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Funding: Hoge Veluwe great tits: the NIOO-KNAW, ERC, and numerous funding agencies; Wytham great tits: Biotechnology and Biological Sciences Research Council, ERC, and the UK Natural Environment Research Council (NERC). The rate of adaptive evolution, the contribution of selection to genetic changes that increase mean fitness, is determined by the additive genetic variance in individual relative fitness. To date, there are few robust estimates of this parameter for natural populations, and it is therefore unclear whether adaptive evolution can play a meaningful role in short-term population dynamics. We developed and applied quantitative genetic methods to long-term datasets from 19 wild bird and mammal populations and found that, while estimates vary between populations, additive genetic variance in relative fitness is often substantial and, on average, twice that of previous estimates. We show that these rates of contemporary adaptive evolution can affect population dynamics and hence that natural selection has the potential to partly mitigate effects of current environmental change. Postprint

Genomic prediction, the technique whereby an individual’s genetic component of their phenotype is estimated from its genome, has revolutionised animal and plant breeding and medical genetics. However, despite being first introduced nearly two decades ago, it has hardly been adopted by the evolutionary genetics community studying wild organisms. Here, genomic prediction is performed on eight traits in a wild population of Soay sheep. The population has been the focus of a >30 year evolutionary ecology study and there is already considerable understanding of the genetic architecture of the focal Mendelian and quantitative traits. We show that the accuracy of genomic prediction is high for all traits, but especially those with loci of large effect segregating. Five different methods are compared, and the two methods that can accommodate zero-effect and large-effect loci in the same model tend to perform best. If the accuracy of genomic prediction is similar in other wild populations, then there is a real opportunity for pedigree-free molecular quantitative genetics research to be enabled in many more wild populations; currently the literature is dominated by studies that have required decades of field data collection to generate sufficiently deep pedigrees. Finally, some of the potential applications of genomic prediction in wild populations are discussed.

Inbreeding is often avoided in natural populations by passive processes such as sex-biased dispersal. But, in many social animals, opposite-sexed adult relatives are spatially clustered, generating a risk of incest and hence selection for active inbreeding avoidance. Here we show that in long-tailed tits (Aegithalos caudatus), a cooperative breeder that risks inbreeding by living alongside opposite-sex relatives, inbreeding carries fitness costs and is avoided by active kin discrimination during mate choice. First, we identified a positive association between heterozygosity and fitness, indicating that inbreeding is costly. We then compared relatedness within breeding pairs to that expected under multiple mate choice models, finding that pair relatedness is consistent with avoidance of first-order kin as partners. Finally, we show that the similarity of vocal cues offers a plausible mechanism for discrimination against first-order kin during mate choice. Long-tailed tits are known to discriminate between the calls of close kin and non-kin, and they favor first-order kin in cooperative contexts, so we conclude that long-tailed tits use the same kin discrimination rule to avoid inbreeding as they do to direct help towards kin.

The house sparrow is an important model species for studying physiological, ecological and evolutionary processes in wild populations. Here, we present a medium density, genome wide linkage map for house sparrow (Passer domesticus) that has aided the assembly of the house sparrow reference genome, and that will provide an important resource for ongoing mapping of genes controlling important traits in the ecology and evolution of this species. Using a custom house sparrow 10 K iSelect Illumina SNP chip we have assigned 6,498 SNPs to 29 autosomal linkage groups, based on a mean of 430 informative meioses per SNP. The map was constructed by combining the information from linkage with that of the physical position of SNPs within scaffold sequences in an iterative process. Averaged between the sexes; the linkage map had a total length of 2,004 cM, with a longer map for females (2,240 cM) than males (1,801 cM). Additionally, recombination rates also varied along the chromosomes. Comparison of the linkage map to the reference genomes of zebra finch, collared flycatcher and chicken, showed a chromosome fusion of the two avian chromosomes 8 and 4A in house sparrow. Lastly, information from the linkage map was utilized to conduct analysis of linkage disequilibrium (LD) in eight populations with different effective population sizes (Ne) in order to quantify the background level LD. Together, these results aid the design of future association studies, facilitate the development of new genomic tools and support the body of research that describes the evolution of the avian genome.

Sperm competition is an important selective force in many organisms. As a result, sperm have evolved to be among the most diverse cells in the animal kingdom. However, the relationship between sperm morphology, sperm motility and fertilization success is only partially understood. The extent to which between-male variation is heritable is largely unknown, and remarkably few studies have investigated the genetic architecture of sperm traits, especially sperm morphology. Here we use high-density genotyping and gene expression profiling to explore the considerable sperm trait variation that exists in the zebra finch Taeniopygia guttata. We show that nearly all of the genetic variation in sperm morphology is caused by an inversion polymorphism on the Z chromosome acting as a ‘supergene’. These results provide a striking example of two evolutionary genetic predictions. First, that in species where females are the heterogametic sex, genetic variation affecting sexually dimorphic traits will accumulate on the Z chromosome. Second, recombination suppression at the inversion allows beneficial dominant alleles to become fixed on whichever haplotype they first arise, without being exchanged onto other haplotypes. Finally, we show that the inversion polymorphism will be stably maintained by heterozygote advantage, because heterozygous males have the fastest and most successful sperm. Sperm morphology is remarkably variable yet its genetic architecture is poorly known. Now, sperm morphology variation in zebra finches is shown to be largely explained by an inversion polymorphism on the Z chromosome acting as a supergene.

