The origin of menopause



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Abstract

The origin of menopause is mysterious and difficult to explain in terms of evolutionary theory. Menopause is described in humans and in four cetacean species. Natural selection cannot act on a trait that appears after the end of reproduction; therefore, it cannot be formed by the classical selection mechanism. All the proposed theories of the onset of menopause, adaptive and non-adaptive, can explain the benefits of menopause, but are completely untenable from the point of view of the theory of evolution and do not answer the main question - how did it arise. We propose a hypothesis based on the assertion that menopause is a byproduct of the rapid increase in the size of the cerebral cortex during the formation of Homo sapiens. Genes associated with the development of congenital microcephaly, which are responsible for the development of the cerebral cortex, were identified, and clear traces of natural selection were found in them, and a powerful evolutionary process continues up to the present. Most products of these genes are associated with the process of formation of the cell division spindle, both in the process of mitosis and meiosis. We hypothesize that the rapid evolutionary process that led to the growth of the cerebral cortex in humans, as a side effect, led to the formation of a high frequency of aneuploidy in oocytes. A similar process has also led to the formation of menopause in cetaceans.

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About the authors

K. Yu Boyarsky

I.I. Mechnikov North-Western State Medical University; Medical Center for Personal Health and Reproduction

Email: konstantinboyarsky@icloud.com

V. A Skobeeva

Lomonosov Moscow State University

O. B Chekhonina

Moscow State Regional University

E. I Kahiani

I.I. Mechnikov North-Western State Medical University

References

  1. Greendale G.A., Lee N.P., Arriola E.R. The menopause. The Lancet 1999; 353(9152): 571-80.
  2. Takahashi T.A., Johnson K.M. Menopause 2015; 99(3): 521-34.
  3. Peccei J.S. Menopause: adaptation or epiphenomenon? Evolutionary Anthropology: Issues, News, and Reviews 2001; 10(2): 43-57.
  4. Schoenaker D.A. J. M., Jackson C.A., Rowlands J.V., Mishra G.D. Socioeconomic position, lifestyle factors and age at natural menopause: a systematic review and meta-analyses of studies across six continents. Int. J. Epidem. 2014; 43(5): 1542-62.
  5. Nelson L.M. Primary ovarian insufficiency. New Engl. J. Med. 2009; 360(6): 606-14.
  6. Dunson D.B., Colombo B., Baird D.D. Changes with age in the level and duration of fertility in the menstrual cycle. Human reproduction 2002; 17(5): 1399-403.
  7. Broekmans F.J., Knauff E.A.H., te Velde E.R. et al. Female reproductive ageing: current knowledge and future trends. Trends in Endocrinol. Metabol. 2007; 18(2): 58-65.
  8. Eijkemans M.J.C., van Poppel F., Habbema D.F. et al. Too old to have children? Lessons from natural fertility populations. Human Reproduction 2014; 29(6): 1304-312.
  9. Hawkes K., Smith K.R. Do women stop early? Similarities in fertility decline in humans and chimpanzees. Annals of the New York Acad. Sci. 2010; 1204: 43.
  10. Gruhn J.R., Zielinska A.P., Shukla V. et al. Chromosome errors in human eggs shape natural fertility over reproductive life span. Science 2019; 365(6460): 1466-9.
  11. Wallace W.H.B., Kelsey T.W. Human ovarian reserve from conception to the menopause. PlosOne 2010; 5(1): e8772.
  12. Huber S., Fieder M. Evidence for a maximum “shelf-life” of oocytes in mammals suggests that human menopause may be an implication of meiotic arrest. Scientific reports 2018; 8(1): 1-5.
  13. Webster A., Schuh M. Mechanisms of aneuploidy in human eggs. Trends in cell biol. 2017; 27(1): 55-68.
  14. Holubcova Z., Blayney M., Elder K., Schuh M. Error-prone chromosome-mediated spindle assembly favors chromosome segregation defects in human oocytes. Science 2015; 348(6239): 1143-7.
  15. Austad S.N. Menopause: an evolutionary perspective. Exp. gerontol. 1994; 29(3-4): 255-63.
  16. Nattrass S., Croft D.P., Ellis S. et al. Postreproductive killer whale grandmothers improve the survival of their grandoffspring. PNAS USA 2019; 116(52): 26669-73.
