Distribution pattern and radiation of the European subterranean genus Verhoeffiella (Collembola, Entomobryidae)

摘要

One of the most striking features of obligate subterranean species is their narrow distribution ranges. These prevail not only at specific, but often also at generic level. However, some subterranean genera have continental scale and disjunct distribution, which challenges their monophyly and questions the scenarios of their origin and colonization. In our study, we investigated the subterranean collembolan genus Verhoeffiella, currently known from five remote karst regions of Europe. Four nuclear and one mitochondrial genes were assembled to reveal the evolutionary history of the genus. We tested the monophyly of the genus, explored its relationship with putative surface relatives, and its temporal patterns of molecular diversification. The phylogeny revealed a complex relationship of Verhoeffiella with surface species Heteromurus nitidus and partially disentangled the biogeographical question of its disjunct distribution. Further on, several lineages of Verhoeffiella were recognized in the Dinarides, showing highly underestimated diversity and, compared with the number of described species, a sevenfold increase in the number of MOTUs. The radiation is relatively recent, with the events triggering the diversification linked to the Messinian salinity crisis and Pleistocene climatic shifts. The combination of this extensive subterranean radiation and close evolutionary links with epigean relatives makes Verhoeffiella an exceptional case within the subterranean fauna of temperate areas, which significantly contributes to our understanding of subterranean colonization and diversification patterns.