Europe PMC

This website requires cookies, and the limited processing of your personal data in order to function. By using the site you are agreeing to this as outlined in our privacy notice and cookie policy.

Abstract 


Males of the nematode Caenorhabditis elegans are shorter lived than hermaphrodites when maintained in single-sex groups. We observed that groups of young males form clumps and that solitary males live longer, indicating that male-male interactions reduce life span. By contrast, grouped or isolated hermaphrodites exhibited the same longevity. In one wild isolate of C. elegans, AB2, there was evidence of copulation between males. Nine uncoordinated (unc) mutations were used to block clumping behavior. These mutations had little effect on hermaphrodite life span in most cases, yet many increased male longevity even beyond that of solitary wild-type males. In one case, the neuronal function mutant unc-64(e246), hermaphrodite life span was also increased by up to 60%. The longevity of unc-4(e120), unc-13(e51), and unc-32(e189) males exceeded that of hermaphrodites by 70-120%. This difference appears to reflect a difference in sex-specific life span potential revealed in the absence of male behavior that is detrimental to survival. The greater longevity of males appears not to be affected by daf-2, but is influenced by daf-16. In the absence of male-male interactions, median (but not maximum) male life span was variable. This variability was reduced when dead bacteria were used as food. Maintenance on dead bacteria extended both male and hermaphrodite longevity.

Free full text 


Logo of geneticsLink to Publisher's site
Genetics. 2000 Apr; 154(4): 1597–1610.
PMCID: PMC1461011
PMID: 10747056

Genetic, behavioral and environmental determinants of male longevity in Caenorhabditis elegans.

Abstract

Males of the nematode Caenorhabditis elegans are shorter lived than hermaphrodites when maintained in single-sex groups. We observed that groups of young males form clumps and that solitary males live longer, indicating that male-male interactions reduce life span. By contrast, grouped or isolated hermaphrodites exhibited the same longevity. In one wild isolate of C. elegans, AB2, there was evidence of copulation between males. Nine uncoordinated (unc) mutations were used to block clumping behavior. These mutations had little effect on hermaphrodite life span in most cases, yet many increased male longevity even beyond that of solitary wild-type males. In one case, the neuronal function mutant unc-64(e246), hermaphrodite life span was also increased by up to 60%. The longevity of unc-4(e120), unc-13(e51), and unc-32(e189) males exceeded that of hermaphrodites by 70-120%. This difference appears to reflect a difference in sex-specific life span potential revealed in the absence of male behavior that is detrimental to survival. The greater longevity of males appears not to be affected by daf-2, but is influenced by daf-16. In the absence of male-male interactions, median (but not maximum) male life span was variable. This variability was reduced when dead bacteria were used as food. Maintenance on dead bacteria extended both male and hermaphrodite longevity.