The age of potential mates has been proposed to be an important target for mate choice by females. Alternative hypotheses predict preferences in either direction. Females might be expected to prefer older males because such males have demonstrated their capacity to survive. Alternatively, they might prefer younger males that have not accumulated deleterious mutations. Preferences in both directions have been observed in laboratory experiments, suggesting that this is an issue that needs to be understood within its ecological context. We measured individual behaviour and reproductive success in a natural population of the field cricket Gryllus campestris over 10 years. We found that in this annual insect, a male's age relative to his peers was poorly correlated with his life span. This suggests that there is limited potential for selection to favour female choice for older males because a strategy of choosing older males would not significantly increase a female's likelihood of mating with a long-lived male. Older males were more successful at pairing up with females at a burrow, but once paired they were less likely to mate with them. By genotyping the next generation of adults we confirmed that observations of both pairing up with a female and matings were associated with successful offspring production. However, there was no relationship between how old a male was at mating and how many adult offspring he had. This lack of evidence for any fitness benefits to females from mate choice in relation to male age was consistent with the observation that the age of males had opposite effects on their success in pairing up with females compared to their success in mating with them.

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.

Virtually the first thing a young population genetics student will learn is that changes in gene frequency can be caused by genetic drift, natural selection, and migration. However, quantifying the relative importance of these mechanisms on changes in a population’s genetic composition is a major challenge in any study system. In PNAS, Chen et al. (1) meet this challenge and describe a framework in which genetic change within a population can be tracked and understood. They did so with the help of two vital ingredients. First, they recognized that any investigation of allele frequency change requires an accurate family tree (or pedigree), along with detailed knowledge of gene flow into and out of the study population. Long-term monitoring of a wild population of Florida Scrub-Jays ( Aphelocoma coerulescens ) (Fig. 1) since 1969 has allowed an observational pedigree spanning many generations to be constructed for their study system. The extensive dataset produced by painstaking field work has been augmented by the collection of high-quality DNA genotype data for most birds alive since 1990 (2), meaning that the pedigree is confirmed with molecular tools and is therefore highly accurate. The second ingredient, which requires an accurate pedigree, is the estimation of every individual bird’s genetic contribution (Box 1) to the population, something which is rarely measured in real populations. The expected genetic contribution estimated using this approach is closely related to the theoretical idea of an individual’s reproductive value (Box 1), a concept that was first defined almost a century ago by Ronald Fisher (3). Genetic contributions and reproductive value have been shown to be comparable when estimated for a population’s descendants far enough in the future (4). Thus, by estimating an ancestral individual’s genetic contribution to the pedigree, the contribution that it makes to the future population can be estimated. This individual … [↵][1]1To whom correspondence may be addressed. Email: d.hunter{at}sheffield.ac.uk or j.slate{at}sheffield.ac.uk. [1]: #xref-corresp-1-1

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.

Currently, there is much debate on the genetic architecture of quantitative traits in wild populations. Is trait variation influenced by many genes of small effect or by a few genes of major effect? Where is additive genetic variation located in the genome? Do the same loci cause similar phenotypic variation in different populations? Great tits (Parus major) have been studied extensively in long‐term studies across Europe and consequently are considered an ecological ‘model organism’. Recently, genomic resources have been developed for the great tit, including a custom SNP chip and genetic linkage map. In this study, we used a suite of approaches to investigate the genetic architecture of eight quantitative traits in two long‐term study populations of great tits—one in the Netherlands and the other in the United Kingdom. Overall, we found little evidence for the presence of genes of large effects in either population. Instead, traits appeared to be influenced by many genes of small effect, with conservative estimates of the number of contributing loci ranging from 31 to 310. Despite concordance between population‐specific heritabilities, we found no evidence for the presence of loci having similar effects in both populations. While population‐specific genetic architectures are possible, an undetected shared architecture cannot be rejected because of limited power to map loci of small and moderate effects. This study is one of few examples of genetic architecture analysis in replicated wild populations and highlights some of the challenges and limitations researchers will face when attempting similar molecular quantitative genetic studies in free‐living populations.

High‐density SNP microarrays (“SNP chips”) are a rapid, accurate and efficient method for genotyping several hundred thousand polymorphisms in large numbers of individuals. While SNP chips are routinely used in human genetics and in animal and plant breeding, they are less widely used in evolutionary and ecological research. In this article, we describe the development and application of a high‐density Affymetrix Axiom chip with around 500,000 SNP s, designed to perform genomics studies of great tit (Parus major ) populations. We demonstrate that the per‐SNP genotype error rate is well below 1% and that the chip can also be used to identify structural or copy number variation. The chip is used to explore the genetic architecture of exploration behaviour (EB ), a personality trait that has been widely studied in great tits and other species. No SNP s reached genomewide significance, including at DRD 4 , a candidate gene. However, EB is heritable and appears to have a polygenic architecture. Researchers developing similar SNP chips may note: (i) SNP s previously typed on alternative platforms are more likely to be converted to working assays; (ii) detecting SNP s by more than one pipeline, and in independent data sets, ensures a high proportion of working assays; (iii) allele frequency ascertainment bias is minimized by performing SNP discovery in individuals from multiple populations; and (iv) samples with the lowest call rates tend to also have the greatest genotyping error rates.

