Genomic Signatures After Five Generations of Intensive Selective Breeding: Runs of Homozygosity and Genetic Diversity in Representative Domestic and Wild Populations of Turbot (Scophthalmus maximus).

Oscar Aramburu,Carmen Bouza,Alan Le Moan,Dorte Bekkevold,Francisco Ceballos,Jakob Hemmer-Hansen,Adrián Casanova,Paulino Martínez

doi:10.3389/fgene.2020.00296

Abstract

Massive genotyping of single nucleotide polymorphisms (SNP) has opened opportunities for analyzing the way in which selection shapes genomes. Artificial or natural selection usually leaves genomic signatures associated with selective sweeps around the responsible locus. Strong selective sweeps are most often identified either by lower genetic diversity than the genomic average and/or islands of runs of homozygosity (ROHi). Here, we conducted an analysis of selective sweeps in turbot (Scophthalmus maximus) using two SNP datasets from a Northeastern Atlantic population (36 individuals) and a domestic broodstock (46 individuals). Twenty-six families (∼ 40 offspring per family) from this broodstock and three SNP datasets applying differing filtering criteria were used to adjust ROH calling parameters. The best-fitted genomic inbreeding estimate (FROH) was obtained by the sum of ROH longer than 1 Mb, called using a 21,615 SNP panel, a sliding window of 37 SNPs and one heterozygous SNP per window allowed. These parameters were used to obtain the ROHi distribution in the domestic and wild populations (49 and 0 ROHi, respectively). Regions with higher and lower genetic diversity within each population were obtained using sliding windows of 37 SNPs. Furthermore, those regions were mapped in the turbot genome against previously reported genetic markers associated with QTL (Quantitative Trait Loci) and outlier loci for domestic or natural selection to identify putative selective sweeps. Out of the 319 and 278 windows surpassing the suggestive pooled heterozygosity thresholds (ZHp) in the wild and domestic population, respectively, 78 and 54 were retained under more restrictive ZHp criteria. A total of 116 suggestive windows (representing 19 genomic regions) were linked to either QTL for production traits, or outliers for divergent or balancing selection. Twenty-four of them (representing 3 genomic regions) were retained under stricter ZHp thresholds. Eleven QTL/outlier markers were exclusively found in suggestive regions of the domestic broodstock, 7 in the wild population and one in both populations; one (broodstock) and two (wild) of those were found in significant regions retained under more restrictive ZHp criteria in the broodstock and the wild population, respectively. Genome mining and functional enrichment within regions associated with selective sweeps disclosed relevant genes and pathways related to aquaculture target traits, including growth and immune-related pathways, metabolism and response to hypoxia, which showcases how this genome atlas of genetic diversity can be a valuable resource to look for candidate genes related to natural or artificial selection in turbot populations.

Highlights

Artificial selection has been accomplished by humans to domesticate species with desirable properties, in order to reach more profitable phenotypes
The objectives of this study are: (i) to conduct a genomewide characterization of runs of homozygosity (ROH) and genetic diversity in wild and domestic turbot using a large number of SNP loci; obtaining firstly meaningful computational conditions to accurately call ROH and estimate the genomic inbreeding coefficient (FROH), and secondly the ROH distribution and from ROH (FROH) in the wild and domestic turbot samples; (ii) to co-localize previously reported QTL and outlier markers associated with productive traits and adaptive variability with genomic regions of high and low genetic diversity suggestive of selection in wild and domestic turbot; and (iii) to explore gene functions and pathways associated with these regions through preliminary genome mining and functional annotation analyses
This was addressed by analyzing the distribution of ROH and by classifying low- versus high-genetic diversity (GD) regions across the turbot genome, an approach that has been frequently carried out in terrestrial livestock species, but scarcely to date in fish (Cano et al, 2006; Vasemägi et al, 2012; Sun et al, 2014)

Summary

Introduction

Artificial selection has been accomplished by humans to domesticate species with desirable properties, in order to reach more profitable phenotypes. Despite its differences with natural selection, both fit to the same general principle: selective pressure is indirectly applied on specific genomic regions where genes controlling relevant traits are found, modifying the allelic frequencies in the target population (Brito et al, 2017). The main difference between them is that domestication involves the relaxation of the selective pressure applied on fitness traits relevant for survival in wild populations, while the pressure on traits relevant for production is intensified (Sun et al, 2014). A pattern of linkage disequilibrium (LD) will emerge around the locus targeted by selection. This train of “dragging” events is known as a selective sweep and leaves behind detectable signatures at the genome level (Smith and Haigh, 1974; Qanbari et al, 2012)

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