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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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Plasticity-led evolution: evaluating the key prediction of frequency-dependent adaptation
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.
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- Award ID(s):
- 1753865
- PAR ID:
- 10097185
- Date Published:
- Journal Name:
- Proceedings of the Royal Society of London. Series B, Biological sciences
- Volume:
- 286
- ISSN:
- 0080-4649
- Page Range / eLocation ID:
- 20182754
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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.more » « less
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Increasing evidence suggests that many novel traits might have originated via plasticity-led evolution (PLE). Yet, little is known of the developmental processes that underpin PLE, especially in its early stages. One such process is ‘phenotypic accommodation’, which occurs when, in response to a change in the environment, an organism experiences adjustments across variable parts of its phenotype that improve its fitness. Here, we asked if environmentally induced changes in gene expression are enhanced or reversed during phenotypic accommodation of a novel, complex phenotype in spadefoot toad tadpoles ( Spea multiplicata ). More genes than expected were affected by both the environment and phenotypic accommodation in the liver and brain. However, although phenotypic accommodation primarily reversed environmentally induced changes in gene expression in liver tissue, it enhanced these changes in brain tissue. Thus, depending on the tissue, phenotypic accommodation may either minimize functional disruption via reversal of gene expression patterns or promote novelty via enhancement of existing expression patterns. Our study thereby provides insights into the developmental origins of a novel phenotype and the incipient stages of PLE.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/https://doi.org/10.1098/rspb.2018.2754
