Gene reuse enabled rapid parallel diversification of the Asian honeybee

Honeybees are key pollinators with diverse diets, accustomed to a wide range of habitats that are characterized by variable flora. Many Apis species are, however, facing unprecedented challenges derived from habitat lost and diet change. In this context, it is critical to understand their evolutionary history and how they became adapted to diverse habitats, in particular diet shift caused by variable flowering phonologies. We hypothesize that the species have undergone parallel diversification to occupy the current distribution range and that during this evolutionary process, genes, in particular those responsible for foraging division, must have been repeatedly selected to adapt to new flora.

By sequencing over 300 Apis cerana genomes from the mainland lineage, we revealed that the current population structure is the result of a series of historical population contractions and expansions. Several independent peripheral populations diverged at a subspecies level have evolved parallelly from a common ancestral central population. Gene reuse is a common mechanism during the evolution of Apis cerana and one gene that has been constantly selected during population diversification, the Lkr gene, can directly regulate sucrose sensitivity of the honeybee worker, which is in turn associated with foraging task division.

Ji, Y.#, X. Li#, T. Ji*, J. Tang#, L. Qiu, J. Hu, J. Dong, S. Luo, S. Liu, P. B. Frandsen, X-G Zhou, S. H. Parey, Q. Niu*, and X. Zhou*. 2020. Gene reuse facilitates rapid radiation and independent adaptation to diverse habitats in the Asian honeybee. Science Advances 6(51): eabd3590. PDF

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.