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Molecular basis of the copulatory plug polymorphism in Caenorhabditis elegans

Abstract

Heritable variation is the raw material for evolutionary change, and understanding its genetic basis is one of the central problems in modern biology. We investigated the genetic basis of a classic phenotypic dimorphism in the nematode Caenorhabditis elegans. Males from many natural isolates deposit a copulatory plug after mating, whereas males from other natural isolates?including the standard wild-type strain (N2 Bristol) that is used in most research laboratories?do not deposit plugs1. The copulatory plug is a gelatinous mass that covers the hermaphrodite vulva, and its deposition decreases the mating success of subsequent males2. We show that the plugging polymorphism results from the insertion of a retrotransposon into an exon of a novel mucin-like gene, plg-1, whose product is a major structural component of the copulatory plug. The gene is expressed in a subset of secretory cells of the male somatic gonad, and its loss has no evident effects beyond the loss of male mate-guarding. Although C. elegans descends from an obligate-outcrossing, male?female ancestor3,4, it occurs primarily as self-fertilizing hermaphrodites5,6,7. The reduced selection on male?male competition associated with the origin of hermaphroditism may have permitted the global spread of a loss-of-function mutation with restricted pleiotropy.

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Figure 1: The plg-1 gene.
Figure 2: The mucin gene is plg-1.
Figure 3: The copulatory plug contains carbohydrate structures typical of mucins and plg-1 is expressed in only a small number of male cells.
Figure 4: The plg-1 loss-of-function allele is globally distributed and Cer1 has been recently active.

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Acknowledgements

We thank the Caenorhabditis Genetics Center, M. Ailion, E. Dolgin, A. Barrière, M.-A. Félix and P. McGrath for strains and reagents. Work at Bowdoin College was supported by college funds, by the NIH (grant P20 RR-016463 from the INBRE Program of the National Center for Research Resources), the NSF (grant 0110994), and by an award to Bowdoin College by the Howard Hughes Medical Institute under the Undergraduate Science Education Program. Work at Princeton University was supported by grants from the NIH (R01 HG004321 to L.K. and P50 GM071508 to the Lewis-Sigler Institute), a James S. McDonnell Foundation Centennial Fellowship (L.K.), and a Jane Coffin Childs Fellowship (M.V.R.). We thank S. Civillico for assistance in the laboratory, F. Hagen for experimental advice, and E. Anderson, H. Coller, L. Gordon and H. Seidel for comments on the manuscript.

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Correspondence to Michael F. Palopoli.

Supplementary information

Supplementary Information 1

The file contains Supplementary Methods and Supplementary Figures S1-S5 with Legends. (PDF 1761 kb)

Supplementary Information 2

The file contains Supplementary Movie 1. Three-dimensional reconstruction of a stack of confocal images of an F1 male from a cross between CB4856 and QX1193, which carries the integrated plg-1::GFP transgene qqIs1. (AVI 16770 kb)

Supplementary Information 3

The file contains Supplementary Table 1 including natural isolate strains, localities, phenotypes, and genotypes. (XLS 32 kb)

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Palopoli, M., Rockman, M., TinMaung, A. et al. Molecular basis of the copulatory plug polymorphism in Caenorhabditis elegans. Nature 454, 1019–1022 (2008). https://doi.org/10.1038/nature07171

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