Multigenerational downregulation of insulin/IGF-1 signaling in adulthood improves lineage survival, reproduction, and fitness in Caenorhabditis elegans supporting the developmental theory of ageing.
Ageing
germline
life-history evolution
mutation accumulation
senescence
Journal
Evolution; international journal of organic evolution
ISSN: 1558-5646
Titre abrégé: Evolution
Pays: United States
ID NLM: 0373224
Informations de publication
Date de publication:
12 2022
12 2022
Historique:
revised:
18
07
2022
received:
21
03
2022
accepted:
08
09
2022
pubmed:
7
10
2022
medline:
20
12
2022
entrez:
6
10
2022
Statut:
ppublish
Résumé
Adulthood-only downregulation of insulin/IGF-1 signaling (IIS), an evolutionarily conserved pathway regulating resource allocation between somatic maintenance and reproduction, increases life span without fecundity cost in the nematode, Caenorhabditis elegans. However, long-term multigenerational effects of reduced IIS remain unexplored and are proposed to carry costs for offspring quality. To test this hypothesis, we ran a mutation accumulation (MA) experiment and downregulated IIS in half of the 400 MA lines by silencing daf-2 gene expression using RNA interference (RNAi) across 40 generations. Contrary to the prediction, adulthood-only daf-2 RNAi reduced extinction of MA lines both under UV-induced and spontaneous MA. Fitness of the surviving UV-induced MA lines was higher under daf-2 RNAi. Reduced IIS increased intergenerational F1 offspring fitness under UV stress but had no quantifiable transgenerational effects. Functional hrde-1 was required for the benefits of multigenerational daf-2 RNAi. Overall, we found net benefit to fitness from multigenerational reduction of IIS and the benefits became more apparent under stress. Because reduced daf-2 expression during development carries fitness costs, we suggest that our findings are best explained by the developmental theory of ageing, which maintains that the decline in the force of selection with age results in poorly regulated gene expression in adulthood.
Identifiants
pubmed: 36199198
doi: 10.1111/evo.14640
pmc: PMC10092551
doi:
Substances chimiques
Caenorhabditis elegans Proteins
0
Insulin
0
Insulin-Like Growth Factor I
67763-96-6
Receptor, Insulin
EC 2.7.10.1
Banques de données
figshare
['10.6084/m9.figshare.12783650.v1']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2829-2845Informations de copyright
© 2022 The Authors. Evolution published by Wiley Periodicals LLC on behalf of The Society for the Study of Evolution.
Références
Nature. 2010 Mar 25;464(7288):504-12
pubmed: 20336132
Evolution. 2000 Aug;54(4):1234-46
pubmed: 11005291
Nucleic Acids Res. 2008 Mar;36(4):1380-9
pubmed: 18203746
Epigenetics Chromatin. 2016 Jan 15;9:3
pubmed: 26779286
Proc Natl Acad Sci U S A. 2008 Apr 29;105(17):6368-73
pubmed: 18434551
J Vis Exp. 2020 May 28;(159):
pubmed: 32538915
Evol Lett. 2021 Sep 08;5(5):551-564
pubmed: 34621540
J Gerontol A Biol Sci Med Sci. 2016 Jul;71(7):882-90
pubmed: 26472877
Genetics. 1985 May;110(1):17-72
pubmed: 3996896
Basic Life Sci. 1987;42:209-18
pubmed: 3435387
J Theor Biol. 1966 Sep;12(1):12-45
pubmed: 6015424
Ecology. 2019 Jul;100(7):e02706
pubmed: 30916779
Ageing Res Rev. 2005 Jan;4(1):67-82
pubmed: 15619471
Proc Natl Acad Sci U S A. 2020 Apr 21;117(16):8973-8979
