Genomic analysis of Asian honeybee populations in China reveals evolutionary relationships and adaptation to abiotic stress

Abstract

The geographic and biological diversity of China has resulted in the differential adaptation of the eastern honeybee, <i>Apis cerana</i>, to these varied habitats. <i>A. cerana</i> were collected from 14 locations in China. Their genomes were sequenced, and nucleotide polymorphisms were identified at more than 9 million sites. Both STRUCTURE and principal component analysis placed the bees into seven groups. Phylogenomic analysis groups the honeybees into many of the same clusters with high bootstrap values (91%-100%). Populations from Tibet and South Yunnan are sister taxa and together represent the earliest diverging lineage included in this study. We propose that the evolutionary origin of <i>A. cerana</i> in China was in the southern region of Yunnan Province and expanded from there into the southeastern regions and into the northeastern mountain regions. The Cold-Temperate West Sichuan Plateau and Tropical Diannan populations were compared to identify genes under adaptive selection in these two habitats. Pathway enrichment analysis showing genes under selection, including the Hippo signaling pathway, GABAergic pathway, and trehalose-phosphate synthase, indicates that most genes under selection pressure are involved in the process of signal transduction and energy metabolism. qRT-PCR analysis reveals that one gene under selection, the <i>AcVIAAT</i> gene, involved in the GABAergic pathway, is responding to cold temperature stress. Through homologous recombination, we show that the <i>AcVIAAT</i> gene is able to replace the <i>CNAG_</i>01904 gene in the fungus <i>Cryptococcus neoformans</i> and that it makes the fungus less sensitive to conditions of oxidative stress and variations in temperature. Our results contribute to our understanding of the evolutionary origin of <i>A. cerana</i> in China and the molecular basis of environmental adaptation.