Investigating structural variant, indel and single nucleotide polymorphism differentiation between locally adapted Atlantic salmon populations

Abstract

Genomic structural variants (SVs) are now recognized as an integral component of intraspecific polymorphism and are known to contribute to evolutionary processes in various organisms. However, they are inherently difficult to detect and genotype from readily available short‐read sequencing data, and therefore remain poorly documented in wild populations. Salmonid species displaying strong interpopulation variability in both life history traits and habitat characteristics, such as Atlantic salmon (Salmo salar), offer a prime context for studying adaptive polymorphism, but the contribution of SVs to fine‐scale local adaptation has yet to be explored. Here, we performed a comparative analysis of SVs, single nucleotide polymorphisms (SNPs) and small indels (<50 bp) segregating in the Romaine and Puyjalon salmon, two putatively locally adapted populations inhabiting neighboring rivers (Québec, Canada) and showing pronounced variation in life history traits, namely growth, fecundity, and age at maturity and smoltification. We first catalogued polymorphism using a hybrid SV characterization approach pairing both short‐ (16X) and long‐read sequencing (20X) for variant discovery with graph‐based genotyping of SVs across 60 salmon genomes, along with characterization of SNPs and small indels from short reads. We thus identified 115,907 SVs, 8,777,832 SNPs and 1,089,321 short indels, with SVs covering 4.8 times more base pairs than SNPs. All three variant types revealed a highly congruent population structure and similar patterns of FST and density variation along the genome. Finally, we performed outlier detection and redundancy analysis (RDA) to identify variants of interest in the putative local adaptation of Romaine and Puyjalon salmon. Genes located near these variants were enriched for biological processes related to nervous system function, suggesting that observed variation in traits such as age at smoltification could arise from differences in neural development. This study therefore demonstrates the feasibility of large‐scale SV characterization and highlights its relevance for salmonid population genomics.

Advances in salmonid genetics—Insights from Coastwide and beyond

“…Several studies in this Special Issue investigated the crucial role of genomic diversity in maintaining life history variation and enabling natural populations to adapt to local environments. Three papers investigated genomic variation associated with locally adapted traits across populations (Lecomte et al, 2024;Narum et al, 2024;Willis et al, 2024), two others focused on genomic variation to adapt under scenarios of climate change (Tigano et al, 2024) or persist through ecological disturbance (Frei et al, 2024), and another on genomic differences between hatchery reared versus wild stocks (Howe et al, 2024). Lecomte et al (2024) examined SNPs, structural variants (SVs), and small indels between two populations of Atlantic Salmon in North America with differences in life history traits (i.e., age at smoltification and maturity).…”

“…Three papers investigated genomic variation associated with locally adapted traits across populations (Lecomte et al, 2024;Narum et al, 2024;Willis et al, 2024), two others focused on genomic variation to adapt under scenarios of climate change (Tigano et al, 2024) or persist through ecological disturbance (Frei et al, 2024), and another on genomic differences between hatchery reared versus wild stocks (Howe et al, 2024). Lecomte et al (2024) examined SNPs, structural variants (SVs), and small indels between two populations of Atlantic Salmon in North America with differences in life history traits (i.e., age at smoltification and maturity). This was the only study in this Special Issue to collect both short-read (~16× coverage per sample of Illumina paired-end 150 base; NovaSeq6000) and long-read (~20× coverage per sample of Oxford Nanopore; PromethION24) sequencing data for individual fish within a study.…”

“…Lecomte et al. ( 2024 ) examined SNPs, structural variants (SVs), and small indels between two populations of Atlantic Salmon in North America with differences in life history traits (i.e., age at smoltification and maturity). This was the only study in this Special Issue to collect both short‐read (~16× coverage per sample of Illumina paired‐end 150 base; NovaSeq6000) and long‐read (~20× coverage per sample of Oxford Nanopore; PromethION24) sequencing data for individual fish within a study.…”