Retention of a chromosomal inversion from an anadromous ancestor provides the genetic basis for alternative freshwater ecotypes in rainbow trout

Abstract

Migratory behaviour patterns in animals are controlled by a complex genetic architecture. Rainbow trout (Oncorhynchus mykiss) is a salmonid fish that spawns in streams but exhibits three primary life history pathways: stream‐resident (fluvial), lake‐migrant (adfluvial) and ocean‐migrant (anadromous). Previous studies examining fluvial and anadromous O. mykiss have identified several genes associated with life history divergence including the presence of an inversion complex within chromosome 5 (Omy05) that appears to maintain a suite of linked genes controlling migratory behaviour. However, adfluvial trout are migratory without being anadromous, and the genetic basis for this life history has not been investigated from evolutionary perspectives. We sampled wild, native nonanadromous rainbow trout occupying connected stream and lake habitats in a southwest Alaskan watershed to determine whether these fish exhibit genetic divergence between fluvial and adfluvial ecotypes, and whether that divergence parallels that documented in fluvial and anadromous O. mykiss. Data from restriction site‐associated DNA (RAD) sequencing revealed an association between frequencies of both the Omy05 inversion complex and other single nucleotide polymorphisms (SNPs) with habitat type (stream or lake), supporting the genetic divergence of fluvial and adfluvial individuals in sympatry. The presence of a genetic basis for migration into lakes, analogous to that documented for anadromy, indicates that the adfluvial ecotype must be recognized separately from the fluvial form of O. mykiss even though neither is anadromous. These results highlight the genetic architecture underlying migration and the importance of chromosomal inversions in promoting and sustaining intraspecific diversity.

Reliance on lakes by salmon, trout and charr (Oncorhynchus,SalmoandSalvelinus): An evaluation of spawning habitats, rearing strategies and trophic polymorphisms

“…In post‐glacial systems colonized by anadromous ancestors, adfluvial fish represent a derived form (e.g. O. mykiss —Arostegui, Quinn, Seeb, Seeb, & McKinney, ; O. nerka —Wood et al., ; S. salar —Nilsen, Ebbesson, & Stefansson, ; S. trutta —Lemopoulos, Uusi‐Heikkilä, Huusko, Vasemägi, & Vainikka, ). In the case of species with anadromous, adfluvial and fluvial individuals (e.g.…”

“…Hall's panicgrass, Panicum hallii , Poaceae—Lowry et al., ; Atlantic cod, Gadus morhua , Gadidae—Sodeland et al., ). Most recently, a large chromosomal inversion was characterized in O. mykiss in which one haplotype promotes stream residency while the other promotes migration to the ocean (Pearse et al., ) or to lakes (Arostegui et al., ). Increasing the number of individuals sequenced and populations studied for each salmonid species will facilitate identification of duplicated loci, chromosomal inversions and other genomic features influencing phenotypic expression.…”

Multiple chromosomal inversions contribute to adaptive divergence of a dune sunflower ecotype

“…The laboriousness and/or expense of these methods have hindered our understanding of the frequency and importance of inversions in natural populations. Recently, population genomic approaches have been applied to detect potential inverted regions, including methods based on linkage disequilibrium (LD) (Faria et al, 2019; Arostegui, Quinn, Seeb, Seeb, & McKinney, 2019) and local population structure (Li & Ralph, 2019). The LD approach takes advantage of the expectation that inversions will create high LD between (but not within) inversion haplotypes.…”

Patterns of linkage disequilibrium reveal genome architecture in chum salmon

“…Inversions have been implicated in the formation and divergence of sex chromosomes (Lemaitre et al 2009) and establishment of reproductive barriers leading to speciation (Noor et al 2001). Inversions often exhibit elevated divergence due to inhibited recombination, which can manifest as population substructure in genetic analyses (Tian et al 2008, Arostegui et al 2019), and the extended LD exhibited by large inversions facilitates their detection in marker-dense next generation sequencing projects (Kemppainen et al 2015). An understanding of the extent and geographic distribution of inversions is now a critically important part of genetic analyses of natural populations.…”

“…Identification of genomic features should be a routine step in genomic analyses to avoid biases outlined above (Benestan et al 2017, Arostegui et al 2019). Genome assemblies allow direct visualization of LD patterns along the chromosome, but most species do not have assembled genomes.…”