Rapid diversification associated with a macroevolutionary pulse of developmental plasticity.

Vladislav Susoy,Erik J Ragsdale,Natsumi Kanzaki,Ralf J Sommer

doi:10.7554/elife.05463

Abstract

Developmental plasticity has been proposed to facilitate phenotypic diversification in plants and animals, but the macroevolutionary potential of plastic traits remains to be objectively tested. We studied the evolution of feeding structures in a group of 90 nematodes, including Caenorhabditis elegans, some species of which have evolved a mouthpart polyphenism, moveable teeth, and predatory feeding. Comparative analyses of shape and form, using geometric morphometrics, and of structural complexity revealed a rapid process of diversification associated with developmental plasticity. First, dimorphism was associated with a sharp increase in complexity and elevated evolutionary rates, represented by a radiation of feeding-forms with structural novelties. Second, the subsequent assimilation of a single phenotype coincided with a decrease in mouthpart complexity but an even stronger increase in evolutionary rates. Our results suggest that a macroevolutionary 'pulse' of plasticity promotes novelties and, even after the secondary fixation of phenotypes, permits sustained rapid exploration of morphospace.

Highlights

Developmental plasticity has been proposed to affect evolution by facilitating adaptive change (Pigliucci, 2001; Schlichting, 2003; West-Eberhard, 2003; Moczek et al, 2011) but the relevant processes resulting in evolutionary diversity remain elusive
To know the macroevolutionary potential of developmental plasticity, objectively measured plastic traits must be compared by deep taxon sampling in a robust phylogenetic framework
We test the role of developmental plasticity in evolutionary tempo and novelty by measuring change in feeding structures in a group of 90 nematodes, including Caenorhabditis elegans, of which some species show a mouthpart polyphenism, moveable teeth, and predatory feeding

Summary

Introduction

Developmental (phenotypic) plasticity has been proposed to affect evolution by facilitating adaptive change (Pigliucci, 2001; Schlichting, 2003; West-Eberhard, 2003; Moczek et al, 2011) but the relevant processes resulting in evolutionary diversity remain elusive. Whether plasticity accelerates evolution by allowing faster evolutionary responses (Baldwin, 1896; Waddington, 1953; Suzuki and Nijhout, 2006) or hinders it by allowing adaptation without the need for genetic assimilation (Williams, 1966) is still a matter of debate (e.g., de Jong, 2005; Wund, 2012). We test the role of developmental plasticity in evolutionary tempo and novelty by measuring change in feeding structures in a group of 90 nematodes, including Caenorhabditis elegans, of which some species show a mouthpart polyphenism, moveable teeth, and predatory feeding. We made the surprising finding that whereas the appearance of polyphenism coincided with increased complexity and evolutionary rates, these rates were even higher after the assimilation of a single phenotype

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Conclusion