Many organisms facultatively produce different phenotypes depending on their environment, yet relatively little is known about the genetic bases of such plasticity in natural populations. In this study, we describe the genetic variation underlying an extreme form of plasticity––resource polyphenism––in Mexican spadefoot toad tadpoles, Spea multiplicata. Depending on their environment, these tadpoles develop into one of two drastically different forms: a carnivore morph or an omnivore morph. We collected both morphs from two ponds that differed in which morph had an adaptive advantage and performed genome-wide association studies of phenotype (carnivore vs. omnivore) and adaptive plasticity (adaptive vs. maladaptive environmental assessment). We identified four quantitative trait loci associated with phenotype and nine with adaptive plasticity, two of which exhibited signatures of minor allele dominance and two of which (one phenotype locus and one adaptive plasticity locus) did not occur as minor allele homozygotes. Investigations into the genetics of plastic traits in natural populations promise to provide novel insights into how such complex, adaptive traits arise and evolve.
more »
« less
Assessment and the regulation of adaptive phenotypic plasticity
ABSTRACT Organisms can react to environmental variation by altering their phenotype, and such phenotypic plasticity is often adaptive. This plasticity contributes to the diversity of phenotypes across the tree of life. Generally, the production of these phenotypes must be preceded by assessment, where the individual acquires information about its environment and phenotype relative to that environment, and then determines if and how to respond with an alternative phenotype. The role of assessment in adaptive plasticity is, therefore, crucial. In this Review, we (1) highlight the need for explicitly considering the role of assessment in plasticity; (2) present two different models for how assessment and the facultative production of phenotypes are related; and (3) describe an overarching framework for how assessment evolves. In doing so, we articulate avenues of future work and suggest that explicitly considering the role of assessment in the evolution of plasticity is key to explaining how and when plasticity occurs. Moreover, we emphasize the need to understand the role of assessment in adaptive versus maladaptive plasticity, which is an issue that will become increasingly important in a rapidly changing world.
more »
« less
- PAR ID:
- 10612613
- Publisher / Repository:
- The Company of Biologists Ltd
- Date Published:
- Journal Name:
- Development
- Volume:
- 151
- Issue:
- 20
- ISSN:
- 0950-1991
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Dr Andrea E. A. Stephens (Ed.)To forecast extinction risks of natural populations under climate change and direct human impacts, an integrative understanding of both phenotypic plasticity and adaptive evolution is essential. To date, the evidence for whether, when, and how much plasticity facilitates adaptive responses in changing environments is contradictory. We argue that explicitly considering three key environmental change components – rate of change, variance, and temporal autocorrelation – affords a unifying framework of the impact of plasticity on adaptive evolution. These environmental components each distinctively effect evolutionary and ecological processes underpinning population viability. Using this framework, we develop expectations regarding the interplay between plasticity and adaptive evolution in natural populations. This framework has the potential to improve predictions of population viability in a changing world.more » « less
-
Fluctuating environmental conditions are ubiquitous in natural systems, and populations have evolved various strategies to cope with such fluctuations. The particular mechanisms that evolve profoundly influence subsequent evolutionary dynamics. One such mechanism is phenotypic plasticity, which is the ability of a single genotype to produce alternate phenotypes in an environmentally dependent context. Here, we use digital organisms (self-replicating computer programs) to investigate how adaptive phenotypic plasticity alters evolutionary dynamics and influences evolutionary outcomes in cyclically changing environments. Specifically, we examined the evolutionary histories of both plastic populations and non-plastic populations to ask: (1) Does adaptive plasticity promote or constrain evolutionary change? (2) Are plastic populations better able to evolve and then maintain novel traits? And (3), how does adaptive plasticity affect the potential for maladaptive alleles to accumulate in evolving genomes? We find that populations with adaptive phenotypic plasticity undergo less evolutionary change than non-plastic populations, which must rely on genetic variation from de novo mutations to continuously readapt to environmental fluctuations. Indeed, the non-plastic populations undergo more frequent selective sweeps and accumulate many more genetic changes. We find that the repeated selective sweeps in non-plastic populations drive the loss of beneficial traits and accumulation of maladaptive alleles, whereas phenotypic plasticity can stabilize populations against environmental fluctuations. This stabilization allows plastic populations to more easily retain novel adaptive traits than their non-plastic counterparts. In general, the evolution of adaptive phenotypic plasticity shifted evolutionary dynamics to be more similar to that of populations evolving in a static environment than to non-plastic populations evolving in an identical fluctuating environment. All natural environments subject populations to some form of change; our findings suggest that the stabilizing effect of phenotypic plasticity plays an important role in subsequent adaptive evolution.more » « less
-
Plasticity-led evolution occurs when a change in the environment triggers a change in phenotype via phenotypic plasticity, and this pre-existing plasticity is subsequently refined by selection into an adaptive phenotype. A critical, but largely untested prediction of plasticity-led evolution (and evolution by natural selection generally) is that the rate and magnitude of evolutionary change should be positively associated with a phenotype’s frequency of expression in a population. Essentially, the more often a phenotype is expressed and exposed to selection, the greater its opportunity for adaptive refinement. We tested this prediction by competing against each other spadefoot toad tadpoles from different natural populations that vary in how frequently they express a novel, environmentally induced carnivore ecomorph. As expected, laboratory-reared tadpoles whose parents were derived from populations that express the carnivore ecomorph more frequently were superior competitors for the resource for which this ecomorph is specialized—fairy shrimp. These tadpoles were better at using this resource both because they were more efficient at capturing and consuming shrimp and because they produced more exaggerated carnivore traits. Moreover, they exhibited these more carnivore-like features even without experiencing the inducing cue, suggesting that this ecomorph has undergone an extreme form of plasticity-led evolution—genetic assimilation. Thus, our findings provide evidence that the frequency of trait expression drives the magnitude of adaptive refinement, thereby validating a key prediction of plasticity-led evolution specifically and adaptive evolution generally.more » « less
-
Abstract Polyphenism—in which multiple distinct phenotypes are produced from a single genotype owing to differing environmental conditions—is commonplace, but its molecular bases are poorly understood. Here, we examine the transcriptomic bases of a polyphenism in Mexican spadefoot toads (Spea multiplicata). Depending on their environment, their tadpoles develop into either a default “omnivore” morph or a novel “carnivore” morph. We compared patterns of gene expression among sibships that exhibited high versus low production of carnivores when reared in conditions that induce the carnivore morph versus those that do not. We found that production of the novel carnivore morph actually involved changes in fewer genes than did the maintenance of the default omnivore morph in the inducing environment. However, only body samples showed this pattern; head samples showed the opposite pattern. We also found that changes to lipid metabolism (especially cholesterol biosynthesis) and peroxisome contents and function might be crucial for establishing and maintaining differences between the morphs. Thus, our findings suggest that carnivore phenotype might have originally evolved following the breakdown of robustness mechanisms that maintain the default omnivore phenotype, and that the carnivore morph is developmentally regulated by lipid metabolism and peroxisomal form, function, and/or signaling. This study also serves as a springboard for further exploration into the nature and causes of plasticity in an emerging model system.more » « less
An official website of the United States government

