Natural fertility and longevity
2015; Elsevier BV; Volume: 103; Issue: 5 Linguagem: Inglês
10.1016/j.fertnstert.2015.03.030
ISSN1556-5653
Autores Tópico(s)Genetics, Aging, and Longevity in Model Organisms
ResumoMuch empirical work suggests an association between fertility patterns and longevity. I review this association, focusing on natural fertility populations and emphasizing the role of both the timing and the intensity of fertility. Overall, it appears that although age at last reproduction routinely correlates with post-reproductive longevity, suggesting a slower rate of senescence among late fertile women, the same is not true for age at first reproduction and parity. I discuss some of the conceptual and methodologic issues, as well as the sources of the biases, that have been a persistent feature of this body of research. I conclude by suggesting avenues of research that could be initiated or pursued in the area. Much empirical work suggests an association between fertility patterns and longevity. I review this association, focusing on natural fertility populations and emphasizing the role of both the timing and the intensity of fertility. Overall, it appears that although age at last reproduction routinely correlates with post-reproductive longevity, suggesting a slower rate of senescence among late fertile women, the same is not true for age at first reproduction and parity. I discuss some of the conceptual and methodologic issues, as well as the sources of the biases, that have been a persistent feature of this body of research. I conclude by suggesting avenues of research that could be initiated or pursued in the area. Discuss: You can discuss this article with its authors and with other ASRM members at http://fertstertforum.com/gagnona-natural-fertility-longevity/ Discuss: You can discuss this article with its authors and with other ASRM members at http://fertstertforum.com/gagnona-natural-fertility-longevity/ Concomitantly with large decreases in overall fertility, age at maternity has increased appreciably in modern society. Fertility has plunged below population replacement levels, sometimes rebounding to slightly above them (1Myrskylä M. Kohler H.-P. Billari F.C. Advances in development reverse fertility declines.Nature. 2009; 460: 741-743Crossref PubMed Scopus (346) Google Scholar, 2Sobotka T. Is lowest-low fertility in Europe explained by the postponement of childbearing?.Popul Dev Rev. 2004; 30: 195-220Crossref Scopus (205) Google Scholar), as couples have elected to have their children at later stages of the life cycle, in contrast to the earlier days of the demographic transition, when fertility control essentially consisted of "stopping" and "spacing" behaviors (3Knodel J.E. Demographic behavior in the past: a study of fourteen German village populations in the eighteenth and nineteenth centuries. Cambridge University Press, Cambridge, U.K1988Crossref Google Scholar). This major shift holds important health implications for future generations. If smaller family size may benefit the health of progeny through improvements in per capita access to resources, education, and human capital, older maternal age at birth may on the other hand represent a "longevity penalty," as suggested by recent studies showing that long-lived individuals are more likely born to younger rather than older mothers (4Jarry V. Gagnon A. Bourbeau R. Maternal age, birth order and other early-life factors: a family-level approach to exploring exceptional survival.Vienna Yearb Popul Res. 2013; 11: 267-294Crossref Scopus (5) Google Scholar, 5Gavrilov L.A. Gavrilova N.S. New developments in the biodemography of aging and longevity.Gerontology. 2014; (Available at: www.karger.com/Article/Abstract/369011. Accessed February 9, 2015)PubMed Google Scholar). This fundamental shift in fertility patterns is also likely to affect mothers themselves, because women delaying childbearing to older ages may face increased health risks and complications associated with deliveries past reproductive prime (6Gilbert W.M. Nesbitt T.S. Danielsen B. Childbearing beyond age 40: pregnancy outcome in 24,032 cases.Obstet Gynecol. 1999; 93: 9-14Crossref PubMed Scopus (252) Google Scholar). However, research reviewed here shows that relatively low—but not null—parities and late ages at last reproduction often correlate with a long post-reproductive life. Given these trends, it becomes imperative to know whether women actually gain health benefits from having fewer babies later in life. Unfortunately, data from contemporary populations may not always provide the best means to address this question. Fertility choice, which correlates with a number of factors that may be associated with health, such as education and socioeconomic position, may blur the relationship between fertility patterns and post-reproductive mortality. Assisted reproductive technologies that allow increasing numbers of women to reproduce at