SummaryThe interplay between selection and aspects of the genetic architecture of traits (such as linkage, dominance, and epistasis) can either drive or constrain speciation [1–3]. Despite accumulating evidence that speciation can progress to “intermediate” stages—with populations evolving only partial reproductive isolation—studies describing selective mechanisms that impose constraints on speciation are more rare than those describing drivers. The stick insect Timema cristinae provides an example of a system in which partial reproductive isolation has evolved between populations adapted to different host plant environments, in part due to divergent selection acting on a pattern polymorphism [4, 5]. Here, we demonstrate how selection on a green/melanistic color polymorphism counteracts speciation in this system. Specifically, divergent selection between hosts does not occur on color phenotypes because melanistic T. cristinae are cryptic on the stems of both host species, are resistant to a fungal pathogen, and have a mating advantage. Using genetic crosses and genome-wide association mapping, we quantify the genetic architecture of both the pattern and color polymorphism, illustrating their simple genetic control. We use these empirical results to develop an individual-based model that shows how the melanistic phenotype acts as a “genetic bridge” that increases gene flow between populations living on different hosts. Our results demonstrate how variation in the nature of selection acting on traits, and aspects of trait genetic architecture, can impose constraints on both local adaptation and speciation.

Genes of the major histocompatibility complex (MHC) are regarded as a potentially important target of mate choice due to the fitness benefits that may be conferred to the offspring. According to the complementary genes hypothesis, females mate with MHC dissimilar males to enhance the immunocompetence of their offspring or to avoid inbreeding depression. Here, we investigate whether selection favours a preference for maximally dissimilar or optimally dissimilar MHC class I types, based on MHC genotypes, average amino acid distances and the functional properties of the antigen-binding sites (MHC supertypes); and whether MHC type dissimilarity predicts relatedness between mates in a wild great tit population. In particular, we explore the role that MHC class I plays in female mate choice decisions while controlling for relatedness and spatial population structure, and examine the reproductive fitness consequences of MHC compatibility between mates. We find no evidence for the hypotheses that females select mates on the basis of either maximal or optimal MHC class I dissimilarity. A weak correlation between MHC supertype sharing and relatedness suggests that MHC dissimilarity at functional variants may not provide an effective index of relatedness. Moreover, the reproductive success of pairs did not vary with MHC dissimilarity. Our results provide no support for the suggestion that selection favours, or that mate choice realizes, a preference for complimentary MHC types.

Size-selective harvesting is assumed to alter life histories of exploited fish populations, thereby negatively affecting population productivity, recovery, and yield. However, demonstrating that fisheries-induced phenotypic changes in the wild are at least partly genetically determined has proved notoriously difficult. Moreover, the population-level consequences of fisheries-induced evolution are still being controversially discussed. Using an experimental approach, we found that five generations of size-selective harvesting altered the life histories and behavior, but not the metabolic rate, of wild-origin zebrafish (Danio rerio). Fish adapted to high positively size selective fishing pressure invested more in reproduction, reached a smaller adult body size, and were less explorative and bold. Phenotypic changes seemed subtle but were accompanied by genetic changes in functional loci. Thus, our results provided unambiguous evidence for rapid, harvest-induced phenotypic and evolutionary change when harvesting is intensive and size selective. According to a life-history model, the observed life-history changes elevated population growth rate in harvested conditions, but slowed population recovery under a simulated moratorium. Hence, the evolutionary legacy of size-selective harvesting includes populations that are productive under exploited conditions, but selectively disadvantaged to cope with natural selection pressures that often favor large body size.

The work was supported by the National Environment Research Council (grant NE/E015255/1 to MGR and RKB) and the Academy of Finland (project 132619 to AH). We investigated the genetic architecture of courtship song and cuticular hydrocarbon traits in two phygenetically distinct populations of Drosophila montana. To study natural variation in these two important traits, we analysed within-population crosses among individuals sampled from the wild. Hence, the genetic variation analysed should represent that available for natural and sexual selection to act upon. In contrast to previous between-population crosses in this species, no major quantitative trait loci (QTLs) were detected, perhaps because the between-population QTLs were due to fixed differences between the populations. Partitioning the trait variation to chromosomes suggested a broadly polygenic genetic architecture of within-population variation, although some chromosomes explained more variation in one population compared with the other. Studies of natural variation provide an important contrast to crosses between species or divergent lines, but our analysis highlights recent concerns that segregating variation within populations for important quantitative ecological traits may largely consist of small effect alleles, difficult to detect with studies of moderate power. Postprint

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.

