Considerable gene flow in troglomorphic cockroach species across a vast subterranean landscape

Aim: There has been growing interest in non-cave subterranean habitats and their influence on the evolution of troglomorphic (i.e. ‘subterranean adapted’) species. Studies on the diversification of aquatic subterranean organisms in these habitats generally support the ‘subterranean island’ hypothesis, whereby isolated subterranean refuges lead to patterns of short-range endemism. However, their terrestrial counterparts have received less attention. We aimed to elucidate the applicability of the ‘subterranean island’ hypothesis to terrestrial subterranean fauna through genetic analyses of two widespread troglomorphic cockroach species. To investigate the influence of subterranean biogeography, we also analysed a closely related species that inhabits ‘classic’ cave environments to represent a contrasting biogeographic comparison. Location: Pilbara region, Western Australia, and the Chillagoe-Mungana Caves, Queensland (Australia). Taxa: Cave cockroach species: Nocticola cockingi, Nocticola quartermainei and Nocticola australiensis. Methods: We used DArTseq to generate genome-wide SNPs in 78 samples, and Sanger sequencing to generate 16S mtDNA data. We then applied various population genomic analyses to characterize the distribution of genetic diversity within the three study species. Results: We identified distinct genetic clusters within the two Pilbara species; however, there appeared to be a notable lack of discernible population differentiation across large parts of their range (>135 km), opposing the subterranean island hypothesis. The highest level of population differentiation in the three study species was between the two caves in Queensland, ~3 km apart. Main Conclusions: The Pilbara subterranean habitat appeared to be conducive to gene flow across relatively large distances, contrasting high levels of endemism observed in other subterranean taxa within the region. The disparate patterns of gene flow among the Pilbara and Queensland study species emphasize the significance of differing subterranean habitats on patterns of dispersal and vicariance. These inferences will inform conservation genetic management of these species, and may help elucidate the evolutionary paradox of widespread subterranean fauna.