Adaptive Evolution Is Common in Rapid Evolutionary Radiations

Bruno Nevado,Edgar L.Y Wong,Owen G Osborne,Dmitry A Filatov

doi:10.1016/j.cub.2019.07.059

Abstract

One of the most long-standing and important mysteries in evolutionary biology is why biological diversity is so unevenly distributed across space and taxonomic lineages. Nowhere is this disparity more evident than in the multitude of rapid evolutionary radiations found on oceanic islands and mountain ranges across the globe [1-5]. The evolutionary processes driving these rapid diversification events remain unclear [6-8]. Recent genome-wide studies suggest that natural selection may be frequent during rapid evolutionary radiations, as inferred from work in cichlid fish [9], white-eye birds [10], new world lupins [11], and wild tomatoes [12]. However, whether frequent adaptive evolution is a general feature of rapid evolutionary radiations remains untested. Here we show that adaptive evolution is significantly more frequent in rapid evolutionary radiations compared to background levels in more slowly diversifying lineages. This result is consistent across a wide range of angiosperm lineages analyzed: 12 evolutionary radiations, which together comprise 1,377 described species, originating from some of the most biologically diverse systems on Earth. In addition, we find a significant negative correlation between population size and frequency of adaptive evolution in rapid evolutionary radiations. A possible explanation for this pattern is that more frequent adaptive evolution is at least partly driven by positive selection for advantageous mutations that compensate for the fixation of slightly deleterious mutations in smaller populations.

Highlights

IntroductionTo test whether adaptive evolution is a common feature of evolutionary radiations, we estimate the genome-wide frequency of adaptive evolution occurring across 12 rapid evolutionary radiations of angiosperms (Figure 1; Table S1) and compare these estimates to background values obtained in previous studies [11, 17]
An alternative way to understand the role of natural selection in rapid diversification is to quantify the extent to which natural selection drives evolution in these systems and, in particular, ask whether adaptive evolution is more common in lineages that diversify rapidly compared to those that do not
To test whether adaptive evolution is a common feature of evolutionary radiations, we estimate the genome-wide frequency of adaptive evolution occurring across 12 rapid evolutionary radiations of angiosperms (Figure 1; Table S1) and compare these estimates to background values obtained in previous studies [11, 17]

Summary

Introduction

To test whether adaptive evolution is a common feature of evolutionary radiations, we estimate the genome-wide frequency of adaptive evolution occurring across 12 rapid evolutionary radiations of angiosperms (Figure 1; Table S1) and compare these estimates to background values obtained in previous studies [11, 17]. We focus on evolutionary radiations from some of the most species-rich biodiversity hotspots in the world (the Andes, the Rockies, the Himalayas, Hawaii, and the Canary Islands), including both oceanic island chains and large mountain ranges—geographic regions that have long fascinated evolutionary biologists due to the unparalleled abundance of rapidly diversifying lineages of many different taxonomic groups [1,2,3]. For each evolutionary radiation analyzed, we obtained fresh tissue for RNA extraction from multiple species from different Botanic Gardens throughout the UK (Table S1), with the exception of Lupinus and Schiedea, for which plants were grown from seed in greenhouses in Oxford.

Methods

Results

Conclusion