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Evolutionary biology
Evolutionary biology
A trade-off between having many sons and shorter maternal post-reproductive survival in pre-industrial Finland
Published:23 April 2013https://doi.org/10.1098/rsbl.2013.0034
Abstract
A bias in reproduction towards sons, which are energetically more costly than daughters, has been suggested to shorten parental lifespan, but previous results have been mixed. Reproductive costs should be most evident in low rather than high resource settings, and are not expected to be severe in men, because women pay higher direct costs of reproduction. We, therefore, used demographic data from pre-industrial Finland to investigate whether the number of sons and daughters born affected their parents’ post-reproductive survival and whether this was related to parent's resource availability. Irrespective of access to resources, mothers, but not fathers, with many sons suffered from reduced post-reproductive survival, and this association decreased as mothers aged. Our results provide evidence that Finnish mothers traded long post-reproductive lifespan for giving birth to many sons.
References
- 1
Kirkwood TBL& Rose MR . 1991 Evolution of senescence: late survival sacrifised for reproduction. Phil. Trans. R. Soc. Lond. B 332, 15–24.doi:10.1098/rstb.1991.0028 (doi:10.1098/rstb.1991.0028). Link, Web of Science, Google Scholar - 2
Penn DJ& Smith KR . 2007 Differential fitness costs of reproduction between the sexes. Proc. Natl Acad. Sci. USA 104, 553–558.doi:10.1073/pnas.0609301103 (doi:10.1073/pnas.0609301103). Crossref, PubMed, Web of Science, Google Scholar - 3
van Noordwijk AJ& de Jong G . 1986 Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat. 128, 137–142.doi:10.1086/284547 (doi:10.1086/284547). Crossref, Web of Science, Google Scholar - 4
Hamel S, Côté SD, Gaillard J-M& Festa-Bianchet M . 2009 Individual variation in reproductive costs of reproduction: high-quality females always do better. J. Anim. Ecol. 78, 143–151.doi:10.1111/j.1365-2656.2008.01459.x (doi:10.1111/j.1365-2656.2008.01459.x). Crossref, PubMed, Web of Science, Google Scholar - 5
Ardia DR . 2004 Individual quality mediates trade-offs between reproductive effort and immune function in tree swallows. J. Anim. Ecol. 74, 517–524.doi:10.1111/j.1365-2656.2005.00950.x (doi:10.1111/j.1365-2656.2005.00950.x). Crossref, Web of Science, Google Scholar - 6
Messina FJ& Fry JD . 2003 Environment-dependent reversal of a life history trade-off in the seed beetle Callosobruchus maculatus. J. Evol. Biol. 16, 501–509.doi:10.1046/j.1420-9101.2003.00535.x (doi:10.1046/j.1420-9101.2003.00535.x). Crossref, PubMed, Web of Science, Google Scholar - 7
Helle S, Lummaa V& Jokela J . 2005 Are reproductive and somatic senescence coupled in humans? Late, but not early, reproduction correlated with longevity in historical Sami women. Proc. R. Soc. B 272, 29–37.doi:10.1098/rspb.2004.2944 (doi:10.1098/rspb.2004.2944). Link, Web of Science, Google Scholar - 8
Hurt LS, Ronsmans C& Thomas SL . 2006 The effect of number of births on women's mortality: systematic review of the evidence for women who have completed their childbearing. Popul. Stud. 60, 55–71.doi:10.1080/00324720500436011 (doi:10.1080/00324720500436011). Crossref, Google Scholar - 9
Le Bourg E . 2007 Does reproduction decrease longevity in human beings? Ageing Res. Rev. 6, 141–149.doi:10.1016/j.arr.2007.04.002 (doi:10.1016/j.arr.2007.04.002). Crossref, PubMed, Web of Science, Google Scholar - 10
Jasienska G . 2009 Reproduction and lifespan: trade-offs, overall energy budgets, intergenerational costs, and costs neglected by research. Am. J. Hum. Biol. 21, 524–532.doi:10.1002/ajhb.20931 (doi:10.1002/ajhb.20931). Crossref, PubMed, Web of Science, Google Scholar - 11
Hindmarsh PC, Geary MPP, Rodeck CH, Kingdom JCP& Cole TJ . 2002 Intrauterine growth and its relationship to size and shape at birth. Pediat. Res. 52, 263–268.doi:10.1203/00006450-200208000-00020 (doi:10.1203/00006450-200208000-00020). Crossref, PubMed, Web of Science, Google Scholar - 12
