Oocyte production and sperm utilization patterns in semi-fertile strains of Caenorhabditis elegans

BMC Developmental Biology

Andrew Singson¹  Pavan Kadandale¹ 

[1] Waksman Institute and Department of Genetics, Rutgers University, Piscataway, New Jersey 08854, USA

Others  :  1173688
DOI  :  10.1186/1471-213X-4-3

 received in 2004-03-04, accepted in 2004-04-15,  发布年份 2004

【 摘 要 】

Background

Caenorhabditis elegans hermaphrodites are capable of producing hundreds of progeny. However, genetic and environmental factors can keep many animals from attaining their full reproductive potential. In these situations, efficient use of any functional gametes becomes more important for reproductive success. To learn about this aspect of C. elegans reproductive biology, we examined oocyte production and sperm utilization patterns in a unique collection of semi-fertile sperm function mutants.

Results

In the mutants examined here, broods can be very small but sperm induced high levels of ovulation. Ovulation rates reach maximum levels between the first and second day of adulthood. Ovulations rates remain high during the reproductive period and gradually decline with age. These results further demonstrate a decoupling of the ability of sperm to fertilize oocytes and induce ovulation. We also observe that in our semi-fertile mutants the peak of successful fertilization events precedes the bulk of oocyte production. Mixing populations of functional and nonfunctional sperm under conditions without sperm competition also shows that functional sperm are utilized efficiently. Although overall brood size can be similar for different mutant strains, slight differences in the pattern of sperm utilization in these strains can lead to significant differences in resource utilization and population growth.

Conclusions

This study represents the first detailed description of oocyte and progeny production patterns over the entire reproductive period for wild-type and fertility impaired strains of C. elegans. The phenotype of our mutants provide an ideal system for studying sperm utilization patterns since they only affect one major process, the ability to fertilize oocytes. In semi-fertile mutants, the nature of the reproductive process and/or specific molecular mechanisms ensures that any functional sperm are utilized quickly. Only a fraction of the sperm produced by our semi-sterile mutants are functional as opposed to every sperm having a low but equal chance of fertilizing an oocyte. In addition to the number of progeny produced, the pattern of progeny production can have an important influence on the dynamics of population growth.

【 授权许可】

   
2004 Kadandale and Singson; licensee BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose, provided this notice is preserved along with the article's original URL.

【 图 表 】

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【 参考文献 】

• [1]Brenner Sydney: The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
• [2]Meyer Barbara J.: Sex determination and X chromosome dosage compensation. In C. Elegans II. Edited by Donald L Riddle, Thomas Blumenthal, Barbara J Meyer and James R Priess. Cold Spring Harbor, Cold Spring Harbor Laboratory; 1997:209-240.
• [3]Ward Samuel, Miwa Johji: Characterization of temperature-sensitive, fertilization-defective mutants of the nematode Caenorhabditis elegans. Genetics 1978, 88:285-303.
• [4]Hirsh D, Oppenheim D, Klass M: Development of the reproductive system of Caenorhabditis elegans. Dev Biol 1976, 49:200-219.
• [5]Singson A: Every sperm is sacred: fertilization in Caenorhabditis elegans. Dev Biol 2001, 230:101-109.
• [6]Miller MA, Ruest PJ, Kosinski M, Hanks SK, Greenstein D: An Eph receptor sperm-sensing control mechanism for oocyte meiotic maturation in Caenorhabditis elegans. Genes Dev 2003, 17:187-200.
• [7]Miller MA, Nguyen VQ, Lee MH, Kosinski M, Schedl T, Caprioli RM, Greenstein D: A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 2001, 291:2144-2147.
• [8]Ward Samuel, Carrel John S.: Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 1979, 73:304-321.
• [9]LaMunyon Craig W., Ward Samuel: Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proceedings of the Royal Society, Series B 1998, 265:1997-2002.
• [10]LaMunyon CW, Ward S: Sperm precedence in a hermaphroditic nematode Caenorhabditis elegans is due to competitive superiority of male sperm. Experientia 1995, 51:817-823.
• [11]LaMunyon CW, Ward S: Evolution of sperm size in nematodes: sperm competition favours larger sperm. Proceedings of the Royal Society, Series B 1999, 266:263-267.
• [12]Singson A, Hill KL, L'Hernault SW: Sperm competition in the absence of fertilization in Caenorhabditis elegans. Genetics 1999, 152:201-208.
• [13]L'Hernault Steven W., Shakes Diane C., Ward Samuel: Developmental genetics of chromosome I spermatogenesis-defective mutants in the nematode Caenorhabditis elegans. Genetics 1988, 120:435-452.
• [14]Singson Andrew, Mercer Kristina B., L'Hernault Steven W.: The C. elegans spe-9 gene encodes a sperm transmembrane protein that contains EGF-like repeats and is required for fertilization. Cell 1998, 93:71-79.
• [15]Hodgkin J, Barnes TM: More is not better: brood size and population growth in a self-fertilizing nematode. Proc R Soc Lond B Biol Sci 1991, 246:19-24.
• [16]Hodgkin J, Kuwabara PE, Corneliussen B: A novel bacterial pathogen, Microbacterium nematophilum, induces morphological change in the nematode C. elegans. Curr Biol 2000, 10:1615-1618.
• [17]Riddle DL, Albert PS: Genetic and environmental regulation of dauer larva development. In C. elegans II. Edited by Priess JR. Cold Spring Harbor Laboratory Press; 1997:739-768.
• [18]Doniach T, Hodgkin J: A sex-determining gene, fem-1, required for both male and hermaphrodite development in Caenorhabditis elegans. Dev Biol 1984, 106:223-235.
• [19]Hodgkin J, Papp A, Pulak R, Ambros V, Anderson P: A new kind of informational suppression in the nematode Caenorhabditis elegans. Genetics 1989, 123:301-313.
• [20]Page MF, Carr B, Anders KR, Grimson A, Anderson P: SMG-2 is a phosphorylated protein required for mRNA surveillance in Caenorhabditis elegans and related to Upf1p of yeast. Mol Cell Biol 1999, 19:5943-5951.
• [21]Cali BM, Anderson P: mRNA surveillance mitigates genetic dominance in Caenorhabditis elegans. Mol Gen Genet 1998, 260:176-184.
• [22]Fire A, Harrison SW, Dixon D: A modular set of lacZ fusion vectors for studying gene expression in Caenorhabditis elegans. Gene 1990, 93:189-198.
• [23]Kelly WG, Xu S, Montgomery MK, Fire A: Distinct requirements for somatic and germline expression of a generally expressed Caernorhabditis elegans gene. Genetics 1997, 146:227-238.
• [24]L'Hernault SW, Roberts TM: Cell biology of nematode sperm. Methods Cell Biol 1995, 48:273-301.