Social interactions are rarely random. In some instances animals exhibit homophily or heterophily, the tendency to interact with similar or dissimilar conspecifics respectively. Genetic homophily and heterophily influence the evolutionary dynamics of populations, because they potentially affect sexual and social selection. Here we investigate the link between social interactions and allele frequencies in foraging flocks of great tits (Parus major) over three consecutive years. We constructed co-occurrence networks which explicitly described the splitting and merging of 85,602 flocks through time (fission-fusion dynamics), at 60 feeding sites. Of the 1711 birds in those flocks we genotyped 962 individuals at 4701 autosomal single- nucleotide polymorphisms (SNPs). By combining genome-wide genotyping with repeated field observations of the same individuals we were able to investigate links between social structure and allele frequencies at a much finer scale than was previously possible. We explicitly accounted for potential spatial effects underlying genetic structure at the population level. We modelled social structure and spatial configuration of great tit fission-fusion dynamics with eigenvector maps. Variance partitioning revealed that allele frequencies were strongly affected by group fidelity (explaining 27-45% of variance) as individuals tended to maintain associations with the same conspecifics. These conspecifics were genetically more dissimilar than expected, shown by genome-wide heterophily for pure social (i.e. space-independent) grouping preferences. Genome-wide homophily was linked to spatial configuration, indicating spatial segregation of genotypes. We did not find evidence for homophily or heterophily for putative socially relevant candidate genes or any other SNP markers. Together, these results demonstrate the importance of distinguishing social and spatial processes in determining population structure.

International audience; Linking variation in quantitative traits to variation in the genome is an important, but challenging task in the study of life-history evolution. Linkage maps provide a valuable tool for the unravelling of such trait Àgene associations. Moreover, they give insight into recombination landscapes and between-species karyotype evolution. Here we used genotype data, generated from a 10k single-nucleotide polymorphism (SNP) chip, of over 2000 individuals to produce high-density linkage maps of the great tit (Parus major), a passerine bird that serves as a model species for ecological and evolutionary questions. We created independent maps from two distinct populations: a captive F2-cross from The Netherlands (NL) and a wild population from the United Kingdom (UK). The two maps contained 6554 SNPs in 32 linkage groups, spanning 2010 cM and 1917 cM for the NL and UK populations, respectively, and were similar in size and marker order. Subtle levels of heterochiasmy within and between chromosomes were remarkably consistent between the populations, suggesting that the local departures from sex-equal recombination rates have evolved. This key and surprising result would have been impossible to detect if only one population was mapped. A comparison with zebra finch Taeniopygia guttata, chicken Gallus gallus and the green anole lizard Anolis carolinensis genomes provided further insight into the evolution of avian karyotypes.

The discipline of molecular ecology has undergone enormous changes since the journal bearing its name was launched approximately two decades ago. The field has seen great strides in analytical methods development, made groundbreaking discoveries and experienced a revolution in genotyping technology. Here, we provide brief perspectives on the main subdisciplines of molecular ecology, describe key questions and goals, discuss common challenges, predict future research directions and suggest research priorities for the next 20 years., We thank the participants in the Molecular Ecology Symposium and Online Forum for many of the ideas put forward in this article.

We isolated and characterized Eastern spiny mouse, Acomys dimidiatus microsatellite loci. A microsatellite-enriched library was created and A. dimidiatus fragments sequenced using 454 sequencing. In total, 1,221 primer-designable microsatellite sequences were identified. We designed primer sets for 20 loci. Loci were characterized in A. dimidiatus individuals from a semi-isolated desert wadi (valley) in St. Katherine Protectorate, Egypt. After initial trails, 18 microsatellite loci were genotyped in 67 mice. The number of alleles displayed in the 18 markers ranged from three to nine (mean = 6) with mean expected and observed heterozygosities of 0.63 and 0.65, respectively. All 18 selected loci were in Hardy–Weinberg equilibrium (P > 0.01). These markers will be used to investigate the fine-scale spatial patterns of genetic diversity and divergence of A. dimidiatus populations. The isolated loci are of potential utility in other murines, including 260 threatened species.

The relationship between sperm energetics and sperm function is poorly known, but is central to our understanding of the evolution of sperm traits. The aim of this study was to examine how sperm morphology and ATP content affect sperm swimming velocity in the zebra finch Taeniopygia guttata . We exploited the high inter-male variation in this species and created extra experimental power by increasing the number of individuals with very long or short sperm through artificial selection. We found a pronounced quadratic relationship between total sperm length and swimming velocity, with velocity increasing with length up to a point, but declining in the very longest sperm. We also found an unexpected negative association between midpiece length and ATP content: sperm with a short midpiece generally contained the highest concentration of ATP. Low intracellular ATP is therefore unlikely to explain reduced swimming velocity among the very longest sperm (which tend to have a shorter midpiece).

Conventionally, small populations living on islands are expected to lose genetic variation by drift. Fluctuations in population size, combined with polygynous mating systems, are expected to contribute to the process by increasing sampling effects on genetic variation. However, in individually monitored populations of Red deer on Rum and Soay sheep on St. Kilda, which experience fluctuations in population size, two processes have been identified which mitigate loss of genetic variation. First, in a number of examples, population reductions are associated with selection. Selection may be in favour of heterozygotes, or, as we have documented in several cases, it may fluctuate in direction temporally. Second, in Soay sheep, in which mortality over population crashes is male-biased, ostensibly leading to low effective numbers of males, molecular studies show that there are systematic changes in the reproductive success of young males, and in variance in male success, that broaden genetic representation compared with expectation.

