Gene reuse facilitates rapid radiation and independent adaptation to diverse habitats in the Asian honeybee

Abstract

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.

Tachykinin signaling inhibits task-specific behavioral responsiveness in honeybee workers

“…Although AML and ACC are close relatives with similar basic biology, some behavioral differences have evolved since their speciation [78]. AML and ACC share the age-based division of labor, with younger bees specializing on nursing before maturing to foraging activities [79] and ACC foragers also specialize in nectar or pollen collection [28,80] similar to AML [27]. Accordingly, we found the main differences of stimulus responsiveness and TRPs expression among worker phenotypes conserved.…”

“…Moreover, foragers often specialize on collecting only one of the principal food sources, pollen or nectar [27]. Specialized nurses, nectar foragers and pollen foragers are also found in the closely-related Eastern honeybee, Apis cerana [28], thus offering a suitable parallel system for our study.…”

“…Neuropeptides mediate pheromonal effects on physiology [41,42] and usually exhibit a high degree of specificity [43,44]. Therefore, neuropeptides are prime candidates for mediating the independent adjustment of socially relevant response thresholds and they have been implicated in honeybee worker specialization and division of labor [28,45].…”

“…More than 100 mature neuropeptides derived from 22 protein precursors have been identified in the Western honeybee, Apis mellifera [46,47]. Several neuropeptides, including allatostatin, leucokinin, and tachykinin-related peptides (TRPs), may be involved in the control of social behavior of A. mellifera and the closely related A. cerana, such as aggression [48], foraging [28,45], brood care [46], and possibly a wide array of other behaviors [49].…”

Leucokinins: Multifunctional Neuropeptides and Hormones in Insects and Other Invertebrates

“…However, since orthologs of LKRs have been identified in five sequenced bee genomes, it is likely that LK signaling is present in these hymenopterans, but not in ants [62,72]. In support of the importance of LK signaling in honeybees, a recent paper showed that the lkr gene influences labor division in foraging for pollen and nectar in the Asian honeybee (Apis cerana) [73].…”