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Co-option of the hormone-signalling module dafachronic acid–DAF-12 in nematode evolution

Nature volume 466, pages 494–497 (2010)Cite this article

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Abstract

Morphological novelties are lineage-specific traits that serve new functions1,2. Developmental polyphenisms have been proposed to be facilitators of phenotypic evolution, but little is known about the interplay between the associated genetic and environmental factors3,4,5,6,7,8,9,10,11. Here, we study two alternative morphologies in the mouth of the nematode Pristionchus pacificus and the formation of teeth-like structures that are associated with bacteriovorous feeding and predatory behaviour on fungi and other worms12,13,14,15,16. These teeth-like denticles represent an evolutionary novelty, which is restricted to some members of the nematode family Diplogastridae but is absent from Caenorhabditis elegans and related nematodes14. We show that the mouth dimorphism is a polyphenism that is controlled by starvation and the co-option of an endocrine switch mechanism. Mutations in the nuclear hormone receptor DAF-12 and application of its ligand, the sterol hormone dafachronic acid, strongly influence this switch mechanism. The dafachronic acid–DAF-12 module has been shown to control the formation of arrested dauer larvae in both C. elegans and P. pacificus, as well as related life-history decisions in distantly related nematodes17,18,19,20. The comparison of dauer formation and mouth morphology switch reveals that different thresholds of dafachronic acid signalling provide specificity. This study shows how hormonal signalling acts by coupling environmental change and genetic regulation and identifies dafachronic acid as a key hormone in nematode evolution.

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Figure 1: Ecology and mouth dimorphism in Pristionchus pacificus.
Figure 2: Mouth dimorphism is an environmentally induced polyphenism.
Figure 3: The dafachronic acid–DAF-12 endocrine signalling module was co-opted for the mouth polyphenism.
Figure 4: Different pheromone and hormone thresholds for dauer and mouth formation provide specificity in the phenotypic responses.

References

  1. Mayr, E. Evolution after Darwin (Univ. Chicago Press, 1960)

    Google Scholar 

  2. Moczek, A. P. On the origins of novelty in development and evolution. BioEssays 30, 432–447 (2008)

    Article  PubMed  Google Scholar 

  3. Waddington, C. H. Genetic assimilation of an acquired character. Evolution 7, 118–126 (1953)

    Article  Google Scholar 

  4. Brakefield, P. M., Kesbeke, F. & Koch, P. B. The regulation of phenotypic plasticity of eyespots in the butterfly Bicyclus anynana . Am. Nat. 152, 853–860 (1998)

    Article  CAS  PubMed  Google Scholar 

  5. Pigliucci, M. Phenotypic Plasticity – Beyond Nature and Nurture (The Johns Hopkins Univ. Press, 2001)

    Google Scholar 

  6. West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, 2003)

    Google Scholar 

  7. Nijhout, H. F. Development and evolution of adaptive polyphenisms. Evol. Dev. 5, 9–18 (2003)

    Article  PubMed  Google Scholar 

  8. Schlichting, C. D. Origins of differentiation via phenotypic plasticity. Evol. Dev. 5, 98–105 (2003)

    Article  PubMed  Google Scholar 

  9. Pigliucci, M., Murren, C. J. & Schlichting, C. D. Phenotypic plasticity and evolution by genetic assimilation. J. Exp. Biol. 209, 2362–2367 (2006)

    Article  PubMed  Google Scholar 

  10. Suzuki, Y. & Nijhout, H. F. Evolution of a polyphenism by genetic assimilation. Science 311, 650–652 (2006)

    Article  ADS  CAS  PubMed  Google Scholar 

  11. Saenko, S. V., French, V., Brakefield, P. M. & Beldade, P. Conserved developmental processes and the formation of evolutionary novelties: examples from butterfly wings. Phil. Trans. R. Soc. B 363, 1549–1555 (2008)

    Article  PubMed Central  PubMed  Google Scholar 

  12. Hirschmann, H. Über das Vorkommen zweier Mundhöhlentypen bei Diplogaster lheritieri MAUPAS und Diplogaster biformis n. sp. und die Entstehung dieser hermaphroditischen Art aus Diplogaster lheritieri . Zool. Jahrb. (Syst.) 80, 132–170 (1951)

    Google Scholar 

  13. Sommer, R. J., Carta, L. K., Kim, S.-Y. & Sternberg, P. W. Morphological, genetic and molecular description of Pristionchus pacificus sp. n. (Nematoda: Neodiplogastridae). Fundam. Appl. Nematol. 19, 511–521 (1996)

    Google Scholar 

  14. von Lieven, A. F. & Sudhaus, W. Comparative and functional morphology of the buccal cavity of Diplogastrina (Nematoda) and a first outline of the phylogeny of this taxon. J. Zool. Syst. Evol. Res. 38, 37–63 (2000)

    Article  Google Scholar 

  15. Herrmann, M. et al. The nematode Pristionchus pacificus (Nematoda: Diplogastridae) is associated with the oriental beetle Exomala orientalis (Coleoptera: Scarabaeidae) in Japan. Zool. Sci. 24, 883–889 (2007)

