The genomics of ecological vicariance in threespine stickleback fish

Abstract

Populations occurring in similar habitats and displaying similar phenotypes are increasingly used to explore parallel evolution at the molecular level. This generally ignores the possibility that parallel evolution can be mimicked by the fragmentation of an ancestral population followed by genetic exchange with ecologically different populations. Here we demonstrate such an ecological vicariance scenario in multiple stream populations of threespine stickleback fish divergent from a single adjacent lake population. On the basis of demographic and population genomic analyses, we infer the initial spread of a stream-adapted ancestor followed by the emergence of a lake-adapted population, that selective sweeps have occurred mainly in the lake population, that adaptive lake–stream divergence is maintained in the face of gene flow from the lake into the streams, and that this divergence involves major inversion polymorphisms also important to marine-freshwater stickleback divergence. Overall, our study highlights the need for a robust understanding of the demographic and selective history in evolutionary investigations.

Interpreting differentiation landscapes in the light of long-term linked selection

“…Following this approach that considered single comparisons, Berner and Salzburger (2015) suggested to account for differentiation patterns resulting from BGS in low-recombination regions by adjusting observed differentiation for background differentiation observed across multiple comparisons. This comparative approach using so-called delta differentiation ( F ST ) has found application, for example, in crow speciation genomics work (Vijay et al 2016) to formulate baseline levels of differentiation based on mean differentiation estimated from a reference set of independent comparisons, and was extended to other population genetic parameters, such as linkage and haplotype structure in research on stickleback adaptation (Roesti et al 2015). This approach empirically adapts baselines across the genome to take into account heterogeneity in population genetic parameters due to processes unrelated to ecologically relevant lineage-specific positive selection.…”

“…Approaches like these are expected to yield sets of genomic regions enriched for candidate regions that evolved under positive selection. To verify this prediction, the comparison of distributions of parameters more explicitly related to positive selection, such as haplotype structure (Voight et al 2006;Sabeti et al 2007;Tang et al 2007;Ferrer-Admetlla et al 2014) among candidate regions and the genomic background is helpful (e.g., Roesti et al 2015). Furthermore, parameter distributions within genomic regions with consistently accentuated differentiation across independent comparisons may constitute more conservative baselines against which to discriminate candidate regions than the genomic background.…”

Toward conservation of genetic and phenotypic diversity in Japanese sticklebacks

“…cis-Regulatory changes in key developmental genes, such as Eda, Pitx1 and GDF6, contribute to morphological divergence between populations inhabiting contrasting environments (Chan et al, 2010;O'Brown et al, 2015;Indjeian et al, 2016). Furthermore, recent advances in genomic technologies make it possible to find regions under divergent selection between populations in multiple pairs of ecotypes (Mäkinen et al, 2008a(Mäkinen et al, , 2008bHohenlohe et al, 2010;Jones et al, 2012aJones et al, , 2012bRoesti et al, 2014Roesti et al, , 2015Feulner et al, 2015).…”

Evolution of heterogeneous genome differentiation across multiple contact zones in a crow species complex

“…In addition to temporal multi-population sampling at different stages of the ‘speciation continuum', independent population replication across repeated (often ecological) contrasts has proven powerful to unveil parallel selection pressures contributing to increased local genetic differentiation. For instance, global sampling of stickleback populations across a variety of repeated ecological contrasts revealed recurrent effects of the same major effect genes, but also peculiarities given each genotypic background2021.…”