Abstract

BackgroundMutation accumulation (MA) has profound ecological and evolutionary consequences. One example is that accumulation of conditionally neutral mutations leads to fitness trade-offs among heterogenous habitats which cause population divergence. Here we suggest that temperature, which controls the rates of all biochemical and biophysical processes, should play a crucial role for determining mutational effects. Particularly, warmer temperatures may mitigate the effects of some, not all, deleterious mutations and cause stronger environmental dependence in MA effects.ResultsWe experimentally tested the above hypothesis by measuring the growth performance of ten Escherichia coli genotypes on six carbon resources across ten temperatures, where the ten genotypes were derived from a single ancestral strain and accumulated spontaneous mutations. We analyzed resource dependence of MA consequences for growth yields. The MA genotypes typically showed reduced growth yields relative to the ancestral type; and the magnitude of reduction was smaller at intermediate temperatures. Stronger resource dependence in MA consequences for growth performance was observed at higher temperatures. Specifically, the MA genotypes were more likely to show impaired growth performance on all the six carbon resources when grown at lower temperatures; but suffered growth performance loss only on some, not all the six, carbon substrates at higher temperatures.ConclusionsHigher temperatures increase the chance that MA causes conditionally neutral fitness effects while MA is more likely to cause fitness loss regardless of available resources at lower temperatures. This finding has implications for understanding how geographic patterns in population divergence may emerge, and how conservation practices, particularly protection of diverse microhabitats, may mitigate the impacts of global warming.

Highlights

  • Mutation accumulation (MA) has profound ecological and evolutionary consequences

  • Relative growth performance scores of the mutation accumulation (MA) genotypes were typically negative, suggesting that MA genotypes generally showed reduced, not increased, growth yields compared with the ancestral type (Figs. 1, 2; Additional file 1: Table S1; note that no relationship was found between the number of base-pair substitutions and growth performance; Additional file 1: Tables S2 and S3)

  • Relative growth performance differed among genotypes (Figs. 1, 2; linear mixed-effect model, χ29,522 = 1213.076, P < 2 × ­10–16), and carbon resources (χ25,522 = 27.880, P = 4 × ­10–5)

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Summary

Introduction

Mutation accumulation (MA) has profound ecological and evolutionary consequences. One example is that accumulation of conditionally neutral mutations leads to fitness trade-offs among heterogenous habitats which cause population divergence. While the comparisons between benign and obviously stressful environments (involving factors such as antibiotics, temperature, osmolarity and pH) are clearcut, it remains poorly understood how prevalent environmental dependence in MA effects is on a finer scale of environmental heterogeneity. This question is crucial for understanding the evolution of fitness trade-offs among natural populations which are often located in relatively benign environments with only subtle differences, e.g., in substitutable resources [24, 25]. We suggest that temperature, which controls the rates of all biochemical and biophysical processes, should play a crucial role for determining mutational effects, and the environment-dependence of MA effects. Note that our hypothesis is based on temperature effects on rate-limiting processes; and it may hold for’normal’ temperature ranges that natural populations are typically faced with [33, 34], but not stressfully high temperatures where protein thermal stability, instead of the rates of physiological processes, may determine growth performance [35,36,37]

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