Rapid Divergence Followed by Adaptation to Contrasting Ecological Niches of Two Closely Related Columbine Species Aquilegia japonica and A. oxysepala.

Ming-Rui Li,Ning Ding,Bao Liu,Hua-Ying Wang,Lin-Feng Li,Hong-Xing Xiao,Ye-Chao Huang,Tianyuan Lu,David Bryant

doi:10.1093/gbe/evz038

Abstract

Elucidating the mechanisms underlying the genetic divergence between closely related species is crucial to understanding the origin and evolution of biodiversity. The genus Aquilegia L. has undergone rapid adaptive radiation, generating about 70 well-recognized species that are specialized to distinct habitats and pollinators. In this study, to address the underlying evolutionary mechanisms that drive the genetic divergence, we analyzed the whole genomes of two ecologically isolated Aquilegia species, A. oxysepala and A. japonica as well as their putative hybrid. Our comparative genomic analyses reveal that while the two species diverged only recently and experienced recurrent gene flow, a high level of genetic divergence is observed in their nuclear genomes. In particular, candidate genomic regions that show signature of selection differ dramatically between the two species. Given that the splitting time of the two species is broadly matched with the decrease in effective population sizes, we propose that allopatric isolation together with natural selection have preceded the interspecific gene flow in the process of speciation. The observed high genetic divergence is likely an outcome of combined effects of natural selection, genetic drift and divergent sorting of ancestral polymorphisms. Our study provides a genome-wide view of how genetic divergence has evolved between closely related species.

Highlights

Unravelling the evolutionary mechanisms whereby the species arise and adapt to diverse environments is fundamental to understanding the origin and persistence of biodiversity (Schluter 2000; Coyne and Orr 2004; Nosil 2012)
The general view holds that closely related species are expected to show high level of genetic similarity because their recent divergence from a common ancestor, incomplete sorting of ancestral polymorphisms, and gene flow during and after the speciation (Nosil and Feder 2012; Seehausen et al 2014; Wolf and Ellegren 2017)
Population genomic analyses have demonstrated that the combination of ancient polymorphisms, gene flow, and natural selection has resulted in a heterogeneous pattern of genetic divergence among these finch species (Han et al 2017)

Summary

Introduction

Unravelling the evolutionary mechanisms whereby the species arise and adapt to diverse environments is fundamental to understanding the origin and persistence of biodiversity (Schluter 2000; Coyne and Orr 2004; Nosil 2012). A critical step in elucidating this issue is to determine how the genetic divergence evolved between incipient species and to what extent it caused the occurrence of reproductive isolation (RI) (Coyne and Orr 2004; Gavrilets 2004; Nosil and Feder 2012).

Methods

Results

Conclusion