Abstract
Two major goals of laboratory evolution experiments are to integrate from genotype to phenotype to fitness, and to understand the genetic basis of adaptation in natural populations. Here we demonstrate that both goals are possible by re-examining the outcome of a previous laboratory evolution experiment in which the bacteriophage G4 was adapted to high temperatures. We quantified the evolutionary changes in the thermal reaction norms—the curves that describe the effect of temperature on the growth rate of the phages—and decomposed the changes into modes of biological interest. Our analysis indicated that changes in optimal temperature accounted for almost half of the evolutionary changes in thermal reaction norm shape, and made the largest contribution toward adaptation at high temperatures. Genome sequencing allowed us to associate reaction norm shape changes with particular nucleotide mutations, and several of the identified mutations were found to be polymorphic in natural populations. Growth rate measures of natural phage that differed at a site that contributed substantially to adaptation in the lab indicated that this mutation also underlies thermal reaction norm shape variation in nature. In combination, our results suggest that laboratory evolution experiments may successfully predict the genetic bases of evolutionary responses to temperature in nature. The implications of this work for viral evolution arise from the fact that shifts in the thermal optimum are characterized by tradeoffs in performance between high and low temperatures. Optimum shifts, if characteristic of viral adaptation to novel temperatures, would ensure the success of vaccine development strategies that adapt viruses to low temperatures in an attempt to reduce virulence at higher (body) temperatures.
Highlights
The study of evolutionary responses to temperature has served as an important model for understanding the process of adaptation to novel environments [1], in part because the evolutionary and mechanistic causes of thermal adaptation are relatively transparent
Responses to Selection at High Temperature To determine the consequences of adaptation to high temperature, we measured the growth rate of the ancestral phage and three evolved phages at six temperatures between 27 8C and 44 8C (Figure 3)
The evolved genotypes were isolated from the Holder and Bull [20] evolving population after the 20th, 50th, and 100th serial transfers at high temperature, and a visual inspection of the data indicates that evolution occurred between each of these time points (Figure 3A)
Summary
The study of evolutionary responses to temperature has served as an important model for understanding the process of adaptation to novel environments [1], in part because the evolutionary and mechanistic causes of thermal adaptation are relatively transparent. Most of the studies that did observe trade-offs stand out because they measured performance at five or more temperatures across the entire thermal niche [7,8,9,10,11,12,13]. Few of these studies were sufficiently powerful to describe the nature of the genetic constraint governing the trade-off [8,10]
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