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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.

Thermal tolerance range, based on temperatures that result in incapacitating effects, influences species’ distributions and has been used to predict species’ response to increasing temperature. Reproductive performance may also be negatively affected at less extreme temperatures, but such sublethal heat-induced sterility has been relatively ignored in studies addressing the potential effects of, and ability of species’ to respond to, predicted climate warming. The few studies examining the link between increased temperature and reproductive performance typically focus on adults, although effects can vary between life history stages. Here we assessed how sublethal heat stress during development impacted subsequent adult fertility and its plasticity, both of which can provide the raw material for evolutionary responses to increased temperature. We quantified phenotypic and genetic variation in fertility of Drosophila melanogaster reared at standardized densities in three temperatures (25, 27, and 29°C) from a set of lines of the Drosophila Genetic Reference Panel (DGRP). We found little phenotypic variation at the two lower temperatures with more variation at the highest temperature and for plasticity. Males were more affected than females. Despite reasonably large broad-sense heritabilities, a genome-wide association study found little evidence for additive genetic variance and no genetic variants were robustly linked with reproductive performance at specific temperatures or for phenotypic plasticity. We compared results on heat-induced male sterility with other DGRP results on relevant fitness traits measured after abiotic stress and found an association between male susceptibility to sterility and male lifespan reduction following oxidative stress. Our results suggest that sublethal stress during development has profound negative consequences on male adult reproduction, but despite phenotypic variation in a population for this response, there is limited evolutionary potential, either through adaptation to a specific developmental temperature or plasticity in response to developmental heat-induced sterility.

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.

The genetic architecture of a trait usually refers to the number and magnitude of loci that explain phenotypic variation. A description of genetic architecture can help us to understand how genetic variation is maintained, how traits have evolved and how phenotypes might respond to selection. However, linkage mapping and association studies can suffer from problems of bias, especially when conducted in natural populations where the opportunity to perform studies with very large sample sizes can be limited. In this issue of Molecular Ecology, Li and colleagues perform an association study of brain traits in ninespine sticklebacks Pungitius pungitius. They use a sophisticated approach that models all of the genotyped markers simultaneously; conventional approaches fit each marker individually. Although the single-marker and multi-marker approaches find similar regions of the genome that explain phenotypic variation, the overall conclusions about trait architecture are somewhat different, depending on the approach used. Single-marker methods identify regions that explain quite large proportions of genetic variation, whereas the multi-marker approach suggests the traits are far more polygenic. Simulations suggest the multi-marker approach is robust. This study highlights how molecular quantitative genetics in wild populations can be used to address hypothesis-driven questions, without making unrealistic assumptions about effect sizes of individual quantitative trait loci.

Population genetic theory predicts that selection should be more effective when the effective population size (Ne) is larger, and that the efficacy of selection should correlate positively with recombination rate. Here, we analyzed the genomes of ten great tits and ten zebra finches. Nucleotide diversity at 4-fold degenerate sites indicates that zebra finches have a 2.83-fold larger Ne. We obtained clear evidence that purifying selection is more effective in zebra finches. The proportion of substitutions at 0-fold degenerate sites fixed by positive selection (α) is high in both species (great tit 48%; zebra finch 64%) and is significantly higher in zebra finches. When α was estimated on GC-conservative changes (i.e., between A and T and between G and C), the estimates reduced in both species (great tit 22%; zebra finch 53%). A theoretical model presented herein suggests that failing to control for the effects of GC-biased gene conversion (gBGC) is potentially a contributor to the overestimation of α, and that this effect cannot be alleviated by first fitting a demographic model to neutral variants. We present the first estimates in birds for α in the untranslated regions, and found evidence for substantial adaptive changes. Finally, although purifying selection is stronger in high-recombination regions, we obtained mixed evidence for α increasing with recombination rate, especially after accounting for gBGC. These results highlight that it is important to consider the potential confounding effects of gBGC when quantifying selection and that our understanding of what determines the efficacy of selection is incomplete.

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

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.

Bright-red colors in vertebrates are commonly involved in sexual, social, and interspecific signaling [1-8] and are largely produced by ketocarotenoid pigments. In land birds, ketocarotenoids such as astaxanthin are usually metabolically derived via ketolation of dietary yellow carotenoids [9, 10]. However, the molecular basis of this gene-environment mechanism has remained obscure. Here we use the yellowbeak mutation in the zebra finch (Taeniopygia guttata) to investigate the genetic basis of red coloration. Wild-type ketocarotenoids were absent in the beak and tarsus of yellowbeak birds. The yellowbeak mutation mapped to chromosome 8, close to a cluster of cytochrome P450 loci (CYP2J2-like) that are candidates for carotenoid ketolases. The wild-type zebra finch genome was found to have three intact genes in this cluster: CYP2J19A, CYP2J19B, and CYP2J40. In yellowbeak, there are multiple mutations: loss of a complete CYP2J19 gene, a modified remaining CYP2J19 gene (CYP2J19(yb)), and a non-synonymous SNP in CYP2J40. In wild-type birds, CYP2J19 loci are expressed in ketocarotenoid-containing tissues: CYP2J19A only in the retina and CYP2J19B in the beak and tarsus and to a variable extent in the retina. In contrast, expression of CYP2J19(yb) is barely detectable in the beak of yellowbeak birds. CYP2J40 has broad tissue expression and shows no differences between wild-type and yellowbeak. Our results indicate that CYP2J19 genes are strong candidates for the carotenoid ketolase and imply that ketolation occurs in the integument in zebra finches. Since cytochrome P450 enzymes include key detoxification enzymes, our results raise the intriguing possibility that red coloration may be an honest signal of detoxification ability., Current Biology, 26 (11), ISSN:0960-9822, ISSN:1879-0445

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

For over 50 years, the great tit (Parus major) has been a model species for research in evolutionary, ecological and behavioural research; in particular, learning and cognition have been intensively studied. Here, to provide further insight into the molecular mechanisms behind these important traits, we de novo assemble a great tit reference genome and whole-genome re-sequence another 29 individuals from across Europe. We show an overrepresentation of genes related to neuronal functions, learning and cognition in regions under positive selection, as well as increased CpG methylation in these regions. In addition, great tit neuronal non-CpG methylation patterns are very similar to those observed in mammals, suggesting a universal role in neuronal epigenetic regulation which can affect learning-, memory- and experience-induced plasticity. The high-quality great tit genome assembly will play an instrumental role in furthering the integration of ecological, evolutionary, behavioural and genomic approaches in this model species.

Quantitative genetic analysis is often fundamental for understanding evolutionary processes in wild populations. Avian populations provide a model system due to the relative ease of inferring relatedness among individuals through observation. However, extra-pair paternity (EPP) creates erroneous links within the social pedigree. Previous work has suggested this causes minor underestimation of heritability if paternal misassignment is random and hence not influenced by the trait being studied. Nevertheless, much literature suggests numerous traits are associated with EPP and the accuracy of heritability estimates for such traits remains unexplored. We show analytically how nonrandom pedigree errors can influence heritability estimates. Then, combining empirical data from a large great tit (Parus major) pedigree with simulations, we assess how heritability estimates derived from social pedigrees change depending on the mode of the relationship between EPP and the focal trait. We show that the magnitude of the underestimation is typically small (