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Developmental Plasticity: A Facilitator of Novelty

© Ralf Sommer/MPI for Developmental Biology, Tübingen

Developmental (phenotypic) plasticity has long been proposed to facilitate the response of organisms towards changing environmental conditions. More recently, developmental plasticity is also considered to play a crucial role in facilitating phenotypic novelty at the morphological level. Pristionchus represents an interesting case study to test this hypothesis.

Pristionchus
species, like others in the family Diplogastridae, show a case of developmental plasticity in the form of the buccal cavity. The mouth-form dimorphism includes one simple form (stenostomatous) that is reminiscent of outgroups, including Caenorhabditis elegans, in which the buccal cavity is narrow and has limited internal armature. The alternate form (eurystomatous) in Pristionchus is much wider and has distinctive teeth, including a claw-like dorsal tooth and an additional, opposing subventral tooth. The dimorphism is qualitative, irreversible, and discrete, suggesting that distinct genetic modules regulate the development of either form. The variation in buccal cavity morphology is thought to be related to different feeding habits:

Stenostomatous nematodes primarily feed on bacteria, whereas eurystomatous nematodes can also feed on fungi and other nematodes. The dimorphism therefore has implications for the evolution of novel feeding forms and expansion into otherwise inaccessible ecological niches.

We want to understand the genetic basis of developmental plasticity and identify its significance for the evolution of novelty. We have shown that changing environments (e.g. starvation) strongly influence the response of the organism. Moreover, the phenotype decision has co-opted an endocrine signaling mechanism (DAF-12/∆ 7-dafachronic acid) that is involved in development of the resistant dauer stage. Using forward genetics we have produced mutants that are constitutive for each of the two forms; we are now mapping the genes responsible for executing the phenotype decision in development. Studies of inheritance in males suggest that dimorphism is also sex-linked. Ultimately, mechanistic details of the dimorphism will inform comparative analysis, enabled by a robust phylogenetic framework. In such an approach we can test whether genes in mutant animals reflect processes in natural history, such as by how they correlate with observed variation within the species (microevolution) and across the genus (macroevolution). Also we have began to study the interactions between the genetic machinary regulating plasticity with the environment.

Scientists involved:

  • Dr. Michael Werner, Postdoc
  • Mohannad Dardiry, Ph.D. Student
  • Maša Lenuzzi, Ph.D. Student 
  • Suryesh Namdeo, Ph.D. Student
  • Tess Renahan, Ph.D. Student
  • Bogdan Sieriebriennikov, Ph.D. Student

Selected References:

Serobyan, V., Xiao, H., Rödelsperger, C., Namdeo, S., Röseler, W., Witte, H. & Sommer, R. J. (2016): Chromatin remodeling and antisense-mediate up-regulation of the developmental switch gene eud-1 control predatory feeding plasticity. Nature Commun., 7, 12337.

Kieninger, M. R., Ivers, N. A., Rödelsperger, C., Markov, G. V., Sommer, R. J.  & Ragsdale, E. J. (2016):
 The nuclear hormone receptor NHR-40 acts downstream of the sulfatase EUD-1 as part of a developmental plasticity switch in PristionchusCurrent Biology, 26, 2174-2179.

Susoy, V., Herrmann, M., Kanzaki, N., Kruger, M., Nguyen, C.N., Rödelsperger, C., Röseler, W., Weiler, C., Giblin-Davis, R.M., Ragsdale, E.J. & Sommer, R. J. (2016):
 Large-scale diversification without genetic isolation in nematode symbionts of figs. Science Advance, 2, e1501031.

Susoy, V., Ragsdale, E. J., Kanzaki, N. & Sommer, R. J. (2015):
Rapid diversification associated with a macroevolutionary pulse of developmental plasticity. eLIFE, 4:e05463. Featured in: Nijhout, H.F. (2015): To plasticity and back again. eLIFE, 4: e06995.

Serobyan, V., Ragsdale, E. J. & Sommer, R. J. (2014): Adaptive value of a predatory mouth-form in a dimorphic nematode. Proc. Roy. Soc. B, 281: 20141334.

Ragsdale, E. J., Mueller, M. R., Roedelsperger, C. & Sommer, R. J. (2013): A developmental switch coupled to the evolution of plasticity acts through a sulfatase. Cell, 155, 922-933.

Featured in:
Hartenstein, V. & Jacobs, D. (2013):
Developmental plasticity, straight from the worm´s mouth. Cell, 155, 742-743.

Ragsdale, E. J., Kanzaki, N., Roeseler, W., Herrmann, M. & Sommer, R. J. (2013): Three new species of Pristionchus (Nematoda: Diplogastridae) show morphological divergence through evolutionary intermediates of a novel feeding polymorphism. Zool. J. Linn. Soc., 168, 671-698.

Serobyan, V., Ragsdale, E. J., Müller, M. R. & Sommer, R. J. (2013): Feeding plasticity in the nematode Pristionchus pacificus is influenced by gender and social context and is linked to developmental speed. Evolution & Development, 15, 173-182.

Bose, N., Ogawa, A., von Reuss, S. H., Yim, J. J., Ragsdale, E. J., Sommer, R. J. & Schroeder, F. C. (2012):
Complex small molecular architectures regulate phenotypic plasticity in a nematode. Angewandte Chemie, 51, 12438-12443.

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