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06 08, 2021;13 (6):

Gene Coexpression Network Reveals Highly Conserved, Well-Regulated Anti-Ageing Mechanisms in Old Ant Queens.

Mark C Harrison, Luisa M Jaimes Niño, Marisa Almeida Rodrigues, Judith Ryll, Thomas Flatt, Jan Oettler, Erich Bornberg-Bauer
Author Information
  1. Mark C Harrison: Institute for Evolution and Biodiversity, University of Münster, Germany. ORCID
  2. Luisa M Jaimes Niño: Institut für Zoologie/Evolutionsbiologie, University of Regensburg, Germany.
  3. Marisa Almeida Rodrigues: Department of Biology, University of Fribourg, Switzerland.
  4. Judith Ryll: Institute for Evolution and Biodiversity, University of Münster, Germany.
  5. Thomas Flatt: Department of Biology, University of Fribourg, Switzerland. ORCID
  6. Jan Oettler: Institut für Zoologie/Evolutionsbiologie, University of Regensburg, Germany. ORCID
  7. Erich Bornberg-Bauer: Department of Biology, University of Fribourg, Switzerland. ORCID
PMID: 33944936 DOI: 10.1093/gbe/evab093

Abstract

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.

Keywords

ageing longevity/fecundity trade-off selection shadow social insects

References

  1. Science. 1998 Oct 30;282(5390):943-6 [PMID: 9794765]
  2. Genome Biol. 2014;15(12):550 [PMID: 25516281]
  3. Biogerontology. 2018 Dec;19(6):547-566 [PMID: 29492790]
  4. Genes Dev. 2021 Apr 1;35(7-8):470-482 [PMID: 33861721]
  5. Nature. 2010 Mar 25;464(7288):504-12 [PMID: 20336132]
  6. Bioinformatics. 2015 Jan 15;31(2):166-9 [PMID: 25260700]
  7. Curr Opin Insect Sci. 2016 Aug;16:51-57 [PMID: 27720050]
  8. Nucleic Acids Res. 2019 Jan 8;47(D1):D759-D765 [PMID: 30364959]
  9. Nat Commun. 2014 Dec 16;5:5495 [PMID: 25510865]
  10. Mol Biol Evol. 2015 Dec;32(12):3173-85 [PMID: 26341296]
  11. J Gerontol A Biol Sci Med Sci. 2014 Jun;69(6):633-9 [PMID: 24077437]
  12. Genome Biol Evol. 2019 Aug 1;11(8):2306-2311 [PMID: 31329228]
  13. Cell. 2013 Jun 6;153(6):1194-217 [PMID: 23746838]
  14. Cell. 2011 Sep 2;146(5):682-95 [PMID: 21884931]
  15. Nature. 1977 Nov 24;270(5635):301-4 [PMID: 593350]
  16. Methods Mol Biol. 2014;1079:155-70 [PMID: 24170401]
  17. Aging Cell. 2019 Aug;18(4):e12965 [PMID: 31062469]
  18. PLoS Comput Biol. 2011 Jan 20;7(1):e1001057 [PMID: 21283776]
  19. Nucleic Acids Res. 2016 Jan 4;44(D1):D793-800 [PMID: 26578564]
  20. Curr Biol. 2005 Feb 8;15(3):267-70 [PMID: 15694312]
  21. Exp Gerontol. 2009 Sep;44(9):586-93 [PMID: 19563879]
  22. Ageing Res Rev. 2011 Apr;10(2):205-15 [PMID: 20152936]
  23. Free Radic Biol Med. 2012 May 1;52(9):1954-69 [PMID: 22401853]
  24. Cell Death Discov. 2018 Aug 20;4:26 [PMID: 30155276]
  25. Sci Rep. 2019 May 13;9(1):7270 [PMID: 31086243]
  26. PLoS One. 2013 May 16;8(5):e63747 [PMID: 23696853]
  27. Curr Opin Insect Sci. 2016 Aug;16:58-63 [PMID: 27720051]
  28. Nat Biotechnol. 2019 Aug;37(8):907-915 [PMID: 31375807]
  29. BMC Bioinformatics. 2007 Aug 09;8:298 [PMID: 17688688]
  30. Insect Biochem Mol Biol. 2010 Jan;40(1):30-7 [PMID: 20035867]
  31. BMC Biol. 2018 Aug 20;16(1):93 [PMID: 30124168]
  32. PLoS Genet. 2011 Sep;7(9):e1002253 [PMID: 21931558]
