Whole-genome resequencing reveals genetic evolution of honeybees (Apis cerana) in high-altitude and overwintering adaptation.

Abstract

Over time, populations of Apis cerana across diverse geographical regions have undergone distinct phenotypic adaptations in response to varied climates, arising from prolonged natural evolutionary processes. Understanding the molecular genetic underpinnings and the implications of climate change on the adaptive evolution of A. cerana is crucial for its conservation amidst environmental shifts. Here, we conducted a comprehensive analysis of 110 bee individuals sourced from 11 regions at comparable temperatures, environments, and altitudes. A total of 525.56 Gb of filter-trimmed sequencing data were utilised for population genetic analysis of honeybees. The findings indicate genetic differentiation among bee populations from various geographical regions, with higher levels of population divergence observed in different altitudinal environments. Particularly noteworthy is the significant genetic divergence of the bee population from Haikou (HK) compared to populations in other areas, characterised by higher inbreeding coefficients and runs of homozygosity (ROHs), as well as lower nucleotide diversity. However, populations from Guangzhou (GZ), Jinzhai (JZ), Qimen (QM), Shennongjia (SNJ), and Suzhou (SZ) exhibit a close genetic relationship. Using comparisons across multiple bee populations from different groups, we identified selective signatures across different environmental temperatures and altitudes. Furthermore, by integrating genomic selection signals with comparative transcriptomic analysis, we identified genes potentially involved in bee adaptation to high altitude, such as g9950.t1 (alcohol dehydrogenase), g5267.t1 (diacylglycerol kinase theta-like isoform 2), gene g4025.t1 (Tyrosine 3-monooxygenase), and g3609.t1 (heme oxygenase). Our results indicate that both temperature and altitude contribute to the genetic differentiation and geographical adaptability of A. cerana populations.