Comparative phylogeography of two hemipteran species (Geisha distinctissima and Megacopta cribraria) in the Zhoushan Archipelago of China reveals contrasting genetic structures despite concordant historical demographies

Abstract

Continental islands are useful models to explore the roles of shared historical factors in the evolution of sympatric species. However, China’s largest continental group of islands, the Zhoushan Archipelago, was neglected by most studies focusing on biodiversity hotspots. Here we investigated the phylogeographic patterns and the historical demography of two sympatric hemipteran insects (Geisha distinctissima and Megacopta cribraria), which shared historical factors in the Zhoushan Archipelago. The results based on mtDNA (COX1, COX2-COX3, and CYTB) and nDNA (28S and ITS2) showed that G. distinctissima diverged into three genetic lineages (L1–L3) ~8.9–13.7 thousand years ago (kya), which coincided with the period of island isolation. However, the three lineages exhibit no clear phylogeographic patterns for frequent asymmetrical gene flow (starting around 5\u2009kya) from the mainland and adjacent islands to other distant islands due to subsequent human activities. In contrast, only one genetic lineage exists for M. cribraria, without any phylogeographic structures. The ancestral range in the mainland as well as in neighboring islands, together with the frequent asymmetrical gene flow of M. cribraria (from the mainland and neighboring islands to more distant islands) within the last 5000 years suggests that human activities may have lead to the colonization of this species in the Zhoushan Archipelago. The contrasting genetic structures indicate shared historical factors but independent evolutionary histories for the two sympatric species in the Zhoushan Archipelago. Our demographic analysis clearly showed that both species underwent population expansion before 5\u2009kya during the post-LGM (Last Glacial Maximum), which indicates that the two species shared concordant historical demographies. This result suggests that the population size of the two species was affected similarly by the climatic oscillations of post-LGM in Eastern China. Together, our findings reveal that the two insect species in the Zhoushan Archipelago exhibit contrasting genetic structures despite concordant historical demographies, which provides an important framework for the exploration of the evolution patterns of sympatric species in the continental island.