed a continental-scale analysis of genetic variation in the great tit - a widespread songbird that has been the focus of extensive ecological research. We first used genomic data to reconstruct the historical colonisation of great tits across Europe, and showed that during the last ice age, this species was likely restricted to a single region in Eastern Europe, from which they spread across the continent. We then studied how patterns of variation differ along the genome, and show that recombination rate is a key driver of variation among all populations. Importantly, by comparing many populations we were able to identify genes that have been subject to natural selection in specific geographical regions. We found that natural selection appeared to be strongest in populations on the edges of the great tit’s range acting on traits such as morphology, stress response and colouration. Large-scale genetic analyses such as ours are therefore useful approaches for understanding how evolution operates in the wild.

Dimethylsulfoniopropionate (DMSP) and its catabolite dimethyl sulfide (DMS) are key marine nutrients1,2 that have roles in global sulfur cycling2, atmospheric chemistry3, signalling4,5 and, potentially, climate regulation6,7. The production of DMSP was previously thought to be an oxic and photic process that is mainly confined to the surface oceans. However, here we show that DMSP concentrations and/or rates of DMSP and DMS synthesis are higher in surface sediment from, for example, saltmarsh ponds, estuaries and the deep ocean than in the overlying seawater. A quarter of bacterial strains isolated from saltmarsh sediment produced DMSP (up to 73 mM), and we identified several previously unknown producers of DMSP. Most DMSP-producing isolates contained dsyB8, but some alphaproteobacteria, gammaproteobacteria and actinobacteria used a methionine methylation pathway independent of DsyB that was previously only associated with higher plants. These bacteria contained a methionine methyltransferase gene (mmtN)—a marker for bacterial synthesis of DMSP through this pathway. DMSP-producing bacteria and their dsyB and/or mmtN transcripts were present in all of the tested seawater samples and Tara Oceans bacterioplankton datasets, but were much more abundant in marine surface sediment. Approximately 1 × 108 bacteria g−1 of surface marine sediment are predicted to produce DMSP, and their contribution to this process should be included in future models of global DMSP production. We propose that coastal and marine sediments, which cover a large part of the Earth’s surface, are environments with high levels of DMSP and DMS productivity, and that bacteria are important producers of DMSP and DMS within these environments. Bacterial dimethylsulfoniopropionate (DMSP) production was recently demonstrated in surface oceans. Here the authors show that bacterial production is higher in sediment from coastal areas and the deep ocean, and identify an alternative pathway for its synthesis, indicating that coastal and marine sediments are important sources of this climate-relevant metabolite.

Chromosome inversions have clear effects on genome evolution and have been associated with speciation, adaptation, and the evolution of the sex chromosomes. In birds, these inversions may play an important role in hybridization of species and disassortative mating. We identified a large (≈64 Mb) inversion polymorphism in the great tit (Parus major) that encompasses almost 1,000 genes and more than 90% of Chromosome 1A. The inversion occurs at a low frequency in a set of over 2,300 genotyped great tits in the Netherlands with only 5% of the birds being heterozygous for the inversion. In an additional analysis of 29 resequenced birds from across Europe, we found two heterozygotes. The likely inversion breakpoints show considerable genomic complexity, including multiple copy number variable segments. We identified different haplotypes for the inversion, which differ in the degree of recombination in the center of the chromosome. Overall, this remarkable genetic variant is widespread among distinct great tit populations and future studies of the inversion haplotype, including how it affects the fitness of carriers, may help to understand the mechanisms that maintain it.

Inferring adaptation and evolutionary change by combining data from field studies and genomics is an exciting new area in evolutionary biology but also presents challenges. These challenges are particularly acute when the focal trait has a polygenic architecture, because many long‐term field studies are sample‐size‐limited compared to studies of humans and model organisms, making the detection of loci that contribute to trait variation difficult. In a recent comment, Perrier and Charmantier (2018); hereafter P&C, highlight these issues and draw attention to several analyses described in our recent publication (Bosse et al. 2017) on the evolution of longer bill length in UK populations of the great tit (Parus major). While we support the overall message of P&C – that caution should be exercised when making inferences about long‐term evolutionary trends from shorter ecological time series – we also address some of the specific criticisms that P&C raised about the analyses described in Bosse et al. (2017). P&C's comments can broadly be split into two sets of queries. The first considers how phenotypic variation is distributed in space and time. The second explores how signatures of selective sweeps can be sensitive to local (in the genomic sense) variation in recombination rate.