older ages may confound the issue further. Additionally, because the age at death of people alive today is unknown, we cannot address how a woman's fertility affects her longevity per se (7le Bourg E. Does reproduction decrease longevity in human beings?.Ageing Res Rev. 2007; 6: 141-149Crossref PubMed Scopus (70) Google Scholar). In this context, the use of data on "natural fertility" from historical populations appears to be indicated. Individuals from such populations have no intentional or deliberate use of contraception and should offer the best observational ground to connect fertility patterns with post-reproductive survival. But data from these populations are not without limitations, owing to the usual issues arising from observational studies (adjustments for confounding factors, selection, direction of causality, and so on). As an illustration, the relationship between a late age at last reproduction and a long post-reproductive life among women, a finding reproduced in many studies, has been interpreted as the result of positive selection for slower rate of aging or, alternatively, as a direct effect of late fertility on health through biological changes caused by late pregnancy. The confusion that has accompanied the recent publication of a paper from the Long life Family Study, showing that mothers having babies after age 33 years live longer (8Sun F. Sebastiani P. Schupf N. Bae H. Andersen S.L. McIntosh A. et al.Extended maternal age at birth of last child and women's longevity in the Long Life Family Study.Menopause. 2015; 22: 26-31Crossref PubMed Scopus (36) Google Scholar), is revealing. Although the authors were adamant in arguing that the findings did not imply that women should wait to have children at older ages to improve their longevity, some press reports were quick to declare the study good news for older mothers. Psychology Today wrote, "Given the pressure on women to find jobs and establish careers before becoming mothers or adding to their families, the findings do remove a modicum of pressure to hurry into motherhood or having your last child when you don't feel ready … with the added bonus of maybe living longer" (9Newman S. Good news for "older" mothers: you may live longer.Psychol Today. 2014; (Available at: www.psychologytoday.com/blog/singletons/201407/good-news-older-mothers-you-may-live-longer. Last accessed April 8, 2015.)Google Scholar). Clearly, there is a need for more research to disentangle the potential role of fertility in molding old age mortality. In the present paper, I first review the concept of natural fertility and its usefulness for the study of the relationship between reproduction and longevity. I then address the role of the timing of fertility through a review of results on ages at first and last reproduction before reporting results on the role of the number of children ever born. These three measurements are presented separately, but as this review will show, any study aiming to assess the effect of reproduction on longevity should consider all three simultaneously. I then conclude by proposing new research avenues. Throughout the review, I highlight methodologic and theoretic (evolutionary) issues permeating this field. "Natural fertility" broadly refers to the level of fertility reached in the absence of birth control. The Hutterites and the Amish traditionally do not practice birth control, and they usually have very large families (10Henry L. Fécondité des mariages: nouvelle méthode de mesure. Institut National d'Étude Démographiques, Paris1953Google Scholar). In contrast, in much of the modern world fertility is lower than natural fertility levels because of a lengthening of the intervals between menarche and first birth and between successive births, or because of stopping childbearing once the desired family size is attained. The idea behind the concept, developed by historical demographer Louis Henry (10Henry L. Fécondité des mariages: nouvelle méthode de mesure. Institut National d'Étude Démographiques, Paris1953Google Scholar, 11Henry L. Some data on natural fertility.Eugen Q. 1961; 8: 81-91Crossref PubMed Scopus (416) Google Scholar), was to create a physiologic benchmark against which researchers could judge the fertility patterns when contraception is used (12Wilson C. Oeppen J. Pardoe M. What is natural fertility? The modelling of a concept.Popul Index. 1988; 54: 4-20Crossref PubMed Scopus (52) Google Scholar). At first, "fertility control" was operationalized to assess the stopping behavior, but later the concept was extended by demographers Coale and Trussell to include spacing (13Coale A.J. Trussell T.J. Model fertility schedules: variations in the age structure of childbearing in human populations.Popul Index. 