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Developmental Plasticity: A Facilitator of Novelty

© Ralf Sommer/MPI for Developmental Biology, Tübingen

Environmental responsiveness and phenotypic plasticity are found everywhere in nature. All organisms are exposed to an environment and most of these environments are changing constantly, often in an unpredictable manner. Not surprisingly therefore, plasticity is found in all domains of life and at all levels of biological organization.

Developmental (phenotypic) plasticity describes the property of a genotype to respond to environmental variation by producing distinct phenotypes. The concept of plasticity dates back to the beginning of the 20th century and has continuously been developed to arrive at its current state, where many practitioners consider plasticity to represent a major facilitator of evolutionary diversification. In our lab, we investigate developmental plasticity at an integrative level.

HOW DO WE APPROACH PLASTICITY?

We are trying to answer the following questions:

1.    What are the molecular mechanisms underlying developmental plasticity?
2.    How do genes end the environment interact to regulate plastic traits?
3.    What is the evidence for plasticity as facilitator of diversity and what is it´s exact macro-evolutionary potential?
4.    How is environmental information becoming encoded and integrated into the organism?

WHAT IS OUR MODEL SYSTEM?

We are using a mouth-form dimorphism in Pristionchus pacificus and its relatives to study the questions mentioned above.

P. pacificus
and related nematodes lives on scarab beetles, i.e. cockchafers and stag beetles. Pristionchus waits for the beetle to die before exiting the arrested dauer stage. At that time, there is enormous competition for food and survival between many animals and microbes all living on the carcass.
It is long known that Pristionchus and relatives form teeth-like denticles in their mouth, which allow predatory feeding (see figure above). In the case of P. pacificus, animals decide during larval development in an irreversible manner to adopt a eurystomatous (Eu) or a stenostomatous (St) mouth-form. Eu animals form two teeth with a wide buccal cavity, representing predators. In contrast, St animals have a single tooth with a narrow buccal cavity and are strict microbial feeders. This dimorphism represents an example of phenotypic plasticity (Bento et al., 2010) and it is discrete and adaptive. Most importantly, mouth-form plasticity is regulated by conditional factors such as crowding, but also contains stochastic elements of regulation: a nearly constant ratio of 70-90% Eu : 30-10% St animals is formed under fixed environmental conditions. It is this aspect of stochastic regulation that allows manipulation of plasticity by genetic and molecular tools.

GENETIC AND EPIGENETIC REGULATION

Unbiased genetic screens resulted in the isolation of mutants that would only form one of the two mouth-forms and some of these mutants were characterized to represent “developmental switch genes”. eud-1 and nhr-40 mutants are monomorphic, being all-St and all-Eu, respectively (Ragsdale et al., 2013; Kieninger et al., 2016). Both genes are part of a developmental switch with loss-of-function and overexpression, resulting in complete, but opposite phenotypes. Developmental switches had long been predicted to play an important role in plasticity regulation, but due to the absence of genetic models of plasticity little genetic evidence was obtained. More recent studies in our lab began to investigate the epigenetic and potential trans-generational effects in the control of mouth-form plasticity.

MACRO-EVOLUTIONARY POTENTIAL OF PLASTICITY AND FACILITATION OF DIVERSITY

Is plasticity important for evolutionary diversification and novelty? Answering this question requires comparative studies that when performed in a phylogenetic context can provide insight into the significance of plasticity for evolutionary processes. Two recent studies have moved this analysis to the macro-evolutionary level, suggesting that phenotypic plasticity indeed facilitates rapid diversification. First, we studied the evolution of feeding structures in more than 90 nematode species using geometric morphometrics (Susoy et al., 2015). This study found that feeding dimorphism was indeed associated with a strong increase in complexity of mouth-form structures. At the same time, the subsequent assimilation of a single mouth-form phenotype coincided with a decrease in morphological complexity, but an increase in evolutionary rates.

A second case of mouth-form plasticity increasing morphological diversification came from a striking example of fig-associated Pristionchus nematodes (Susoy et al., 2016). These nematodes form five distinct mouth-forms that occur in succession in developing fig synconia, thereby increasing the polyphenism from two to five distinct morphs. Additionally, the morphological diversity of these five morphs exceeds that of several higher taxa, although all five morphs are formed by the same species. These findings strongly support the facilitator hypothesis and they also indicate that ecological diversity can be maintained in the absence of genetic variation as all this diversity is seen within a single species and without associated speciation and radiation events.

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
  • Tobias Loschko, Technian
  • Devansh Raj, Master Student

Selected References:

Serobyan, V. & Sommer, R. J. (2017): Developmental systems of plasticity and trans-generational inheritance in nematodes. Curr. Opin. Genet. & Devel., 45, 51-57.

Sommer, R. J., Dardiry, M., Lenuzzi, M., Namdeo, S., Renahan, T., Sieriebriennikov, B. & Werner, M. (2017): The genetics of phenotypic plasticity in nematode feeding structures. Open Biology, 7, 160332.

Sieriebriennikov, B., Markov, G. V., Witte, H., & Sommer, R. J. (2017): The role of DAF-21/Hsp90 in mouth-form plasticity in Pristionchus pacificus. Molecular Biology & Evolution, in press.

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.

Bento, G., Ogawa, A. & Sommer, R. J. (2010): Co-option of the hormone-signalling module dafachronic acid–DAF-12 in nematode evolution. Nature, 466, 494-497.