Genomic Signature of Adaptive Divergence despite Strong Nonadaptive Forces on Edaphic Islands: A Case Study of Primulina juliae

Abstract

Both genetic drift and divergent selection are expected to be strong evolutionary forces driving population differentiation on edaphic habitat islands. However, the relative contribution of genetic drift and divergent selection to population divergence has rarely been tested simultaneously. In this study, restriction-site associated DNA-based population genomic analyses were applied to assess the relative importance of drift and divergent selection on population divergence of Primulina juliae, an edaphic specialist from southern China. All populations were found with low standing genetic variation, small effective population size (NE), and signatures of bottlenecks. Populations with the lowest genetic variation were most genetically differentiated from other populations and the extent of genetic drift increased with geographic distance from other populations. Together with evidence of isolation by distance, these results support neutral drift as a critical evolutionary driver. Nonetheless, redundancy analysis revealed that genomic variation is significantly associated with both edaphic habitats and climatic factors independently of spatial effects. Moreover, more genomic variation was explained by environmental factors than by geographic variables, suggesting that local adaptation might have played an important role in driving population divergence. Finally, outlier tests and environment association analyses identified 31 single-nucleotide polymorphisms as candidates for adaptive divergence. Among these candidates, 26 single-nucleotide polymorphisms occur in/near genes that potentially play a role in adaptation to edaphic specialization. This study has important implications that improve our understanding of the joint roles of genetic drift and adaptation in generating population divergence and diversity of edaphic specialists.

Keywords: Primulina juliae; adaptation; edaphic specialist; isolation by distance; isolation by environment; population genomics.