1974; 40: 185-258Crossref PubMed Scopus (335) Google Scholar). In alternative formulations, fertility control also includes traditional means of pregnancy avoidance such as coitus interruptus, sexual abstinence, celibacy, or delayed age at marriage. Fertility control has additionally been demonstrated as a response to economic stress in pre-transitional Europe (14Bengtsson T. Dribe M. Deliberate control in a natural fertility population: southern Sweden, 1766-1864.Demography. 2006; 43: 727-746Crossref PubMed Scopus (88) Google Scholar). Although many researchers have called into question the validity of a dichotomy opposing natural to controlled fertility (12Wilson C. Oeppen J. Pardoe M. What is natural fertility? The modelling of a concept.Popul Index. 1988; 54: 4-20Crossref PubMed Scopus (52) Google Scholar), the analysis of populations in which childbearing is in principle unaffected by conscious choice has proved to be useful in the study of the influence of fertility on longevity. To be sure, fertility is never fully natural nor is it ever fully controlled, but deliberate control, when generalized, has the potential to introduce almost insurmountable problems of statistical modeling. For example, perceived health status may influence fertility decisions—a process that is usually not observable—and this may in turn lead to biased estimates of the effect of fertility on mortality if the less healthy individuals choose to limit their family size precisely because they assess their health to be poor (15Grundy E. Kravdal Ø. Reproductive history and mortality in late middle age among Norwegian men and women.Am J Epidemiol. 2008; 167: 271-279Crossref PubMed Scopus (116) Google Scholar). In contrast, in a natural fertility context, perceived health should not influence the decision to have another child, although poor health may itself be decisive if it affects fecundity (i.e., the biological capacity to reproduce). Given natural fertility, life tables show that most married women bear children until age 35–39 years, with a drastic fall of fertility after these ages. Only a tiny minority conceive naturally and are able to bring a pregnancy to term successfully after the age of 45 years. Because there are no parity-specific checks to reproduction, late-fertile women usually also have the largest family sizes. These highly select women, who have been extensively written about, are shown to have long lives in many of the studies reviewed below. They represent an important puzzle for evolutionary theories of aging (16Medawar P.B. An unsolved problem of biology: an inaugural lecture delivered at University College, London, 6 December, 1951. H. K. Lewis, London1952Google Scholar, 17Williams G.C. Pleiotropy, natural selection, and the evolution of senescence.Evolution. 1957; 11: 398-411Crossref Google Scholar, 18Kirkwood T.B. Evolution of ageing.Nature. 1977; 270: 301-304Crossref PubMed Scopus (1312) Google Scholar). According to evolutionary theories of aging, forces postponing the timing of reproduction should postpone aging and increase longevity. This prediction arises from the antagonistic pleiotropy theory, which postulates that deleterious mutations having a late age of onset freely accumulate if theses mutations favor vigor and reproduction at younger ages (17Williams G.C. Pleiotropy, natural selection, and the evolution of senescence.Evolution. 1957; 11: 398-411Crossref Google Scholar), and from the disposable soma theory, according to which it is selectively advantageous to trade the maintenance of somatic cells for accelerated development and reproduction, even though this implies faster senescence (18Kirkwood T.B. Evolution of ageing.Nature. 1977; 270: 301-304Crossref PubMed Scopus (1312) Google Scholar). Consequently, we should observe that delayed age at reproduction correlates with lower post-reproductive mortality. Although supported by comparative analysis of mammals, and well documented in model organisms (19Clutton-Brock T. Isvaran K. Sex differences in ageing in natural populations of vertebrates.Proc Biol Sci. 2007; 274: 3097-3104Crossref PubMed Scopus (271) Google Scholar, 20Jones O.R. Gaillard J.-M. Tuljapurkar S. Alho J.S. Armitage K.B. Becker et al.Senescence rates are determined by ranking on the fast-slow life-history continuum.Ecol Lett. 2008; 11: 664-673Crossref PubMed Scopus (265) Google Scholar), prediction regarding age at first birth has met with little success in human populations. A number of studies of contemporary populations have identified a detrimental effect of early childbirth on post-reproductive mortality, regardless of socioeconomic circumstances (21Lund E. Arnesen E. Borgan J.K. Pattern of childbearing and mortality in married women—a national prospective study from Norway.J Epidemiol Community Health. 1990; 44: 237-240Crossref PubMed Scopus (57) Google Scholar, 22Doblhammer G. Reproductive history and mortality later in life: a comparative study of England and Wales and Austria.Popul Stud (Camb). 2000; 54: 169-176Crossref PubMed Scopus (119) Google Scholar, 23Mirowsky J. Age at first birth, health, and mortality.J Health Soc Behav. 