Mating Induces Shrinking and Death in Caenorhabditis Mothers

Overview

Journal Science

Specialty Science

Date 2013 Dec 21

PMID 24356112

Citations 70

Authors

Cheng Shi

Coleen T Murphy

Affiliations

Soon will be listed here.

Abstract

Interactions between the germ line and the soma help optimize reproductive success. We discovered a phenomenon linking reproductive status to longevity: In both hermaphroditic and gonochoristic Caenorhabditis, mating leads to female shrinking and death, compressing postreproductive life span. Male sperm induces germline- and DAF-9/DAF-12-dependent shrinking, osmotic stress susceptibility, and subsequent life-span decrease, whereas seminal fluid induces DAF-16-dependent life-span decrease and fat loss. Our study provides insight into the communication between males and the female germ line and soma to regulate reproduction and longevity, revealing a high-reproduction, low-life-span state induced by mating. Postmating somatic collapse may be an example of the sexually antagonistic influence that males in many species exert on female behavior to maximize their own reproductive success.

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References

Kokko H, Brooks R, Jennions M, Morley J . The evolution of mate choice and mating biases. Proc Biol Sci. 2003; 270(1515):653-64. PMC: 1691281. DOI: 10.1098/rspb.2002.2235. View

Kimble J, Crittenden S . Germline proliferation and its control. WormBook. 2007; :1-14. PMC: 4781503. DOI: 10.1895/wormbook.1.13.1. View

Lamitina S, Strange K . Transcriptional targets of DAF-16 insulin signaling pathway protect C. elegans from extreme hypertonic stress. Am J Physiol Cell Physiol. 2004; 288(2):C467-74. DOI: 10.1152/ajpcell.00451.2004. View

Wu D, Tedesco P, Phillips P, Johnson T . Fertility/longevity trade-offs under limiting-male conditions in mating populations of Caenorhabditis elegans. Exp Gerontol. 2012; 47(10):759-63. PMC: 3437009. DOI: 10.1016/j.exger.2012.06.010. View

Gems D, Riddle D . Longevity in Caenorhabditis elegans reduced by mating but not gamete production. Nature. 1996; 379(6567):723-5. DOI: 10.1038/379723a0. View

Luo S, Murphy C . Caenorhabditis elegans reproductive aging: Regulation and underlying mechanisms. Genesis. 2010; 49(2):53-65. DOI: 10.1002/dvg.20694. View

Lapierre L, Gelino S, Melendez A, Hansen M . Autophagy and lipid metabolism coordinately modulate life span in germline-less C. elegans. Curr Biol. 2011; 21(18):1507-14. PMC: 3191188. DOI: 10.1016/j.cub.2011.07.042. View

Morsci N, Haas L, Barr M . Sperm status regulates sexual attraction in Caenorhabditis elegans. Genetics. 2011; 189(4):1341-6. PMC: 3241412. DOI: 10.1534/genetics.111.133603. View

Murphy C, Lee S, Kenyon C . Tissue entrainment by feedback regulation of insulin gene expression in the endoderm of Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2007; 104(48):19046-50. PMC: 2141905. DOI: 10.1073/pnas.0709613104. View

10.

Kenyon C . The genetics of ageing. Nature. 2010; 464(7288):504-12. DOI: 10.1038/nature08980. View

11.

Murphy C, McCarroll S, Bargmann C, Fraser A, Kamath R, Ahringer J . Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature. 2003; 424(6946):277-83. DOI: 10.1038/nature01789. View

12.

Sun A, Lambie E . gon-2, a gene required for gonadogenesis in Caenorhabditis elegans. Genetics. 1998; 147(3):1077-89. PMC: 1208235. DOI: 10.1093/genetics/147.3.1077. View

13.

Wolfner M . "S.P.E.R.M." (seminal proteins (are) essential reproductive modulators): the view from Drosophila. Soc Reprod Fertil Suppl. 2007; 65:183-99. View

14.

Berman J, Kenyon C . Germ-cell loss extends C. elegans life span through regulation of DAF-16 by kri-1 and lipophilic-hormone signaling. Cell. 2006; 124(5):1055-68. DOI: 10.1016/j.cell.2006.01.039. View

15.

ORourke E, Soukas A, Carr C, Ruvkun G . C. elegans major fats are stored in vesicles distinct from lysosome-related organelles. Cell Metab. 2009; 10(5):430-5. PMC: 2921818. DOI: 10.1016/j.cmet.2009.10.002. View

16.

McCormick M, Chen K, Ramaswamy P, Kenyon C . New genes that extend Caenorhabditis elegans' lifespan in response to reproductive signals. Aging Cell. 2011; 11(2):192-202. PMC: 4342234. DOI: 10.1111/j.1474-9726.2011.00768.x. View

17.

Argon Y, Ward S . Caenorhabditis elegans fertilization-defective mutants with abnormal sperm. Genetics. 1980; 96(2):413-33. PMC: 1214308. DOI: 10.1093/genetics/96.2.413. View

18.

Fisher A, Lithgow G . The nuclear hormone receptor DAF-12 has opposing effects on Caenorhabditis elegans lifespan and regulates genes repressed in multiple long-lived worms. Aging Cell. 2006; 5(2):127-38. DOI: 10.1111/j.1474-9726.2006.00203.x. View

19.

Luo S, Kleemann G, Ashraf J, Shaw W, Murphy C . TGF-β and insulin signaling regulate reproductive aging via oocyte and germline quality maintenance. Cell. 2010; 143(2):299-312. PMC: 2955983. DOI: 10.1016/j.cell.2010.09.013. View

20.

Hsin H, Kenyon C . Signals from the reproductive system regulate the lifespan of C. elegans. Nature. 1999; 399(6734):362-6. DOI: 10.1038/20694. View