Extensive introgression at late stages of species formation: Insights from grasshopper hybrid zones

The process of species formation is characterised by the accumulation of multiple reproductive barriers. The evolution of hybrid male sterility, or Haldane's rule, typically characterises later stages of species formation, when total reproductive isolation is strongest. Yet, understanding how quickly reproductive barriers evolve and their consequences for maintaining genetic boundaries between emerging species remains a challenging task because it requires studying taxa that hybridise in nature. Here, we address these questions using the meadow grasshopper Pseudochorthippus parallelus, where populations that show multiple reproductive barriers, including hybrid male sterility, hybridise in two natural hybrid zones. Using mitochondrial data, we infer that such populations have diverged some 100,000 years ago, at the beginning of the last glacial cycle in Europe. Nuclear data shows that contractions at multiple glacial refugia, and post-glacial expansions have facilitated genetic differentiation between lineages that today interact in hybrid zones. We find extensive introgression throughout the sampled species range, irrespective of current strength of reproductive isolation. Populations exhibiting hybrid male sterility in two hybrid zones show repeatable patterns of genomic differentiation, consistent with shared genomic constraints affecting ancestral divergence or with the role of those regions in reproductive isolation. Together, our results suggest that reproductive barriers that characterise late stages of species formation can evolve relatively quickly within species, particularly when associated with strong demographic changes. Moreover, we show that such barriers persist in the face of extensive gene flow, allowing future studies to identify associated genomic regions.Funding provided by: H2020 Marie Skłodowska-Curie ActionsCrossref Funder Registry ID: http://dx.doi.org/10.13039/100010665Award Number: No. 658706Funding provided by: Deutsche ForschungsgemeinschaftCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100001659Award Number: HA7255/2-612-1Funding provided by: Ministerio de Ciencia e InnovaciónCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100004837Award Number: PID2019 - 104952GB - I00/AEI/10.13039/5011000110