Hybridization but minimal introgression: ecologically-based divergent selection maintains a steep hybrid zone in parapatric stickleback fish

Abstract

Steep hybrid zones provide key insights into the mechanisms of speciation by reflecting incomplete reproductive isolation between diverging populations. However, the specific reproductive barriers preventing the fusion of such populations generally remain unclear, particularly the role of ecologically-based divergent selection. To address the latter, we here investigate a steep hybrid zone between lake and stream ecotypes of threespine stickleback fish inhabiting contiguous habitats within a single watershed. Given the spatial proximity of these habitats and the systems postglacial age, historical allopatry is unlikely to have contributed to the evolution of reproductive isolation. Using individual whole-genome sequencing from clinal sampling sites, we find that hybridization occurs within a narrow zone - just a few hundred meters long - at the transition between lake and stream habitat. Individuals in this contact zone exhibit strongly bimodal genome-wide ancestry, with a rapid shift toward the stream ecotypes genomic background, consistent with strong selection against lake-derived alleles in the stream habitat. Individual-based simulations tailored to this system demonstrate that divergent ecological selection alone can maintain the observed sharp cline, and illustrate the sustained antagonism between gene flow and selection near the habitat transition. Our findings underscore the power of ecological divergence to generate and maintain reproductive isolation, even in the absence of historical separation, and motivate further empirical work on the ecological underpinnings of steep hybrid zones.