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

The genetics of phenotypic plasticity in nematode feeding structures

“…These species included dimorphic taxa, such as P. pacificus , but also monomorphic species that never evolved feeding plasticity, such as C. elegans (primary monomorphic), and those that had secondarily lost it (secondary monomorphic). This study found that feeding dimorphism was indeed associated with a strong increase in complexity of mouth-form structures [44]. At the same time, the subsequent assimilation of a single mouth-form phenotype (secondary monomorphism) coincided with a decrease in morphological complexity, but an increase in evolutionary rates.…”

“…Two recent studies have moved this analysis to the macro-evolutionary level, suggesting that phenotypic plasticity indeed facilitates rapid diversification. Susoy and co-workers studied the evolution of feeding structures in more than 90 nematode species using geometric morphometrics [44]. These species included dimorphic taxa, such as P. pacificus , but also monomorphic species that never evolved feeding plasticity, such as C. elegans (primary monomorphic), and those that had secondarily lost it (secondary monomorphic).…”

Predatory feeding behaviour in Pristionchus nematodes is dependent on a phenotypic plasticity and induced by serotonin

“…Furthermore, recent mapping of the pharyngeal connectome has exposed fundamental wiring differences between P. pacificus and C. elegans, perhaps guiding behavioural changes between the species (Bumbarger et al, 2013). The mouth dimorphism in P. pacificus has also been intensely studied as a model for developmental ( phenotypic) plasticity, thought to be a major process driving novelty in evolution (Susoy et al, 2015). The developmental pathways guiding the mouth dimorphism represent a complex regulatory network including small molecules (Bose et al, 2012).…”

Hedgehog signaling enables nutrition-responsive inhibition of an alternative morph in a polyphenic beetle

“…For instance, in many butterfly species, seasonal conditions critically alter selective environments, and seasonal sensitivity in eye spot formation is able to adjust wing phenotypes, thereby maintaining high fitness across fluctuating environments (9). Similarly, environment-dependent induction of carnivory in spadefoot toad tadpoles (10,11) or tooth formation and bacterial predation in nematodes (12), two striking and complex evolutionary novelties, greatly affect the adaptive significance of each innovation, thereby facilitating their adaptive radiations (13). Here, we investigate the functional significance of the Hedgehog (Hh) signaling pathway, a deeply conserved cellular transduction pathway, in the development of beetles horns, a striking evolutionary novelty (14), and specifically, the origins of environment-responsive horn formation, alternative male phenotypes, and body size thresholds, emergent phenotypes that have greatly impacted patterns of morphological radiation among horned beetles (15)(16)(17).…”