Loos RJF, Derom C, Eeckels R, Derom R& Vlietinck R . 2001 Length of gestation and birth weight in dizygotic twins. Lancet 358, 560–561.doi:10.1016/S0140-6736(01)05716-6 (doi:10.1016/S0140-6736(01)05716-6). Crossref, PubMed, Web of Science, Google Scholar - 13
Tamimi RM, Lagiou P, Mucci LA, Hsieh C-C, Adami H-O& Trichopoulos D . 2003 Average energy intake among pregnant women carrying a boy compared with a girl. Brit. Med. J. 326, 1245–1246.doi:10.1136/bmj.326.7401.1245 (doi:10.1136/bmj.326.7401.1245). Crossref, PubMed, Google Scholar - 14
Sellen DW . 2007 Lactation, complementary feeding, and human life history. The evolution of human life history (eds, Hawkes K& Paine RR ), pp. 155–196. Santa Fe, NM: School of American Research Press. Google Scholar - 15
Helle S, Lummaa V& Jokela J . 2002 Sons reduced maternal longevity in preindustrial humans. Science 296, 1085.doi:10.1126/science.1070106 (doi:10.1126/science.1070106). Crossref, PubMed, Web of Science, Google Scholar - 16
Helle S, Lummaa V& Jokela J . 2010 On the number of sons born and shorter lifespan in historical Sami mothers. Proc. R. Soc. B 277, 2909–2911.doi:10.1098/rspb.2009.2114 (doi:10.1098/rspb.2009.2114). Link, Web of Science, Google Scholar - 17
Pham-Kanter G& Goldman N . 2012 Do sons reduce parental mortality? J. Epidemiol. Commun. Health 66, 710–715.doi:10.1136/jech.2010.123323 (doi:10.1136/jech.2010.123323). Crossref, PubMed, Web of Science, Google Scholar - 18
- 19
Pettay JE, Helle S, Jokela J& Lummaa V . 2007 Natural selection on female life-history traits in relation to socio-economic class in preindustrial Finland. PLoS ONE 2, e606.doi:10.1371/journal.pone.0000606 (doi:10.1371/journal.pone.0000606). Crossref, PubMed, Web of Science, Google Scholar - 20
Allison PD . 2010 Survival analysis using SAS: a practical guide, 2nd edn. Cary, NC: SAS Institute Inc. Google Scholar - 21
Gelman A& Hill J . 2007 Data analysis using regression and multilevel/hierarchial models. Cambridge, UK: Cambridge University Press. Google Scholar - 22
Helle S, Lummaa V& Jokela J . 2004 Accelerated immunosenescence in preindustrial twin mothers. Proc. Natl Acad. Sci. USA 101, 12391–12396.doi:10.1073/pnas.0402215101 (doi:10.1073/pnas.0402215101). Crossref, PubMed, Web of Science, Google Scholar - 23
Grant VJ& Chamley LW . 2010 Can mammalian mothers influence the sex of their offspring peri-conceptually? Reproduction 140, 425–433.doi:10.1530/REP-10-0137 (doi:10.1530/REP-10-0137). Crossref, PubMed, Web of Science, Google Scholar - 24
James WH . 2008 Evidence that mammalian sex ratios are partially controlled by parental hormone levels around the time of conception. J. Endocrinol. 198, 3–15.doi:10.1677/JOE-07-0446 (doi:10.1677/JOE-07-0446). Crossref, PubMed, Web of Science, Google Scholar - 25
Klein JL . 2000 The effects of hormones on sex differences in infection: from genes to behaviour. Neurosci. Biobehav. Rev. 24, 627–638.doi:10.1016/S0149-7634(00)00027-0 (doi:10.1016/S0149-7634(00)00027-0). Crossref, PubMed, Web of Science, Google Scholar - 26
James WH . 2006 The sex ratios of offspring of diabetic parents. Diab. Med. 23, 1043–1044.doi:10.1111/j.1464-5491.2006.01807.x (doi:10.1111/j.1464-5491.2006.01807.x). Crossref, PubMed, Web of Science, Google Scholar - 27
Barbieri M, Boccardi V, Papa M& Paolisso G . 2009 Healthy ageing: what role does metabolism play? Int. Diab. Monit. 21, 43–47. Google Scholar - 28
Moslehi R, Singh R, Lessner L& Fiedman JM . 2011 Impact of BRCA mutations on female fertility and offspring sex ratio. Am. J. Hum. Biol. 22, 201–205. Web of Science, Google Scholar - 29
Smith KR, Hanson HA, Mineau GP& Buys SS . 2011 Effects of BRCA1 and BRCA2 mutations on female fetility. Proc. R. Soc. B 279, 1389–1395.doi:10.1098/rspb.2011.1697 (doi:10.1098/rspb.2011.1697). Link, Web of Science, Google Scholar