The fitness consequences of inbreeding and outbreeding are poorly understood in natural populations. We explore two microsatellite-based variables, individual heterozygosity (likely to correlate with recent inbreeding) and a new individual-specific internal distance measure, mean d2 (focusing on events deeper in the pedigree), in relation to two measures of fitness expressed early in life, birth weight and neonatal survival, in 670 red deer calves (Cervus elaphus) born on the Isle of Rum between 1982 and 1996. For comparison, we also analyse inbreeding coefficients derived from pedigrees in which paternity was inferred by molecular methods. Only 14 out of 231 calves (6.1%) had non-zero inbreeding coefficients, and neither inbreeding coefficient nor individual heterozygosity was consistently related to birth weight or neonatal survival. However, mean d2 was consistently related to both fitness measures. Low mean d2 was associated with low birth weight, especially following cold Aprils, in which foetal growth is reduced. Low mean d2 was also associated with low neonatal survival, but this effect was probably mediated by birth weight because fitting birth weight to the neonatal survival model displaced mean d2 as an explanatory variable. We conclude that in the deer population fitness measures expressed early in life do not show evidence of inbreeding depression, but they do show evidence of heterosis, possibly as a result of population mixing. We also demonstrate the practical problems of estimating inbreeding via pedigrees compared with a direct marker-based estimate of individual heterozygosity. We suggest that, together, individual heterozygosity and mean d2, estimated using microsatellites, are useful tools for exploring inbreeding and outbreeding in natural population.

When selection differs between the sexes for traits that are genetically correlated between the sexes, there is potential for the effect of selection in one sex to be altered by indirect selection in the other sex, a situation commonly referred to as intralocus sexual conflict (ISC). While potentially common, ISC has rarely been studied in wild populations. Here, we studied ISC over a set of morphological traits (wing length, tarsus length, bill depth, and bill length) in a wild population of great tits (Parus major) from Wytham Woods, UK. Specifically, we quantified the microevolutionary impacts of ISC by combining intra- and inter-sex additive genetic (co)variances and sex-specific selection estimates in a multivariate framework. Large genetic correlations between homologous male and female traits combined with evidence for sex-specific multivariate survival selection suggested that ISC could play an appreciable role in the evolution of this population. Together, multivariate sex-specific selection and additive genetic (co)variance for the traits considered accounted for additive genetic variance in fitness was uncorrelated between the sexes (cross-sex genetic correlation = -0.003, 95% CI = -0.83, 0.83). Gender load, defined as the reduction in a population's rate of adaptation due to sex-specific effects, was estimated at 50% (95% CI = 13%, 86%). This study provides novel insights into the evolution of sexual dimorphism in wild populations and illustrates how quantitative genetics and selection analyses can be combined in a multivariate framework to quantify the microevolutionary impacts of ISC. This article is protected by copyright. All rights reserved.

Clutch size and egg mass are life history traits that have been extensively studied in wild bird populations, as life history theory predicts a negative trade-off between them, either at the phenotypic or at the genetic level. Here, we analyse the genomic architecture of these heritable traits in a wild great tit (Parus major) population, using three marker-based approaches - chromosome partitioning, quantitative trait locus (QTL) mapping and a genome-wide association study (GWAS). The variance explained by each great tit chromosome scales with predicted chromosome size, no location in the genome contains genome-wide significant QTL, and no individual SNPs are associated with a large proportion of phenotypic variation, all of which may suggest that variation in both traits is due to many loci of small effect, located across the genome. There is no evidence that any regions of the genome contribute significantly to both traits, which combined with a small, nonsignificant negative genetic covariance between the traits, suggests the absence of genetic constraints on the independent evolution of these traits. Our findings support the hypothesis that variation in life history traits in natural populations is likely to be determined by many loci of small effect spread throughout the genome, which are subject to continued input of variation by mutation and migration, although we cannot exclude the possibility of an additional input of major effect genes influencing either trait.

Meiotic recombination breaks down linkage disequilibrium (LD) and forms new haplotypes, meaning that it is an important driver of diversity in eukaryotic genomes. Understanding the causes of variation in recombination rate is important in interpreting and predicting evolutionary phenomena and in understanding the potential of a population to respond to selection. However, despite attention in model systems, there remains little data on how recombination rate varies at the individual level in natural populations. Here we used extensive pedigree and high-density SNP information in a wild population of Soay sheep (Ovis aries) to investigate the genetic architecture of individual autosomal recombination rates. Individual rates were high relative to other mammal systems and were higher in males than in females (autosomal map lengths of 3748 and 2860 cM, respectively). The heritability of autosomal recombination rate was low but significant in both sexes (h2 = 0.16 and 0.12 in females and males, respectively). In females, 46.7% of the heritable variation was explained by a subtelomeric region on chromosome 6; a genome-wide association study showed the strongest associations at locus RNF212, with further associations observed at a nearby ∼374-kb region of complete LD containing three additional candidate loci, CPLX1, GAK, and PCGF3. A second region on chromosome 7 containing REC8 and RNF212B explained 26.2% of the heritable variation in recombination rate in both sexes. Comparative analyses with 40 other sheep breeds showed that haplotypes associated with recombination rates are both old and globally distributed. Both regions have been implicated in rate variation in mice, cattle, and humans, suggesting a common genetic architecture of recombination rate variation in mammals.

