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

Susanne Holst Pedersen,Dorte Bekkevold,Michael M Hansen,Mia S Bertelsen,Anne-Laure Ferchaud

doi:10.1186/s12862-017-0982-3

Susanne Holst Pedersen, Dorte Bekkevold + Show 3 more

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https://doi.org/10.1186/s12862-017-0982-3

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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.

Highlights

Distinct hybrid zones and phenotypic and genomic divergence is often observed between marine and freshwater threespine sticklebacks (Gasterosteus aculeatus)
Based on the answers to these questions we considered possible scenarios that can explain why distinct molecular and phenotypic differences between freshwater and marine sticklebacks are evident in some systems but not in others, and from a general perspective why hybrid zones occur in some settings but are weak and absent in others within the same species
We found no evidence for sex-biased dispersal, despite the fact that spatial autocorrelation was analyzed over an environmental gradient that could incur fitness loss of dispersing males, if spiggin glue used for nest-building is adapted to different water chemistries [47]

Summary

Introduction

Distinct hybrid zones and phenotypic and genomic divergence is often observed between marine and freshwater threespine sticklebacks (Gasterosteus aculeatus). When selection is combined with gene flow across populations, this may lead to the establishment of clines. It has been suggested that disruptive/divergent selection acting along an environmental gradient can gradually sharpen clinal variation until a single ancestral population fragments into two or more species [7]. Clines may occur when previously isolated populations come into secondary contact and establish hybrid zones [8, 9]. The shape and width of clines are strongly affected by gene flow or dispersal, defined as the geographical distance between the sites of reproduction by parents and their offspring [8]. It has been suggested that different types of selection may underlie these different categories, with prezygotic isolation being important for bimodal zones [9]

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