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

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.

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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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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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