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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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References

  1. Mayr, E. in Evolution after Darwin Vol. 1 (ed. Tax, S.) 349–380 (Univ. Chicago Press, Chicago, 1959).

  2. Wagner, G. P. & Lynch, V. J. Evolutionary novelties. Curr. Biol. 20, R48–R52 (2010).

    CAS  PubMed  Google Scholar 

  3. Schwander, T. & Leimar, O. Genes as leaders and followers in evolution. Trends Ecol. Evol. 26, 143–151 (2011).

    PubMed  Google Scholar 

  4. Santos, M. E., Le Bouquin, A., Crumière, A. J. J. & Khila, A. Taxon-restricted genes at the origin of a novel trait allowing access to a new environment. Science 358, 386–390 (2017).

    CAS  PubMed  Google Scholar 

  5. West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, New York, 2003).

  6. Moczek, A. P. et al. The role of developmental plasticity in evolutionary innovation. Proc. R. Soc. B 278, 2705–2713 (2011).

    PubMed  Google Scholar 

  7. Levis, N. A. & Pfennig, D. W. Evaluating ‘plasticity-first’ evolution in nature: key criteria and empirical approaches 31, 563–574. Trends Ecol. Evol. 31, 563–574 (2016).

    PubMed  Google Scholar 

  8. Wray, G. A. et al. Does evolutionary theory need a rethink? No, all is well. Nature 514, 161–164 (2014).

    PubMed  Google Scholar 

  9. Gilbert, S. F., Bosch, T. C. G. & Ledón-Rettig, C. Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents. Nat. Rev. Genet. 16, 611–622 (2015).

    CAS  PubMed  Google Scholar 

  10. Ghalambor, C. K., McKay, J. K., Carroll, S. P. & Reznick, D. N. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21, 394–407 (2007).

    Google Scholar 

  11. Standen, E. M., Du, T. Y. & Larsson, H. C. Developmental plasticity and the origin of tetrapods. Nature 513, 54–58 (2014).

    CAS  PubMed  Google Scholar 

  12. Ledón-Rettig, C. C., Pfennig, D. W. & Nascone-Yoder, N. Ancestral variation and the potential for genetic accommodation in larval amphibians: implications for the evolution of novel feeding strategies. Evol. Dev. 10, 316–325 (2008).

    PubMed  Google Scholar 

  13. Kulkarni, S. S., Denver, R. J., Gomez-Mestre, I. & Buchholz, D. R. Genetic accommodation via modified endocrine signalling explains phenotypic divergence among spadefoot toad species. Nat. Commun. 8, 993 (2017).

    PubMed  PubMed Central  Google Scholar 

  14. Badyaev, A. V. Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation. Proc. R. Soc. B 272, 877–886 (2005).

    PubMed  Google Scholar 

  15. Rutherford, S. L. & Lindquist, S. Hsp90 as a capacitor for morphological evolution. Nature 396, 336–342 (1998).

    CAS  PubMed  Google Scholar 

  16. Ghalambor, C. K. et al. Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature 525, 372–375 (2015).

    CAS  PubMed  Google Scholar 

  17. Scheiner, S. M. Genetics and evolution of phenotypic plasticity. Annu. Rev. Ecol. Syst. 24, 35–68 (1993).

    Google Scholar 

  18. Scheiner, S. M. Selection experiments and the study of phenotypic plasticity. J. Evol. Biol. 15, 889–898 (2002).

    Google Scholar 

  19. Pfennig, D. W. Polyphenism in spadefoot toad tadpoles as a locally adjusted evolutionarily stable strategy. Evolution 46, 1408–1420 (1992).

    PubMed  Google Scholar 

  20. Wells, K. D. The Ecology and Behavior of Amphibians (Univ. Chicago Press, Chicago, 2007).

  21. Pfennig, D. W. The adaptive significance of an environmentally-cued developmental switch in an anuran tadpole. Oecologia 85, 101–107 (1990).

    PubMed  Google Scholar 

  22. Levis, N. A., de la Serna Buzon, S. & Pfennig, D. W. An inducible offense: carnivore morph tadpoles induced by tadpole carnivory. Ecol. Evol. 5, 1405–1411 (2015).

    PubMed  PubMed Central  Google Scholar 

  23. Pfennig, D. W. & Murphy, P. J. How fluctuating competition and phenotypic plasticity mediate species divergence. Evolution 56, 1217–1228 (2002).

    PubMed  Google Scholar 

  24. Pfennig, D. W. & Murphy, P. J. A test of alternative hypotheses for character divergence between coexisting species. Ecology 84, 1288–1297 (2003).

    Google Scholar 

  25. Pfennig, D. W. & Martin, R. A. Evolution of character displacement in spadefoot toads: different proximate mechanisms in different species. Evolution 64, 2331–2341 (2010).

    PubMed  Google Scholar 

  26. Ledón-Rettig, C. C., Pfennig, D. W. & Crespi, E. J. Diet and hormonal manipulation reveal cryptic genetic variation: implications for the evolution of novel feeding strategies. Proc. R. Soc. B 277, 3569–3578 (2010).

    PubMed  Google Scholar 

  27. Zeng, C., Gomez-Mestre, I. & Wiens, J. J. Evolution of rapid development in spadefoot toads is unrelated to arid environments. PLoS ONE 9, e96637 (2014).

    PubMed  PubMed Central  Google Scholar 

  28. Gomez-Mestre, I. & Buchholz, D. R. Developmental plasticity mirrors differences among taxa in spadefoot toads linking plasticity and diversity. Proc. Natl Acad. Sci. USA 103, 19021–19026 (2006).