  17. Johnstone R.A., Cant M.A. Evolution of menopause. Current Biol. 2019; 29(4): R112-5.
  18. Schubert C. Benefits of Menopause: Good Fishing. Biol. Reproduct. 2015; 92(6): 135.
  19. Cant M.A., Johnstone R.A. Reproductive conflict and the separation of reproductive generations in humans. PNAS USA 2008; 105(14): 5332-6.
  20. Lahdenpera M., Gillespie D.O.S., Lummaa V., Russell A.F. Severe intergenerational reproductive conflict and the evolution of menopause. Ecol. letters 2012; 15(11): 1283-90.
  21. Croft D.P., Johnstone R.A., Ellis S., Nattrass S. et al. Reproductive conflict and the evolution of menopause in killer whales. Current Biol. 2017; 27(2): 298-304.
  22. Williams G.C. Pleiotropy, natural selection, and the evolution of senescence. Evolution 1957; 11(4): 398-411.
  23. Peccei J.S. A hypothesis for the origin and evolution of menopause. Maturitas 1995; 21(2): 83-9.
  24. Cooper G.S., Sandler D.P. Age at natural menopause and mortality. Ann. Epidemiol. 1998; 8(4): 229-35.
  25. Marlowe F. The patriarch hypothesis. Human Nature 2000; 11(1): 27-42.
  26. Austad S.N. Sex differences in longevity and aging. Handbook of the Biology of Aging (Seventh Edition) 2011: 479-95.
  27. Morton R.A., Stone J.R., Singh R.S. Mate choice and the origin of menopause. PlosOne 2013; 9(6): e1003092.
  28. Muller M.N., Thompson M.E., Wrangham R.W. Male chimpanzees prefer mating with old females. Current Biol. 2006; 16(22): 2234-8.
  29. Jamison C.S., Cornell L.L., Jamison P.L., Nakazato H. Are all grandmothers equal? A review and a preliminary test of the “grandmother hypothesis” in Tokugawa Japan. Am.J. Physic. Anthropol. 2002; 119(1): 67-76.
  30. Lahdenpera M., Lummaa V., Helle S. et al. Fitness benefits of prolonged post-reproductive lifespan in women. Nature 2004; 428(6979): 178-81.
  31. Lahdenpera M., Russell A. F., Lummaa V. Selection for long lifespan in men: benefits of grandfathering? Proceedings of the Royal Society of London B: Biological Sciences 2007; 274(1624): 2437-44.
  32. Tully T., Lambert A. The evolution of postreproductive life span as an insurance against indeterminacy. Evolution 2011; 65(10): 3013-20.
  33. Pavard S., Sibert A., Heyer E. The effect of maternal care on child survival: a demographic, genetic, and evolutionary perspective. Evolution: Int. J. Organic Evol. 2007; 61(5): 1153-61.
  34. Sauer M. V., Paulson R. J., Lobo R.A. Pregnancy: Oocyte donation to women of advanced reproductive age: pregnancy results and obstetrical outcomes in patients 45 years and older. Hum. Reproduct. 1996; 11(11): 2540-3.
  35. Hill K., Hurtado A.M. The evolution of premature reproductive senescence and menopause in human females. Human Nature 1991; 2(4): 313-50.
  36. Hawkes K., O’Connell J.F., Blurton Jones N.G. et al. Grandmothering, menopause, and the evolution of human life histories. PNAS USA 1998; 95(3): 1336-9.
  37. Hawkes K. The grandmother effect. Nature 2004; 428(6979): 128-9.
  38. Cant M.A., Johnstone R.A. Reproductive conflict and the separation of reproductive generations in humans. PNAS USA 2008; 105(14): 5332-6.
  39. Reeve H. K., Emlen S. T., Keller L. Reproductive sharing in animal societies: reproductive incentives or incomplete control by dominant breeders? // Behavioral Ecology. - 1998. - Т. 9. - №. 3. - С. 267-278. 10.1093/beheco/9.3.267
  40. Mace R., Alvergne A. Female reproductive competition within families in rural Gambia. Proceedings of the Royal Society B: Biological Sciences 2012; 279(1736): 2219-27.
  41. Marlowe F.W. Marital residence among foragers. Current Anthropol. 2004; 45(2): 277-84.
  42. Johnstone R.A., Cant M.A. The evolution of menopause in cetaceans and humans: the role of demography. Proceedings of the Royal Society B: Biological Sciences 2010; 277(1701): 3765-71.
  43. Ubeda F., Ohtsuki H., Gardner A. Ecology drives intragenomic conflict over menopause. Ecology letters 2014; 17(2): 165-74.
  44. Jayaraman D., Bae B. I., Walsh C.A. The genetics of primary microcephaly. Ann. Rev. Genomics Hum. Gen. 2018; 19: 177-200.
