Hybridization among naturally separate taxa is increasing owing to human impact, and can result in taxon loss. Previous classification of anthropogenic hybridization has largely ignored the case of ...bimodal hybrid zones, in which hybrids commonly mate with parental species, resulting in many backcrossed individuals with a small proportion of introgressed genome. Genetic markers can be used to detect such hybrids, but until recently too few markers have been used to detect the true extent of introgression. Recent studies of wolves and trout have employed thousands of markers to reveal previously undetectable backcrosses. This improved resolution will lead to increased detection of late-generation backcrosses, shed light on the consequences of anthropogenic hybridization, and pose new management issues for conservation scientists.
Anthropogenic hybridization is increasingly common and is likely to result in a breakdown of reproductive isolation between ‘good’ species.
Backcrossed individuals that have only a small proportion of one parental genome are difficult to differentiate from parental individuals by using the most common current technologies.
Bimodal hybrid zones are characterized by introgression and backcrossing. The majority of hybrid individuals in these systems have low levels of introgression. The problems posed by bimodal hybrid zones have been largely overlooked in the literature.
Genome-wide sampling of genetic markers at high densities allow increased precision in the estimate of admixture proportions, which makes it feasible to detect multi-generation backcrosses, and will thus make it easier to differentiate bimodal hybrid zones from hybrid swarms or systems without introgression.
Inbreeding depression is of major concern for the conservation of threatened species, and inbreeding avoidance is thought to be a key driver in the evolution of mating systems. However, the ...estimation of individual inbreeding coefficients in natural populations has been challenging, and, consequently, the full effect of inbreeding on fitness remains unclear. Genomic inbreeding coefficients may resolve the long-standing paucity of data on inbreeding depression in adult traits and total fitness. Here we investigate inbreeding depression in a range of life history traits and fitness in a wild population of red deer (Cervus elaphus) in Scotland using individual inbreeding coefficients derived from dense Single-Nucleotide Polymorphism (SNP) data (F
grm). We find associations between F
grm and annual breeding success in both sexes, and between maternal inbreeding coefficient and offspring survival. We also confirm previous findings of inbreeding depression in birth weight and juvenile survival. In contrast, inbreeding coefficients calculated from a deep and comparatively complete pedigree detected inbreeding depression in juvenile survival, but not in any adult fitness component. The total effect of inbreeding on lifetime breeding success (LBS) was substantial in both sexes: for F
grm = 0.125, a value resulting from a half-sib mating, LBS declined by 72% for females and 95% for males. Our results demonstrate that SNP-based estimates of inbreeding provide a powerful tool for evaluating inbreeding depression in natural populations, and suggest that, to date, the prevalence of inbreeding depression in adult traits may have been underestimated.
► Inbreeding depression is often assumed to cause selection for inbreeding avoidance. ► Animals sometimes tolerate inbreeding, or even prefer to mate with relatives. ► Existing theory and data do not ...adequately predict or quantify inbreeding strategy. ► We specify that multiple theoretical and empirical advances are now required.
Animal ecologists commonly assume that the reduced fitness that often afflicts inbred offspring will inevitably cause selection for inbreeding avoidance. Although early empirical studies often reported inbreeding avoidance, recent studies suggest that animals sometimes show no avoidance or even prefer to mate with relatives. However, current theory is insufficient to predict whether animals should avoid, tolerate, or prefer inbreeding and hence to understand overall inbreeding strategy. Furthermore, quantifying inbreeding strategy is challenging, requiring relatedness among unbiased sets of actual and potential mates to be accurately estimated. Here, we highlight key limitations of current theory and empirical tests, and summarise the advances required to predict, quantify, and understand animal inbreeding strategies.
