Rapid genome-wide evolution in Brassica rapa populations following drought revealed by sequencing of ancestral and descendant gene pools.

Steven J. Franks,Silas Tittes,Nolan C. Kane,Joshua S. Rest,Niamh B. O'Hara

doi:10.1111/mec.13615

Abstract

There is increasing evidence that evolution can occur rapidly in response to selection. Recent advances in sequencing suggest the possibility of documenting genetic changes as they occur in populations, thus uncovering the genetic basis of evolution, particularly if samples are available from both before and after selection. Here, we had a unique opportunity to directly assess genetic changes in natural populations following an evolutionary response to a fluctuation in climate. We analysed genome‐wide differences between ancestors and descendants of natural populations of Brassica rapa plants from two locations that rapidly evolved changes in multiple phenotypic traits, including flowering time, following a multiyear late‐season drought in California. These ancestor‐descendant comparisons revealed evolutionary shifts in allele frequencies in many genes. Some genes showing evolutionary shifts have functions related to drought stress and flowering time, consistent with an adaptive response to selection. Loci differentiated between ancestors and descendants (F ST outliers) were generally different from those showing signatures of selection based on site frequency spectrum analysis (Tajima's D), indicating that the loci that evolved in response to the recent drought and those under historical selection were generally distinct. Very few genes showed similar evolutionary responses between two geographically distinct populations, suggesting independent genetic trajectories of evolution yielding parallel phenotypic changes. The results show that selection can result in rapid genome‐wide evolutionary shifts in allele frequencies in natural populations, and highlight the usefulness of combining resurrection experiments in natural populations with genomics for studying the genetic basis of adaptive evolution.

Highlights

With climate change and habitat loss threatening the viability of many species worldwide, understanding the ability of species to cope with these changes is crucial
This approach offers some distinct advantages over indirect methods of detecting signatures of selection such as those based on site frequency spectrum analyses, in situations in which evolutionary changes are expected to result from selection acting on standing genetic variation rather than new or very low-frequency mutations
We investigated the genetic basis of these documented contemporary evolutionary changes through direct comparisons of predrought (1997) ancestral and postdrought (2004) descendant gene pools in two southern California populations of B. rapa

Summary

Introduction

With climate change and habitat loss threatening the viability of many species worldwide, understanding the ability of species to cope with these changes is crucial. We still know little about the genetic basis of contemporary adaptive evolutionary changes over time in natural populations (Rokas & Abbot 2009), in part because the genotypes of ancestral populations are typically unknown One solution to this problem is to combine genomics with resurrection experiments to study evolution. Combining resurrection experiments with genomics is ideal for assessing the degree to which genetic responses to selection are parallel or divergent in different populations, which is a long-standing question in evolution (Stern & Orgogozo 2009). Despite these advantages, genomics has previously only been combined with resurrection experiments in studies of laboratory populations, such as Drosophila melanogaster (Burke et al 2010) and Escherichia coli (Blank et al 2014)

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