    Article  CAS  Google Scholar 

  16. Dieterich, C. et al. The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nature Genet. 40, 1193–1198 (2008)

    Article  CAS  PubMed  Google Scholar 

  17. Antebi, A. et al. daf-12 encodes a nuclear hormone receptor that regulates the dauer diapause and developmental age in C. elegans . Genes Dev. 14, 1512–1527 (2000)

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Motola, D. L. et al. Identification of ligands for DAF-12 that govern dauer formation and reproduction in C. elegans . Cell 124, 1209–1223 (2006)

    Article  CAS  PubMed  Google Scholar 

  19. Ogawa, A., Streit, A., Antebi, A. & Sommer, R. J. A conserved endocrine mechanism controls the formation of dauer and infective larvae in nematodes. Curr. Biol. 19, 67–71 (2009)

    Article  CAS  PubMed  Google Scholar 

  20. Wang, Z. et al. Identification of the nuclear receptor DAF-12 as a therapeutic target in parasitic nematodes. Proc. Natl Acad. Sci. USA 106, 9138–9143 (2009)

    Article  ADS  CAS  PubMed Central  PubMed  Google Scholar 

  21. Cassada, R. C. & Russell, R. L. The dauer larva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans . Dev. Biol. 46, 326–342 (1975)

    Article  CAS  PubMed  Google Scholar 

  22. Golden, J. W. & Riddle, D. L. A pheromone influences larval development in the nematode Caenorhabditis elegans . Science 218, 578–580 (1982)

    Article  ADS  CAS  PubMed  Google Scholar 

  23. Fielenbach, N. & Antebi, A. C. elegans dauer formation and the molecular basis of plasticity. Genes Dev. 22, 2149–2165 (2008)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Jeong, P.-Y. et al. Chemical structure and biological activity of the Caenorhabditis elegans dauer-inducing pheromone. Nature 433, 541–545 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  25. Butcher, R. A., Fujita, M., Schroeder, F. C. & Clardy, J. Small-molecule pheromones that control dauer development in Caenorhabditis elegans . Nature Chem. Biol. 3, 420–422 (2007)

    Article  CAS  Google Scholar 

  26. Srinivasan, J. et al. A blend of small molecules regulates both mating and development in Caenorhabditis elegans . Nature 454, 1115–1118 (2008)

    Article  ADS  CAS  PubMed Central  PubMed  Google Scholar 

  27. Macosko, E. Z. et al. A hub-and-space circuit drives pheromone attraction and social behaviour in C. elegans . Nature 458, 1171–1175 (2009)

    Article  ADS  CAS  PubMed Central  PubMed  Google Scholar 

  28. Nijhout, H. F. Insect Pheromones. (Princeton Univ. Press, 1994)

    Google Scholar 

  29. Moczek, A. P. & Nijhout, H. F. Developmental mechanisms of threshold evolution in a polyphenic beetle. Evol. Dev. 4, 252–264 (2002)

    Article  PubMed  Google Scholar 

  30. Creelman, R. A. & Mullet, J. E. Jasmoic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proc. Natl Acad. Sci. USA 92, 4114–4119 (1995)

    Article  ADS  CAS  PubMed Central  PubMed  Google Scholar 

  31. Quinn, G. P. & Keough, M. J. Experimental design and data analysis for biologists. (Cambridge Univ. Press, 2002)

    Book  Google Scholar 

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Acknowledgements

We would like to thank A. Weller for the footage of the video in Supplementary Fig. 1, M. Herrmann, D. Bumbarger and A. Weller for the photos in Fig. 1a–c, M. Riebesell for help in obtaining the photos in Fig. 1d–f, and D. Bumbarger, F. Brown and M. Herrmann for critically reading the manuscript.

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Authors and Affiliations

  1. Department for Evolutionary Biology, Max-Planck-Institute for Developmental Biology, Spemannstrasse 37; D-72076 Tübingen, Germany,

    Gilberto Bento, Akira Ogawa & Ralf J. Sommer

  2. D-72076 Tübingen, Germany,

    Gilberto Bento, Akira Ogawa & Ralf J. Sommer

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  1. Gilberto Bento
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  2. Akira Ogawa
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  3. Ralf J. Sommer
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Contributions

G.B. performed all experiments except the experiments described in Supplementary Fig. 1b, which were performed by A.O.; G.B., A.O. and R.J.S. designed the experiments and wrote the manuscript.

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Correspondence to Ralf J. Sommer.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Figure

This file contains Supplementary Figure S1 with legend. (PDF 162 kb)

Supplementary Movie 1

This movie shows P. pacificus adult hermaphrodite killing and feeding on L2 larva of C. elegans. Imaged captured with Nomarsky microscope. (MOV 9022 kb)

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Bento, G., Ogawa, A. & Sommer, R. Co-option of the hormone-signalling module dafachronic acid–DAF-12 in nematode evolution. Nature 466, 494–497 (2010). https://doi.org/10.1038/nature09164

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