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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.
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Morphological novelty emerges from pre-existing phenotypic plasticity
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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- Award ID(s):
- 1753865
- PAR ID:
- 10097184
- Date Published:
- Journal Name:
- Nature ecology & evolution
- Volume:
- 2
- ISSN:
- 2397-334X
- Page Range / eLocation ID:
- 1289-1297
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/https://doi.org/10.1038/s41559-018-0601-8