Understanding the spatial scale at which selection acts upon adaptive genetic variation in natural populations is fundamental to our understanding of evolutionary ecology, and has important ramifications for conservation. The environmental factors to which individuals of a population are exposed can vary at fine spatial scales, potentially generating localized patterns of adaptation. Here, we compared patterns of neutral and major histocompatibility complex (MHC) variation within an island population of Berthelot's pipit (Anthus berthelotii) to assess whether landscape-level differences in pathogen-mediated selection generate fine-scale spatial structuring in these immune genes. Specifically, we tested for spatial associations between the distribution of avian malaria, and the factors previously shown to influence that distribution, and MHC variation within resident individuals. Although we found no overall genetic structure across the population for either neutral or MHC loci, we did find localized associations between environmental factors and MHC variation. One MHC class I allele (ANBE48) was directly associated with malaria infection risk, while the presence of the ANBE48 and ANBE38 alleles within individuals correlated (positively and negatively, respectively) with distance to the nearest poultry farm, an anthropogenic factor previously shown to be an important determinant of disease distribution in the study population. Our findings highlight the importance of considering small spatial scales when studying the patterns and processes involved in evolution at adaptive loci.

Studies of birds have made a fundamental contribution to elucidating sperm competition processes, experimentally demonstrating the role of individual mechanisms in competitive fertilization. However, the relative importance of these mechanisms and the way in which they interact under natural conditions remain largely unexplored. Here, we conduct a detailed behavioural study of freely mating replicate groups of red junglefowl, Gallus gallus , to predict the probability that competing males fertilize individual eggs over the course of 10-day trials. Remating frequently with a female and mating last increased a male's probability of fertilization, but only for eggs ovulated in the last days of a trial. Conversely, older males, and those mating with more polyandrous females, had consistently lower fertilization success. Similarly, resistance to a male's mating attempts, particularly by younger females, reduced fertilization probability. After considering these factors, male social status, partner relatedness and the estimated state of male extragonadal sperm reserves did not predict sperm competition outcomes. These results shed new light on sperm competition dynamics in taxa such as birds, with prolonged female sperm storage and staggered fertilizations. This article is part of the theme issue ‘Fifty years of sperm competition’.

Island species provide excellent models for investigating how selection and drift operate in wild populations, and for determining how these processes act to influence local adaptation and speciation. Here, we examine the role of selection and drift in shaping genomic and phenotypic variation across recently separated populations of Berthelot's pipit (Anthus berthelotii), a passerine bird endemic to three archipelagos in the Atlantic. We first characterized genetic diversity and population structuring that supported previous inferences of a history of recent colonizations and bottlenecks. We then tested for regions of the genome associated with the ecologically important traits of bill length and malaria infection, both of which vary substantially across populations in this species. We identified a SNP associated with variation in bill length among individuals, islands, and archipelagos; patterns of variation at this SNP suggest that both phenotypic and genotypic variation in bill length is largely shaped by founder effects. Malaria was associated with SNPs near/within genes involved in the immune response, but this relationship was not consistent among archipelagos, supporting the view that disease resistance is complex and rapidly evolving. Although we found little evidence for divergent selection at candidate loci for bill length and malaria resistance, genome scan analyses pointed to several genes related to immunity and metabolism as having important roles in divergence and adaptation. Our findings highlight the utility and challenges involved with combining association mapping and population genetic analysis in nonequilibrium populations, to disentangle the effects of drift and selection on shaping genotypes and phenotypes.

