Dissecting the loci underlying maturation timing in Atlantic salmon using haplotype and multi-SNP based association methods.

Characterizing the role of different mutational effect sizes in the evolution of fitness-related traits has been a major goal in evolutionary biology for a century. Such characterization in a diversity of systems, both model and non-model, will help to understand the genetic processes underlying fitness variation. However, well-characterized genetic architectures of such traits in wild populations remain uncommon. In this study, we used haplotype-based and multi-SNP Bayesian association methods with sequencing data for 313 individuals from wild populations to test the mutational composition of known candidate regions for sea age at maturation in Atlantic salmon (Salmo salar). We detected an association at five loci out of 116 candidates previously identified in an aquaculture strain with maturation timing in wild Atlantic salmon. We found that at four of these five loci, variation explained by the locus was predominantly driven by a single SNP suggesting the genetic architecture of this trait includes multiple loci with simple, non-clustered alleles and a locus with potentially more complex alleles. This highlights the diversity of genetic architectures that can exist for fitness-related traits. Furthermore, this study provides a useful multi-SNP framework for future work using sequencing data to characterize genetic variation underlying phenotypes in wild populations.

Beyond large-effect loci: large-scale GWAS reveals a mixed large-effect and polygenic architecture for age at maturity of Atlantic salmon.

BACKGROUND: Understanding genetic architecture is essential for determining how traits will change in response to evolutionary processes such as selection, genetic drift and/or gene flow. In Atlantic salmon, age at maturity is an important life history trait that affects factors such as survival, reproductive success, and growth. Furthermore, age at maturity can seriously impact aquaculture production. Therefore, characterizing the genetic architecture that underlies variation in age at maturity is of key interest. RESULTS: Here, we refine our understanding of the genetic architecture for age at maturity of male Atlantic salmon using a genome-wide association study of 11,166 males from a single aquaculture strain, using imputed genotypes at 512,397 single nucleotide polymorphisms (SNPs). All individuals were genotyped with a 50K SNP array and imputed to higher density using parents genotyped with a 930K SNP array and pedigree information. We found significant association signals on 28 of 29 chromosomes (P-values: 8.7 × 10-133-9.8 × 10-8), including two very strong signals spanning the six6 and vgll3 gene regions on chromosomes 9 and 25, respectively. Furthermore, we identified 116 independent signals that tagged 120 candidate genes with varying effect sizes. Five of the candidate genes found here were previously associated with age at maturity in other vertebrates, including humans. DISCUSSION: These results reveal a mixed architecture of large-effect loci and a polygenic component that consists of multiple smaller-effect loci, suggesting a more complex genetic architecture of Atlantic salmon age at maturity than previously thought. This more complex architecture will have implications for selection on this key trait in aquaculture and for management of wild salmon populations.

Publisher Correction: Sex-dependent dominance maintains migration supergene in rainbow trout.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Sex-dependent dominance maintains migration supergene in rainbow trout.

Males and females often differ in their fitness optima for shared traits that have a shared genetic basis, leading to sexual conflict. Morphologically differentiated sex chromosomes can resolve this conflict and protect sexually antagonistic variation, but they accumulate deleterious mutations. However, how sexual conflict is resolved in species that lack differentiated sex chromosomes is largely unknown. Here we present a chromosome-anchored genome assembly for rainbow trout (Oncorhynchus mykiss) and characterize a 55-Mb double-inversion supergene that mediates sex-specific migratory tendency through sex-dependent dominance reversal, an alternative mechanism for resolving sexual conflict. The double inversion contains key photosensory, circadian rhythm, adiposity and sex-related genes and displays a latitudinal frequency cline, indicating environmentally dependent selection. Our results show sex-dependent dominance reversal across a large autosomal supergene, a mechanism for sexual conflict resolution capable of protecting sexually antagonistic variation while avoiding the homozygous lethality and deleterious mutations associated with typical heteromorphic sex chromosomes.

Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon.

