Ancestry and adaptive evolution of anadromous, resident, and adfluvial rainbow trout (Oncorhynchus mykiss) in the San Francisco bay area: application of adaptive genomic variation to conservation in a highly impacted landscape.

Maeva Leitwein,Devon E Pearse,John Carlos Garza

doi:10.1111/eva.12416

Abstract

The streams draining of into San Francisco Bay, California, have been impacted by habitat alteration for over 150 years, and roads, dams, water diversions, and other impediments now block the paths of many aquatic migratory species. These changes can affect the genetic structure of fish populations, as well as driving adaptive evolution to novel environmental conditions. Here, we determine the evolutionary relationships of San Francisco Bay Area steelhead/rainbow trout (Oncorhynchus mykiss) populations and show that (i) they are more closely related to native coastal steelhead than to the California Central Valley lineage, with no evidence of introgression by domesticated hatchery rainbow trout, (ii) populations above and below barriers within watersheds are each other's closest relatives, and (iii) adaptive genomic variation associated with migratory life‐history traits in O. mykiss shows substantial evolutionary differences between fish above and below dams. These findings support continued habitat restoration and protection of San Francisco Bay Area O. mykiss populations and demonstrate that ecological conditions in novel habitats above barriers to anadromy influence life‐history evolution. We highlight the importance of considering the adaptive landscape in conservation and restoration programs for species living in highly modified habitats, particularly with respect to key life‐history traits.

Highlights

Many animal populations are threatened by human impacts and accelerating global climate change (Urban, 2015), which affect biodiversity at multiple scales: individual, population, species, community, and ecosystem (Rands et al, 2010)
Evaluation of microsatellite and single nucleotide polymorphism (SNP) marker data demonstrated that San Francisco Bay Area O. mykiss populations are primarily derived from native coastal steelhead ancestry, and no significant hatchery rainbow trout introgression was detected in any population
This pattern is supported by (i) structure clustering and principal component analysis (PCA) analyses showing that fish from San Francisco Bay Area streams align with coastal populations; (ii) the unrooted neighbor-joining tree, in which San Francisco Bay Area populations branch with coastal populations to the exclusion of Central Valley populations and hatchery rainbow trout strains; and (iii) the strong linkage disequilibrium between two loci located in the Omy5 Migration Associated Region (MAR), which is similar to the LD

Summary

| INTRODUCTION

Many animal populations are threatened by human impacts and accelerating global climate change (Urban, 2015), which affect biodiversity at multiple scales: individual, population, species, community, and ecosystem (Rands et al, 2010). Expression of life-history variation, such as the timing of migration and maturation, may differ in relation to the phylogeographic structure of populations (Arciniega et al, 2016; Vähä et al, 2011) This phenotypic variation may be influenced by a combination of plasticity and heritable variation in salmonid fishes, including O. mykiss (Abadía- Cardoso, Anderson, Pearse, & Garza, 2013; Liedvogel, Åkesson, & Bensch, 2011; Phillis et al, 2016; Quinn, Kinnison, & Unwin, 2001). We use two SNP loci linked to the chromosome Omy MAR to test the hypothesis that genetic variation associated with migratory life history may be favoured above dams with large reservoirs that can support an adfluvial population (Holecek et al, 2012; Pearse et al, 2014) Together, these analyses will inform ongoing and future management of this protected species and provide insight into the potential for the evolutionary application of adaptive genomic variation in conservation

| MATERIALS AND METHODS

Ck Guadalupe R

| DISCUSSION