Animals with recent shared ancestry frequently adapt in parallel to new but similar habitats, a process often underlined by repeated selection of the same genes. Yet, in contrast, few examples have demonstrated the significance of gene reuse in colonization of multiple disparate habitats. By analyzing 343 genomes of the widespread Asian honeybee, Apis cerana, we showed that multiple peripheral subspecies radiated from a central ancestral population and adapted independently to diverse habitats. We found strong evidence of gene reuse in the Leucokinin receptor (Lkr), which was repeatedly selected in almost all peripheral subspecies. Differential expression and RNA interference knockdown revealed the role of Lkr in influencing foraging labor division, suggesting that Lkr facilitates collective tendency for pollen/nectar collection as an adaptation to floral changes. Our results suggest that honeybees may accommodate diverse floral shifts during rapid radiation through fine-tuning individual foraging tendency, a seemingly complex process accomplished by gene reuse.

Background: Exploration of adaptive evolution of organisms in response to environmental change can help to understand the evolutionary history of species and the underlying mechanisms of adaptation to local environments, thus guiding future conservation programmes. Before the introduction of Apis mellifera in China, eastern honey bees (Apis cerana) were the only species used for beekeeping in this region. In the mountains of Changbai, populations of A. cerana are considered a distinct ecotype of the species which formed through the distinct selective pressures in this area over time. Result: We performed a measure of 300 wing specimens of eastern honey bees and obtained the geometric morphological variation in the wing of A. cerana in Changbai Mountain. A total of 3,859,573 high-quality SNP loci were yielded via the whole-genome resequencing of 130 individuals in 5 geographic regions. Conclusion: Corresponding geometric morphology and population genomics confirmed the particularity of the A. cerana in Changbai Mountain. Genetic differentiation at the subspecies level exists between populations in Changbai Mountain and remaining geographic regions, and a significant reduction in the effective population size and an excessive degree of inbreeding may be responsible for a substantial loss of population genetic diversity. Candidate genes potentially associated with cold environmental adaptations in populations under natural selection were identified, which may represent local adaptations in populations. Our study provided insights into the evolutionary history and adaptation of A. cerana in Changbai Mountain, as well as its conservation.

Honey bees, Apis mellifera , have for millennia been managed and exploited by humans and introduced into most suitable regions worldwide. However, given the lack of records for many introduction events, treating A. mellifera populations as native would predictably bias genetic studies regarding origin and evolution. Here, we used the Dongbei bee, a well-documented population, introduced beyond the natural distribution range approximately 100 years ago, to elucidate the effects of local domestication on animal population genetic analyses. Strong domestication pressure was detected in this population, and the genetic divergence between Dongbei bee and its ancestral subspecies was found to have occurred at the lineage level. Results of phylogenetic and time divergence analyses could consequently be misinterpreted. Proposing new subspecies or lineages and performing analyses of origin should thus strive to eliminate anthropogenic effects. We highlight the need for definitions of landrace and breed in honey bee sciences and make preliminary suggestions.

Background: Apis cerana is widely distributed in China and, prior to the introduction of western honeybees, was the only bee species kept in China. During the long-term natural evolutionary process, many unique phenotypic variations have occurred among A. cerana populations in different geographical regions under varied climates. Understanding the molecular genetic basis and the effects of climate change on the adaptive evolution of A. cerana can promote A. cerana conservation in face of climate change and allow for the effective utilization of its genetic resources. Result: To investigate the genetic basis of phenotypic variations and the impact of climate change on adaptive evolution, A. cerana workers from 100 colonies located at similar geographical latitudes or longitudes were analyzed. Our results revealed an important relationship between climate types and the genetic variation of A. cerana in China, and a greater influence of latitude compared with longitude was observed. Upon selection and morphometry analyses combination for populations under different climate types, we identified a key gene RAPTOR, which was deeply involved in developmental processes and influenced the body size. Conclusion: The selection of RAPTOR at the genomic level during adaptive evolution could allow A. cerana to actively regulate its metabolism, thereby fine-tuning body sizes in response to harsh conditions caused by climate change, such as food shortages and extreme temperatures, which may partially elucidate the size differences of A. cerana populations. This study provides crucial support for the molecular genetic basis of the expansion and evolution of naturally distributed honeybee populations.

The health of the western honeybee, Apis mellifera, the most crucial pollinator, has been challenged globally over the past decades. An ectoparasitic mite, Varroa destructor, together with the viruses it vectored, is generally regarded as the vital pathogenic agent. Although the poor health status of A. mellifera compared to its eastern counterpart, Apis cerana, has been broadly identified, the underlying mechanism remains poorly understood and comparison between susceptible and resistant hosts will potentially ameliorate this predicament. Here, we investigated the impacts of two widespread viruses—deformed wing virus type A (DWV-A) and Israeli acute paralysis virus (IAPV), mediated by V. destructor mite, on the capped developing honeybee brood, in the absence of adult workers, of A. mellifera and A. cerana, with positive and negative controls. Our results demonstrated that the endogenous viruses imposed limited damage on the hosts even if the brood was wounded. In contrast, the exogenous viruses introduced by ectoparasites triggered variable mortality of the infested brood between host species. Intriguingly, death causes of both honeybee species presented a similar trend: the acute IAPV generally causes morbidity and mortality of late larvae, while the chronic DWV-A typically leads to brood mortality during and after pupation. Notably, the susceptible immature A. cerana individuals, supported by higher observed mortality and a lower virus tolerance, serve the interests of the colony and foster the overall survival of a resistant honeybee superorganism. These results improve our understanding of the interactions between viruses carried by ectoparasites and their developing hosts, and the novel insight of weak individuals fostering strong colonies may promote breeding efforts to mitigate the indefensible colony losses globally.