  33. Nature. 2012 Sep 13;489(7415):263-8 [PMID: 22922647]
  34. PLoS One. 2015 Sep 18;10(9):e0137969 [PMID: 26383861]
  35. Ageing Res Rev. 2016 Aug;29:50-65 [PMID: 27328278]
  36. Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W609-12 [PMID: 16845082]
  37. Proc Natl Acad Sci U S A. 2005 Oct 4;102(40):14338-43 [PMID: 16176987]
  38. Mech Ageing Dev. 2005 Nov;126(11):1230-8 [PMID: 16139867]
  39. Nucleic Acids Res. 2019 Jan 8;47(D1):D506-D515 [PMID: 30395287]
  40. PLoS Genet. 2009 Dec;5(12):e1000776 [PMID: 20019809]
  41. Annu Rev Physiol. 2013;75:621-44 [PMID: 23190075]
  42. Aging Cell. 2010 Aug;9(4):558-69 [PMID: 20477758]
  43. Nature. 2010 Sep 9;467(7312):179-84 [PMID: 20829789]
  44. J Exp Zool B Mol Dev Evol. 2016 Dec;326(8):453-463 [PMID: 28074535]
  45. J Biol Chem. 2005 Jun 10;280(23):22222-32 [PMID: 15799966]
  46. Genome Res. 2003 Nov;13(11):2498-504 [PMID: 14597658]
  47. Aging (Albany NY). 2016 Sep 6;8(9):1940-1951 [PMID: 27617474]
  48. J Immunol. 2008 Apr 15;180(8):5413-22 [PMID: 18390723]
  49. PLoS One. 2013 Aug 05;8(8):e69870 [PMID: 23940531]
  50. Nature. 2007 Nov 8;450(7167):203-18 [PMID: 17994087]
  51. Mol Immunol. 2009 Aug;46(13):2647-54 [PMID: 19535145]
  52. Science. 2003 Feb 28;299(5611):1346-51 [PMID: 12610294]
  53. J Clin Invest. 2012 Jul;122(7):2601-12 [PMID: 22706308]
  54. Mol Ecol. 2017 Oct;26(19):5058-5073 [PMID: 28742933]
  55. Gerontology. 2009;55(5):550-8 [PMID: 19546513]
  56. Evol Lett. 2018 Nov 12;2(6):567-579 [PMID: 30564440]
  57. Comput Appl Biosci. 1997 Oct;13(5):555-6 [PMID: 9367129]
  58. Dev Biol. 1998 Apr 1;196(1):42-57 [PMID: 9527880]
  59. Nature. 2000 Nov 9;408(6809):233-8 [PMID: 11089980]
  60. Nature. 2014 Jan 9;505(7482):169-73 [PMID: 24317695]
  61. Exp Gerontol. 2018 Jul 15;108:92-98 [PMID: 29625209]
  62. Exp Gerontol. 2011 May;46(5):376-81 [PMID: 20849947]
  63. Nucleic Acids Res. 2015 Jan;43(Database issue):D213-21 [PMID: 25428371]
  64. Proc Natl Acad Sci U S A. 2007 Apr 24;104(17):7128-33 [PMID: 17438290]
  65. BMC Bioinformatics. 2008 Dec 29;9:559 [PMID: 19114008]
  66. Proc Natl Acad Sci U S A. 2018 May 22;115(21):5504-5509 [PMID: 29735660]
  67. Exp Gerontol. 2016 May;77:52-61 [PMID: 26883339]
  68. Bioinformatics. 2009 Aug 15;25(16):2078-9 [PMID: 19505943]
  69. BMC Genomics. 2006 Mar 03;7:40 [PMID: 16515682]
  70. Am J Pathol. 2012 Mar;180(3):963-972 [PMID: 22210478]
  71. Proc Natl Acad Sci U S A. 1998 May 26;95(11):6239-44 [PMID: 9600949]
  72. Genome Biol. 2015 Aug 06;16:157 [PMID: 26243257]
  73. Trends Biochem Sci. 2009 Feb;34(2):85-96 [PMID: 19135374]
  74. BMC Bioinformatics. 2009 Dec 15;10:421 [PMID: 20003500]
  75. J Mol Biol. 1990 Oct 5;215(3):403-10 [PMID: 2231712]
  76. PLoS One. 2019 Feb 13;14(2):e0210371 [PMID: 30759161]
  77. PLoS One. 2012;7(4):e35201 [PMID: 22509399]
  78. PLoS One. 2017 May 17;12(5):e0176689 [PMID: 28520752]

MeSH Term

Animals
Ants
Biological Evolution
Female
Gene Expression Regulation, Developmental
Gene Regulatory Networks
Longevity
Selection, Genetic
Journal Article Research Support, Non-U.S. Gov't
Article has an altmetric score of 8

Word Cloud

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