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.

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 (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.

Tetraploid inheritance has two extremes: disomic in allotetraploids and tetrasomic in autotetraploids. The possibility of mixed, or intermediate, inheritance models has generally been neglected. These could well apply to newly formed hybrids or to diploidizing (auto)tetraploids. We present a simple likelihood-based approach that is able to incorporate disomic, tetrasomic, and intermediate inheritance models and estimates the double-reduction rate. Our model shows that inheritance of microsatellite markers in natural tetraploids of Rorippa amphibia and R. sylvestris is tetrasomic, confirming their autotetraploid origin. However, in F 1 hybrids inheritance was intermediate to disomic and tetrasomic inheritance. Apparently, in meiosis, chromosomes paired preferentially with the homolog from the same parental species, but not strictly so. Detected double-reduction rates were low. We tested the general applicability of our model, using published segregation data. In two cases, an intermediate inheritance model gave a better fit to the data than the tetrasomic model advocated by the authors. The existence of inheritance intermediate to disomic and tetrasomic has important implications for linkage mapping and population genetics and hence breeding programs of tetraploids. Methods that have been developed for either disomic or tetrasomic tetraploids may not be generally applicable, particularly in systems where hybridization is common.

A 25-year study of wild sheep shows that individuals vary in how quickly they lose weight as parasite infections increase, and that those who lose the least weight when heavily infected produce more offspring.