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.
Human overexploitation of natural resources has placed conservation and management as one of the most pressing challenges in modern societies, particularly regarding highly vulnerable marine ecosystems. Although a large effort has been made to design Marine Protected Areas (MPAs) worldwide, it is still unclear how many species actually exist in these MPAs, what is the genetic connectivity between areas with different protective regimes, and what is their relative genetic diversity. We answer these questions using morphologically cryptic species of the genus Mugil that are sympatric in the largest MPA in the Tropical Southwestern marine province. Population structure analyses show the existence of five highly divergent species (FST > 0.855) and no genetic divergence between two estuaries with different protection status (FST = 0.005). Sympatric individuals are assigned to single clusters and show strong concordance among hundreds of independent gene trees, consistent with full reproductive isolation and no ancestral nor ongoing hybridization. Differences of genetic diversity within species suggest that effective population sizes differ up to two-fold, probably reflecting differences in the magnitude of population expansions during the evolutionary history of these species, rather than recent impact of fisheries. Together, our results suggest that designing MPAs with areas of integral protection in between areas where fisheries are permitted could be an effective way to manage cryptic species that cannot have species-specific quotas. More generally, this work shows a cost-efficient approach that is transferable to other marine or terrestrial organisms of special concern, helping to implement science-based regulations for management and conservation.