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Plasticity-first evolution (PFE) posits that novel features arise when selection refines pre-existing phenotypic plasticity into an adaptive phenotype. However, PFE is controversial because few tests have been conducted in natural populations. Here we present evidence that PFE fostered the origin of an evolutionary novelty that allowed certain amphibians to invade a new niche—a distinctive carnivore morph. We compared morphology, gene expression and growth of three species of spadefoot toad tadpoles when reared on alternative diets: Scaphiopus holbrookii, which (like most frogs) never produce carnivores; Spea multiplicata, which sometimes produce carnivores, but only through diet-induced plasticity; and Spea bombifrons, which often produce carnivores regardless of diet. Consistent with PFE, we found diet-induced plasticity—in morphology and gene expression—in Sc. holbrookii, adaptive refinement of this plasticity in Sp. multiplicata, and further refinement of the carnivore phenotype in Sp. bombifrons. Generally, phenotypic plasticity might play a significant, if underappreciated, role in evolutionary innovation.
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An experimental investigation of how intraspecific competition and phenotypic plasticity can promote the evolution of novel, complex phenotypes
Intraspecific competition has long been considered a key driver of evolutionary diversification, but whether it can also promote evolutionary innovation is less clear. We examined the interplay between competition and phenotypic plasticity in fueling the origins of a novel, complex phenotype––a distinctive carnivore morph found in spadefoot toad tadpoles (genus Spea) that specializes on fairy shrimp. We specifically sought to explore the possible origins of this phenotype by providing shrimp to Scaphiopus holbrookii tadpoles (the sister genus to Spea that does not produce carnivores) while subjecting them to competition for their standard diet of detritus. Previous research had shown that this species will eat shrimp when detritus is limited, and that these shrimp-fed individuals produce features that are redolent of a rudimentary Spea carnivore. In this study, we found that: 1) behavioral and morphological plasticity enabled some individuals to expand their diet to include shrimp; 2) there was heritable variation in this plasticity; and 3) individuals received a growth and development benefit by eating shrimp. Thus, novel resource use can arise via plasticity as an adaptive response to intraspecific competition. More generally, our results show how competition and plasticity may interact to pave the way for the evolution of complex, novel phenotypes, such as the distinctive carnivore morph in present-day Spea.
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- Award ID(s):
- 1753865
- PAR ID:
- 10166602
- Date Published:
- Journal Name:
- Biological journal of the Linnean Society
- Volume:
- in press
- ISSN:
- 1095-8312
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Developmental plasticity can occur at any life stage, but plasticity that acts early in development may give individuals a competitive edge later in life. Here, we asked if early (pre-feeding) exposure to a nutrient-rich resource impacts hatchling morphology in Mexican spadefoot toad tadpoles, Spea multiplicata . A distinctive carnivore morph can be induced when tadpoles eat live fairy shrimp. We investigated whether cues from shrimp––detected before individuals are capable of feeding––alter hatchling morphology such that individuals could potentially take advantage of this nutritious resource once they begin feeding. We found that hatchlings with early developmental exposure to shrimp were larger and had larger jaw muscles––traits that, at later stages, increase a tadpole's competitive ability for shrimp. These results suggest that early developmental stages can assess and respond to environmental cues by producing resource-use phenotypes appropriate for future conditions. Such anticipatory plasticity may be an important but understudied form of developmental plasticity.more » « less
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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
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Ecological character displacement is considered crucial in promoting diversification, yet relatively little is known of its underlying mechanisms. We examined whether evolutionary shifts in gene expression plasticity (‘genetic accommodation’) mediate character displacement in spadefoot toads. Where Spea bombifrons and S. multiplicata occur separately in allopatry (the ancestral condition), each produces alternative, diet-induced, larval ecomorphs: omnivores, which eat detritus, and carnivores, which specialize on shrimp. By contrast, where these two species occur together in sympatry (the derived condition), selection to minimize competition for detritus has caused S. bombifrons to become nearly fixed for producing only carnivores, suggesting that character displacement might have arisen through an extreme form of genetic accommodation (‘genetic assimilation’) in which plasticity is lost. Here, we asked whether we could infer a signature of this process in regulatory changes of specific genes. In particular, we investigated whether genes that are normally expressed more highly in one morph (‘biased’ genes) have evolved reduced plasticity in expression levels among S. bombifrons from sympatry compared to S. bombifrons from allopatry. We reared individuals from sympatry vs. allopatry on detritus or shrimp and measured the reaction norms of nine biased genes. Although different genes displayed different patterns of gene regulatory evolution, the combined gene expression profiles revealed that sympatric individuals had indeed lost the diet-induced gene expression plasticity present in allopatric individuals. Our data therefore pro- vide one of the few examples from natural populations in which genetic accommodation/assimilation can be traced to regulatory changes of specific genes. Such genetic accommodation might mediate character displacement in many systems.more » « less
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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.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/biolinnean/blaa095
