Slower environmental change hinders adaptation from standing genetic variation.

Thiago S Guzella,Ivo M Chelo,Veronica F Pereira,Henrique Teotónio,Stephen R Proulx,Ania Pino-Querido,Snigdhadip Dey

doi:10.1371/journal.pgen.1007731

Abstract

Evolutionary responses to environmental change depend on the time available for adaptation before environmental degradation leads to extinction. Explicit tests of this relationship are limited to microbes where adaptation usually depends on the sequential fixation of de novo mutations, excluding standing variation for genotype-by-environment fitness interactions that should be key for most natural species. For natural species evolving from standing genetic variation, adaptation at slower rates of environmental change may be impeded since the best genotypes at the most extreme environments can be lost during evolution due to genetic drift or founder effects. To address this hypothesis, we perform experimental evolution with self-fertilizing populations of the nematode Caenorhabditis elegans and develop an inference model to describe natural selection on extant genotypes under environmental change. Under a sudden environmental change, we find that selection rapidly increases the frequency of genotypes with high fitness in the most extreme environment. In contrast, under a gradual environmental change selection first favors genotypes that are worse at the most extreme environment. We demonstrate with a second set of evolution experiments that, as a consequence of slower environmental change and thus longer periods to reach the most extreme environments, genetic drift and founder effects can lead to the loss of the most beneficial genotypes. We further find that maintenance of standing genetic variation can retard the fixation of the best genotypes in the most extreme environment because of interference between them. Taken together, these results show that slower environmental change can hamper adaptation from standing genetic variation and they support theoretical models indicating that standing variation for genotype-by-environment fitness interactions critically alters the pace and outcome of adaptation under environmental change.

Highlights

With human activities contributing to climate change [1], it has become urgent to pinpoint the ecological and evolutionary mechanisms by which natural populations adapt at different rates of environmental change
Some genotypes might be initially favored but disfavored and overtaken by other genotypes that are better at more extreme environments if they were not lost by genetic drift or founder effects in the meantime. We addressed this idea with experimental evolution in Caenorhabditis elegans populations with standing variation for genotype-by-environment fitness interactions and by developing a model to describe natural selection on extant genotypes during experimental evolution
All populations were derived from a single ancestor population adapted for 140 generations to lab conditions (25 mM NaCl), after initial hybridization of several wild isolates [19], that has abundant genetic diversity but where individual hermaphrodites reproduce exclusively by self-fertilization

Summary

Introduction

With human activities contributing to climate change [1], it has become urgent to pinpoint the ecological and evolutionary mechanisms by which natural populations adapt at different rates of environmental change. Most species in nature have small populations, are genetically structured by geography, breeding mode or reproduction system, and might have long generation times. In all these cases, adaptation to changing environments will likely depend on standing genetic variation, and less so on de novo mutation [11, 12]. Adaptation will depend on standing genotype-by-environment (GxE) fitness variance [11], until de novo mutations or new recombinant genotypes escape genetic drift and start to be selected upon [15]

Methods

Results

Discussion

Conclusion