2005; 46: 32-50Crossref PubMed Scopus (66) Google Scholar, 24Grundy E. Tomassini C. Fertility history and health in later life: a record linkage study in England and Wales.Soc Sci Med. 2005; 61: 217-228Crossref PubMed Scopus (139) Google Scholar, 25Grundy E. Women's fertility and mortality in late mid life: a comparison of three contemporary populations.Am J Hum Biol. 2009; 21: 541-547Crossref PubMed Scopus (35) Google Scholar, 26Wang X. Byars S.G. Stearns S.C. Genetic links between post-reproductive lifespan and family size in Framingham.Evol Med Public Health. 2013; 2013: 241-253Crossref Google Scholar). However, results from studies that have addressed the issue of longevity per se (and not simply post-reproductive mortality) in a natural fertility context are mixed. Westendorp and Kirkwood (27Westendorp R.G. Kirkwood T.B. Human longevity at the cost of reproductive success.Nature. 1998; 396: 743-746Crossref PubMed Scopus (392) Google Scholar) and Tabatabaie et al. (28Tabatabaie V. Atzmon G. Rajpathak S.N. Freeman R. Barzilai N. Crandall J. Exceptional longevity is associated with decreased reproduction.Aging. 2011; 3: 1202-1205PubMed Google Scholar) found the expected positive association between age at first reproduction and longevity, but others found no clear associations (29Smith K.R. Mineau G.P. Bean L.L. Fertility and post-reproductive longevity.Soc Biol. 2002; 49: 185-205PubMed Google Scholar, 30Mueller U. Does late reproduction extend the life span? Findings from European royalty.Popul Dev Rev. 2004; 30: 449-466Crossref Scopus (13) Google Scholar, 31Dribe M. Long-term effects of childbearing on mortality: evidence from pre-industrial Sweden.Popul Stud. 2004; 58: 297-310Crossref Scopus (55) Google Scholar, 32Helle S. Lummaa V. Jokela J. Are reproductive and somatic senescence coupled in humans? Late, but not early, reproduction correlated with longevity in historical Sami women.Proc Biol Sci. 2005; 272: 29-37Crossref PubMed Scopus (76) Google Scholar, 33Gagnon A. Smith K.R. Tremblay M. Vezina H. Pare P.P. Desjardins B. Is there a trade-off between fertility and longevity? A comparative study of women from three large historical databases accounting for mortality selection.Am J Hum Biol. 2009; 21: 533-540Crossref PubMed Scopus (104) Google Scholar). In an appendix presenting a summary of studies, Helle et al. (32Helle S. Lummaa V. Jokela J. Are reproductive and somatic senescence coupled in humans? Late, but not early, reproduction correlated with longevity in historical Sami women.Proc Biol Sci. 2005; 272: 29-37Crossref PubMed Scopus (76) Google Scholar) identified only two out of eleven studies (18%) reporting the predicted outcome. Many investigations that were interested in the long-term effect of parity (reviewed in the "Number of children ever born" section of this article) included age at first birth only as a control variable, without reporting the associated parameter estimates, thus indirectly impinging on our knowledge of the implications of this variable for longevity. The reason why empirical results are mixed probably has a lot to do with the presence of unmeasured influences and selection effects that may vary widely between study populations, even though these populations are usually, perhaps abusively, lumped together under the umbrella of "natural fertility populations." For example, poor health can lead to delayed age at marriage as well as to limited fecundity; this in turn is expected to lead to delayed age at first birth and to correlate with increased mortality later in life (33Gagnon A. Smith K.R. Tremblay M. Vezina H. Pare P.P. Desjardins B. Is there a trade-off between fertility and longevity? A comparative study of women from three large historical databases accounting for mortality selection.Am J Hum Biol. 2009; 21: 533-540Crossref PubMed Scopus (104) Google Scholar). Selection can also work in the opposite direction. For instance, a positive relationship between age at first birth and longevity is to be expected if individuals from higher socioeconomic statuses (presumably healthier) delay marriage because of inheritance rules aimed at preventing fragmentation of familial holdings. Thus, although the number of progeny is in all likelihood underestimated in the British peerage (34Gavrilov L.A. Gavrilova N.S. Is there a reproductive cost for human longevity?.J Anti Aging Med. 1999; 2: 120-123Google Scholar), very small average family size (fewer than two children) may also result from delayed entry into marriage (28Tabatabaie V. Atzmon G. Rajpathak S.N. Freeman R. Barzilai N. Crandall J. Exceptional longevity is associated with decreased reproduction.Aging. 