  45. Zhou X., Zhi Y., Yu J., Xu D. The Yin and Yang of Autosomal Recessive Primary Microcephaly Genes: Insights from Neurogenesis and Carcinogenesis. Int. J. Mol. Sci. 2020; 21(5): 1691.
  46. Naveed M., Kazmi S.K., Amin M. et al. Comprehensive review on the molecular genetics of autosomal recessive primary microcephaly (MCPH). Gen. Res. 2018; 100: e7.
  47. Bond J., Roberts E., Mochida G.H. et al. ASPM is a major determinant of cerebral cortical size. Nature genetics 2002; 32(2): 316-20.
  48. Kouprina N., Pavlicek A., Collins N.K. et al. The microcephaly ASPM gene is expressed in proliferating tissues and encodes for a mitotic spindle protein. Hum. Mol. Gen. 2005; 14(15): 2155-65.
  49. Xu X.L., Ma W., Zhu Y.-B. et al. The microtubule-associated protein ASPM regulates spindle assembly and meiotic progression in mouse oocytes. PlosOne 2012; 7(11): e49303.
  50. Mekel-Bobrov N., Gilbert S.L., Evans P.D. Ongoing adaptive evolution of ASPM, a brain size determinant in Homo sapiens. Science 2005; 309(5741): 1720-2.5
  51. Wong P.C.M., Gilbert S.L., Evans P.D. et al. ASPM-lexical tone association in speakers of a tone language: Direct evidence for the genetic-biasing hypothesis of language evolution. Science adv. 2020; 6(22): eaba5090.
  52. Evans P.D., Anderson J.R., Vallender E.J. et al. Reconstructing the evolutionary history of microcephalin, a gene controlling human brain size. Hum. Mol. Gen. 2004; 13(11): 1139-45.
  53. Lagirand-Cantaloube J., Ciabrini C., Charrasse S. et al. Loss of centromere cohesion in aneuploid human oocytes correlates with decreased kinetochore localization of the sac proteins Bub1 and Bubr1. Scientific reports 2017; 7: 44001.
  54. Shi L., Hu E., Wang Z. et al. Regional selection of the brain size regulating gene CASC5 provides new insight into human brain evolution. Human genetics 2017; 136(2): 193-204.
  55. Dzhindzhev N.S., Yu Q.D., Weiskopf K. et al. Asterless is a scaffold for the onset of centriole assembly. Nature 2010; 467(7316): 714-8.
  56. Yu K.W., Zhong N., Xiao Y., She Z.-Y. Mechanisms of kinesin-7 CENP-E in kinetochore-microtubule capture and chromosome alignment during cell division. Biol. Cell. 2019; 111(6): 143-60.
  57. Marchetti F., Venkatachalam S. The multiple roles of Bub1 in chromosome segregation during mitosis and meiosis. Cell Cycle 2010; 9(1): 58-63.
  58. Wang X., Baumann C., De La Fuente R., Viveiros M.M. CEP215 and AURKA regulate spindle pole focusing and aMTOC organization in mouse oocytes. Reproduct. 2020; 159(3): 261-74.
  59. Houlard M., Godwin J., Metson J. et al. Condensin confers the longitudinal rigidity of chromosomes. Nature Cell Biology 2015; 17(6): 771-81.
  60. Liskova L., Susor A., Pivonkova K. et al. Detection of condensin I. and II in maturing pig oocytes. Rep. Fert. Dev. 2010; 22(4): 644-52.
  61. Xu S., Sun X., Niu X. et al. Genetic basis of brain size evolution in cetaceans: insights from adaptive evolution of seven primary microcephaly (MCPH) genes. BMC Evolutionary Biology 2017; 17(1): 206.
  62. Ellis S., Franks D.W., Nattrass S. et al. Analyses of ovarian activity reveal repeated evolution of post-reproductive lifespans in toothed whales. Scientific reports 2018; 8(1): 1-10.
  63. Ruth K.S., Murray A. Lessons from genome-wide association studies in reproductive medicine: menopause. Seminars in reproductive medicine. Thieme Medical Publ. 2016; 34(4): 215-23.
  64. Laven J.S.E., Visser J.A., Uitterlinden A.G. et al. Menopause: genome stability as new paradigm. Maturitas 2016; 92: 15-23.
  65. Altendorfer E., Lascarez-Lagunas L.I., Nadarajan S. et al. Crossover Position Drives Chromosome Remodeling for Accurate Meiotic Chromosome Segregation. Current Biol. 2020; 30(7): 1329-38e7.
  66. Ubaldi F.M., Cimadomo D., Capalbo A. et al. Preimplantation genetic diagnosis for aneuploidy testing in women older than 44 years: a multicenter experience. Fertility and sterility 2017; 107(5): 1173-80.
  67. Wang S., Liu Y., Shang Y. et al. Crossover Interference, Crossover Maturation and Human Aneuploidy. BioEssays 2019; 41(10): 1800221.
  68. So C., Menelaou K., Uraji J. et al. Mechanism of spindle pole organization and instability in human oocytes. Science 2022; 375(6581): eabj3944.

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