Significance In nature, animals must compete with their neighbors for access to limited resources. Since conflict over resources can be extremely costly in terms of time, energy, and reproductive success, investigating how individuals resolve conflict is crucial to understanding the evolution of social behaviors. In the Seychelles warbler, we demonstrate two mechanisms by which individuals minimize costs of conflict and show the benefits individuals gain from doing so. Birds that live near relatives or familiar individuals invest less energy in defending and maintaining territory borders and also show less aging-related signs of physiological damage. Our results suggest that conflict between neighbors can be mitigated by kin-selected benefits of sharing resources with relatives but also through direct mutual benefits of cooperation., Because virtually all organisms compete with others in their social environment, mechanisms that reduce conflict between interacting individuals are crucial for the evolution of stable families, groups, and societies. Here, we tested whether costs of social conflict over territorial space between Seychelles warblers (Acrocephalus sechellensis) are mitigated by kin-selected (genetic relatedness) or mutualistic (social familiarity) mechanisms. By measuring longitudinal changes in individuals’ body mass and telomere length, we demonstrated that the fitness costs of territoriality are driven by a complex interplay between relatedness, familiarity, local density, and sex. Physical fights were less common at territory boundaries shared between related or familiar males. In line with this, male territory owners gained mass when living next to related or familiar males and also showed less telomere attrition when living next to male kin. Importantly, these relationships were strongest in high-density areas of the population. Males also had more rapid telomere attrition when living next to unfamiliar male neighbors, but mainly when relatedness to those neighbors was also low. In contrast, neither kinship nor familiarity was linked to body mass or telomere loss in female territory owners. Our results indicate that resolving conflict over territorial space through kin-selected or mutualistic pathways can reduce both immediate energetic costs and permanent somatic damage, thus providing an important mechanism to explain fine-scale population structure and cooperation between different social units across a broad range of taxa.

Many studies have found evidence of rapid evolution in response to environmental change. In most cases, there has been some suggestion of which traits might be most responsive ahead of time. Bosse et al. turn this approach on its head by using genomic regions with a signature of selection to identify traits that are changing. In great tits (Parus major) in the United Kingdom, genomic regions showing selection invariably contained genes associated with bill growth. Indeed, U.K. birds not only have longer bills, but these longer bills are associated with increased fitness. These changes likely reflect an increase in domestic garden bird feeders over the past several decades.Science, this issue p. 365We used extensive data from a long-term study of great tits (Parus major) in the United Kingdom and Netherlands to better understand how genetic signatures of selection translate into variation in fitness and phenotypes. We found that genomic regions under differential selection contained candidate genes for bill morphology and used genetic architecture analyses to confirm that these genes, especially the collagen gene COL4A5, explained variation in bill length. COL4A5 variation was associated with reproductive success, which, combined with spatiotemporal patterns of bill length, suggested ongoing selection for longer bills in the United Kingdom. Last, bill length and COL4A5 variation were associated with usage of feeders, suggesting that longer bills may have evolved in the United Kingdom as a response to supplementary feeding.

Dimethylsulfoniopropionate (DMSP) is a globally important organosulfur molecule and the major precursor for dimethyl sulfide. These compounds are important info-chemicals, key nutrients for marine microorganisms, and are involved in global sulfur cycling, atmospheric chemistry and cloud formation1–3. DMSP production was thought to be confined to eukaryotes, but heterotrophic bacteria can also produce DMSP through the pathway used by most phytoplankton4, and the DsyB enzyme catalysing the key step of this pathway in bacteria was recently identified5. However, eukaryotic phytoplankton probably produce most of Earth’s DMSP, yet no DMSP biosynthesis genes have been identified in any such organisms. Here we identify functional dsyB homologues, termed DSYB, in many phytoplankton and corals. DSYB is a methylthiohydroxybutryate methyltransferase enzyme localized in the chloroplasts and mitochondria of the haptophyte Prymnesium parvum, and stable isotope tracking experiments support these organelles as sites of DMSP synthesis. DSYB transcription levels increased with DMSP concentrations in different phytoplankton and were indicative of intracellular DMSP. Identification of the eukaryotic DSYB sequences, along with bacterial dsyB, provides the first molecular tools to predict the relative contributions of eukaryotes and prokaryotes to global DMSP production. Furthermore, evolutionary analysis suggests that eukaryotic DSYB originated in bacteria and was passed to eukaryotes early in their evolution.

