Reproductive aging: theoretical perspectives, mechanisms, nonhuman models, and health correlatesHaaga, John; O'Connor, Kathleen; Weinstein, Maxine; Wise, Phyllis
doi: 10.1111/j.1749-6632.2010.05700.xpmid: 20738270
Every 365.2421999 days—more or less—the earth rotates, revolves, wobbles, and precesses along an elliptical path around the sun. Those of us who survive the journey are a year older: we have aged one solar year. Some years we seem to age faster than other years; some people seem to age faster than other people; some systems seem to age faster than other systems. As we begin to mature, reach our middle years, and become elderly, reproductive changes are among the markers of aging that are most notable, particularly among women. What—if anything—can we learn about more general processes of aging from reproductive aging? Does our postreproductive survival contribute to our fitness, or is it just a chance event, a result of selection on other characteristics? Can our insights and research be translated into improved clinical practice? We explore reproductive aging with a wide‐angle multidisciplinary lens that we use to focus on four articulating areas: theoretical perspectives, mechanisms, nonhuman models, and health correlates. We propose directions for future work.a
Life historical perspectives on human reproductive agingEllison, Peter T.
doi: 10.1111/j.1749-6632.2010.05611.xpmid: 20738271
A commentary is offered on the chapters that comprise the section on Theoretical Foundations, emphasizing novel contributions of each. Three additional points are then made. First, while the biology of reproductive aging may be common to all human populations, its actual course can be expected to vary between individuals and between populations depending on ecological conditions and developmental histories. Second, increasing fertility (such as that typical of humans compared with hominoid relatives and imputed ancestral species) decreases the opportunity and impact of contributions from ascendant relatives and increases the opportunity and impact of contributions from collateral and descendent relatives in promoting the fitness of a focal individual. Finally, an argument is made that the major change in human life history physiology in the Pleistocene has been the extension of adult lifespan, not any change in ovarian physiology or rate of reproductive senescence, and that extended lifespan created a selection pressure for the emergence of indirect reproductive effort among postreproductive individuals, not the reverse.
Learning, menopause, and the human adaptive complexKaplan, Hillard; Gurven, Michael; Winking, Jeffrey; Hooper, Paul L.; Stieglitz, Jonathan
doi: 10.1111/j.1749-6632.2010.05528.xpmid: 20738273
This paper presents a new two‐sex learning‐ and skills‐based theory for the evolution of human menopause. The theory proposes that the role of knowledge, skill acquisition, and transfers in determining economic productivity and resource distribution is the distinctive feature of the traditional human ecology that is responsible for the evolution of menopause. The theory also proposes that male reproductive cessation and post‐reproductive investment in descendants is a fundamental characteristic of humans living in traditional foraging and simple horticultural economies. We present evidence relevant to the theory. The data show that whereas reproductive decline is linked to increasing risks of mortality in chimpanzees, human reproductive senescence precedes somatic senescence. Moreover under traditional conditions, most human males undergo reproductive cessation at the same time as their wives. We then present evidence that after ceasing to reproduce, both men and women provide net economic transfers to children and grandchildren. Given this pattern of economic productivity, delays in menopause would produce net economic deficits within families.
Do women stop early? Similarities in fertility decline in humans and chimpanzeesHawkes, Kristen; Smith, Ken R.
doi: 10.1111/j.1749-6632.2010.05527.xpmid: 20738274
Two kinds of evidence suggest that female fertility may end at an earlier age in modern people than in ancestral populations or in our closest living relatives, chimpanzees. We investigate both to see whether fertility schedules or ovarian follicle counts falsify the alternative hypothesis that the age of terminal fertility changed little in the human lineage while greater longevity evolved due to grandmother effects. We use 19th century Utah women to represent non‐contracepting humans, and compare their fertility by age with published records for wild chimpanzees. Then we revisit published counts of ovarian follicular stocks in both species. Results show wide individual variation in age at last birth and oocyte stocks in both humans and chimpanzees. This heterogeneity, combined with interspecific differences in adult mortality, has large and opposing effects on fertility schedules. Neither realized fertility nor rates of follicular atresia stand as evidence against the hypothesis that ages at last birth changed little while greater longevity evolved in our lineage.
An evolutionary and life history perspective on human male reproductive senescenceBribiescas, Richard G.
doi: 10.1111/j.1749-6632.2010.05524.xpmid: 20738275
Unlike menopause, male reproductive senescence does not involve an acute drop in fertility. Men do, however, manifest distinct changes in somatic and gonadal function with age. Moreover, population variation in male reproductive senescence reveals phenotypic plasticity resulting from environmental, lifestyle, and genetic factors. An evolutionary and life history perspective is vital for understanding male reproductive senescence because aging involves biological constraint as well as adjustments to reproductive strategies and the allocation of somatic resources. An awareness of life history–related tradeoffs between energetic and time constraints is especially useful because biological aspects of male senescence are products of environmental challenges and natural selection. This article reviews the adaptive significance of the evolutionary biology of human male senescence with particular attention to population variation. An evolutionary perspective cannot only shed light on the origins and biology of human male senescence but also provide insights into contemporary issues of male aging and health.
