Genomic islands of divergence reveal selection on the alternate homeolog in upper Fraser River sockeye run-timing groups

Technical Summary

Problem Statement
Effective wildlife conservation and management require a comprehensive understanding of both neutral and adaptive intraspecific genomic variation. While population structure is often well-characterized for ecologically and economically important species, the extensive genomic resources necessary to identify putatively adaptive variation—specifically within punctuated genomic regions—have only recently become available for many species, if at all. This study addresses the need to characterize such adaptive variation in sockeye salmon (Oncorhynchus nerka) within the upper Fraser River system, specifically focusing on run-timing groups.

Methodology
The authors utilized recently published whole-genome resequencing data to analyze sockeye populations in the upper Fraser River and the Nechako Watershed. The study employed population genomic metrics to identify regions of divergence, specifically looking for extended homozygosity and reduced Tajima's D values, which are indicative of selective sweeps. The analysis focused on comparing populations with different run timings, including the Nadina and Stellako River sockeye, the Stuart-Summer run timing group, and the geographically proximal Early Stuart sockeye. Furthermore, the researchers investigated the gene content of identified divergence islands and compared these findings with the known lrrc9 region on Chromosome 12 (Chr12), a locus previously associated with life history traits and run timing across the species' range.

Key Results
The analysis identified a large "island of divergence" located at approximately 56.3–58.0 Mbp on Chromosome 18 (Chr18). This region exhibits extended homozygosity and reduced Tajima's D in specific populations, namely the Nadina and Stellako River sockeye and the Stuart-Summer run timing group. Notably, this haploblock is absent in the geographically proximal Early Stuart sockeye, where genetic variation in this region resembles the background variation found elsewhere on the chromosome.

Gene content analysis of the Chr18 island revealed the presence of the leucine rich-repeat containing 9-like (lrrc9-like) gene. This region is homeologous to the lrrc9 region on Chr12, which is a conserved and selected island of divergence known to be associated with run timing throughout the species' range. When inspecting the Chr12 haploblock across the samples, three distinct genotypic states were observed; however, the Stuart River run timing groups were found to contain primarily the reference haplotype. In contrast, no other regions of major differentiation were observed in the available samples for the Chilcotin or Quesnel River systems.

Significance and Claims
The paper claims that these findings provide additional evidence for the importance of homeologous regions containing both lrrc9 and lrrc9-like in different geographic regions. The study underscores the uniqueness of the upper Fraser River sockeye regarding this potentially adaptive island of divergence on Chr18. By identifying these specific genomic regions associated with run-timing differences, the work contributes to the broader understanding of adaptive variation necessary for the conservation and management of this species, highlighting how specific genomic architectures can vary even among geographically proximate populations.