Rapid genetic adaptation to a novel environment despite a genome‐wide reduction in genetic diversity

Abstract

Introduced species often colonize regions that have vastly different ecological and environmental conditions than those found in their native range. As such, species introductions can provide a deeper understanding into the process of adaptive evolution. In the 1880s, steelhead trout (Oncorhynchus mykiss) from California were introduced into Lake Michigan (Laurentian Great Lakes, North America) where they established naturally reproducing populations. In their native range, steelhead hatch in rivers, migrate to the ocean and return to freshwater to spawn. Steelhead in Lake Michigan continue to swim up rivers to spawn, but now treat the freshwater environment of the Great Lakes as a surrogate ocean. To examine the effects of this introduction, we sequenced the genomes of 264 fish. By comparing steelhead from Lake Michigan to steelhead from their ancestral range, we determined that the introduction led to consistent reductions in genetic diversity across all 29 chromosomes. Despite this reduction in genetic diversity, three chromosomal regions were associated with rapid genetic adaptation to the novel environment. The first region contained functional changes to ceramide kinase, which likely altered metabolic and wound-healing rates in Lake Michigan steelhead. The second and third regions encoded carbonic anhydrases and a solute carrier protein, both of which are critical for osmoregulation, and demonstrate how steelhead physiologically adapted to freshwater. Furthermore, the contemporary release of diverse hatchery strains into the lake increased genetic diversity but reduced the signature of genetic adaptation. This study illustrates that species can rapidly adapt to novel environments despite genome-wide reductions in genetic diversity.

The effects of diadromy and its loss on genomic divergence: The case of amphidromous Galaxias maculatus populations

“…In sticklebacks, for instance, resident populations appear to be the result of independent colonization events (Defaveri, Shikano, Shimada, Goto, & Merilä, ). A reduction in genetic diversity is expected if these populations are the product of different founder effects as shown in steelhead trout (Willoughby, Harder, Tennessen, Scribner, & Christie, ). Under this scenario, local adaptation would be expected to play an important role in the differentiation between ecotypes.…”

Effects of temperature and a piscivorous fish on diel winter behaviour of juvenile brown trout (Salmo trutta)

“…As freshwater fish populations will probably be affected by climate change, one important aspect to bear in mind is the possibility of these animals adapting to ongoing climate warming. Adaptation to new environmental conditions in salmonids can be rapid, even in small populations with low genetic variation (Koskinen, Haugen, & Primmer, ; Willoughby, Harder, Tennessen, Scribner, & Christie, ), and physiological and genomic studies on salmonids support potential thermal adaptation (Chen, Farrell, Matala, Hoffman, & Narum, ; Chen, Farrell, Matala, & Narum, ; Narum et al., ). Many organisms, including salmonids, already show adaptive responses to climate‐driven changes such as elevated temperatures (Crozier & Hutchings, ; Jensen et al., ; Merilä & Hendry, ).…”

Comparison of Lake and River Fishery Performance between Two Strains of Steelhead in Eastern Lake Michigan

“…More recently, Willoughby et al. (in press) reported evidence of the blunting of local adaptions among steelhead from multiple Lake Michigan tributaries at a genome‐wide level after the stocking of non‐Michigan strains relative to the period before they were stocked. We found that regardless of the strain stocked or the receiving river, the straying proportion centered around 0.073.…”

“…Approaches included the development of models to infer the effects of age and straying on catch rates and the development of growth models to determine the extent to which strain and sex influenced the ability to reach trophy size. We discuss straying results in terms of the potential deleterious effects of gene flow between stocked steelhead strays and self‐sustaining wild stocks, which may be adapting to local conditions (Waples ; Bartron and Scribner ; Willoughby et al., in press). By quantifying the degree to which each strain meets explicit strain‐specific fishery management objectives as well as how each strain supports steelhead management aims at the species level, fisheries managers can be more effective and efficient in the use of stocking as a tool to achieve desired outcomes.…”