Inbreeding results in more homozygous offspring that should suffer reduced fitness, but it can be difficult to quantify these costs for several reasons. First, inbreeding depression may vary with ecological or physiological stress and only be detectable over long time periods. Second, parental homozygosity may indirectly affect offspring fitness, thus confounding analyses that consider offspring homozygosity alone. Finally, measurement of inbreeding coefficients, survival and reproductive success may often be too crude to detect inbreeding costs in wild populations. Telomere length provides a more precise measure of somatic costs, predicts survival in many species and should reflect differences in somatic condition that result from varying ability to cope with environmental stressors. We studied relative telomere length in a wild population of Seychelles warblers (Acrocephalus sechellensis) to assess the lifelong relationship between individual homozygosity, which reflects genome‐wide inbreeding in this species, and telomere length. In juveniles, individual homozygosity was negatively associated with telomere length in poor seasons. In adults, individual homozygosity was consistently negatively related to telomere length, suggesting the accumulation of inbreeding depression during life. Maternal homozygosity also negatively predicted offspring telomere length. Our results show that somatic inbreeding costs are environmentally dependent at certain life stages but may accumulate throughout life.

Understanding individual‐level variation in response to the environment is fundamental to understanding life‐history evolution and population dynamics. Telomeres, the protective caps at the ends of chromosomes, shorten in response to oxidative stress, and telomere shortening is correlated with reduced survival and life span. Investigating telomere dynamics may help us quantify individual variation in the costs experienced from social and ecological factors, and enhance our understanding of the dynamics of natural populations.Here, we study spatio‐temporal variation in lifelong telomere dynamics in the Seychelles warbler, Acrocephalus sechellensis. We combine long‐term life history and ecological data with a large longitudinal dataset of mean telomere lengths, consisting of 1,808 samples from 22 cohorts born between 1993 and 2014. We provide a detailed analysis of how telomere dynamics vary over individual life spans and cohorts, and with spatio‐temporal variation in the social and ecological environment.We found that telomere length decreases with cross‐sectional and longitudinal measures of age, and most rapidly very early in life. However, both cross‐sectional and longitudinal data suggested that against this overall pattern of shortening, bouts of telomere length increase occur in some individuals. Using a large number of repeated measurements we show statistically that these increases are unlikely to be explained solely by qPCR measurement error.Telomere length varied markedly among cohorts. Telomere length was positively associated with temporal variation in island‐wide insect abundance—a key resource for the insectivorous Seychelles warbler—suggesting that the costs associated with living in harsher environments can be studied by investigating telomere dynamics. We also found evidence for sex‐specific relationships between telomeres and tarsus length, potentially reflecting differential costs of growth.Our long‐term data show that in a natural population, telomere dynamics vary in a complex manner over individual life spans, and across space and time. Variance in telomere dynamics among individuals is the product of a wide array of genetic, parental and environmental factors. Explaining this variation more fully will require the integration of comprehensive long‐term ecological and genetic data from multiple populations and species.

Discerning the relative roles of adaptive and non-adaptive processes in generating differences among populations and species, as well as how these processes interact, are fundamental aims in biology. Both genetic and phenotypic divergence across populations can be the product of limited dispersal and gradual genetic drift across populations (isolation by distance), of colonisation history and founder effects (isolation by colonisation) or of adaptation to different environments preventing migration between populations (isolation by adaptation). Here we attempt to differentiate between these processes using island populations of Berthelot's pipit (Anthus berthelotii), a passerine bird endemic to three Atlantic archipelagos. Using microsatellite markers and approximate Bayesian computation, we reveal that the northwards colonisation of this species ca 8,500 years ago resulted in genetic bottlenecks in the colonised archipelagos. We then show that high levels of genetic structure exist across archipelagos, and that these are consistent with a pattern of isolation by colonisation, but not with isolation by distance or adaptation. Finally, we show that substantial morphological divergence also exists and that this is strongly concordant with patterns of genetic structure and bottleneck history, but not with environmental differences or geographic distance. Overall our data suggest that founder effects are responsible for both genetic and phenotypic changes across archipelagos. Our findings provide a rare example of how founder effects can persist over evolutionary timescales, and suggest that they may play an important role in the early stages of speciation. This article is protected by copyright. All rights reserved.

A preference for mating with similar individuals can have a key role in speciation. Research on Darwin’s finches suggests that individuals might use the likeness of their parents as a guide for choosing mates. Sexual imprinting drives mating choices in Darwin’s finches.

