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Selection and gene flow shape niche-associated variation in pheromone response

Abstract

From quorum sensing in bacteria to pheromone signalling in social insects, chemical communication mediates interactions among individuals in local populations. In Caenorhabditis elegans, ascaroside pheromones can dictate local population density; high levels of pheromones inhibit the reproductive maturation of individuals. Little is known about how natural genetic diversity affects the pheromone responses of individuals from diverse habitats. Here, we show that a niche-associated variation in pheromone receptor genes contributes to natural differences in pheromone responses. We identified putative loss-of-function deletions that impair duplicated pheromone receptor genes (srg-36 and srg-37), which were previously shown to be lost in population-dense laboratory cultures. A common natural deletion in srg-37 arose recently from a single ancestral population that spread throughout the world; this deletion underlies reduced pheromone sensitivity across the global C. elegans population. We found that many local populations harbour individuals with a wild-type or a deletion allele of srg-37, suggesting that balancing selection has maintained the recent variation in this pheromone receptor gene. The two srg-37 genotypes are associated with niche diversity underlying boom-and-bust population dynamics. We hypothesize that human activities likely contributed to the gene flow and balancing selection of srg-37 variation through facilitating the migration of species and providing a favourable niche for the recently arisen srg-37 deletion.

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Fig. 1: An HTDA measures the natural variation of the dauer-pheromone response.
Fig. 2: GWA mapping reveals four major loci underlying natural variation in the dauer-pheromone response.
Fig. 3: A natural variant in the ascr#5 receptor gene, srg-37, underlies natural differences in dauer formation.
Fig. 4: Worldwide and niche-associated gene flow shapes the ascr#5 pheromone receptor locus.

Data availability

All datasets, including HTDA raw data, for generating figures are available on GitHub (https://github.com/AndersenLab/DauerSRG3637).

Code availability

All code for generating figures is available on GitHub (https://github.com/AndersenLab/DauerSRG3637).

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Acknowledgements

This work was supported by an NSF CAREER Award to E.C.A. S.Z was supported by the Cell and Molecular Basis of Disease training grant (no. T32GM008061) and the Bernard and Martha Rappaport Fellowship. D.E.C. received the National Science Foundation Graduate Research Fellowship (no. DGE-1324585). Members of the Andersen Lab helped with manuscript editing, and Y. K. Zhang assisted with the synthesis of ascarosides. Some strains were provided by the CGC, which is funded by the NIH Office of Research Infrastructure Programs (grant no. P40 OD010440). We thank WormBase for providing genomic data on Caenorhabditis species.

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D.L. and E.C.A. conceived and designed the study. D.L. performed the high-throughput assay, CRISPR–Cas9 genome editing, population genomic analyses and niche enrichment tests. S.Z. performed the GWA mapping, identified genetic variants in the dauf-1 locus, generated the genome-wide tree of 249 wild C. elegans strains and edited the manuscript. D.E.C. analysed the haplotype composition of 249 wild strains. L.F., J-C.H., M.G.S., J.A.G.R., J.W., J.E.K., C.B. and M.-A.F. contributed wild isolates to the C. elegans strain collection. F.C.S. provided the dauer pheromone. D.L. and E.C.A. analysed the data and wrote the manuscript.

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Correspondence to Erik C. Andersen.

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Supplementary Information

Supplementary Figs. 1–16 and Table 1.

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Supplementary Data 1

Information for wild C. elegans strains isolated in the cosampling zone.

Supplementary Data 2

Sampling information for wild C. elegans strains.

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Lee, D., Zdraljevic, S., Cook, D.E. et al. Selection and gene flow shape niche-associated variation in pheromone response. Nat Ecol Evol 3, 1455–1463 (2019). https://doi.org/10.1038/s41559-019-0982-3

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