Gene Coexpression Network Reveals Highly Conserved, Well-Regulated Anti-Ageing Mechanisms in Old Ant Queens.
ageing
longevity/fecundity trade-off
selection shadow
social insects
Journal
Genome biology and evolution
ISSN: 1759-6653
Titre abrégé: Genome Biol Evol
Pays: England
ID NLM: 101509707
Informations de publication
Date de publication:
08 06 2021
08 06 2021
Historique:
accepted:
23
04
2021
pubmed:
5
5
2021
medline:
10
2
2022
entrez:
4
5
2021
Statut:
ppublish
Résumé
Evolutionary theories of ageing predict a reduction in selection efficiency with age, a so-called "selection shadow," due to extrinsic mortality decreasing effective population size with age. Classic symptoms of ageing include a deterioration in transcriptional regulation and protein homeostasis. Understanding how ant queens defy the trade-off between fecundity and lifespan remains a major challenge for the evolutionary theory of ageing. It has often been discussed that the low extrinsic mortality of ant queens, that are generally well protected within the nest by workers and soldiers, should reduce the selection shadow acting on old queens. We tested this by comparing strength of selection acting on genes upregulated in young and old queens of the ant, Cardiocondyla obscurior. In support of a reduced selection shadow, we find old-biased genes to be under strong purifying selection. We also analyzed a gene coexpression network (GCN) with the aim to detect signs of ageing in the form of deteriorating regulation and proteostasis. We find no evidence for ageing. In fact, we detect higher connectivity in old queens indicating increased transcriptional regulation with age. Within the GCN, we discover five highly correlated modules that are upregulated with age. These old-biased modules regulate several antiageing mechanisms such as maintenance of proteostasis, transcriptional regulation, and stress response. We observe stronger purifying selection on central hub genes of these old-biased modules compared with young-biased modules. These results indicate a lack of transcriptional ageing in old C. obscurior queens, possibly facilitated by strong selection at old age and well-regulated antiageing mechanisms.
Identifiants
pubmed: 33944936
pii: 6263858
doi: 10.1093/gbe/evab093
pmc: PMC8214412
pii:
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
Références
Science. 1998 Oct 30;282(5390):943-6
pubmed: 9794765
Genome Biol. 2014;15(12):550
pubmed: 25516281
Biogerontology. 2018 Dec;19(6):547-566
pubmed: 29492790
Genes Dev. 2021 Apr 1;35(7-8):470-482
pubmed: 33861721
Nature. 2010 Mar 25;464(7288):504-12
pubmed: 20336132
Bioinformatics. 2015 Jan 15;31(2):166-9
pubmed: 25260700
Curr Opin Insect Sci. 2016 Aug;16:51-57
pubmed: 27720050
Nucleic Acids Res. 2019 Jan 8;47(D1):D759-D765
pubmed: 30364959
Nat Commun. 2014 Dec 16;5:5495
pubmed: 25510865
Mol Biol Evol. 2015 Dec;32(12):3173-85
pubmed: 26341296
J Gerontol A Biol Sci Med Sci. 2014 Jun;69(6):633-9
pubmed: 24077437
Genome Biol Evol. 2019 Aug 1;11(8):2306-2311
pubmed: 31329228
Cell. 2013 Jun 6;153(6):1194-217
pubmed: 23746838
Cell. 2011 Sep 2;146(5):682-95
pubmed: 21884931
Nature. 1977 Nov 24;270(5635):301-4
pubmed: 593350
Methods Mol Biol. 2014;1079:155-70
pubmed: 24170401
Aging Cell. 2019 Aug;18(4):e12965
pubmed: 31062469
PLoS Comput Biol. 2011 Jan 20;7(1):e1001057
pubmed: 21283776