Full Text

The Full Text of this article is available as a PDF (194K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Hsin H, Kenyon C. Signals from the reproductive system regulate the lifespan of C. elegans. Nature. 1999 May 27;399(6734):362–366. [Abstract] [Google Scholar]
  • Johnson TE. Increased life-span of age-1 mutants in Caenorhabditis elegans and lower Gompertz rate of aging. Science. 1990 Aug 24;249(4971):908–912. [Abstract] [Google Scholar]
  • Johnson TE, Hutchinson EW. Absence of strong heterosis for life span and other life history traits in Caenorhabditis elegans. Genetics. 1993 Jun;134(2):465–474. [Europe PMC free article] [Abstract] [Google Scholar]
  • Johnson TE, Wood WB. Genetic analysis of life-span in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6603–6607. [Europe PMC free article] [Abstract] [Google Scholar]
  • Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R. A C. elegans mutant that lives twice as long as wild type. Nature. 1993 Dec 2;366(6454):461–464. [Abstract] [Google Scholar]
  • Ailion M, Inoue T, Weaver CI, Holdcraft RW, Thomas JH. Neurosecretory control of aging in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1999 Jun 22;96(13):7394–7397. [Europe PMC free article] [Abstract] [Google Scholar]
  • Kimura KD, Tissenbaum HA, Liu Y, Ruvkun G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science. 1997 Aug 15;277(5328):942–946. [Abstract] [Google Scholar]
  • Ailion M, Inoue T, Weaver CI, Holdcraft RW, Thomas JH. Neurosecretory control of aging in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1999 Jun 22;96(13):7394–7397. [Europe PMC free article] [Abstract] [Google Scholar]
  • Apfeld J, Kenyon C. Cell nonautonomy of C. elegans daf-2 function in the regulation of diapause and life span. Cell. 1998 Oct 16;95(2):199–210. [Abstract] [Google Scholar]
  • Klass MR. Aging in the nematode Caenorhabditis elegans: major biological and environmental factors influencing life span. Mech Ageing Dev. 1977 Nov-Dec;6(6):413–429. [Abstract] [Google Scholar]
  • Lakowski B, Hekimi S. The genetics of caloric restriction in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1998 Oct 27;95(22):13091–13096. [Europe PMC free article] [Abstract] [Google Scholar]
  • Larsen PL, Albert PS, Riddle DL. Genes that regulate both development and longevity in Caenorhabditis elegans. Genetics. 1995 Apr;139(4):1567–1583. [Europe PMC free article] [Abstract] [Google Scholar]
  • Bronson RT. Age at death of necropsied intact and neutered cats. Am J Vet Res. 1981 Sep;42(9):1606–1608. [Abstract] [Google Scholar]
  • Lin K, Dorman JB, Rodan A, Kenyon C. daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science. 1997 Nov 14;278(5341):1319–1322. [Abstract] [Google Scholar]
  • Carey JR, Liedo P, Orozco D, Vaupel JW. Slowing of mortality rates at older ages in large medfly cohorts. Science. 1992 Oct 16;258(5081):457–461. [Abstract] [Google Scholar]
  • Malone EA, Inoue T, Thomas JH. Genetic analysis of the roles of daf-28 and age-1 in regulating Caenorhabditis elegans dauer formation. Genetics. 1996 Jul;143(3):1193–1205. [Europe PMC free article] [Abstract] [Google Scholar]
  • Masoro EJ. Dietary restriction. Exp Gerontol. 1995 May-Aug;30(3-4):291–298. [Abstract] [Google Scholar]
  • Croll NA, Smith JM, Zuckerman BM. The aging process of the nematode Caenorhabditis elegans in bacterial and axenic culture. Exp Aging Res. 1977 May;3(3):175–189. [Abstract] [Google Scholar]
  • Mitchell DH, Stiles JW, Santelli J, Sanadi DR. Synchronous growth and aging of Caenorhabditis elegans in the presence of fluorodeoxyuridine. J Gerontol. 1979 Jan;34(1):28–36. [Abstract] [Google Scholar]
  • Curtsinger JW, Fukui HH, Townsend DR, Vaupel JW. Demography of genotypes: failure of the limited life-span paradigm in Drosophila melanogaster. Science. 1992 Oct 16;258(5081):461–463. [Abstract] [Google Scholar]
  • Ogg S, Paradis S, Gottlieb S, Patterson GI, Lee L, Tissenbaum HA, Ruvkun G. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature. 1997 Oct 30;389(6654):994–999. [Abstract] [Google Scholar]