2011; 3: 1202-1205PubMed Google Scholar). These figures are worlds apart from the reproductive prowess measured in founder populations, where large fractions of women are married by the age of 20 years and where total parity may reach an average of ten in complete families (33Gagnon A. Smith K.R. Tremblay M. Vezina H. Pare P.P. Desjardins B. Is there a trade-off between fertility and longevity? A comparative study of women from three large historical databases accounting for mortality selection.Am J Hum Biol. 2009; 21: 533-540Crossref PubMed Scopus (104) Google Scholar). In a founder population, where access to land is largely unlimited and family establishment is thus highly facilitated, it may very well be that the most healthy girls, or those who have the best nutritional conditions, will reach menarche first, leading to a negative relationship between age at first birth and longevity if nubile women marry first (33Gagnon A. Smith K.R. Tremblay M. Vezina H. Pare P.P. Desjardins B. Is there a trade-off between fertility and longevity? A comparative study of women from three large historical databases accounting for mortality selection.Am J Hum Biol. 2009; 21: 533-540Crossref PubMed Scopus (104) Google Scholar). Given the characteristically high rates of maternal mortality in such populations, particularly among very young mothers, women who are capable of reproducing very early and of surviving their whole reproductive span were probably very healthy to begin with. Pressure for early reproduction in a rapidly expanding population would potentially counteract opposite influences anticipated by life history theories that associate longevity with delayed age at maturity. According to the predictive adaptive response (PAR) hypothesis, reproductive scheduling is partly projected and determined by the developing organism from cues in the prenatal and early life environment (35Nettle D. Frankenhuis W.E. Rickard I.J. The evolution of predictive adaptive responses in human life history.Proc R Soc Lond B Biol Sci. 2013; 280: 20131343Crossref Scopus (199) Google Scholar). This would suggest that early reproduction is adaptive when morbidity and mortality are high, and childhood adversity has indeed been found to be associated with earlier ages at first birth and early ages at menarche (35Nettle D. Frankenhuis W.E. Rickard I.J. The evolution of predictive adaptive responses in human life history.Proc R Soc Lond B Biol Sci. 2013; 280: 20131343Crossref Scopus (199) Google Scholar), but not always (36Núñez-de la Mora A. Chatterton R.T. Choudhury O.A. Napolitano D.A. Bentley G.R. Childhood conditions influence adult progesterone levels.PLoS Med. 2007; 4: e167Crossref PubMed Scopus (78) Google Scholar, 37Kulathinal S. Säävälä M. Fertility intentions and early life health stress among women in eight Indian cities: testing the reproductive acceleration hypothesis.J Biosoc Sci. 2014; 13: 1-18Crossref Scopus (1) Google Scholar). Be that as it may, variation in age at first reproduction does not necessarily reflect variation in age at maturation (32Helle S. Lummaa V. Jokela J. Are reproductive and somatic senescence coupled in humans? Late, but not early, reproduction correlated with longevity in historical Sami women.Proc Biol Sci. 2005; 272: 29-37Crossref PubMed Scopus (76) Google Scholar, 38Gagnon A. Mazan R. Desjardins B. Smith K.R. Postreproductive longevity in a natural fertility population.in: Bengtsson T. Mineau G.P. Kinship and demographic behavior in the past. Springer Netherlands, Vol. 8. The Netherlands2008: 225-241Crossref Google Scholar). In most populations for which data are available, social and familial norms, kinship systems, inheritance rules, or demographic pressure determine the time at which individuals marry (39Dillon L. Parental and sibling influences on the timing of marriage, XVIIth and XVIIIth century Québec.Ann Demogr Hist (Paris). 2010; 119: 139-180Google Scholar) (and thus first reproduce), rather than evolutionary traits that might influence the timing of maturation. Variations in these social norms or practices could be largely responsible for the oscillation, from positive to negative, of the correlation between age at first birth and longevity from one study to the next. In contrast, age at last reproduction is probably much less socially constrained, leaving more room for a consistent association to evolve for this trait (32Helle S. Lummaa V. Jokela J. Are reproductive and somatic senescence coupled in humans? Late, but not early, reproduction correlated with longevity in historical Sami women.Proc Biol Sci. 2005; 272: 29-37Crossref PubMed Scopus (76) Google Scholar). In a study from the Boston area, Perls et al. (40Perls T.T. Alpert L. Fretts R.C. Middle-aged mothers live longer.Nature. 1997; 389: 133Crossref PubMed Scopus (139) Google Scholar) found that female centenarians were four times more likely to have had children after age 40 than women who died before age 74. Substantial research disclosed a positive relationship between age at last reproduction and post-reproductive survival in natural fertility populations (8Sun F. Sebastiani P. Schupf N. Bae H. Andersen S.L. 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