Three strikingly different alternative male mating morphs (aggressive 'independents', semicooperative 'satellites' and female-mimic 'faeders') coexist as a balanced polymorphism in the ruff, Philomachus pugnax, a lek-breeding wading bird(1-3). Major differences in body size, ornamentation, and aggressive and mating behaviors are inherited as an autosomal polymorphism(4,5). We show that development into satellites and faeders is determined by a supergene(6-8) consisting of divergent alternative, dominant and non-recombining haplotypes of an inversion on chromosome 11, which contains 125 predicted genes. Independents are homozygous for the ancestral sequence. One breakpoint of the inversion disrupts the essential CENP-N gene (encoding centromere protein N), and pedigree analysis confirms the lethality of homozygosity for the inversion. We describe new differences in behavior, testis size and steroid metabolism among morphs and identify polymorphic genes within the inversion that are likely to contribute to the differences among morphs in reproductive traits.

Identifying the genes underlying phenotypic variation in natural populations can provide novel insight into the evolutionary process. The candidate gene approach has been applied to studies of a number of traits in various species, in an attempt to elucidate their genetic basis. Here, we test the application of the candidate gene approach to identify the loci involved in variation in gastrointestinal parasite burden, a complex trait likely to be controlled by many loci, in a wild population of Soay sheep. A comprehensive literature review, Gene Ontology databases, and comparative genomics resources between cattle and sheep were used to generate a list of candidate genes. In a pilot study, these candidates, along with 50 random genes, were then sequenced in two pools of Soay sheep; one with low gastrointestinal nematode burden and the other high, using a NimbleGen sequence capture experiment. Further candidates were identified from single nucleotide polymorphisms (SNPs) that were highly differentiated between high- and low-resistance sheep breeds. A panel of 192 candidate and control SNPs were then typed in 960 individual Soay sheep to examine whether they individually explained variation in parasite burden, as measured as faecal egg count, as well as two immune measures (Teladorsagia circumcincta-specific antibodies and antinuclear antibodies). The cumulative effect of the candidate and control SNPs were estimated by fitting genetic relationship matrices (GRMs) as random effects in animal models of the three traits. No more significant SNPs were identified in the pilot sequencing experiment and association study than expected by chance. Furthermore, no significant difference was found between the proportions of candidate or control SNPs that were found to be significantly associated with parasite burden/immune measures. No significant effect of the candidate or control gene GRMs was found. There is thus little support for the candidate gene approach to the identification of loci explaining variation in parasitological and immunological traits in this population. However, a number of SNPs explained significant variation in multiple traits and significant correlations were found between the proportions of variance explained by individual SNPs across multiple traits. The significant SNPs identified in this study may still, therefore, merit further investigation.

Although single nucleotide polymorphisms (SNPs) are increasingly being recognized as powerful molecular markers, their application to non-model organisms can bring significant challenges. Among these are imperfect conversion rates of assays designed from in silico resources and the enhanced potential for genotyping error relative to pre-validated, highly optimized human SNPs. To explore these issues, we used Illumina's GoldenGate assay to genotype 480 Antarctic fur seal (Arctocephalus gazella) individuals at 144 putative SNPs derived from a 454 transcriptome assembly. One hundred and thirty-five polymorphic SNPs (93.8%) were automatically validated by the program GenomeStudio, and the initial genotyping error rate, estimated from nine replicate samples, was 0.004 per reaction. However, an almost tenfold further reduction in the error rate was achieved by excluding 31 loci (21.5%) that exhibited unclear clustering patterns, manually editing clusters to allow rescoring of ambiguous or incorrect genotypes, and excluding 18 samples (3.8%) with unreliable genotypes. After stringent quality filtering, we also found a counter-intuitive negative relationship between in silico minor allele frequency and the conversion rate, suggesting that some of our assays may have been designed from paralogous loci. Nevertheless, we obtained over 45 000 individual SNP genotypes with a final error rate of 0.0005, indicating that the GoldenGate assay is eminently capable of generating large, high-quality data sets for non-model organisms. This has positive implications for future studies of the evolutionary, behavioural and conservation genetics of natural populations.

