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.