Rowan D. H. Barrett

Natural Selection on a Major Armor Gene in Threespine Stickleback

Experimental estimates of the effects of selection on genes determining adaptive traits add to our understanding of the mechanisms of evolution. We measured selection on genotypes of the Ectodysplasin locus, which underlie differences in lateral plates in threespine stickleback fish. A derived allele (low) causing reduced plate number has been fixed repeatedly after marine stickleback colonized freshwater from the sea, where the ancestral allele (complete) predominates. We transplanted marine sticklebacks carrying both alleles to freshwater ponds and tracked genotype frequencies over a generation. The low allele increased in frequency once lateral plates developed, most likely via a growth advantage. Opposing selection at the larval stage and changing dominance for fitness throughout life suggest either that the gene affects additional traits undergoing selection or that linked loci also are affecting fitness.

Rapid evolution of cold tolerance in stickleback

Climate change is predicted to lead to increased average temperatures and greater intensity and frequency of high and low temperature extremes, but the evolutionary consequences for biological communities are not well understood. Studies of adaptive evolution of temperature tolerance have typically involved correlative analyses of natural populations or artificial selection experiments in the laboratory. Field experiments are required to provide estimates of the timing and strength of natural selection, enhance understanding of the genetics of adaptation and yield insights into the mechanisms driving evolutionary change. Here, we report the experimental evolution of cold tolerance in natural populations of threespine stickleback fish (Gasterosteus aculeatus). We show that freshwater sticklebacks are able to tolerate lower minimum temperatures than marine sticklebacks and that this difference is heritable. We transplanted marine sticklebacks to freshwater ponds and measured the rate of evolution after three generations in this environment. Cold tolerance evolved at a rate of 0.63 haldanes to a value 2.5°C lower than that of the ancestral population, matching values found in wild freshwater populations. Our results suggest that cold tolerance is under strong selection and that marine sticklebacks carry sufficient genetic variation to adapt to changes in temperature over remarkably short time scales.

Experimental Evolution of Pseudomonas fluorescens in Simple and Complex Environments

In complex environments that contain several substitutable resources, lineages may become specialized to consume only one or a few of them. Here we investigate the importance of environmental complexity in determining the evolution of niche width over ∼900 generations in a chemically defined experimental system. We propagated 120 replicate lines of the bacterium Pseudomonas fluorescens in environments of different complexity by using between one and eight carbon substrates in each environment. Genotypes from populations selected in complex environments evolved greater mean and variance in fitness than those from populations selected in simple environments. Thus, lineages were able to adapt to several substrates simultaneously without any appreciable loss of function with respect to other substrates present in the media. There was greater genetic and genotype‐by‐environment interaction variance for fitness within populations selected in complex environments. It is likely that genetic variance in populations grown on complex media was maintained because the identity of the fittest genotype varied among carbon substrates. Our results suggest that evolution in complex environments will result neither in narrow specialists nor in complete generalists but instead in overlapping imperfect generalists, each of which has become adapted to a certain range of substrates but not to all.

Environment specific pleiotropy facilitates divergence at the Ectodysplasin locus in threespine stickleback.

Adaptive radiation occurs when divergent natural selection in different environments leads to phenotypic differentiation. The pleiotropic effects of underlying genes can either promote or constrain this diversification. Identifying the pleiotropic effects of genes responsible for divergent traits, and testing how the environment influences these effects, can therefore help to provide an understanding of how ecology drives evolutionary change between populations. Positive selection on low-armor alleles at the Ectodysplasin (Eda) locus in threespine stickleback has led to the repeated evolution of reduced armor in populations following freshwater colonization by fully armored marine sticklebacks. Here, we demonstrate that Eda has environmentally determined pleiotropic effects on armor and growth. When raised in freshwater, reduced armor sticklebacks carrying “low” alleles at Eda had increased growth rate relative to fully armored sticklebacks carrying “complete” alleles. In saltwater treatments this growth advantage was present during juvenile growth but lost during adult growth, suggesting that in this environment stickleback are able to develop full armor plates without sacrificing overall growth rate. The environment specific pleiotropic effects of Eda demonstrate that ecological factors can mediate the influence of genetic architecture in driving phenotypic evolution. Furthermore, because size is important for mate choice in stickleback, the growth rate differences influenced by Eda may have effects on reproductive isolation between marine and freshwater populations.

Natural selection and the genetics of adaptation in threespine stickleback

Growing knowledge of the molecular basis of adaptation in wild populations is expanding the study of natural selection. We summarize ongoing efforts to infer three aspects of natural selection—mechanism, form and history—from the genetics of adaptive evolution in threespine stickleback that colonized freshwater after the last ice age. We tested a mechanism of selection for reduced bony armour in freshwater by tracking genotype and allele frequency changes at an underlying major locus (Ectodysplasin) in transplanted stickleback populations. We inferred disruptive selection on genotypes at the same locus in a population polymorphic for bony armour. Finally, we compared the distribution of phenotypic effect sizes of genes underlying changes in body shape with that predicted by models of adaptive peak shifts following colonization of freshwater. Studies of the effects of selection on genes complement efforts to identify the molecular basis of adaptive differences, and improve our understanding of phenotypic evolution.

