Parallel evolution of domesticated Caenorhabditis species targets pheromone receptor genes

Abstract

Evolution can follow predictable genetic trajectories1, indicating that discrete environmental shifts can select for reproducible genetic changes2,3,4. Conspecific individuals are an important feature of an animal’s environment, and a potential source of selective pressures. Here we show that adaptation of two Caenorhabditis species to growth at high density, a feature common to domestic environments, occurs by reproducible genetic changes to pheromone receptor genes. Chemical communication through pheromones that accumulate during high-density growth causes young nematode larvae to enter the long-lived but non-reproductive dauer stage. Two strains of Caenorhabditis elegans grown at high density have independently acquired multigenic resistance to pheromone-induced dauer formation. In each strain, resistance to the pheromone ascaroside C3 results from a deletion that disrupts the adjacent chemoreceptor genes serpentine receptor class g (srg)-36 and -37. Through misexpression experiments, we show that these genes encode redundant G-protein-coupled receptors for ascaroside C3. Multigenic resistance to dauer formation has also arisen in high-density cultures of a different nematode species, Caenorhabditis briggsae, resulting in part from deletion of an srg gene paralogous to srg-36 and srg-37. These results demonstrate rapid remodelling of the chemoreceptor repertoire as an adaptation to specific environments, and indicate that parallel changes to a common genetic substrate can affect life-history traits across species.

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Figure 1: Strains of C. elegans cultivated in liquid are resistant to dauer pheromones.
Figure 2: Resistance to C3 ascaroside is caused by deletion of two srg genes.
Figure 3: The srg genes encode ascaroside receptors.
Figure 4: Evolutionary conservation of srg function.

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Acknowledgements

We thank N. Lu for the LSJ2 strain, M. Rockman for a qgIR1(X,CB4856>N2) introgression strain, J. Ragains for ascaroside synthesis, H. Hang for assistance in purifying pheromones and S. Dewell, K. Foster, N. Ringstad, A. Bendesky, Y. Saheki, M. Zimmer, S. Crosson, E. Feinberg, E. Toro, M. Rockman and L. Kruglyak for comments and advice. P.T.M. was funded by a Damon Runyon Fellowship. Y.X. was supported by Medical Scientist Training Program (MSTP) grant GM07739 and a Paul and Daisy Soros Fellowship. J.L.G. was an HHMI fellow of the Helen Hay Whitney Foundation and is funded by National Institutes of Health (NIH) K99 GM092859. R.A.B. is supported by R00GM87533. C.I.B. is an investigator of the Howard Hughes Medical Institute. This work was supported by the HHMI.

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Contributions

P.T.M. and C.I.B. designed and interpreted experiments and wrote the paper. P.T.M. performed all genetic, molecular and behavioural experiments, Y.X. conducted calcium imaging experiments, M.A. identified the dauer-formation defect in the LSJ2 lineage, R.A.B. characterized and synthesized ascarosides and J.L.G. contributed reagents.

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Correspondence to Cornelia I. Bargmann.

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Supplementary information

Supplementary Information

The file contains Supplementary 1-5 with legends and additional references. (PDF 964 kb)

Supplementary Table 1

This file contains genotyping data for 94 recombinant inbred lines (RILs). Figure S1 contains a schematic of how these RILs were created. (XLS 1316 kb)

Supplementary Table 2

This file contains a list of all the SNPs identified using next-generation of sequencing for a variety of strains. See Figure 1b for a description of the lineages referenced within this file. (XLS 86 kb)

Supplementary Table 3

This file contains a list of all the insertions and deletions identified in either the LSJ2 or the N2 lineage. (XLS 41 kb)

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McGrath, P., Xu, Y., Ailion, M. et al. Parallel evolution of domesticated Caenorhabditis species targets pheromone receptor genes. Nature 477, 321–325 (2011). https://doi.org/10.1038/nature10378

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