A challenge in evolutionary biology is to understand the operation of sexual selection on males in polyandrous groups, where sexual selection occurs before and after mating. Here, we combine fine-grained behavioral information (41,000 interactions) with molecular parentage data to study sexual selection in replicated, age-structured groups of polyandrous red junglefowl, Gallus gallus. Male reproductive success was determined by the number of females mated (precopulatory sexual selection) and his paternity share, which was driven by the polyandry of his female partners (postcopulatory sexual selection). Pre- and postcopulatory components of male reproductive success covaried positively; males with high mating success also had high paternity share. Two male phenotypes affected male pre- and postcopulatory performance: average aggressiveness toward rival males and age. Aggressive males mated with more females and more often with individual females, resulting in higher sexual exclusivity. Similarly, younger males mated with more females and more often with individual females, suffering less intense sperm competition than older males. Older males had a lower paternity share even allowing for their limited sexual exclusivity, indicating they may produce less competitive ejaculates. These results show that-in these populations-postcopulatory sexual selection reinforces precopulatory sexual selection, consistently promoting younger and more aggressive males.

Oceanic islands are excellent systems for allowing biologists to test evolutionary hypotheses due to their relative simplicity of habitats, naturally replicated study design and high levels of endemic taxa with conspicuous variation in form, colour and behaviour. Over the last two decades the Canary Islands archipelago has proved an ideal system for evolutionary biologists who seek to unravel how biodiversity arises and disappears. In this review we have evaluated the contribution of the study of Canarian birds to our understanding of how and why species occur and change over time. We focus our attention on both extant and extinct Canarian taxa, and describe how research on these species has filled gaps in our understanding of avian speciation and extinction. In addition, we discuss the necessity of revising the current taxonomy in the Canarian avian taxa, especially the status of the endemic subspecies, some of which might be better treated as full species. An accurate classification of Canarian birds is not only necessary for testing evolutionary, biogeographic and ecological hypotheses, but also for effective decision making about conservation and environmental management. Finally we introduce future avenues of research that we feel will yield the most exciting and promising findings on island evolution in the coming years., LGS is supported by a fellowship from the Edward Grey Institute at the University of Oxford, and ERE is funded through a pre-doctoral contract from the Spanish Ministry of Economy (BES-2013-065192).

Inbreeding results in more homozygous offspring that should suffer reduced fitness, but it can be difficult to quantify these costs for several reasons. First, inbreeding depression may vary with ecological or physiological stress and only be detectable over long time periods. Second, parental homozygosity may indirectly affect offspring fitness, thus confounding analyses that consider offspring homozygosity alone. Finally, measurement of inbreeding coefficients, survival and reproductive success may often be too crude to detect inbreeding costs in wild populations. Telomere length provides a more precise measure of somatic costs, predicts survival in many species and should reflect differences in somatic condition that result from varying ability to cope with environmental stressors. We studied relative telomere length in a wild population of Seychelles warblers (Acrocephalus sechellensis) to assess the lifelong relationship between individual homozygosity, which reflects genome-wide inbreeding in this species, and telomere length. In juveniles, individual homozygosity was negatively associated with telomere length in poor seasons. In adults, individual homozygosity was consistently negatively related to telomere length, suggesting the accumulation of inbreeding depression during life. Maternal homozygosity also negatively predicted offspring telomere length. Our results show that somatic inbreeding costs are environmentally dependent at certain life stages but may accumulate throughout life.

Population bottlenecks can restrict variation at functional genes, reducing the ability of populations to adapt to new and changing environments. Understanding how populations generate adaptive genetic variation following bottlenecks is therefore central to evolutionary biology. Genes of the major histocompatibility complex (MHC) are ideal models for studying adaptive genetic variation due to their central role in pathogen recognition. While de novo MHC sequence variation is generated by point mutation, gene conversion can generate new haplotypes by transferring sections of DNA within and across duplicated MHC loci. However, the extent to which gene conversion generates new MHC haplotypes in wild populations is poorly understood. We developed a 454 sequencing protocol to screen MHC class I exon 3 variation across all 13 island populations of Berthelot’s pipit (Anthus berthelotii). We reveal that just 11–15 MHC haplotypes were retained when the Berthelot’s pipit dispersed across its island range in the North Atlantic ca. 75 000 years ago. Since then, at least 26 new haplotypes have been generated in situ across populations. We show that most of these haplotypes were generated by gene conversion across divergent lineages, and that the rate of gene conversion exceeded that of point mutation by an order of magnitude. Gene conversion resulted in significantly more changes at nucleotide sites directly involved with pathogen recognition, indicating selection for functional variants. We suggest that the creation of new variants by gene conversion is the predominant mechanism generating MHC variation in genetically depauperate populations, thus allowing them to respond to pathogenic challenges.

