Genetic and phenotypic variation along an ecological gradient in lake trout Salvelinus namaycush.

Shauna M Baillie,Michael J Hansen,Andrew M Muir,Paul Bentzen,Charles C Krueger

doi:10.1186/s12862-016-0788-8

Abstract

BackgroundAdaptive radiation involving a colonizing phenotype that rapidly evolves into at least one other ecological variant, or ecotype, has been observed in a variety of freshwater fishes in post-glacial environments. However, few studies consider how phenotypic traits vary with regard to neutral genetic partitioning along ecological gradients. Here, we present the first detailed investigation of lake trout Salvelinus namaycush that considers variation as a cline rather than discriminatory among ecotypes. Genetic and phenotypic traits organized along common ecological gradients of water depth and geographic distance provide important insights into diversification processes in a lake with high levels of human disturbance from over-fishing.ResultsFour putative lake trout ecotypes could not be distinguished using population genetic methods, despite morphological differences. Neutral genetic partitioning in lake trout was stronger along a gradient of water depth, than by locality or ecotype. Contemporary genetic migration patterns were consistent with isolation-by-depth. Historical gene flow patterns indicated colonization from shallow to deep water. Comparison of phenotypic (Pst) and neutral genetic variation (Fst) revealed that morphological traits related to swimming performance (e.g., buoyancy, pelvic fin length) departed more strongly from neutral expectations along a depth gradient than craniofacial feeding traits. Elevated phenotypic variance with increasing water depth in pelvic fin length indicated possible ongoing character release and diversification. Finally, differences in early growth rate and asymptotic fish length across depth strata may be associated with limiting factors attributable to cold deep-water environments.ConclusionWe provide evidence of reductions in gene flow and divergent natural selection associated with water depth in Lake Superior. Such information is relevant for documenting intraspecific biodiversity in the largest freshwater lake in the world for a species that recently lost considerable genetic diversity and is now in recovery. Unknown is whether observed patterns are a result of an early stage of incipient speciation, gene flow-selection equilibrium, or reverse speciation causing formerly divergent ecotypes to collapse into a single gene pool.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0788-8) contains supplementary material, which is available to authorized users.

Highlights

Adaptive radiation involving a colonizing phenotype that rapidly evolves into at least one other ecological variant, or ecotype, has been observed in a variety of freshwater fishes in post-glacial environments
Because depth stratum was the strongest variable associated with group genetic structure according to analysis of molecular variance (AMOVA), subsequent genetic analyses were performed with fish samples grouped by water depth, and not by ecotype or zone, except where stated otherwise
We provide evidence of reductions in gene flow and divergent natural selection associated with water depth in Lake Superior

Summary

Introduction

Adaptive radiation involving a colonizing phenotype that rapidly evolves into at least one other ecological variant, or ecotype, has been observed in a variety of freshwater fishes in post-glacial environments. Genetic and phenotypic traits organized along common ecological gradients of water depth and geographic distance provide important insights into diversification processes in a lake with high levels of human disturbance from over-fishing. Baillie et al BMC Evolutionary Biology (2016) 16:219 are exposed to new ecological opportunities [5] This character release stage typically shows high levels of within-group phenotypic variance where phenotypic responses to the environment may be mainly epigenetic (i.e., due to gene expression). A collapse into panmixis can occur when divergent selection is relaxed [5] This relaxation can be brought about by environmental change in which a heterogeneous environment (e.g., Enos Lake sticklebacks [9]) or diverse food sources are homogenized, as Darwin’s finches experienced after seed type homogenization [10]. The stage of speciation may be assessed, the direction of evolutionary change cannot be discerned unless timeseries data are available to assess directionality of selection and divergence

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