    CAS  PubMed  Google Scholar 

  29. McDiarmid, R. W. & Altig, R. Tadpoles: The Biology of Anuran Larvae (Univ. Chicago Press, Chicago, 1999).

  30. Leichty, A. R., Pfennig, D. W., Jones, C. D. & Pfennig, K. S. Relaxed genetic constraint is ancestral to the evolution of phenotypic plasticity. Integr. Comp. Biol. 52, 16–30 (2012).

    PubMed  PubMed Central  Google Scholar 

  31. Levis, N. A., Serrato-Capuchina, A. & Pfennig, D. W. Genetic accommodation in the wild: evolution of gene expression plasticity during character displacement. J. Evol. Biol. 30, 1712–1723 (2017).

    CAS  PubMed  Google Scholar 

  32. Huang, Y. & Agrawal, A. F. Experimental evolution of gene expression and plasticity in alternative selective regimes. PLoS Genet. 12, e1006336 (2016).

    PubMed  PubMed Central  Google Scholar 

  33. van Gestel, J. & Weissing, F. J. Is plasticity caused by single genes? Nature 555, E19–E20 (2018).

    PubMed  Google Scholar 

  34. Paull, J. S., Martin, R. A. & Pfennig, D. W. Increased competition as a cost of specialization during the evolution of resource polymorphism. Biol. J. Linn. Soc. 107, 845–853 (2012).

    Google Scholar 

  35. Levis, N. A., Martin, R. A., O’Donnell, K. A. & Pfennig, D. W. Intraspecific adaptive radiation: competition, ecological opportunity, and phenotypic diversification within species. Evolution 71, 2496–2509 (2017).

    PubMed  Google Scholar 

  36. Ledón-Rettig, C. C., Pfennig, D. W. & Crespi, E. J. Stress hormones and the fitness consequences associated with the transition to a novel diet in larval amphibians. J. Exp. Biol. 212, 3743–3750 (2009).

    PubMed  Google Scholar 

  37. Ho, W. C. & Zhang, J. Evolutionary adaptations to new environments generally reverse plastic phenotypic changes. Nat. Commun. 9, 350 (2018).

    PubMed  PubMed Central  Google Scholar 

  38. Casasa, S. & Moczek, A. P. The role of ancestral phenotypic plasticity in evolutionary diversification: population density effects in horned beetles. Anim. Behav. 137, 53–61 (2018).

    Google Scholar 

  39. Pfennig, D. W., Rice, A. M. & Martin, R. A. Ecological opportunity and phenotypic plasticity interact to promote character displacement and species coexistence. Ecology 87, 769–779 (2006).

    PubMed  Google Scholar 

  40. Gosner, K. L. A simplified table for staging anuran embryos with notes on identification. Herpetologica 16, 183–190 (1960).

    Google Scholar 

  41. lme4 R Package (R Foundation for Statistical Computing, Vienna, 2014).

  42. Masek, T., Vopalensky, V., Suchomelova, P. & Pospisek, M. Denaturing RNA electrophoresis in TAE agarose gels. Anal. Biochem. 336, 46–50 (2005).

    CAS  PubMed  Google Scholar 

  43. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the Method. Methods 25, 402–408 (2001).

    CAS  Google Scholar 

  44. Pfennig, D. W. & Murphy, P. J. Character displacement in polyphenic tadpoles. Evolution 54, 1738–1749 (2000).

    CAS  PubMed  Google Scholar 

  45. Pfennig, D. W., Rice, A. M. & Martin, R. A. Field and experimental evidence for competition’s role in phenotypic divergence. Evolution 61, 257–271 (2007).

    PubMed  Google Scholar 

  46. Martin, R. A. & Pfennig, D. W. Widespread disruptive selection in the wild is associated with intense resource competition. BMC Evol. Biol. 12, 136 (2012).

    PubMed  PubMed Central  Google Scholar 

  47. Martin, R. A. & Pfennig, D. W. Disruptive selection in natural populations: the roles of ecological specialization and resource competition. Am. Nat. 174, 268–281 (2009).

    PubMed  Google Scholar 

  48. Martin, R. A. & Pfennig, D. W. Field and experimental evidence that competition and ecological opportunity promote resource polymorphism. Biol. J. Linn. Soc. 100, 73–88 (2010).

    Google Scholar 

  49. Pfennig, D. W. Proximate and functional causes of polyphenism in an anuran tadpole. Funct. Ecol. 6, 167–174 (1992).

    Google Scholar 

  50. Collyer, M. L. & Adams, D. C. Analysis of two-state multivariate phenotypic change in ecological studies. Ecology 88, 683–692 (2007).

    PubMed  Google Scholar 

  51. Adams, D. C., Collyer, M. L. & Kaliontzopoulou, A. geomorph: Software for Geometric Morphometric Analyses R Package Version 3.0.6 (2018); https://cran.r-project.org/package=geomorph

  52. Collyer, M. L., Sekora, D. J. & Adams, D. C. A method for analysis of phenotypic change for phenotypes described by high-dimensional data. Heredity 115, 357–365 (2015).

    CAS  PubMed  Google Scholar 

  53. Roff, D. A. Evolutionary Quantitative Genetics (Chapman and Hall, New York, 1997).

  54. Levis, N. A. & Pfennig, D. W. Phenotypic plasticity, canalization, and the origins of novelty: evidence and mechanisms from amphibians. Semin. Cell Dev. Biol. https://doi.org/10.1016/j.semcdb.2018.01.012 (2018).

    Google Scholar 

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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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