Although the process of species formation is notoriously idiosyncratic,
the observation of pervasive patterns of reproductive isolation across
species pairs suggests that generalities, or “rules”, underlie species
formation in all animals. Haldane’s rule states that whenever a sex is
absent, rare or sterile in a cross between two taxa, that sex is usually
the heterogametic sex. Yet, understanding how Haldane’s rule first
evolves and whether it is associated to genome wide barriers to gene
flow remains a challenging task because this rule is usually studied in
highly divergent taxa that no longer hybridize in nature. Here, we
address these questions using the meadow grasshopper Pseudochorthippus
parallelus where populations that readily hybridize in two natural
hybrid zones show hybrid male sterility in laboratorial crosses. Using
mitochondrial data, we infer that such populations have diverged some
100,000 years ago, surviving multiple glacial periods in isolated
Pleistocenic refugia. Nuclear data shows that secondary contact has led
to extensive introgression throughout the species range, including
between populations showing hybrid male sterility. We find repeatable
patterns of genomic differentiation across the two hybrid zones, yet
such patterns are consistent with shared genomic constraints across taxa
rather than their role in reproductive isolation. Together, our results
suggest that Haldane’s rule can evolve relatively quickly within
species, particularly when associated to strong demographic changes. At
such early stages of species formation, hybrid male sterility still
permits extensive gene flow, allowing future studies to identify genomic
regions associated with reproductive barriers.