Abstract

Evolutionary adaptation to a constant environment is driven by the accumulation of mutations which can have a range of unrealized pleiotropic effects in other environments. These pleiotropic consequences of adaptation can influence the emergence of specialists or generalists, and are critical for evolution in temporally or spatially fluctuating environments. While many experiments have examined the pleiotropic effects of adaptation at a snapshot in time, very few have observed the dynamics by which these effects emerge and evolve. Here, we propagated hundreds of diploid and haploid laboratory budding yeast populations in each of three environments, and then assayed their fitness in multiple environments over 1000 generations of evolution. We find that replicate populations evolved in the same condition share common patterns of pleiotropic effects across other environments, which emerge within the first several hundred generations of evolution. However, we also find dynamic and environment-specific variability within these trends: variability in pleiotropic effects tends to increase over time, with the extent of variability depending on the evolution environment. These results suggest shifting and overlapping contributions of chance and contingency to the pleiotropic effects of adaptation, which could influence evolutionary trajectories in complex environments that fluctuate across space and time.

Highlights

  • As a population adapts to a given environment, it accumulates mutations that are beneficial in that environment, along with neutral and mildly deleterious ‘hitchhiker’ mutations

  • We evolved 20 haploid (MATα) yeast populations in YPD at 37°C; these are a subset of populations that did not autodiploidize from a larger haploid evolution experiment

  • Our results offer insight into how pleiotropic effects emerge and change on an evolutionary timescale

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Summary

Introduction

As a population adapts to a given environment, it accumulates mutations that are beneficial in that environment, along with neutral and mildly deleterious ‘hitchhiker’ mutations. R. Hall, Scanlan, and Buckling 2011; Duffy, Turner, and Burch 2006; Duffy, Burch, and Turner 2007; Jerison et al 2020; Li, Petrov, and Sherlock 2019; Leiby and Marx 2014) Pleiotropic fitness tradeoffs, such as those underlying specialization, can arise from either antagonistic pleiotropy (i.e., direct tradeoffs between the fitness effects of individual mutations across conditions), mutation accumulation (i.e., accumulation of mutations that are neutral in the evolution environment but impose fitness costs in other conditions), or some combination of these phenomena. Recent experimental and theoretical work has analyzed how these distributions of mutational effects across environments can lead to an interplay between chance and contingency in determining both the typical pleiotropic consequences of adaptation and the predictability of these effects (Jerison et al 2020; Ardell and Kryazhimskiy 2020)

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