Pathogens can exert strong selective forces upon host populations. However, before we can make any predictions about the consequences of pathogen-mediated selection, we first need to determine whether patterns of pathogen distribution are consistent over spatiotemporal scales. We used molecular techniques to screen for a variety of blood pathogens (avian malaria, pox and trypanosomes) over a three-year time period across 13 island populations of the Berthelot's pipit (Anthus berthelotii). This species has only recently dispersed across its range in the North Atlantic, with little subsequent migration, providing an ideal opportunity to examine the causes and effects of pathogenic infection in populations in the early stages of differentiation. We screened 832 individuals, and identified two strains of Plasmodium, four strains of Leucocytozoon, and one pox strain. We found strong differences in pathogen prevalence across populations, ranging from 0 to 65%, and while some fluctuations in prevalence occurred, these differences were largely stable over the time period studied. Smaller, more isolated islands harboured fewer pathogen strains than larger, less isolated islands, indicating that at the population level, colonization and extinction play an important role in determining pathogen distribution. Individual-level analyses confirmed the island effect, and also revealed a positive association between Plasmodium and pox infection, which could have arisen due to dual transmission of the pathogens by the same vectors, or because one pathogen lowers resistance to the other. Our findings, combined with an effect of infection on host body condition, suggest that Berthelot's pipits are subject to different levels of pathogen-mediated selection both across and within populations, and that these selective pressures are consistent over time., Grant from the Natural Environment Research Council to DSR and LGS, and a Spanish fellowship (Ramón y Cajal program) to JCI.

Genes of the major histocompatibility complex (MHC) form a vital part of the vertebrate immune system and play a major role in pathogen resistance. The extremely high levels of polymorphism observed at the MHC are hypothesised to be driven by pathogen-mediated selection. Although the exact nature of selection remains unclear, three main hypotheses have been put forward; heterozygote advantage, negative frequency-dependence and fluctuating selection. Here, we report the effects of MHC genotype on survival in a cohort of semi-natural red junglefowl (Gallus gallus) that suffered severe mortality as a result of an outbreak of the disease coccidiosis. The cohort was followed from hatching until 250 days of age, approximately the age of sexual maturity in this species, during which time over 80% of the birds died. We show that on average birds with MHC heterozygote genotypes survived infection longer than homozygotes and that this effect was independent of genome-wide heterozygosity, estimated across microsatellite loci. This MHC effect appeared to be caused by a single susceptible haplotype (CD_c) the effect of which was masked in all heterozygote genotypes by other dominant haplotypes. The CD_c homozygous genotype had lower survival than all other genotypes, but CD_c heterozygous genotypes had survival probabilities equal to the most resistant homozygote genotype. Importantly, no heterozygotes conferred greater resistance than the most resistant homozygote genotype, indicating that the observed survival advantage of MHC heterozygotes was the product of dominant, rather than overdominant processes. This pattern and effect of MHC diversity in our population could reflect the processes ongoing in similarly small, fragmented natural populations.

Major histocompatibility complex (MHC) genes have been put forward as a model for studying how genetic diversity is maintained in wild populations. Pathogen-mediated selection (PMS) is believed to generate the extraordinary levels of MHC diversity observed. However, establishing the relative importance of the three proposed mechanisms of PMS (heterozygote advantage, rare-allele advantage and fluctuating selection) has proved extremely difficult. Studies have attempted to differentiate between mechanisms of PMS using two approaches: (i) comparing MHC diversity with that expected under neutrality and (ii) relating MHC diversity to pathogen regime. Here, we show that in many cases the same predictions arise from the different mechanisms under these approaches, and that most studies that have inferred one mechanism of selection have not fully considered the alternative explanations. We argue that, while it may be possible to demonstrate that particular mechanisms of PMS are occurring, resolving their relative importance within a system is probably impossible. A more realistic target is to continue to demonstrate when and where the different mechanisms of PMS occur, with the aim of determining their relative importance across systems. We put forward what we believe to be the most promising approaches that will allow us to progress towards achieving this.

