Divergent selection between contrasting habitats can sometimes drive adaptive divergence and the evolution of reproductive isolation in the face of initially high gene flow. "Progress" along this ecological speciation pathway can range from minimal divergence to full speciation. We examine this variation for threespine stickleback fish that evolved independently across eight lake-stream habitat transitions. By quantifying stickleback diets, we show that lake-stream transitions usually coincide with limnetic-benthic ecotones. By measuring genetically based phenotypes, we show that these ecotones often generate adaptive divergence in foraging morphology. By analyzing neutral genetic markers (microsatellites), we show that adaptive divergence is often associated with the presence of two populations maintaining at least partial reproductive isolation in parapatry. Coalescentbased simulations further suggest that these populations have diverged with gene flow within a few thousand generations, although we cannot rule out the possibility of phases of allopatric divergence. Finally, we find striking variation among the eight lake-stream transitions in progress toward ecological speciation. This variation allows us to hypothesize that progress is generally promoted by strong divergent selection and limited dispersal across the habitat transitions. Our study thus makes a case for ecological speciation in a parapatric context, while also highlighting variation in the outcome.
To what extent are patterns of biological diversification determined by natural selection? We addressed this question by exploring divergence in foraging morphology of threespine stickleback fish inhabiting lake and stream habitats within eight independent watersheds. We found that lake fish generally displayed more developed gill structures and had more streamlined bodies than did stream fish. Diet analysis revealed that these morphological differences were associated with limnetic vs. benthic foraging modes, and that the extent of morphological divergence within watersheds reflected differences in prey resources utilized by lake and stream fish. We also found that patterns of divergence were unrelated to patterns of phenotypic trait (co)variance within populations (i.e. the ‘line of least resistance’). Instead, phenotypic (co)variances were more likely to have been shaped by adaptation to lake vs. stream habitats. Our study thus implicates natural selection as a strong deterministic force driving morphological diversification in lake–stream stickleback. The strength of this inference was obtained by complementing a standard analysis of parallel divergence in means between discrete habitat categories (lake vs. stream) with quantitative estimates of selective forces and information on trait (co)variances.
Ecological selection against hybrids between populations occupying different habitats might be an important component of reproductive isolation during the initial stages of speciation. The strength and directionality of this barrier to gene flow depends on the genetic architecture underlying divergence in ecologically relevant phenotypes. We here present line cross analyses of inheritance for two key foraging-related morphological traits involved in adaptive divergence between stickleback ecotypes residing parapatrically in lake and stream habitats within the Misty Lake watershed (Vancouver Island, Canada). One main finding is the striking genetic dominance of the lake phenotype for body depth. Selection associated with this phenotype against first-and later-generation hybrids should therefore be asymmetric, hindering introgression from the lake to the stream population but not vice versa. Another main finding is that divergence in gill raker number is inherited additively and should therefore contribute symmetrically to reproductive isolation. Our study suggests that traits involved in adaptation might contribute to reproductive isolation qualitatively differently, depending on their mode of inheritance
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