title: Dramatic fertility decline in aging C. elegans males is associated with mating execution deficits rather than diminished sperm quality.
abstract: Although much is known about female reproductive aging, fairly little is known about the causes of male reproductive senescence. We developed a method that facilitates culture maintenance of Caenorhabditis elegans adult males, which enabled us to measure male fertility as populations age, without profound loss of males from the growth plate. We find that the ability of males to sire progeny declines rapidly in the first half of adult lifespan and we examined potential factors that contribute towards reproductive success, including physical vigor, sperm quality, mating apparatus morphology, and mating ability. Of these, we find little evidence of general physical decline in males or changes in sperm number, morphology, or capacity for activation, at time points when reproductive senescence is markedly evident. Rather, it is the loss of efficient mating ability that correlates most strongly with reproductive senescence. Low insulin signaling can extend male ability to sire progeny later in life, although insulin impact on individual facets of mating behavior is complex. Overall, we suggest that combined modest deficits, predominantly affecting the complex mating behavior rather than sperm quality, sum up to block effective C. elegans male reproduction in middle adult life.
authors.affiliation: Dept. of Genetics and Waksman Institute, Rutgers University, USA. Electronic address: chatti01@nyu.edu.
authors.forename: Indrani
authors.initials: I
authors.lastname: Chatterjee
authors.forename: Carolina
authors.initials: C
authors.lastname: Ibanez-Ventoso
authors.forename: Priyanka
authors.initials: P
authors.lastname: Vijay
authors.forename: Gunasekaran
authors.initials: G
authors.lastname: Singaravelu
authors.forename: Christopher
authors.initials: C
authors.lastname: Baldi
authors.forename: Julianna
authors.initials: J
authors.lastname: Bair
authors.forename: Susan
authors.initials: S
authors.lastname: Ng
authors.forename: Alexandra
authors.initials: A
authors.lastname: Smolyanskaya
authors.forename: Monica
authors.initials: M
authors.lastname: Driscoll
authors.forename: Andrew
authors.initials: A
authors.lastname: Singson
mesh_terms: D000375:Aging / Q000473:pathology / Q000502:physiology*; D000818:Animals; D017173:Caenorhabditis elegans / Q000033:anatomy & histology / Q000235:genetics / Q000502:physiology*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000502:physiology; D003470:Culture Media; D005260:Female; D005298:Fertility / Q000502:physiology*; D051858:Forkhead Transcription Factors; D005737:Garlic; D017238:Genes, Helminth; D007328:Insulin / Q000502:physiology; D008297:Male; D023421:Models, Animal; D009154:Mutation; D011972:Receptor, Insulin / Q000235:genetics / Q000502:physiology; D012726:Sexual Behavior, Animal / Q000502:physiology*; D015398:Signal Transduction; D013076:Sperm Count; D013094:Spermatozoa / Q000502:physiology; D014157:Transcription Factors / Q000235:genetics / Q000502:physiology
chemical_list: D029742:Caenorhabditis elegans Proteins; D003470:Culture Media; D051858:Forkhead Transcription Factors; D007328:Insulin; D014157:Transcription Factors; C108831:daf-16 protein, C elegans; C107483:DAF-2 protein, C elegans; D011972:Receptor, Insulin
keywords: Aging; C. elegans; Fertility; Males; Sperm
references.citation: PLoS Med. 2009 Mar 10;6(3):e40
references.pmid: 19278291
references.citation: Genetica. 1993;91(1-3):65-77
references.pmid: 8125279
references.citation: WormBook. 2005 Nov 10;:1-22
references.pmid: 18050419
references.citation: Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1598-603
references.pmid: 11818544
references.citation: Exp Gerontol. 2011 Jun;46(6):441-52
references.pmid: 21296648
references.citation: Nature. 2010 Mar 25;464(7288):504-12
references.pmid: 20336132
references.citation: J Pathol. 2007 Jan;211(2):219-31
references.pmid: 17200943
references.citation: Aging Cell. 2003 Jun;2(3):165-73
references.pmid: 12882409
references.citation: Genetics. 2011 Sep;189(1):341-56
references.pmid: 21750263
references.citation: Proc Natl Acad Sci U S A. 1987 Jun;84(11):3777-81
references.pmid: 3473482
references.citation: Obstet Gynecol. 2005 May;105(5 Pt 1):983-90
references.pmid: 15863534
references.citation: Mech Ageing Dev. 1977 Nov-Dec;6(6):413-29
references.pmid: 926867
references.citation: J Neurosci. 2004 Aug 25;24(34):7427-34
references.pmid: 15329389
references.citation: Nature. 1977 Nov 24;270(5635):301-4
references.pmid: 593350
references.citation: J Neurosci. 2011 Jun 22;31(25):9279-88
references.pmid: 21697377
references.citation: Dev Biol. 2001 Feb 15;230(2):101-9
references.pmid: 11161565
references.citation: Ann N Y Acad Sci. 2010 Aug;1204:156-62
references.pmid: 20738286
references.citation: Genesis. 2013 Jan;51(1):1-15
references.pmid: 22945891
references.citation: Genetics. 1998 Sep;150(1):129-55