  • Diamond JM. Big-bang reproduction and ageing in male marsupial mice. Nature. 1982 Jul 8;298(5870):115–116. [Abstract] [Google Scholar]
  • Dorman JB, Albinder B, Shroyer T, Kenyon C. The age-1 and daf-2 genes function in a common pathway to control the lifespan of Caenorhabditis elegans. Genetics. 1995 Dec;141(4):1399–1406. [Europe PMC free article] [Abstract] [Google Scholar]
  • Ragland SS, Sohal RS. Mating behavior, physical activity and aging in the housefly, Musca domestica. Exp Gerontol. 1973 Jun;8(3):135–145. [Abstract] [Google Scholar]
  • Friedman DB, Johnson TE. A mutation in the age-1 gene in Caenorhabditis elegans lengthens life and reduces hermaphrodite fertility. Genetics. 1988 Jan;118(1):75–86. [Europe PMC free article] [Abstract] [Google Scholar]
  • Riddle DL, Swanson MM, Albert PS. Interacting genes in nematode dauer larva formation. Nature. 1981 Apr 23;290(5808):668–671. [Abstract] [Google Scholar]
  • Robertson OH. PROLONGATION OF THE LIFE SPAN OF KOKANEE SALMON (ONCORHYNCHUS NERKA KENNERLYI) BY CASTRATION BEFORE BEGINNING OF GONAD DEVELOPMENT. Proc Natl Acad Sci U S A. 1961 Apr;47(4):609–621. [Europe PMC free article] [Abstract] [Google Scholar]
  • Gems D, Sutton AJ, Sundermeyer ML, Albert PS, King KV, Edgley ML, Larsen PL, Riddle DL. Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans. Genetics. 1998 Sep;150(1):129–155. [Europe PMC free article] [Abstract] [Google Scholar]
  • ROCKSTEIN M, LIEBERMAN HM. A life table for the common house fly, Musca domestica. Gerontologia. 1959;3:23–36. [Abstract] [Google Scholar]
  • HAMILTON JB. RELATIONSHIP OF CASTRATION, SPAYING, AND SEX TO SURVIVAL AND DURATION OF LIFE IN DOMESTIC CATS. J Gerontol. 1965 Jan;20:96–104. [Abstract] [Google Scholar]
  • Saifee O, Wei L, Nonet ML. The Caenorhabditis elegans unc-64 locus encodes a syntaxin that interacts genetically with synaptobrevin. Mol Biol Cell. 1998 Jun;9(6):1235–1252. [Europe PMC free article] [Abstract] [Google Scholar]
  • Hamilton JB, Mestler GE. Mortality and survival: comparison of eunuchs with intact men and women in a mentally retarded population. J Gerontol. 1969 Oct;24(4):395–411. [Abstract] [Google Scholar]
  • Schedl T, Kimble J. fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics. 1988 May;119(1):43–61. [Europe PMC free article] [Abstract] [Google Scholar]
  • Smith DW. Is greater female longevity a general finding among animals? Biol Rev Camb Philos Soc. 1989 Feb;64(1):1–12. [Abstract] [Google Scholar]
  • Hodgkin J. Male Phenotypes and Mating Efficiency in CAENORHABDITIS ELEGANS. Genetics. 1983 Jan;103(1):43–64. [Europe PMC free article] [Abstract] [Google Scholar]
  • Hodgkin J, Doniach T. Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics. 1997 May;146(1):149–164. [Europe PMC free article] [Abstract] [Google Scholar]
  • Vanfleteren JR, De Vreese A. The gerontogenes age-1 and daf-2 determine metabolic rate potential in aging Caenorhabditis elegans. FASEB J. 1995 Oct;9(13):1355–1361. [Abstract] [Google Scholar]
  • Vanfleteren JR, De Vreese A, Braeckman BP. Two-parameter logistic and Weibull equations provide better fits to survival data from isogenic populations of Caenorhabditis elegans in axenic culture than does the Gompertz model. J Gerontol A Biol Sci Med Sci. 1998 Nov;53(6):B393–B408. [Abstract] [Google Scholar]
  • Vaupel JW, Carey JR, Christensen K, Johnson TE, Yashin AI, Holm NV, Iachine IA, Kannisto V, Khazaeli AA, Liedo P, et al. Biodemographic trajectories of longevity. Science. 1998 May 8;280(5365):855–860. [Abstract] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

Citations & impact 


Impact metrics

Jump to Citations
Jump to Data

Citations of article over time

Alternative metrics

Altmetric item for https://www.altmetric.com/details/85690261
Altmetric
Discover the attention surrounding your research
https://www.altmetric.com/details/85690261

Article citations


Go to all (171) article citations

Data 


Funding 


Funders who supported this work.

NIA NIH HHS (1)