Whole genome resequencing identifies local adaptation associated with environmental variation for redband trout

• Published in: Molecular ecology Vol. 32; no. 4; pp. 800 - 818
• Main Authors: Andrews, Kimberly R., Seaborn, Travis, Egan, Joshua P., Fagnan, Matthew W., New, Daniel D., Chen, Zhongqi, Hohenlohe, Paul A., Waits, Lisette P., Caudill, Christopher C., Narum, Shawn R.
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.02.2023; John Wiley and Sons Inc
• Subjects: Acclimatization - genetics; Adaptation; Adaptation, Physiological - genetics; Animals; Body temperature; Climate change; Climatic conditions; Data analysis; Deserts; developmental timing; Divergence; ecological niche modelling; Ecological niches; Elevation; Gene frequency; Gene Frequency - genetics; Gene polymorphism; Genetic analysis; Genome - genetics; genome scan; Genomes; Genomics; genotype–environment association analysis; Habitat loss; Habitats; Nucleotides; Oncorhynchus mykiss; Oncorhynchus mykiss - genetics; Oncorhynchus mykiss gairdneri; Original; ORIGINAL ARTICLES; Outliers (statistics); Polymorphism; Polymorphism, Single Nucleotide - genetics; Population genetics; Population structure; Populations; Salmon; Salmonidae; Salmonids; Signatures; Single-nucleotide polymorphism; SIX gene family; Temperature gradients; thermal gradient; Trout; thermal gradient; Oncorhynchus mykiss gairdneri; developmental timing; ecological niche modelling; genotype-environment association analysis; genome scan
• ISSN: 0962-1083; 1365-294X
• DOI: 10.1111/mec.16810

Aquatic ectotherms are predicted to harbour genomic signals of local adaptation resulting from selective pressures driven by the strong influence of climate conditions on body temperature. We investigated local adaptation in redband trout (Oncorhynchus mykiss gairdneri) using genome scans for 547 samples from 11 populations across a wide range of habitats and thermal gradients in the interior Columbia River. We estimated allele frequencies for millions of single nucleotide polymorphism loci (SNPs) across populations using low‐coverage whole genome resequencing, and used population structure outlier analyses to identify genomic regions under divergent selection between populations. Twelve genomic regions showed signatures of local adaptation, including two regions associated with genes known to influence migration and developmental timing in salmonids (GREB1L, ROCK1, SIX6). Genotype–environment association analyses indicated that diurnal temperature variation was a strong driver of local adaptation, with signatures of selection driven primarily by divergence of two populations in the northern extreme of the subspecies range. We also found evidence for adaptive differences between high‐elevation desert vs. montane habitats at a smaller geographical scale. Finally, we estimated vulnerability of redband trout to future climate change using ecological niche modelling and genetic offset analyses under two climate change scenarios. These analyses predicted substantial habitat loss and strong genetic shifts necessary for adaptation to future habitats, with the greatest vulnerability predicted for high‐elevation desert populations. Our results provide new insight into the complexity of local adaptation in salmonids, and important predictions regarding future responses of redband trout to climate change.