references.pmid: 9725835
references.citation: J Reprod Fertil. 1979 Nov;57(2):253-9
references.pmid: 513013
references.citation: Eur J Hum Genet. 2011 Feb;19(2):145-51
references.pmid: 21045871
references.citation: Cell. 2010 Oct 15;143(2):299-312
references.pmid: 20946987
references.citation: Genetics. 1998 Feb;148(2):703-17
references.pmid: 9504918
references.citation: Nature. 1999 May 27;399(6734):362-6
references.pmid: 10360574
references.citation: PLoS Genet. 2011 Mar;7(3):e1001326
references.pmid: 21423722
references.citation: Hum Reprod. 2002 Jun;17(6):1437-40
references.pmid: 12042257
references.citation: J Neurosci. 2010 Jun 9;30(23):8001-11
references.pmid: 20534848
references.citation: Aging Cell. 2011 Feb;10(1):5-9
references.pmid: 21078113
references.citation: J Evol Biol. 2009 Feb;22(2):334-44
references.pmid: 19032491
references.citation: Proc Natl Acad Sci U S A. 2011 May 31;108(22):9274-9
references.pmid: 21571636
references.citation: PLoS Genet. 2007 Feb 16;3(2):e25
references.pmid: 17305431
references.citation: Genetics. 1999 May;152(1):201-8
references.pmid: 10224254
references.citation: PLoS Genet. 2009 Dec;5(12):e1000789
references.pmid: 20041217
references.citation: Methods Cell Biol. 2011;106:343-75
references.pmid: 22118284
references.citation: Nature. 1993 Dec 2;366(6454):461-4
references.pmid: 8247153
references.citation: J Vis Exp. 2011 Jan 31;(47):
references.pmid: 21307834
references.citation: Neurobiol Aging. 2012 Jul;33(7):1483.e5-23
references.pmid: 22285759
references.citation: Exp Aging Res. 1977 May;3(3):175-89
references.pmid: 334555
references.citation: Exp Gerontol. 2012 Oct;47(10):759-63
references.pmid: 22771817
references.citation: Cell. 2001 Dec 14;107(6):777-88
references.pmid: 11747813
references.citation: Science. 1997 Nov 14;278(5341):1319-22
references.pmid: 9360933
references.citation: PLoS Genet. 2008 Dec;4(12):e1000295
references.pmid: 19057674
references.citation: Nature. 1997 Oct 30;389(6654):994-9
references.pmid: 9353126
references.citation: Exp Gerontol. 1980;15(4):285-9
references.pmid: 7409025
references.citation: Fetal Diagn Ther. 2011;29(4):263-73
references.pmid: 21228557
references.citation: Genetics. 1988 Oct;120(2):435-52
references.pmid: 3197956
references.citation: Nature. 1996 Feb 22;379(6567):723-5
references.pmid: 8602217
references.citation: Science. 2003 Apr 25;300(5619):644-7
references.pmid: 12690206
references.citation: Genetics. 2000 Apr;154(4):1597-610
references.pmid: 10747056
references.citation: Proc Natl Acad Sci U S A. 2004 May 25;101(21):8084-9
references.pmid: 15141086
references.citation: Genetics. 1974 May;77(1):71-94
references.pmid: 4366476
references.citation: Neuron. 1995 Jan;14(1):79-89
references.pmid: 7826644
references.citation: WormBook. 2006 Jun 19;:1-11
references.pmid: 18050467
references.citation: Nature. 2012 Aug 23;488(7412):471-5
references.pmid: 22914163
references.citation: J Gerontol A Biol Sci Med Sci. 2011 Dec;66(12):1300-8
references.pmid: 21975091
references.citation: Int J Dev Biol. 2008;52(5-6):647-56
references.pmid: 18649278
references.citation: Dev Biol. 1989 Aug;134(2):307-16
references.pmid: 2744235
references.citation: Nat Genet. 2005 Aug;37(8):894-8
references.pmid: 16041374
references.citation: J Gerontol A Biol Sci Med Sci. 2004 Dec;59(12):1251-60
references.pmid: 15699524
references.citation: Science. 2002 Jan 18;295(5554):502-5
references.pmid: 11799246
references.citation: Am J Physiol. 1947 Sep;150(3):511-9
references.pmid: 20265851
references.citation: Science. 2012 Jan 6;335(6064):82-5
references.pmid: 22174126
references.citation: Mech Ageing Dev. 2005 Sep;126(9):938-50
references.pmid: 15935441
references.citation: BMC Dev Biol. 2003 Dec 03;3:10
references.pmid: 14653860
references.citation: J Neurosci. 2012 Jun 27;32(26):8778-90
references.pmid: 22745480
references.citation: WormBook. 2008 Jan 24;:1-21
references.pmid: 18381800
references.citation: J Nutr. 1960 Jul;71(3):242-54
references.pmid: 13799207
references.citation: Science. 1997 Aug 15;277(5328):942-6
references.pmid: 9252323
references.citation: Neurobiol Aging. 2005 Jun;26(6):899-905
references.pmid: 15718049
references.citation: Dis Model Mech. 2010 Jul-Aug;3(7-8):415-9
references.pmid: 20354111
references.citation: Curr Biol. 2008 Dec 9;18(23):1865-71
references.pmid: 19062284
references.citation: Science. 2003 May 16;300(5622):1142-5
references.pmid: 12750521
references.citation: Reprod Biol Endocrinol. 2012 Mar 19;10:19
references.pmid: 22429861
references.citation: Nature. 2002 Oct 24;419(6909):808-14
references.pmid: 12397350
references.citation: Curr Top Dev Biol. 1996;33:103-58
references.pmid: 9138905
references.citation: Cell. 1980 Feb;19(2):457-64
references.pmid: 7357613
references.citation: Methods Cell Biol. 1995;48:273-301
references.pmid: 8531729
references.citation: J Nutr. 1960 Jul;71:255-63
references.pmid: 13855553
references.citation: J Gerontol A Biol Sci Med Sci. 2011 Aug;66(8):842-54
references.pmid: 21622982