Changing environmental conditions cause changes in the distributions of phenotypic traits in natural populations. However, determining the mechanisms responsible for these changes-and, in particular, ...the relative contributions of phenotypic plasticity versus evolutionary responses-is difficult. To our knowledge, no study has yet reported evidence that evolutionary change underlies the most widely reported phenotypic response to climate change: the advancement of breeding times. In a wild population of red deer, average parturition date has advanced by nearly 2 weeks in 4 decades. Here, we quantify the contribution of plastic, demographic, and genetic components to this change. In particular, we quantify the role of direct phenotypic plasticity in response to increasing temperatures and the role of changes in the population structure. Importantly, we show that adaptive evolution likely played a role in the shift towards earlier parturition dates. The observed rate of evolution was consistent with a response to selection and was less likely to be due to genetic drift. Our study provides a rare example of observed rates of genetic change being consistent with theoretical predictions, although the consistency would not have been detected with a solely phenotypic analysis. It also provides, to our knowledge, the first evidence of both evolution and phenotypic plasticity contributing to advances in phenology in a changing climate.
Sexual selection, through intra-male competition or female choice, is assumed to be a source of strong and sustained directional selection in the wild. In the presence of such strong directional ...selection, alleles enhancing a particular trait are predicted to become fixed within a population, leading to a decrease in the underlying genetic variation. However, there is often considerable genetic variation underlying sexually selected traits in wild populations, and consequently, this phenomenon has become a long-discussed issue in the field of evolutionary biology. In wild Soay sheep, large horns confer an advantage in strong intra-sexual competition, yet males show an inherited polymorphism for horn type and have substantial genetic variation in their horn size. Here we show that most genetic variation in this trait is maintained by a trade-off between natural and sexual selection at a single gene, relaxin-like receptor 2 (RXFP2). We found that an allele conferring larger horns, Ho(+), is associated with higher reproductive success, whereas a smaller horn allele, Ho(P), confers increased survival, resulting in a net effect of overdominance (that is, heterozygote advantage) for fitness at RXFP2. The nature of this trade-off is simple relative to commonly proposed explanations for the maintenance of sexually selected traits, such as genic capture ('good genes') and sexually antagonistic selection. Our results demonstrate that by identifying the genetic architecture of trait variation, we can determine the principal mechanisms maintaining genetic variation in traits under strong selection and explain apparently counter-evolutionary observations.
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 (h(2) = 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.
Hosts may mitigate the impact of parasites by two broad strategies: resistance, which limits parasite burden, and tolerance, which limits the fitness or health cost of increasing parasite burden. The ...degree and causes of variation in both resistance and tolerance are expected to influence host-parasite evolutionary and epidemiological dynamics and inform disease management, yet very little empirical work has addressed tolerance in wild vertebrates. Here, we applied random regression models to longitudinal data from an unmanaged population of Soay sheep to estimate individual tolerance, defined as the rate of decline in body weight with increasing burden of highly prevalent gastrointestinal nematode parasites. On average, individuals lost weight as parasite burden increased, but whereas some lost weight slowly as burden increased (exhibiting high tolerance), other individuals lost weight significantly more rapidly (exhibiting low tolerance). We then investigated associations between tolerance and fitness using selection gradients that accounted for selection on correlated traits, including body weight. We found evidence for positive phenotypic selection on tolerance: on average, individuals who lost weight more slowly with increasing parasite burden had higher lifetime breeding success. This variation did not have an additive genetic basis. These results reveal that selection on tolerance operates under natural conditions. They also support theoretical predictions for the erosion of additive genetic variance of traits under strong directional selection and fixation of genes conferring tolerance. Our findings provide the first evidence of selection on individual tolerance of infection in animals and suggest practical applications in animal and human disease management in the face of highly prevalent parasites.
