Skip to main content
Genetics logoLink to Genetics
. 2002 Mar;160(3):983–994. doi: 10.1093/genetics/160.3.983

Why are there males in the hermaphroditic species Caenorhabditis elegans?

J R Chasnov 1, King L Chow 1
PMCID: PMC1462001  PMID: 11901116

Abstract

The free-living nematode worm Caenorhabditis elegans reproduces primarily as a self-fertilizing hermaphrodite, yet males are maintained in wild-type populations at low frequency. To determine the role of males in C. elegans, we develop a mathematical model for the genetic system of hermaphrodites that can either self-fertilize or be fertilized by males and we perform laboratory observations and experiments on both C. elegans and a related dioecious species C. remanei. We show that the mating efficiency of C. elegans is poor compared to a dioecious species and that C. elegans males are more attracted to C. remanei females than they are to their conspecific hermaphrodites. We postulate that a genetic mutation occurred during the evolution of C. elegans hermaphrodites, resulting in the loss of an attracting sex pheromone present in the ancestor of both C. elegans and C. remanei. Our findings suggest that males are maintained in C. elegans because of the particular genetic system inherited from its dioecious ancestor and because of nonadaptive spontaneous nondisjunction of sex chromosomes, which occurs during meiosis in the hermaphrodite. A theoretical argument shows that the low frequency of male mating observed in C. elegans can support male-specific genes against mutational degeneration. This results in the continuing presence of functional males in a 99.9% hermaphroditic species in which outcrossing is disadvantageous to hermaphrodites.

Full Text

The Full Text of this article is available as a PDF (119.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974 May;77(1):71–94. doi: 10.1093/genetics/77.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. C. elegans Sequencing Consortium Genome sequence of the nematode C. elegans: a platform for investigating biology. Science. 1998 Dec 11;282(5396):2012–2018. doi: 10.1126/science.282.5396.2012. [DOI] [PubMed] [Google Scholar]
  3. Crow J. F. Advantages of sexual reproduction. Dev Genet. 1994;15(3):205–213. doi: 10.1002/dvg.1020150303. [DOI] [PubMed] [Google Scholar]
  4. Fitch D. H., Bugaj-Gaweda B., Emmons S. W. 18S ribosomal RNA gene phylogeny for some Rhabditidae related to Caenorhabditis. Mol Biol Evol. 1995 Mar;12(2):346–358. doi: 10.1093/oxfordjournals.molbev.a040207. [DOI] [PubMed] [Google Scholar]
  5. Hassold T., Hunt P. To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet. 2001 Apr;2(4):280–291. doi: 10.1038/35066065. [DOI] [PubMed] [Google Scholar]
  6. Hodgkin J., Barnes T. M. More is not better: brood size and population growth in a self-fertilizing nematode. Proc Biol Sci. 1991 Oct 22;246(1315):19–24. doi: 10.1098/rspb.1991.0119. [DOI] [PubMed] [Google Scholar]
  7. Hodgkin J., Horvitz H. R., Brenner S. Nondisjunction Mutants of the Nematode CAENORHABDITIS ELEGANS. Genetics. 1979 Jan;91(1):67–94. doi: 10.1093/genetics/91.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Johnson T. E., Hutchinson E. W. Absence of strong heterosis for life span and other life history traits in Caenorhabditis elegans. Genetics. 1993 Jun;134(2):465–474. doi: 10.1093/genetics/134.2.465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Keightley P. D., Caballero A. Genomic mutation rates for lifetime reproductive output and lifespan in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):3823–3827. doi: 10.1073/pnas.94.8.3823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. MERRIAM J. R., FROST J. N. EXCHANGE AND NONDISJUNCTION OF THE X CHROMOSOMES IN FEMALE DROSOPHILA MELANOGASTER. Genetics. 1964 Jan;49:109–122. doi: 10.1093/genetics/49.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Stewart Andrew D., Phillips Patrick C. Selection and maintenance of androdioecy in Caenorhabditis elegans. Genetics. 2002 Mar;160(3):975–982. doi: 10.1093/genetics/160.3.975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ward S., Carrel J. S. Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol. 1979 Dec;73(2):304–321. doi: 10.1016/0012-1606(79)90069-1. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES