Mountain speciation driven by high rates of lineage formation and rapid evolution of partial reproductive isolation: insights from a recent radiation of grasshoppers (Orthoptera: Gomphocerinae)

Abstract Mountains contribute disproportionately to global biodiversity, yet the ecological and evolutionary processes that make them important centres of speciation remain poorly understood. Here, we use a complex of Gomphocerinae grasshoppers distributed across the Pyrenees as a model system to investigate the process of speciation in mountain regions. Clustering analyses revealed a marked genetic fragmentation of populations and divergence time estimates indicated that all lineages split during the Pleistocene (<0.9 Mya). Although all taxa currently exhibit allopatric distributions, fine-scale temporal distribution modelling suggests that their ranges probably overlapped across extensive areas during glacial periods. Despite ample opportunities for historical hybridization, introgression tests indicate that gene flow was restricted to peripheral populations and only one population exhibited a high degree of admixed ancestry. Accordingly, our analyses reveal abrupt genetic discontinuities corresponding to the distributional boundaries of each taxon. Although taxa have probably not achieved complete reproductive isolation, semi-permeable species boundaries do not appear to have compromised their evolutionary independence. These results emphasize the interplay between high rates of lineage formation and the rapid evolution of reproductive barriers in promoting microgeographic speciation in topographically complex landscapes, shedding light on the proximate processes underlying the high levels of neo-endemism observed across mountain ranges worldwide.