Estimates of narrow sense heritability derived from genomic data that contain related individuals may be biased due to the within-family effects such as dominance, epistasis and common environmental ...factors. However, for many wild populations, removal of related individuals from the data would result in small sample sizes. In 2013, Zaitlen et al. proposed a method to estimate heritability in populations that include close relatives by simultaneously fitting an identity-by-state (IBS) genomic relatedness matrix (GRM) and an identity-by-descent (IBD) GRM. The IBD GRM is identical to the IBS GRM, except relatedness estimates below a specified threshold are set to 0. We applied this method to a sample of 8557 wild Soay sheep from St. Kilda, with genotypic information for 419,281 single nucleotide polymorphisms. We aimed to see how this method would partition heritability into population-level (IBS) and family-associated (IBD) variance for a range of genetic architectures, and so we focused on a mixture of polygenic and monogenic traits. We also implemented a variant of the model in which the IBD GRM was replaced by a GRM constructed from SNPs with low minor allele frequency to examine whether any additive genetic variance is captured by rare alleles. Whilst the inclusion of the IBD GRM did not significantly improve the fit of the model for the monogenic traits, it improved the fit for some of the polygenic traits, suggesting that dominance, epistasis and/or common environment not already captured by the non-genetic random effects fitted in our models may influence these traits.
The estimation of quantitative genetic parameters in wild populations is generally limited by the accuracy and completeness of the available pedigree information. Using relatedness at genomewide ...markers can potentially remove this limitation and lead to less biased and more precise estimates. We estimated heritability, maternal genetic effects and genetic correlations for body size traits in an unmanaged long‐term study population of Soay sheep on St Kilda using three increasingly complete and accurate estimates of relatedness: (i) Pedigree 1, using observation‐derived maternal links and microsatellite‐derived paternal links; (ii) Pedigree 2, using SNP‐derived assignment of both maternity and paternity; and (iii) whole‐genome relatedness at 37 037 autosomal SNPs. In initial analyses, heritability estimates were strikingly similar for all three methods, while standard errors were systematically lower in analyses based on Pedigree 2 and genomic relatedness. Genetic correlations were generally strong, differed little between the three estimates of relatedness and the standard errors declined only very slightly with improved relatedness information. When partitioning maternal effects into separate genetic and environmental components, maternal genetic effects found in juvenile traits increased substantially across the three relatedness estimates. Heritability declined compared to parallel models where only a maternal environment effect was fitted, suggesting that maternal genetic effects are confounded with direct genetic effects and that more accurate estimates of relatedness were better able to separate maternal genetic effects from direct genetic effects. We found that the heritability captured by SNP markers asymptoted at about half the SNPs available, suggesting that denser marker panels are not necessarily required for precise and unbiased heritability estimates. Finally, we present guidelines for the use of genomic relatedness in future quantitative genetics studies in natural populations.
The MHC is one of the most polymorphic gene clusters in vertebrates and play an essential role in adaptive immunity. Apart from pathogen‐mediated selection, sexual selection can also contribute to ...the maintenance of MHC diversity. MHC‐dependent sexual selection could occur via several mechanisms but at present there is no consensus as to which of these mechanisms are involved and their importance. Previous studies have often suffered from limited genetic and behavioural data and small sample size, and were rarely able to examine all the mechanisms together, determine whether signatures of MHC‐based non‐random mating are independent of genomic effects or differentiate whether MHC‐dependent sexual selection takes place at the pre‐ or post‐copulatory stage. In this study, we use Monte Carlo simulation to investigate evidence for non‐random MHC‐dependent mating patterns by all three mechanisms in a free‐living population of Soay sheep. Using 1710 sheep diplotyped at the MHC class IIa region and genome‐wide SNPs, together with field observations of consorts, we found sexual selection against a particular haplotype in males at the pre‐copulatory stage and sexual selection against female MHC heterozygosity during the rut. We also found MHC‐dependent disassortative mating at the post‐copulatory stage, along with strong evidence of inbreeding avoidance at both stages. However, results from generalized linear mixed models suggest that the pattern of MHC‐dependent disassortative mating could be a by‐product of inbreeding avoidance. Our results therefore suggest that while multiple apparent mechanisms of non‐random mating with respect to the MHC may occur, some of them have alternative explanations.
see also the Perspective by Jamie Winternitz.
PDF
