A conserved haplotype controls parallel adaptation in geographically distant salmonid populations

Abstract

Salmonid fishes exhibit extensive local adaptations owing to abundant environmental variation and precise natal homing. This extensive local adaptation makes conservation and restoration of salmonids a challenge. For example, defining unambiguous units of conservation is difficult, and restoration attempts often fail owing to inadequate adaptive matching of translocated populations. A better understanding of the genetic architecture of local adaptation in salmonids could provide valuable information to assist in conserving and restoring natural populations of these important species. Here, we use a combination of laboratory crosses and next-generation sequencing to investigate the genetic architecture of the parallel adaptation of rapid development rate in two geographically and genetically distant populations of rainbow trout (Oncorhynchus mykiss). Strikingly, we find that not only is a parallel genetic mechanism used but that a conserved haplotype is responsible for this intriguing adaptation. The repeated use of adaptive genetic variation across distant geographical areas could be a general theme in salmonids and have important implications for conservation and restoration.

Rapid parallel evolution of standing variation in a single, complex, genomic region is associated with life history in steelhead/rainbow trout

“…Many of these studies have identified QTL or significant associations between markers on Omy5 and life-history traits such as spawn timing [47,65,68], smoltification [42,46] and development rate or early maturation [17,66,67,70]. Thus, this study supports previous suggestions that the LD block on chromosome Omy5 represents a 'master control region' influencing residency and anadromy in O. mykiss [46,72] and is a parallel selected region [21] that has experienced repeated selection in multiple populations.…”

“…Our results provide data from natural populations in California and Oregon that support prior studies on diverse O. mykiss lineages using candidate genes, genome wide association and QTL mapping to explore the genetic architecture of traits associated with life history in O. mykiss, including migration [17,32,42,46,48,[65][66][67][68][69][70][71][72][73][74][75][76]. Many of these studies have identified QTL or significant associations between markers on Omy5 and life-history traits such as spawn timing [47,65,68], smoltification [42,46] and development rate or early maturation [17,66,67,70].…”

“…Miller et al [17] identified 344 polymorphic SNPs that mapped to chromosome Omy5 with Restriction-site Aided DNA (RAD) sequencing in two divergent strains of hatchery trout. We developed 55 new SNPtype assays (Fluidigm Corporation, So.…”

“…We developed 55 new SNPtype assays (Fluidigm Corporation, So. San Francisco, CA, USA) from these polymorphisms by aligning the flanking sequence around each SNP with up to 150 bp of flanking sequence derived from BAC clones of the Swanson (Sw) strain [17]. In addition to these RAD-derived SNPs, we used assays for five chromosome Omy5 loci developed by Castañ o-Sánchez et al [50], as well as for the three putative Omy5 loci identified by Abadía-Cardoso et al [45].…”

Outlier analyses to test for local adaptation to breeding grounds in a migratory arctic seabird

“…For example, clinal variations in color in the European barn owl ( Tyto alba ) and tawny owl ( Strix aluco ) seem to be maintained by environmental selection (Antoniazza, Burri, Fumagalli, Goudet, & Roulin, 2010; Karell, Ahola, Karstinen, Valkama, & Brommer, 2011), and clinal variation in allele frequencies in functional genes has been associated with various environmental factors, such as altitude (Bonin, Taberlet, Miaud, & Pompanon, 2006; McCracken et al., 2009), latitude (de Jong, Collins, Beldade, Brakefield, & Zwaan, 2013), and photoperiod (Bradshaw & Holzapfel, 2008). In recent years, several studies have highlighted the utility of genome‐wide scans to investigate mechanisms of population divergence and local adaptation (e.g., resolution of species boundaries in Lake Victoria cichlids, Wagner et al., 2013; parallel adaptation in salmonid fishes, Miller et al., 2012; burrowing behavior in oldfield mice Peromyscus polionotus , Weber, Peterson, & Hoekstra, 2013). An exponential increase in the number of genotyped loci and coverage of the genome over previous methods has also increased power to detect loci that deviate from a neutral model of evolution (i.e., outlier loci) and potentially underlie adaptation.…”