Nucleic Acids Res. 2016 Jan 4;44(D1):D793-800
pubmed: 26578564
Curr Biol. 2005 Feb 8;15(3):267-70
pubmed: 15694312
Exp Gerontol. 2009 Sep;44(9):586-93
pubmed: 19563879
Ageing Res Rev. 2011 Apr;10(2):205-15
pubmed: 20152936
Free Radic Biol Med. 2012 May 1;52(9):1954-69
pubmed: 22401853
Cell Death Discov. 2018 Aug 20;4:26
pubmed: 30155276
Sci Rep. 2019 May 13;9(1):7270
pubmed: 31086243
PLoS One. 2013 May 16;8(5):e63747
pubmed: 23696853
Curr Opin Insect Sci. 2016 Aug;16:58-63
pubmed: 27720051
Nat Biotechnol. 2019 Aug;37(8):907-915
pubmed: 31375807
BMC Bioinformatics. 2007 Aug 09;8:298
pubmed: 17688688
Insect Biochem Mol Biol. 2010 Jan;40(1):30-7
pubmed: 20035867
BMC Biol. 2018 Aug 20;16(1):93
pubmed: 30124168
PLoS Genet. 2011 Sep;7(9):e1002253
pubmed: 21931558
Nature. 2012 Sep 13;489(7415):263-8
pubmed: 22922647
PLoS One. 2015 Sep 18;10(9):e0137969
pubmed: 26383861
Ageing Res Rev. 2016 Aug;29:50-65
pubmed: 27328278
Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W609-12
pubmed: 16845082
Proc Natl Acad Sci U S A. 2005 Oct 4;102(40):14338-43
pubmed: 16176987
Mech Ageing Dev. 2005 Nov;126(11):1230-8
pubmed: 16139867
Nucleic Acids Res. 2019 Jan 8;47(D1):D506-D515
pubmed: 30395287
PLoS Genet. 2009 Dec;5(12):e1000776
pubmed: 20019809
Annu Rev Physiol. 2013;75:621-44
pubmed: 23190075
Aging Cell. 2010 Aug;9(4):558-69
pubmed: 20477758
Nature. 2010 Sep 9;467(7312):179-84
pubmed: 20829789
J Exp Zool B Mol Dev Evol. 2016 Dec;326(8):453-463
pubmed: 28074535
J Biol Chem. 2005 Jun 10;280(23):22222-32
pubmed: 15799966
Genome Res. 2003 Nov;13(11):2498-504
pubmed: 14597658
Aging (Albany NY). 2016 Sep 6;8(9):1940-1951
pubmed: 27617474
J Immunol. 2008 Apr 15;180(8):5413-22
pubmed: 18390723
PLoS One. 2013 Aug 05;8(8):e69870
pubmed: 23940531
Nature. 2007 Nov 8;450(7167):203-18
pubmed: 17994087
Mol Immunol. 2009 Aug;46(13):2647-54
pubmed: 19535145
Science. 2003 Feb 28;299(5611):1346-51
pubmed: 12610294
J Clin Invest. 2012 Jul;122(7):2601-12
pubmed: 22706308
Mol Ecol. 2017 Oct;26(19):5058-5073
pubmed: 28742933
Gerontology. 2009;55(5):550-8
pubmed: 19546513
Evol Lett. 2018 Nov 12;2(6):567-579
pubmed: 30564440
Comput Appl Biosci. 1997 Oct;13(5):555-6
pubmed: 9367129
Dev Biol. 1998 Apr 1;196(1):42-57
pubmed: 9527880
Nature. 2000 Nov 9;408(6809):233-8
pubmed: 11089980
Nature. 2014 Jan 9;505(7482):169-73
pubmed: 24317695
Exp Gerontol. 2018 Jul 15;108:92-98
pubmed: 29625209
Exp Gerontol. 2011 May;46(5):376-81
pubmed: 20849947
Nucleic Acids Res. 2015 Jan;43(Database issue):D213-21
pubmed: 25428371
Proc Natl Acad Sci U S A. 2007 Apr 24;104(17):7128-33
pubmed: 17438290
BMC Bioinformatics. 2008 Dec 29;9:559
pubmed: 19114008
Proc Natl Acad Sci U S A. 2018 May 22;115(21):5504-5509
pubmed: 29735660
Exp Gerontol. 2016 May;77:52-61
pubmed: 26883339
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
BMC Genomics. 2006 Mar 03;7:40
pubmed: 16515682
Am J Pathol. 2012 Mar;180(3):963-972
pubmed: 22210478
Proc Natl Acad Sci U S A. 1998 May 26;95(11):6239-44
pubmed: 9600949
Genome Biol. 2015 Aug 06;16:157
pubmed: 26243257
Trends Biochem Sci. 2009 Feb;34(2):85-96
pubmed: 19135374
BMC Bioinformatics. 2009 Dec 15;10:421
pubmed: 20003500
J Mol Biol. 1990 Oct 5;215(3):403-10
pubmed: 2231712
PLoS One. 2019 Feb 13;14(2):e0210371
pubmed: 30759161
PLoS One. 2012;7(4):e35201
pubmed: 22509399
PLoS One. 2017 May 17;12(5):e0176689
pubmed: 28520752