Understanding the maintenance of genetic variation in natural populations is a core aim of evolutionary genetics. Insight can be gained by quantifying selection at the level of the genotype, as opposed to the phenotype. Here, we show that in a natural population of Soay sheep which is polymorphic for coat pattern, recessive genetic variants at the causal gene, agouti signalling protein (ASIP) are associated with reduced lifetime fitness. This was due primarily to a reduction in juvenile survival of uniformly coloured (self-type) sheep, which are homozygous recessive, and occurs despite significantly higher reproductive success in surviving self-type adults. Consistent with their relatively low fitness, we show that the frequency of self-type individuals has declined from 1985 to 2008. Remarkably though, the frequency of the underlying self-allele has increased, because the frequency of heterozygous individuals (who harbour the majority of all self-alleles) has increased. Indeed, the ratio of observed/expected heterozygous individuals has increased during the study, such that there is now a significant excess of heterozygotyes. By employing gene-dropping simulations, we show that microevolutionary trends in the frequency and excess of ASIP heterozygotes are too pronounced to be caused by genetic drift. Studying this polymorphism at the level of phenotype rather than underlying genotype would have failed to detect cryptic fitness differences. We would also have been unable to rule out genetic drift as an evolutionary force driving genetic change. This highlights the importance of resolving the underlying genetic basis of phenotypic variation in explaining evolutionary dynamics.

Inbreeding is common in small and threatened populations and often has a negative effect on individual fitness and genetic diversity. Thus, inbreeding can be an important factor affecting the persistence of small populations. In this study, we investigated the effects of inbreeding on fitness in a small, wild population of house sparrows (Passer domesticus) on the island of Aldra, Norway. The population was founded in 1998 by four individuals (one female and three males). After the founder event, the adult population rapidly increased to about 30 individuals in 2001. At the same time, the mean inbreeding coefficient among adults increased from 0 to 0.04 by 2001 and thereafter fluctuated between 0.06 and 0.10, indicating a highly inbred population. We found a negative effect of inbreeding on lifetime reproductive success, which seemed to be mainly due to an effect of inbreeding on annual reproductive success. This resulted in selection against inbred females. However, the negative effect of inbreeding was less strong in males, suggesting that selection against inbred individuals is at least partly sex specific. To examine whether individuals avoided breeding with close relatives, we compared observed inbreeding and kinship coefficients in the population with those obtained from simulations of random mating. We found no significant differences between the two, indicating weak or absent inbreeding avoidance. We conclude that there was inbreeding depression in our population. Despite this, birds did not seem to actively avoid mating with close relatives, perhaps as a consequence of constraints on mating possibilities in such a small population.

background: Sperm motility is regulated by mitochondrial enzymes that are partially encoded by mitochondrial DNA (mtDNA). MtDNA has therefore been suggested as a putative genetic marker of male fertility. However, recent studies in different populations have identified both significant and non-significant associations between mtDNA variation and sperm motility. Here, we tested whether mtDNA variation was associated with sperm motility in a large cohort of men from the UK, to test the robustness of previous studies and the reliability of mtDNA as a marker of poor sperm motility. methods: A total of 463 men attending for semen analysis as part of infertility investigations were recruited from a UK laboratory. Sperm motility was measured using both computer-assisted sperm analysis and traditional manual measurements. MtDNA haplogroup and haplotype were determined in 357 and 298 men, respectively, using single nucleotide polymorphism (SNP) markers throughout the mtDNA genome, and compared with sperm motility data. The linkage between the SNP markers, and possible associations between individual SNPs and motility, were also investigated. results: We found no statistical association between haplogroup or haplotype and sperm motility, regardless of how it was measured (P . 0.05 in all cases). Moreover, individual SNPs which were in linkage disequilibrium and dispersed across the mitochondrial genome, and therefore sensitive to mtDNA variation, were not predictive of sperm motility. conclusions: Mitochondrial haplotype is unlikely to be a reliable genetic marker of male factor infertility.

Welcome to the inaugural issue of Evolution Letters. The purpose of this editorial is to explain the journal's scope, main features and policies. Before that though, I will give a brief history of how the journal came into being.

The ecological and evolutionary importance of fine-scale genetic structure within populations is increasingly appreciated. However, available data are largely restricted to wild vertebrates and eusocial insects. In addition, there is the expectation that most insects tend to have such large- and high-density populations and are so mobile that they are unlikely to face inbreeding risks through fine-scale population structuring. This has made the growing body of evidence for inbreeding avoidance in insects and its implication in mating systems evolution somewhat enigmatic. We present a 4-year study of a natural population of field crickets. Using detailed video monitoring combined with genotyping, we track the movement of all adults within the population and investigate genetic structure at a fine scale. We find some evidence for relatives being found in closer proximity, both across generations and within a single breeding season. Whilst incestuous matings are not avoided, population inbreeding is low, suggesting that mating is close to random and the limited fine-scale structure does not create significant inbreeding risk. Hence, there is little evidence for selective pressures associated with the evolution of inbreeding avoidance mechanisms in a closely related species.

Understanding the genetic architecture of phenotypic variation in natural populations is a fundamental goal of evolutionary genetics. Wild Soay sheep (Ovis aries) have an inherited polymorphism for horn morphology in both sexes, controlled by a single autosomal locus, Horns. The majority of males have large normal horns, but a small number have vestigial, deformed horns, known as scurs; females have either normal horns, scurs or no horns (polled). Given that scurred males and polled females have reduced fitness within each sex, it is counterintuitive that the polymorphism persists within the population. Therefore, identifying the genetic basis of horn type will provide a vital foundation for understanding why the different morphs are maintained in the face of natural selection. We conducted a genome-wide association study using ∼36000 single nucleotide polymorphisms (SNPs) and determined the main candidate for Horns as RXFP2, an autosomal gene with a known involvement in determining primary sex characters in humans and mice. Evidence from additional SNPs in and around RXFP2 supports a new model of horn-type inheritance in Soay sheep, and for the first time, sheep with the same horn phenotype but different underlying genotypes can be identified. In addition, RXFP2 was shown to be an additive quantitative trait locus (QTL) for horn size in normal-horned males, accounting for up to 76% of additive genetic variation in this trait. This finding contrasts markedly from genome-wide association studies of quantitative traits in humans and some model species, where it is often observed that mapped loci only explain a modest proportion of the overall genetic variation.

