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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.
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Genetic Variants Underlying Plasticity in Natural Populations of Spadefoot Toads: Environmental Assessment versus Phenotypic Response
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.
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- Award ID(s):
- 2306276
- PAR ID:
- 10537800
- Publisher / Repository:
- Genes / MDPI
- Date Published:
- Journal Name:
- Genes
- Volume:
- 15
- Issue:
- 5
- ISSN:
- 2073-4425
- Page Range / eLocation ID:
- 611
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/genes15050611
