Drivers of genomic differentiation landscapes in populations of disparate ecological and geographical settings within mainland Apis cerana

Abstract Elucidating the evolutionary processes that drive population divergence can enhance our understanding of the early stages of speciation and inform conservation management decisions. The honeybee Apis cerana displays extensive population divergence, providing an informative natural system for exploring these processes. The mainland lineage A. cerana includes several peripheral subspecies with disparate ecological and geographical settings radiated from a central ancestor. Under this evolutionary framework, we can explore the patterns of genome differentiation and the evolutionary models that explain them. We can also elucidate the contribution of non‐genomic spatiotemporal mechanisms (extrinsic features) and genomic mechanisms (intrinsic features) that influence these genomic differentiation landscapes. Based on 293 whole genomes, a small part of the genome is highly differentiated between central–peripheral subspecies pairs, while low and partial parallelism partly reflects idiosyncratic responses to environmental differences. Combined elements of recurrent selection and speciation‐with‐gene‐flow models generate the heterogeneous genome landscapes. These elements weight differently between central‐island and other central–peripheral subspecies pairs, influenced by glacial cycles superimposed on different geomorphologies. Although local recombination rates exert a significant influence on patterns of genomic differentiation, it is unlikely that low‐recombination rates regions were generated by structural variation. In conclusion, complex factors including geographical isolation, divergent ecological selection and non‐uniform genome features have acted concertedly in the evolution of reproductive barriers that could reduce gene flow in part of the genome and facilitate the persistence of distinct populations within mainland lineage of A. cerana .