The Asian honeybee, Apis cerana, is one of the only two extant honeybee species that have successfully expanded their range from Asian tropical to the temperate region. Its widespread range has largely overlapped with Asia’s major agricultural region, therefore making significant pollination contribution to the humans. Our recent study on the mainland A. cerana indicated that the current population structure and distribution pattern is a result of repeated range expansions and retractions, in response to climatic oscillation of the ice age. In particular, the common ancestral population has independently invaded distant valleys of the eastern and southern Himalayans, establishing local populations adaptive to mountain habitats. A shared morphological change among mountain honeybees is the convergent elevation of body pigmentation. Although generally assumed as an adaptation to low temperature, it remains unclear how does the darkened coloration improve the fitness of individual foragers and the entire colony, and what the underlying molecular mechanism is. Here we employed 3 pairs of mountain-plain A. cerana populations and ask: 1) how does darkened body coloration benefit the species at low temperature? 2) whether the same genes are responsible for the convergent morphological change and how could natural selection repeatedly work on the same trait/gene? We showed that the darkened foragers increased body temperature more rapidly under rising ambient temperature, and eventually reached a higher balanced temperature. In addition, common garden experiments demonstrated that heat lost during foraging was significantly decreased in darkened foragers, which in-turn improved thermal regulation of the colony. Comparative genomics analyses suggested that the mycC gene, an ortholog of ebony, was repeatedly selected among the 3 independent mountain populations. The expression pattern of mycC was in concordance with the pigmentation process during pupal development. And mycC RNAi led to apparent increase in body darkness, confirming its role in shaping body coloration. Further fine screening of the mycC sequences revealed that selection signals were condensed either in its upstream regulation region or the coding region, in varied populations. These results indicated that the mountain honeybees had evolved improved capability in maintaining colony temperature via darkened body coloration of individual foragers. This parallel adaptive trait was enabled by natural selection independently operating on varied region of the same pigmentation gene.
What forces shape you? The genomics toward the dark side