Tectonic movements and monsoons facilitate the spatio-temporal species diversification of a herbivore lineage

The Hengduan Mountains (HDM) harbor high species diversity that has been linked with the Cenozoic geodiversity, including active orogenesis and dramatic climate changes. However, our understanding of species diversification patterns in the Mesozoic remains limited. The superfamily Eriophyoidea comprises over 5,000 named species, representing an ancient group of strictly herbivorous mites that can be traced back to the Triassic. In this study, we reconstructed a robust dated phylogenetic tree with 301 eriophyoid mite species, covering six biogeographical regions in China, to explore the diversification mechanism. We found multiple dispersal events among six regions, showing high rates in the Mesozoic while low rates in the Cenozoic. These results are partly in contrast to flora and fauna, which showed high interbioregional dispersal rates between the Tibet-Himalaya-Hengduan and adjacent regions in the Cenozoic. The HDM was inferred as a primary source region of eriophyoid mites and served as museum and cradle. Furthermore, the high diversification of eriophyoid mites is strongly associated with colonization, in situ speciation, and vicariance. These events were likely driven by the Qinling-Dabie orogeny, Yanshan orogeny, the uplifts of HDM, and the establishment of the monsoon system. Moreover, both paleotemperature and elevation have an impact on their diversification. The eriophyoid mite lineage has undergone a rapid diversification since the Cretaceous, which is contemporaneous with the angiosperm radiation. In conclusion, this study illustrates how extant herbivorous mites in regional diversification have been shaped by paleogeographic and paleoclimatic events throughout the Mesozoic to the Cenozoic periods.