Understanding highland adaptation of Apis cerana through repeated while independent colonization

Understanding the genetic basis of polygenic adaptation is challenging. Populations that undergo parallel evolution serve as experimental replications enabling the study of molecular mechanism. Apis cerana is widely-distributed in Asia and has repeatedly colonized the Qinghai-Tibet Plateau. The highland populations are derived from lowland colonies while showed not admixture with each other, representing independent events of colonization. We investigated resequencing genomes of five populations to study the genetic basis of highland adaptation in A. cerana. Using two complementary methods, we isolated genes with adaptive signals in each lineage. Although large proportion of adaptive loci are unique to each population, most potentially adaptive polymorphism shared with genetic variation in lowland populations, consistent with widespread signals of soft selection sweeps. Whereas parallelism was low at the level of adaptive loci, it was greater for functional pathways and greatest for phenotypes. Further enrichment analysis found the shared adaptive loci were overrepresented in pathways related to the development of sensory system and body morphogenesis. These highly connected pathways and loci could buffer different genetic paths and maintain developmental stability. Adaptive signals in the development-related loci suggest stabilizing selection further drive phenotypic convergence under similar stress. However, lineage-specific loci and pathways facilitated adaptive divergence in each lineage within the broadly similar highland environment. Our results demonstrate the genetic redundancy of highland adaptation and lineage-specific evolution via independent colonization in A. cerana. This underscores that predicting a populations adaptive potential requires understanding its full adaptive architecture within the ecological context--including abiotic and biotic interactions.