Rapid diversification associated with a macroevolutionary pulse of developmental plasticity

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.

DOI: http://dx.doi.org/10.7554/eLife.05463.001

eLife digest

Every animal and plant grows to a body plan that is defined by its genes. However, the body plan must be flexible enough to allow the organism to respond to whatever the world throws at it. This flexibility—known as developmental plasticity—allows an organism to change certain characteristics in order to survive in varying environmental conditions. For example, nerve cells in the brain need to be able to remodel to form memories.

It has been suggested that developmental plasticity can affect evolution because the ability to grow in different ways opens a diverse treasure trove of options from which to generate new forms and ways to exploit the environment. However, this potential had not previously been tested.

Susoy et al. looked at 90 species of roundworm that look different from one another, particularly in their mouths. Some of the worms have moveable teeth while others are simple and streamlined. Furthermore, of those examined, 23 species were found to be ‘dimorphic’ and have the ability to develop one of two types of mouth: either narrow or wide, depending on their prey.

Susoy et al. looked how similar the sequences of 14 genes were across all 90 species and used this information to build a family tree of how the roundworms are related to one another. Tracking which animals have dimorphic mouths on this tree produced an intriguing result: the strategy arose once in a single ancestor of the worms. Although this ability has been lost at least 10 times in the species that retained teeth, it has persisted in others through long periods of evolutionary time.

Next, Susoy et al. estimated the speed of evolution in these worms based on how quickly the characteristics of the worms' mouths had changed over evolutionary time. The gain of a dimorphic trait was associated with an increased rate of evolution and the appearance of many new species with diverse and more complex mouthparts. However, evolution was even faster where a dimorphism had been lost, even though the mouthparts generally became less complex.

Together, Susoy et al.'s findings demonstrate how developmental plasticity can introduce genetic diversity that can promote the evolution of new forms and species. The next challenges will be to find out how this genetic diversity is stored and released in the worms and to provide examples of the impact of environmental changes on developmental plasticity and shape.

DOI: http://dx.doi.org/10.7554/eLife.05463.002