pubmed: 32245815
Genetics. 2020 Jan;214(1):3-48
pubmed: 31907300
Mutat Res. 2010 Jan 5;683(1-2):57-67
pubmed: 19879883
Genes Dev. 2020 May 1;34(9-10):678-687
pubmed: 32217667
Genome Res. 2014 Oct;24(10):1624-36
pubmed: 25030888
Nature. 2013 Sep 19;501(7467):416-20
pubmed: 23975097
Genome Biol Evol. 2012;4(4):513-22
pubmed: 22436997
Bioessays. 2000 Dec;22(12):1057-66
pubmed: 11084621
PLoS Genet. 2016 Oct 26;12(10):e1006396
pubmed: 27783623
Nature. 1977 Nov 24;270(5635):301-4
pubmed: 593350
Exp Gerontol. 2013 Jul;48(7):596-602
pubmed: 23063987
Science. 2002 Oct 25;298(5594):830-4
pubmed: 12399591
Genetics. 2017 Jul;206(3):1403-1416
pubmed: 28533440
Cell. 2014 Jul 17;158(2):277-287
pubmed: 25018105
Curr Biol. 2018 Aug 20;28(16):2544-2556.e5
pubmed: 30100339
Aging Cell. 2013 Oct;12(5):814-22
pubmed: 23734734
Proc R Soc Lond B Biol Sci. 1979 Sep 21;205(1161):531-46
pubmed: 42059
Evolution. 2009 Jun;63(6):1473-82
pubmed: 19210536
Proc Biol Sci. 2019 Sep 25;286(1911):20191604
pubmed: 31530150
Mech Ageing Dev. 2003 Jan;124(1):43-8
pubmed: 12618005
Methods Mol Biol. 2013;965:485-500
pubmed: 23296679
Nature. 1999 May 27;399(6734):362-6
pubmed: 10360574
Genetics. 2017 May;206(1):55-86
pubmed: 28476862
Mol Cell. 2015 Aug 20;59(4):639-50
pubmed: 26212459
BMC Biol. 2018 Aug 20;16(1):93
pubmed: 30124168
J Exp Zool. 1949 Dec;112(3):485-503
pubmed: 15404785
Nature. 2012 Sep 20;489(7416):447-51
pubmed: 22810588
Methods. 2014 Aug 1;68(3):450-7
pubmed: 24780523
Cell Cycle. 2013 Dec 15;12(24):3736-42
pubmed: 24240128
Trends Ecol Evol. 2020 Apr;35(4):300-302
pubmed: 31973962
Nat Rev Mol Cell Biol. 2010 Aug;11(8):545-55
pubmed: 20628411
Annu Rev Physiol. 2013;75:621-44
pubmed: 23190075
FASEB J. 2012 Dec;26(12):4821-6
pubmed: 22964300
Aging Cell. 2013 Dec;12(6):1073-81
pubmed: 23879233
Science. 2010 Apr 16;328(5976):321-6
pubmed: 20395504
Curr Biol. 2016 Jul 11;26(13):R577-R586
pubmed: 27404253
Proc Biol Sci. 2017 Nov 15;284(1866):
pubmed: 29118134
J Evol Biol. 2005 Jan;18(1):27-34
pubmed: 15669958
Elife. 2015 Mar 30;4:
pubmed: 25822066
Proc Biol Sci. 2021 May 12;288(1950):20210701
pubmed: 33975472
Genetics. 2000 Mar;154(3):1193-201
pubmed: 10757763
Nat Methods. 2019 Jul;16(7):565-566
pubmed: 31217592
Cell. 2019 Jun 13;177(7):1814-1826.e15
pubmed: 31178120
Nature. 1998 Feb 19;391(6669):806-11
pubmed: 9486653
Proc Natl Acad Sci U S A. 2005 Apr 19;102(16):5785-90
pubmed: 15809433
Front Cell Dev Biol. 2021 Sep 16;9:718522
pubmed: 34604218
Cell. 1989 Aug 25;58(4):679-93
pubmed: 2548732
Gene. 2001 Jan 24;263(1-2):103-12
pubmed: 11223248
NPJ Aging Mech Dis. 2018 Jun 13;4:6
pubmed: 29928508
Physiology (Bethesda). 2005 Aug;20:252-9
pubmed: 16024513
Genome Biol. 2007;8(5):R70
pubmed: 17472752
Evol Lett. 2019 Mar 04;3(2):207-216
pubmed: 31007945
Science. 2002 Jan 18;295(5554):502-5
pubmed: 11799246
Cell Death Differ. 2007 Jun;14(6):1129-38
pubmed: 17347667
Trends Ecol Evol. 2009 Mar;24(3):127-35
pubmed: 19185386
J Gerontol A Biol Sci Med Sci. 2007 Feb;62(2):126-35
pubmed: 17339638
Nat Commun. 2014 Sep 11;5:4879
pubmed: 25209682
Proc Biol Sci. 2021 Feb 10;288(1944):20201728
pubmed: 33529563
Exp Gerontol. 2011 May;46(5):369-75
pubmed: 20970491
Science. 2003 May 16;300(5622):1142-5
pubmed: 12750521
Genetics. 2005 Jun;170(2):655-60
pubmed: 15834141
Exp Gerontol. 2006 Oct;41(10):1059-65
pubmed: 16963216