Dynamic heterogeneity and life historiesTuljapurkar, Shripad; Steiner, Ulrich K.
doi: 10.1111/j.1749-6632.2010.05519.xpmid: 20738276
Biodemography is increasingly focused on the large and persistent differences between individuals within populations in fitness components (age at death, reproductive success) and fitness‐related components (health, biomarkers) in humans and other species. To study such variation we propose the use of dynamic models of observable phenotypes of individuals. Phenotypic change in turn determines variation among individuals in their fitness components over the life course. We refer to this dynamic accumulation of fitness differences as dynamic heterogeneity and illustrate it for an animal population in which longitudinal data are studied using multistate capture‐mark‐recapture models. Although our approach can be applied to any characteristic, for our empirical example we use reproduction as the phenotypic character to define stages. We indicate how our stage‐structured model describes the nature of the variation among individual characteristics that is generated by dynamic heterogeneity. We conclude by discussing our ongoing and planned work on animals and humans. We also discuss the connections between our work and recent work on human mortality, disability and health, and life course theory.
Mechanisms of reproductive aging: conserved mechanisms and environmental factorsOttinger, Mary Ann
doi: 10.1111/j.1749-6632.2010.05653.xpmid: 20738277
The interplay of neuroendocrine processes and gonadal function is exquisitely expressed during aging. In females, loss of ovarian function results in decreased circulating estradiol. As a result, estrogen‐dependent endocrine and behavioral responses decline, including impaired cognitive function reflecting the impact of declining estrogen on the hippocampus circuits, and decreased metabolic endocrine function. Concurrently, age‐related changes in neuroendocrine response also contribute to the declining reproductive function. Our session considered key mechanisms in reproductive aging including the roles of ovarian function (Finch and Holmes) and the hypothalamic median eminence (Yin and Gore) with an associated age‐related cognitive decline that accompanies estrogen loss (Morrison and colleagues). Effects of smoking, obesity, and insulin resistance (Sowers and colleagues) impact the timing of the perimenopause transition in women. Animal models provide excellent insights into conserved mechanisms and key overarching events that bring about endocrine and behavioral aging. Environmental factors are key triggers in timing endocrine aging with implications for eventual disease. Session presentations will be considered in the context of the broader topic of indices and predictors of aging‐related change.
Ovarian aging in developmental and evolutionary contextsFinch, Caleb E.; Holmes, Donna J.
doi: 10.1111/j.1749-6632.2010.05610.xpmid: 20738278
Evolutionary theory predicts that aging‐related fertility declines result from tradeoffs between reproduction and somatic maintenance. Developmental programs for oogenesis also contribute to variation in aging‐related reproductive declines among female vertebrates. Documented reproductive aging patterns in female vertebrates, including humans, are consistent with canonical aging patterns determined developmentally and require no special adaptive explanation. Here we discuss patterns of aging‐related ovarian decline in diverse female vertebrates, and place human ovarian aging in comparative context. Depletion of finite oocyte stores accompanied by fertility loss occurs in a variety of nonhuman mammals and vertebrates, including short‐lived rodents, birds, and some fishes; moreover, postreproductive lifespans of considerable length clearly are not limited to long‐lived, social species with well‐developed kin networks. We argue for a more rigorous comparative approach for understanding the evolutionary and developmental bases of ovarian aging in vertebrates with a wider range of aging patterns and social structures.
Relating smoking, obesity, insulin resistance, and ovarian biomarker changes to the final menstrual periodSowers, MaryFran R.; McConnell, Daniel; Yosef, Matheos; Jannausch, Mary L.; Harlow, Sioban D.; Randolph, Jr, John F.
doi: 10.1111/j.1749-6632.2010.05523.xpmid: 20738279
To determine if smoking, obesity, and insulin resistance mediated age at final menstrual period (FMP), we examined anti‐Müllerian hormone (AMH), inhibin B, and follicle‐stimulating hormone (FSH) as biomarkers of changing follicle status and ovarian aging. We performed a longitudinal data analysis from a cohort of premenopausal women followed to their FMP. Our results found that smokers had an earlier age at FMP (P < 0.003) and a more rapid decline in their AMH slope relative to age at FMP (P < 0.002). Smokers had a lower baseline inhibin B level relative to age at the FMP than nonsmokers (P= 0.002). Increasing insulin resistance was associated with a shorter time to FMP (P < 0.003) and associations of obesity and time to FMP were observed (P= 0.004, in model with FSH). Change in ovarian biomarkers did not mediate the time to FMP. We found that smoking was associated with age at FMP and modified associations of AMH and inhibin B with age at FMP. Insulin resistance was associated with shorter time to FMP independent of the biomarkers. Interventions targeting smoking and insulin resistance could curtail the undue advancement of reproductive aging.