One of the approaches to detect genetics variants affecting fitness traits is to identify their surrounding genomic signatures of past selection. With established methods for detecting selection signatures and the current and future availability of large datasets, such studies should have the power to not only detect these signatures but also to infer their selective histories. Domesticated animals offer a powerful model for these approaches as they adapted rapidly to environmental and human-mediated constraints in a relatively short time. We investigated this question by studying a large dataset of 542 individuals from 27 domestic sheep populations raised in France, genotyped for more than 500,000 SNPs. Population structure analysis revealed that this set of populations harbour a large part of European sheep diversity in a small geographical area, offering a powerful model for the study of adaptation. Identification of extreme SNP and haplotype frequency differences between populations listed 126 genomic regions likely affected by selection. These signatures revealed selection at loci commonly identified as selection targets in many species (“selection hotspots”) including ABCG2, LCORL/NCAPG, MSTN, and coat colour genes such as ASIP, MC1R, MITF, and TYRP1. For one of these regions (ABCG2, LCORL/NCAPG), we could propose a historical scenario leading to the introgression of an adaptive allele into a new genetic background. Among selection signatures, we found clear evidence for parallel selection events in different genetic backgrounds, most likely for different mutations. We confirmed this allelic heterogeneity in one case by resequencing the MC1R gene in three black-faced breeds. Our study illustrates how dense genetic data in multiple populations allows the deciphering of evolutionary history of populations and of their adaptive mutations.

The Atlantic herring is a model species for exploring the genetic basis for ecological adaptation, due to its huge population size and extremely low genetic differentiation at selectively neutral loci. However, such studies have so far been hampered because of a highly fragmented genome assembly. Here, we deliver a chromosome-level genome assembly based on a hybrid approach combining a de novo Pacific Biosciences (PacBio) assembly with Hi-C-supported scaffolding. The assembly comprises 26 autosomes with sizes ranging from 12.4 to 33.1 Mb and a total size, in chromosomes, of 726 Mb, which has been corroborated by a high-resolution linkage map. A comparison between the herring genome assembly with other high-quality assemblies from bony fishes revealed few inter-chromosomal but frequent intra-chromosomal rearrangements. The improved assembly facilitates analysis of previously intractable large-scale structural variation, allowing, for example, the detection of a 7.8-Mb inversion on Chromosome 12 underlying ecological adaptation. This supergene shows strong genetic differentiation between populations. The chromosome-based assembly also markedly improves the interpretation of previously detected signals of selection, allowing us to reveal hundreds of independent loci associated with ecological adaptation.

Background: Native Swedish sheep breeds are part of the North European short-tailed sheep group; characterized in part by their genetic uniqueness. Our objective was to study the population structure of native Swedish sheep. Five breeds were genotyped using the 600 K SNP array. Dalapäls and Klövsjö sheep are from the middle of Sweden; Gotland and Gute sheep from Gotland, an island in the Baltic Sea; and Fjällnäs sheep from northern Sweden. We studied population structure by: principal component analysis (PCA), cluster-based analysis of admixture, and an estimated population tree. Results: The analyses of the five Swedish breeds revealed that these breeds are five distinct breeds, while Gute and Gotland are more closely related to each other as seen in all analyses. All breeds had long branch lengths in the population tree indicating they’ve been subjected to drift. We repeated our analyses using 39 K SNP and including 50 K SNP genotypes from other European and southwestern Asian breeds from the Sheep HapMap project and 600 K SNP genotypes from a dataset of French sheep. Results arranged breeds into five groups: south-west Asia, south-west Europe, central Europe, north Europe and north European short-tailed sheep. Within this last group, Norwegian and Icelandic breeds, Finn and Romanov sheep, Scottish breeds, and Gute and Gotland sheep were more closely related while the remaining Swedish breeds and Ouessant sheep were distinct from all breeds and had longer branches in the population tree. Conclusions: We showed population structure of five Swedish breeds and their structure within European and southwestern Asian breeds. Swedish breeds are unique, distinct breeds that have been subjected to drift but group with other north European short-tailed sheep.