Low genetic and phenotypic divergence in a contact zone between freshwater and marine sticklebacks: gene flow constrains adaptation

Abstract

BackgroundDistinct hybrid zones and phenotypic and genomic divergence is often observed between marine and freshwater threespine sticklebacks (Gasterosteus aculeatus). Nevertheless, cases also exist where marine-freshwater divergence is diffuse despite seemingly similar environmental settings. In order to assess what characterizes these highly different outcomes, we focused on the latter kind of system in the Odder River, Denmark. Here, a previous study based on RAD (Restriction site Associated DNA) sequencing found non-significant genome-wide differentiation between marine and freshwater sticklebacks. In the present study, we analyzed samples on a finer geographical scale. We assessed if the system should be regarded as panmictic, or if fine-scale genetic structure and local selection was present but dominated by strong migration. We also asked if specific population components, that is the two sexes and different lateral plate morphs, contributed disproportionally more to dispersal.ResultsWe assessed variation at 96 SNPs and the Eda gene that affects lateral plate number, conducted molecular sex identification, and analyzed morphological traits. Genetic differentiation estimated by FST was non-significant throughout the system. Nevertheless, spatial autocorrelation analysis suggested fine scale genetic structure with a genetic patch size of 770 m. There was no evidence for sex-biased dispersal, but full-plated individuals showed higher dispersal than low- and partial-plated individuals. The system was dominated by full-plated morphs characteristic of marine sticklebacks, but in the upstream part of the river body shape and frequency of low-plated morphs changed in the direction expected for freshwater sticklebacks. Five markers including Eda were under possible diversifying selection. However, only subtle clinal patterns were observed for traits and markers.ConclusionsWe suggest that gene flow from marine sticklebacks overwhelms adaptation to freshwater conditions, but the short genetic patch size means that the effect of gene flow on the most upstream region must be indirect and occurs over generations. The occurrence of both weak unimodal and strong bimodal hybrid zones within the same species is striking. We suggest environmental and demographic factors that could determine these outcomes, but also highlight the possibility that long-term population history and the presence or absence of genomic incompatibilities could be a contributing factor.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0982-3) contains supplementary material, which is available to authorized users.

Small fish, large river: Surprisingly minimal genetic structure in a dispersal‐limited, habitat specialist fish

“…Overall, E. lemniscatum maintains gene flow across its range and is comprised of a single population. Given the small range and linear distribution of the species, we propose a stepping‐stone model of dispersal best explains the observed gene flow across its range, a phenomenon observed in other linearly distributed taxa (Gold, Burridge, & Turner, ; Pedersen, Ferchaud, Bertelsen, Bekkevold, & Hansen, ; Wagner & McCune, ). In general, our observation of higher‐than‐expected connectivity likely stems from adaptation of E. lemniscatum to temporally unstable and patchily distributed habitats.…”

Study of morphological variation of northern Neotropical Ariidae reveals conservatism despite macrohabitat transitions

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Local adaptation in dispersal in multi‐resource landscapes

“…; Pederson et al. ), evolution of dispersal has remained widely ignored in this literature. The few studies that do integrate local adaptation with dispersal evolution use highly simplified or spatially implicit landscapes (e.g., Kisdi ; Billiard and Lenormand ; Berdahl et al.…”