Mutations of intermediate effect are responsible for adaptation in evolving Pseudomonas fluorescens populations

The fixation of a beneficial mutation represents the first step in adaptation, and the average effect of such mutations is therefore a fundamental property of evolving populations. It is nevertheless poorly characterized because the rarity of beneficial mutations makes it difficult to obtain reliable estimates of fitness. We obtained 68 genotypes each containing a single fixed beneficial mutation from experimental populations of Pseudomonas fluorescens, evolving in medium with serine as the sole carbon source and estimated the selective advantage of each by competition with the ancestor. The distribution of selection coefficients is modal and closely resembles the Weibull distribution. The average selection coefficient (2.1) and beneficial mutation rate (3.8×10−8) are high relative to previous studies, possibly because the ancestral population grows poorly in serine-limited medium. Our experiment suggests that the initial stages of adaptation to stressful environments will involve the substitution of mutations with large effect on fitness.

Gene expression plasticity evolves in response to colonization of freshwater lakes in threespine stickleback.

Phenotypic plasticity is predicted to facilitate individual survival and/or evolve in response to novel environments. Plasticity that facilitates survival should both permit colonization and act as a buffer against further evolution, with contemporary and derived forms predicted to be similarly plastic for a suite of traits. On the other hand, given the importance of plasticity in maintaining internal homeostasis, derived populations that encounter greater environmental heterogeneity should evolve greater plasticity. We tested the evolutionary significance of phenotypic plasticity in coastal British Columbian postglacial populations of threespine stickleback (Gasterosteus aculeatus) that evolved under greater seasonal extremes in temperature after invading freshwater lakes from the sea. Two ancestral (contemporary marine) and two derived (contemporary freshwater) populations of stickleback were raised near their thermal tolerance extremes, 7 and 22 °C. Gene expression plasticity was estimated for more than 14 000 genes. Over five thousand genes were similarly plastic in marine and freshwater stickleback, but freshwater populations exhibited significantly more genes with plastic expression than marine populations. Furthermore, several of the loci shown to exhibit gene expression plasticity have been previously implicated in the adaptive evolution of freshwater populations, including a gene involved in mitochondrial regulation (PPARAa). Collectively, these data provide molecular evidence that highlights the importance of plasticity in colonization and adaptation to new environments.

INTERACTIVE EFFECTS OF GENOTYPE, ENVIRONMENT, AND ONTOGENY ON RESISTANCE OF CUCUMBER (Cucumis sativus) TO THE GENERALIST HERBIVORE, Spodoptera exigua

Host-plant genotype, environment, and ontogeny all play a role in determining plant resistance to herbivory, yet little is known about the nature of the interactions among these factors. We investigated resistance of cucumber plants Cucumis sativus to the generalist herbivore Spodoptera exigua in a manipulative experiment involving three factors. In particular, we tested the effects of bitter (cucurbitacins present) vs. sweet (cucurbitacins absent) plants (genotype), with or without previous herbivory (environment), and cotyledons vs. true leaves (ontogeny). Contrary to our expectations, S. exigua growth was 54% higher on bitter plants than on sweet plants; growth was 63% higher, however, on undamaged plants compared to damaged plants, and 59% higher on true leaves compared to cotyledons. Moreover, all two-way interaction terms between genotype, environment, and ontogeny were significant. For example, S. exigua performance was higher on bitter than on sweet plants; however, this effect was strongly influenced by whether the tissue consumed was a cotyledon or true leaf and also whether it had been previously damaged. An examination of leaf nutritional chemistry revealed that some of our results could be explained by genotypic, environmental, and ontogenic differences in foliar nitrogen content. In contrast, the cucurbitacin content of plants did not appear to affect caterpillar growth. Our results provide evidence for the importance of interactions between genotype, environment, and ontogeny in determining herbivory and illustrate the value of manipulative experiments in revealing the complexities of these interactions.

Predicting Responses to Contemporary Environmental Change Using Evolutionary Response Architectures

Rapid environmental change currently presents a major threat to global biodiversity and ecosystem functions, and understanding impacts on individual populations is critical to creating reliable predictions and mitigation plans. One emerging tool for this goal is high-throughput sequencing technology, which can now be used to scan the genome for signs of environmental selection in any species and any system. This explosion of data provides a powerful new window into the molecular mechanisms of adaptation, and although there has been some success in using genomic data to predict responses to selection in fields such as agriculture, thus far genomic data are rarely integrated into predictive frameworks of future adaptation in natural populations. Here, we review both theoretical and empirical studies of adaptation to rapid environmental change, focusing on areas where genomic data are poised to contribute to our ability to estimate species and population persistence and adaptation. We advocate for the need to study and model evolutionary response architectures, which integrate spatial information, fitness estimates, and plasticity with genetic architecture. Understanding how these factors contribute to adaptive responses is essential in efforts to predict the responses of species and ecosystems to future environmental change.

Should I stay or should I go? The Ectodysplasin locus is associated with behavioural differences in threespine stickleback.

Adaptive divergence may be facilitated if morphological and behavioural traits associated with local adaptation share the same genetic basis. It is therefore important to determine whether genes underlying adaptive morphological traits are associated with variation in behaviour in natural populations. Positive selection on low-armour alleles at the Ectodysplasin (Eda) locus in threespine stickleback has led to the repeated evolution of reduced armour, following freshwater colonization by fully armoured marine sticklebacks. This adaptive divergence in armour between marine and freshwater populations would be facilitated if the low allele conferred a behavioural preference for freshwater environments. We experimentally tested whether the low allele is associated with preference for freshwater by measuring the preference of each Eda genotype for freshwater versus saltwater after acclimation to either salinity. We found no association between the Eda low allele and preference for freshwater. Instead, the low allele was significantly associated with a reduced preference for the acclimation environment. This behaviour may facilitate the colonization of freshwater habitats from the sea, but could also hinder local adaptation by promoting migration of low alleles between marine and freshwater environments.