Males and females share many traits that have a common genetic basis; however, selection on these traits often differs between the sexes, leading to sexual conflict. Under such sexual antagonism, theory predicts the evolution of genetic architectures that resolve this sexual conflict. Yet, despite intense theoretical and empirical interest, the specific loci underlying sexually antagonistic phenotypes have rarely been identified, limiting our understanding of how sexual conflict impacts genome evolution and the maintenance of genetic diversity. Here we identify a large effect locus controlling age at maturity in Atlantic salmon (Salmo salar), an important fitness trait in which selection favours earlier maturation in males than females, and show it is a clear example of sex-dependent dominance that reduces intralocus sexual conflict and maintains adaptive variation in wild populations. Using high-density single nucleotide polymorphism data across 57 wild populations and whole genome re-sequencing, we find that the vestigial-like family member 3 gene (VGLL3) exhibits sex-dependent dominance in salmon, promoting earlier and later maturation in males and females, respectively. VGLL3, an adiposity regulator associated with size and age at maturity in humans, explained 39% of phenotypic variation, an unexpectedly large proportion for what is usually considered a highly polygenic trait. Such large effects are predicted under balancing selection from either sexually antagonistic or spatially varying selection. Our results provide the first empirical example of dominance reversal allowing greater optimization of phenotypes within each sex, contributing to the resolution of sexual conflict in a major and widespread evolutionary trade-off between age and size at maturity. They also provide key empirical evidence for how variation in reproductive strategies can be maintained over large geographical scales. We anticipate these findings will have a substantial impact on population management in a range of harvested species where trends towards earlier maturation have been observed.

Contemporary divergence in early life history in grayling (Thymallus thymallus).

BACKGROUND: Following colonization of new habitats and subsequent selection, adaptation to environmental conditions might be expected to be rapid. In a mountain lake in Norway, Lesjaskogsvatnet, more than 20 distinct spawning demes of grayling have been established since the lake was colonized, some 20-25 generations ago. The demes spawn in tributaries consistently exhibiting either colder or warmer temperature conditions during spawning in spring and subsequent early development during early summer. In order to explore the degree of temperature-related divergence in early development, a multi-temperature common-garden experiment was performed on embryos from four different demes experiencing different spring temperatures. RESULTS: Early developmental characters were measured to test if individuals from the four demes respond differently to the treatment temperatures. There was clear evidence of among-deme differences (genotype - environment interactions) in larval growth and yolk-to-body-size conversion efficiency. Under the cold treatment regime, larval growth rates were highest for individuals belonging to cold streams. Individuals from warm streams had the highest yolk-consumption rate under cold conditions. As a consequence, yolk-to-body-mass conversion efficiency was highest for cold-deme individuals under cold conditions. As we observed response parallelism between individuals from demes belonging to similar thermal groups for these traits, some of the differentiation seems likely to result from local adaptation CONCLUSION: The observed differences in length at age during early larval development most likely have a genetic component, even though both directional and random processes are likely to have influenced evolutionary change in the demes under study.

Contemporary isolation-by-distance, but not isolation-by-time, among demes of European Grayling (Thymallus thymallus, Linnaeus) with recent common ancestors.

The development of isolation by distance (IBD) and isolation by time (IBT) was contrasted among demes of European grayling (Thymallus thymallus) that have diverged within the last 25 generations following colonization of a lake (Lesjaskogsvatnet). We find low but significant levels of genetic differentiation among spawning tributaries and a pattern of IBD among them. We do not, however, find evidence for IBT despite an up to four-week difference in spawning date between "warm/early" and "cold/late" spawning demes and differences in the incubation temperatures experienced by offspring. It appears that IBD has developed more rapidly than IBT in this system and that adaptive divergence has been initiated in the absence of IBT. Although analysis of selected loci could reveal reduced recombination in parts of the genome associated with temporal divergence, our analysis of neutral genetic data suggests that IBD is a more important isolating mechanism in the early stages of adaptive divergence in European grayling.

Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata).

Our understanding of the evolution of genes of the major histocompatibility complex (MHC) is rapidly increasing, but there are still enigmatic questions remaining, particularly regarding the maintenance of high levels of MHC polymorphisms in small, isolated populations. Here, we analyze the genetic variation at eight microsatellite loci and sequence variation at exon 2 of the MHC class IIB (DAB) genes in two wild populations of the Trinidadian guppy, Poecilia reticulata. We compare the genetic variation of a small (Ne, 100) and relatively isolated upland population to that of its much larger (Ne approximately 2400) downstream counterpart. As predicted, microsatellite diversity in the upland population is significantly lower and highly differentiated from the population further downstream. Surprisingly, however, these guppy populations are not differentiated by MHC genetic variation and show very similar levels of allelic richness. Computer simulations indicate that the observed level of genetic variation can be maintained with overdominant selection acting at three DAB loci. The selection coefficients differ dramatically between the upland (s > or = 0.2) and lowland (s < or = 0.01) populations. Parasitological analysis on wild-caught fish shows that parasite load is significantly higher on upland than on lowland fish, which suggests that large differences in selection intensity may indeed exist between populations. Based on the infection intensity, a substantial proportion of the upland fish would have suffered direct or indirect fitness consequences as a result of their high parasite loads. Selection by parasites plays a particularly important role in the evolution of guppies in the upland habitat, which has resulted in high levels of MHC diversity being maintained in this population despite considerable genetic drift.