Senescence – the progressive age-dependent decline in performance – occurs in most organisms. There is considerable variation in the onset and rate of senescence between and within species. Yet the causes of this variation are still poorly understood, despite being central to understanding the evolution of senescence. Long-term longitudinal studies on wild animals are extremely well-suited to studying the impact of environmental and individual characteristics (and the interaction between the two) on senescence, and can help us to understand the mechanisms that shape the evolution of senescence. In this review, we summarize and discuss the insights gained from our comprehensive long-term individual-based study of the Seychelles warbler (Acrocephalus sechellensis). This species provides an excellent model system in which to investigate the evolution of senescence in the wild. We found that Seychelles warblers show senescent declines in survival and reproduction, and discuss how individual characteristics (body condition, body size) and environmental effects (low- versus high-quality environments) may affect the onset and rate of senescence. Further, we highlight the evidence for trade-offs between early-life investment and senescence. We describe how key cellular and physiological processes (oxidative stress and telomere shortening) underpinning senescence are affected by individual and environmental characteristics in the Seychelles warbler (e.g. food availability, reproductive investment, disease) and we discuss how such physiological variation may mediate the relationship between environmental characteristics and senescence. Based on our work using Seychelles warblers as a model system, we show how insights from long-term studies of wild animals may help unravel the causes of the remarkable variation in senescence observed in natural systems, and highlight areas for promising future research.

Reproduction through sex carries substantial costs, mainly because only half of sexual adults produce offspring1. It has been theorized that these costs could be countered if sex allows sexual selection to clear the universal fitness constraint of mutation load2,3,4. Under sexual selection, competition between (usually) males and mate choice by (usually) females create important intraspecific filters for reproductive success, so that only a subset of males gains paternity. If reproductive success under sexual selection is dependent on individual condition, which is contingent to mutation load, then sexually selected filtering through ‘genic capture’5 could offset the costs of sex because it provides genetic benefits to populations. Here we test this theory experimentally by comparing whether populations with histories of strong versus weak sexual selection purge mutation load and resist extinction differently. After evolving replicate populations of the flour beetle Tribolium castaneum for 6 to 7 years under conditions that differed solely in the strengths of sexual selection, we revealed mutation load using inbreeding. Lineages from populations that had previously experienced strong sexual selection were resilient to extinction and maintained fitness under inbreeding, with some families continuing to survive after 20 generations of sib × sib mating. By contrast, lineages derived from populations that experienced weak or non-existent sexual selection showed rapid fitness declines under inbreeding, and all were extinct after generation 10. Multiple mutations across the genome with individually small effects can be difficult to clear, yet sum to a significant fitness load; our findings reveal that sexual selection reduces this load, improving population viability in the face of genetic stress., We thank the Natural Environment Research Council and the Leverhulme Trust for financial support, D. Edward for statistical advice and colleagues at the 2013 Biology of Sperm meeting for comments that improved analytical design and interpretation.

Studying the population history and demography of organisms with important ecological roles can aid understanding of evolutionary processes at the community level and inform conservation. We screened genetic variation (mtDNA and microsatellite) across the populations of the southern grey shrike (Lanius meridionalis koenigi) in the Canary Islands, where it is an endemic subspecies and an important secondary seed disperser. We show that the Canarian subspecies is polyphyletic with L. meridionalis elegans from North Africa and that shrikes have colonized the Canary Islands from North Africa multiple times. Substantial differences in genetic diversity exist across islands, which are most likely the product of a combination of historical colonization events and recent bottlenecks. The Eastern Canary Islands had the highest overall levels of genetic diversity and have probably been most recently and/or frequently colonized from Africa. Recent or ongoing bottlenecks were detected in three of the islands and are consistent with anecdotal evidence of population declines due to human disturbance. These findings are troubling given the shrike's key ecological role in the Canary Islands, and further research is needed to understand the community‐level consequences of declines in shrike populations. Finally, we found moderate genetic differentiation among populations, which largely reflected the shrike's bottleneck history; however, a significant pattern of isolation‐by‐distance indicated that some gene flow occurs between islands. This study is a useful first step toward understanding how secondary seed dispersal operates over broad spatial scales., DPP was financed by Ph.D. grants awarded by the UK Natural Environment Research Council and the Canarian Government, and by a postdoctoral fellowship (Ramón y Cajal).