Geological events and climate change drive diversification and speciation of mute cicadas in eastern continental Asia

Abstract

The poor mobility of nymphs living underground, usually for many years, and the weak flying ability of adults make cicadas unique for evolutionary biology and bio-geographical study. Cicadas of the genus Karenia are unusual in Cicadidae in lacking the timbals that produce sound. Population differentiation, genetic structure, dispersal and evolutionary history of the eastern Asian mute cicada Karenia caelatata were investigated based on morphological, acoustic and molecular data. The results reveal a high level of genetic differentiation in this species. Six independent clades with nearly unique sets of haplotypes corresponding to geographically isolated populations are recognized. Genetic and geographic distances are significantly correlated among lineages. The phenotypic differentiation is generally consistent with the high levels of genetic divergence across populations. Results of ecological niche modeling suggest that the potential distribution range of this mountain-habitat specialist during the Last Glacial Maximum was broader than its current range, indicating this species had benefited from the climate change during the early Pleistocene in southern China. Geological events such as orogeny in Southwest China and Pleistocene climate oscillations have driven the differentiation and divergence of this species, and basins, plains and rivers function as natural "barriers" to block the gene flow. Besides significant genetic divergence being found among clades, the populations occurring in the Wuyi Mountains and the Hengduan Mountains are significantly different in the calling song structure from other populations. This may have resulted from significant population differentiation and subsequent adaptation of related populations. We conclude that ecological differences in habitats, coupled with geographical isolation, have driven population divergence and allopatric speciation. This study provides a plausible example of incipient speciation in Cicadidae and improves understanding of population differentiation, acoustic signal diversification and phylogeographic relationships of this unusual cicada species. It informs future studies on population differentiation, speciation and phylogeography of other mountain-habitat insects in the East Asian continent.

Keywords: Acoustic signals; Allopatric speciation; Cicadidae; Geographical isolation; Mountain-habitat insects; Phylogeography.