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Morphological novelty emerges from pre-existing phenotypic plasticity

Abstract

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: Scaphiopusholbrookii, 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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Fig. 1: How plasticity can facilitate the evolution of a novel, complex phenotype.
Fig. 2: Ecology and evolution of the spadefoot toad resource-use polyphenism.
Fig. 3: Diet-induced morphological plasticity of Sc.holbrookii and Sp.multiplicata.
Fig. 4: Diet-induced gene expression plasticity in Sc.holbrookii and Sp.multiplicata.
Fig. 5: Evidence of refinement of the carnivore phenotype among wild-caught tadpoles of different lineages.

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Acknowledgements

We thank W. Zhang and K. O’Donnell for assistance with animal care, A. Serrato-Capuchina for help collecting tadpoles, and K. Pfennig, I. Ehrenreich, C. Ledón-Rettig, D. Matute, C. Martin, R. Martin and A. Levis for comments on the manuscript. Funding was provided by the National Science Foundation grants DEB-1643239 and DEB-1753865.

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N.A.L. and D.W.P. conceived and designed the study; N.A.L. and A.J.I. collected data; N.A.L. analysed the data; N.A.L. and D.W.P. wrote the manuscript. Photos in Figs. 2,3 were taken by D.W.P. All authors discussed the results and commented on the manuscript.

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Correspondence to Nicholas A. Levis.

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Levis, N.A., Isdaner, A.J. & Pfennig, D.W. Morphological novelty emerges from pre-existing phenotypic plasticity. Nat Ecol Evol 2, 1289–1297 (2018). https://doi.org/10.1038/s41559-018-0601-8

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