Genetics, Vol. 160, 983-994, March 2002, Copyright © 2002

Why Are There Males in the Hermaphroditic Species Caenorhabditis elegans?

J. R. Chasnova and King L. Chowb
a Department of Mathematics, Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong
b Department of Biology, Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong

Corresponding author: King L. Chow, Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong., bokchow{at}ust.hk (E-mail)

Communicating editor: D. CHARLESWORTH

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.





This article has been cited by other articles:


Home page
Biol LettHome page
J. R. Pannell
On the problems of a closed marriage: celebrating Darwin 200
Biol Lett, June 23, 2009; 5(3): 332 - 335.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
A. D. Cutter, A. Dey, and R. L. Murray
Evolution of the Caenorhabditis elegans Genome
Mol. Biol. Evol., June 1, 2009; 26(6): 1199 - 1234.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
V. Katju, E. M. LaBeau, K. J. Lipinski, and U. Bergthorsson
Sex Change by Gene Conversion in a Caenorhabditis elegans fog-2 Mutant
Genetics, September 1, 2008; 180(1): 669 - 672.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
C. G. Artieri, W. Haerty, B. P. Gupta, and R. S. Singh
Sexual Selection and Maintenance of Sex: Evidence from Comparisons of Rates of Genomic Accumulation of Mutations and Divergence of Sex-Related Genes in Sexual and Hermaphroditic Species of Caenorhabditis
Mol. Biol. Evol., May 1, 2008; 25(5): 972 - 979.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. D. Cutter, J. D. Wasmuth, and N. L. Washington
Patterns of Molecular Evolution in Caenorhabditis Preclude Ancient Origins of Selfing
Genetics, April 1, 2008; 178(4): 2093 - 2104.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
J. R. Chasnov, W. K. So, C. M. Chan, and K. L. Chow
The species, sex, and stage specificity of a Caenorhabditis sex pheromone
PNAS, April 17, 2007; 104(16): 6730 - 6735.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
L. R. Garcia, B. LeBoeuf, and P. Koo
Diversity in Mating Behavior of Hermaphroditic and Male-Female Caenorhabditis Nematodes
Genetics, April 1, 2007; 175(4): 1761 - 1771.
[Abstract] [Full Text] [PDF]


Home page
Proc R Soc BHome page
D. Manoel, S. Carvalho, P. C Phillips, and H. Teotonio
Selection against males in Caenorhabditis elegans under two mutational treatments
Proc R Soc B, February 7, 2007; 274(1608): 417 - 424.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. D. Cutter, S. E. Baird, and D. Charlesworth
High Nucleotide Polymorphism and Rapid Decay of Linkage Disequilibrium in Wild Populations of Caenorhabditis remanei
Genetics, October 1, 2006; 174(2): 901 - 913.
[Abstract] [Full Text] [PDF]


Home page
Integr. Comp. Biol.Home page
S. C. Weeks, C. Benvenuto, and S. K. Reed
When males and hermaphrodites coexist: a review of androdioecy in animals
Integr. Comp. Biol., August 1, 2006; 46(4): 449 - 464.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. D. Cutter, M.-A. Felix, A. Barriere, and D. Charlesworth
Patterns of Nucleotide Polymorphism Distinguish Temperate and Tropical Wild Isolates of Caenorhabditis briggsae
Genetics, August 1, 2006; 173(4): 2021 - 2031.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. D. Cutter
Nucleotide Polymorphism and Linkage Disequilibrium in Wild Populations of the Partial Selfer Caenorhabditis elegans
Genetics, January 1, 2006; 172(1): 171 - 184.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
M. Haber, M. Schungel, A. Putz, S. Muller, B. Hasert, and H. Schulenburg
Evolutionary History of Caenorhabditis elegans Inferred from Microsatellites: Evidence for Spatial and Temporal Genetic Differentiation and the Occurrence of Outbreeding
Mol. Biol. Evol., January 1, 2005; 22(1): 160 - 173.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
A. D. Cutter and S. Ward
Sexual and Temporal Dynamics of Molecular Evolution in C. elegans Development
Mol. Biol. Evol., January 1, 2005; 22(1): 178 - 188.
[Abstract] [Full Text] [PDF]


Home page
ScienceHome page
V. Prahlad, D. Pilgrim, and E. B. Goodwin
Roles for Mating and Environment in C. elegans Sex Determination
Science, November 7, 2003; 302(5647): 1046 - 1049.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
A. D. Cutter and B. A. Payseur
Selection at Linked Sites in the Partial Selfer Caenorhabditis elegans
Mol. Biol. Evol., May 1, 2003; 20(5): 665 - 673.
[Abstract] [Full Text] [PDF]