Understanding genetic variation responsible for phenotypic differences in natural populations is significantly hampered by a lack of genomic data for many species. Levels of variation can, however, be estimated using microsatellite markers, which may be useful for relating individual fitness to genetic diversity. Prior studies have demonstrated correlations between heterozygosity and individual fitness in some species. These correlations are sometimes driven by a subset of markers, and it is unclear whether this is because those markers best reflect genome-wide heterozygosity, or whether they are linked to fitness-related genes. Differentiating between these scenarios is hindered when the genomic location of markers is unknown. Here, we develop a predicted genomic map of pinniped microsatellite loci based on conservation of primary sequence and genomic location between dog, cat and giant panda. We mapped 210 of 260 (81%) microsatellites from pinnipeds to locations in dog, cat and giant panda genomes. Based on the demonstrable synteny between the genomes of closely related taxa within the Carnivora, we use these data to identify those microsatellites with the greatest chance of cross-species amplification success and demonstrate successful amplification of 21 of 26 loci for cat, dog and two seal species. We also demonstrate the potential to identify candidate genes that may underpin the functional relationship with individual fitness. Overall, we show that this approach provides a rapid and robust method to elucidate genome organisation for nonmodel organisms and have established a resource that facilitates further genetic research on pinnipeds that also has wider applicability to other carnivores.

Insects in the Wild Insects are of fundamental importance to terrestrial ecosystems and provide laboratory model systems for the study of physiology and genetics. Studies examining how natural and sexual selection operate to drive evolution in wild populations have often neglected invertebrates, resulting in a chasm between our understandings of how things work in the lab versus the natural environment. Rodríguez-Muñoz et al. (p. 1269 ; see the Perspective by Zuk ) bridge this gap by comprehensively monitoring the life histories, behavior, and reproductive success of an entire population of field crickets. Adding genetic data allowed evaluation of how behavior impacts reproductive success and confirmed that male reproductive success varies more than that of females.

Over the past decade, long-term studies of vertebrate populations have been the focus of many quantitative genetic studies. As a result, we have a clearer understanding of why some fitness-related traits are heritable and under selection, but are apparently not evolving. An exciting extension of this work is to identify the genes underlying phenotypic variation in natural populations. The advent of next-generation sequencing and high-throughput single nucleotide polymorphism (SNP) genotyping platforms means that mapping studies are set to become widespread in those wild populations for whom appropriate phenotypic data and DNA samples are available. Here, we highlight the progress made in this area and define evolutionary genetic questions that have become tractable with the arrival of these new genomics technologies.

Mitochondrial DNA (mtDNA) variation has been suggested as a possible cause of variation in male fertility because sperm activity is tightly coupled to mitochondrial oxidative phosphorylation and ATP production, both of which are sensitive to mtDNA mutations. Since male-specific phenotypes such as sperm have no fitness consequences for mitochondria due to maternal mitochondrial (and mtDNA) inheritance, mtDNA mutations that are deleterious in males but which have negligible or no fitness effect in females can persist in populations. How often such mutations arise and persist is virtually unknown. To test whether there were associations between mtDNA variation and sperm performance, we haplotyped 250 zebra finches Taeniopygia guttata from a large pedigreed-population and measured sperm velocity using computer-assisted sperm analysis. Using quantitative genetic 'animal' models, we found no effect of mtDNA haplotype on sperm velocity. Therefore, there is no evidence that in this system mitochondrial mutations have asymmetric fitness effects on males and females, leading to genetic variation in male fertility that is blind to natural selection.

Sperm morphology (size and shape) and sperm velocity are both positively associated with fertilization success, and are expected to be under strong selection. Until recently, evidence for a link between sperm morphology and velocity was lacking, but recent comparative studies have shown that species with high levels of sperm competition have evolved long and fast sperm. It is therefore surprising that evidence for a phenotypic or genetic relationship between length and velocity within species is equivocal, even though sperm competition is played out in the intraspecific arena. Here, we first show that sperm velocity is positively phenotypically correlated with measures of sperm length in the zebra finch Taeniopygia guttata. Second, by using the quantitative genetic "animal model" on a dataset from a multigenerational-pedigreed population, we show that sperm velocity is heritable, and positively genetically correlated to a number of heritable components of sperm length. Therefore, selection for faster sperm will simultaneously lead to the evolution of longer sperm (and vice versa). Our results provide, for the first time, a clear phenotypic and genetic link between sperm length and velocity, which has broad implications for understanding how recently described macroevolutionary patterns in sperm traits have evolved.