A recent publication in Nature Communications goes above and beyond in studying how selection on adaptive and/or maladaptive gene expression plasticity may be regulating thermal tolerance in urban anoles. The importance of plasticity in the colonization of new environments is a widely-accepted argument, however, the role of plasticity in facilitating adaptive evolution remains controversial. Plasticity may facilitate novel habitat colonization via phenotypic expression that results in high fitness without the action of natural selection (i.e., “perfect plasticity”), or alternatively plasticity may be insufficient and natural selection may act to further modify the phenotype towards an adaptive optimum (i.e., “evolved plasticity”) (Fig 1). This new study hypothesizes that ancestral variation in thermal tolerance gene expression plasticity acts as the raw materials for adaptive selection. They predicted a scenario of “evolved plasticity” with selection on the underlying genetic variation for adaptive changes and selection against the variation for maladaptive changes in the genomic regulatory system.
Fig 1. Evolution of plasticity in novel environments. Phenotypic plasticity can influence the evolutionary outcome for a population colonizing a novel environment. Ancestral plasticity may move the initial phenotype of a population (x) in any number of directions with respect to the local optimum of the novel environment (adaptive peak, y). These variable responses are adaptive when they move phenotypic values directly into (A) or close to—but outside —the peak y. If sufficient genetic variation is exposed, natural selection can reinforce adaptive plasticity and move phenotypic means towards the new peak (B; dotted lines). However, natural selection is not expected when plasticity puts individuals directly onto the new peak (A). In the case of maladaptive plasticity (C), inappropriate responses to the novel environment move individuals away from the peak, reducing fitness. Selection should reduce/reverse the reaction norm and restore the phenotypic mean back to the original ancestral value. In all cases, the strength of selection increases with distance from the peak (dotted lines in B, C). Based on Fig. 2 in Ghalambor et al. 2007. Figure from primary study.
A history of parallel thermal selection
A previous study by these authors published in Nature Ecology & Evolution 2020 found parallel adaptation of forest anoles to multiple urban heat islands in Puerto Rico. They identified increased heat tolerance in urban Anolis cristatellus and genome-wide signatures of selection associated with thermal tolerance repeated across four urban-forest population pairs. In this new study, the authors sought to describe how natural selection acted on regulatory variation to shape the evolution of thermal plasticity in these populations.
Using gene expression data from both wild-caught and common garden animals from forest and urban habitats across four municipalities in Puerto Rico, they characterized gene expression responses to an acute thermal challenge as adaptive (appropriate response – better thermal tolerance) and maladaptive (inappropriate response – worse thermal tolerance). They used this categorization of changes in gene expression for the remainder of the study to better understand how natural selection acts on adaptive versus maladaptive plasticity. However, because they included animals that were reared in wild conditions, these gene expression patterns include both genetically based differences as well as developmental plasticity and phenotypic flexibility.
Figure 6B. Bar graph representing the number of genes displaying adaptive vs. maladaptive plasticity in common garden lineages from the forest (green) and urban (gray) habitats. Among genes associated with heat tolerance, urban lineages possess a significantly larger proportion displaying adaptive plasticity and a significantly lower proportion than displaying maladaptive plasticity in response to increased temperature. Asterisks represent the degree of significance (equality of proportions test within habitat types, exact binomial test between habitat types: *p < 0.05, ***p < 0.001). Figure from primary study.
Selection on gene expression plasticity
Considering forest populations to be reflective of an ancestral population response with greater historical underlying variation, they found lower heat tolerances and substantially more maladaptive plasticity compared to urban anoles with more canalized expression responses as a result of selection. Analyzing the signatures of polygenic selection in genes associated with heat tolerance, the study showed greater genetic divergence in maladaptive SNPs than adaptive SNPs. This result suggests natural selection may be acting more strongly to reverse the maladaptive responses than to reinforce adaptive responses. Additionally, they suggest different mechanisms of selection on adaptive and maladaptive plasticity, with coding regions as the targets for selection on adaptive plasticity and cis-regulatory regions as targets for selection against maladaptive plasticity. Together, they conclude that there is evidence of selection for reduced and reversed heat-induced maladaptive plasticity in adaptive urban lineages.
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Related Studies:
- Is Plastic Always Fantastic? Selection on Thermal Plasticity in Urban Anoles - December 7, 2021
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