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The Ecology and Evolutionary Endocrinology of Reproduction in the Human Female

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The Ecology and Evolutionary Endocrinology of Reproduction in the Human Female YEARBOOK OF PHYSICAL ANTHROPOLOGY 52:95–136 (2009) The Ecology and Evolutionary Endocrinology of Reproduction in the Human Female Virginia J. Vitzthum1,2,3,4* 1Anthropology Department, Indiana University, Bloomington, IN 47405 2Kinsey Institute for Research in Sex, Gender, and Reproduction, Indiana University, Bloomington, IN 47405 3Center for Integrative Study of Animal Behavior, Indiana University, Bloomington, IN 47405 4Department of Gender Studies, Indiana University, Bloomington, IN 47405 KEY WORDS life history theory; reproductive ecology; ovarian functioning; fecundity; adaptation ABSTRACT Human reproductive ecology (HRE) is ity of conception. Understanding the extent and causes of the study of the mechanisms that link variation in repro- adaptive and non-adaptive variation in ovarian function- ductive traits with variation in local habitats. Empirical ing is fundamental to ascertaining the proximate and and theoretical contributions from biological anthropol- remote determinants of human reproductive patterns. In ogy, physiology, and demography have established the this review I consider what is known and what still needs foundation necessary for developing a comprehensive to be learned of the ecology of women’s reproductive understanding, grounded in life history theory (LHT), of biology, beginning with a discussion of the principal ex- temporal, individual, and populational variation in wom- planatory frameworks in HRE and the biometry of ovar- en’s reproductive functioning. LHT posits that natural ian functioning. Turning next to empirical studies, it is selection leads to the evolution of mechanisms that tend evident that marked variation between cycles, women, to allocate resources to the competing demands of growth, and populations is the norm rather than an aberration. reproduction, and survival such that fitness is locally Other than woman’s age, the determinants of these differ- maximized. (That is, among alternative allocation pat- ences are not well characterized, although developmental terns exhibited in a population, those having the highest conditions, dietary practices, genetic variation, and epige- inclusive fitness will become more common over genera- netic mechanisms have all been hypothesized to play tional time.) Hence, strategic modulation of reproductive some role. It is also evident that the reproductive func- effort is potentially adaptive because investment in a new tioning of women born and living in arduous conditions is conception may risk one’s own survival, future reproduc- not analogous to that of athletes, dieters, or even the tive opportunities, and/or current offspring survival. The lower end of the ‘‘normal range’’ of HPO functioning in hypothalamic-pituitary-ovarian (HPO) axis is the princi- wealthier populations. Contrary to the presumption that pal neuroendocrine pathway by which the human female humans have low fecundity and an inefficient reproduc- modulates reproductive functioning according to the tive system, both theory and present evidence suggest changing conditions in her habitat. Adjustments of repro- that we may actually have very high fecundity and a ductive investment in a potential conception are mani- reproductive system that has evolved to be flexible, ruth- fested in temporal and individual variation in ovarian lessly efficient and, most importantly, strategic. Yrbk cycle length, ovulation, hormone levels, and the probabil- Phys Anthropol 52:95–136, 2009. VC 2009 Wiley-Liss, Inc. It would be instructive to know not only by what Anthropologists are well positioned to contribute to physiological mechanisms a just apportionment is made and gain from these advancements, as evidenced by find- between the nutriment devoted to the gonads and that ings from field studies during the past three decades devoted to the rest of the parental organism, but also what that have broadened our understanding of human, espe- circumstances in the life-history and environment would cially female, reproductive functioning (e.g., Konner and render profitable the diversion of a greater or lesser share of Worthman, 1980; Wood et al., 1985; Leslie and Fry, the available resources towards reproduction. Ronald Fish- 1989; Ellison et al., 1989; Vitzthum, 1989; Holman, 1996; er, 1930. Strassmann, 1997; Bribiescas, 2001; Nepomnaschy et al., Fisher’s two questions are clearly linked, yet histori- 2006 and others discussed later). But there is much cally the answers to each have been pursued largely inde- more work to be done. A cursory examination of medical pendently. With rapidly advancing laboratory technolo- texts on women’s reproductive biology could leave one gies, physiologists have exposed many of the fine details of how organisms function as they do, and with Additional Supporting Information may be found in the online sophisticated analytical tools, evolutionary theorists have version of this article. generated testable explanations of why organisms vary as they do. Propitiously, the relatively recent and invigorat- *Correspondence to: Virginia J. Vitzthum, Kinsey Institute, Mor- ing exchange of ideas and data between these lines of in- rison Hall 302, Indiana University, 1165 E. Third St., Bloomington, quiry has fostered the rapidly expanding field of evolu- IN 47405, USA. E-mail: [email protected] tionary endocrinology. The study of whole organism physi- ology, morphology and behavior in natural, and DOI 10.1002/ajpa.21195 sometimes cleverly modified, settings is at the nexus of Published online in Wiley InterScience these exciting developments in the evolutionary sciences. (www.interscience.wiley.com). VC 2009 WILEY-LISS, INC. 96 V.J. VITZTHUM thinking that the functioning of the ovarian cycle is well ductive investment, even to the extent of rejection of the understood in extraordinary detail. But in fact, there is current opportunity (anovulation or early pregnancy termi- not much that is unequivocally certain about the specifics nation), is largely under maternal control and not costly, as of women’s reproductive biology. Moreover, for all that is only one or very few opportunities for reproduction may be known at the cellular level, there is but a modicum of lost. Figure 1 is a schematic presentation of the principal data on populational variation in these processes, and the approaches used by reproductive ecologists to investigate determinants of that variation are almost entirely conjec- women’s reproductive functioning. Whichever explanatory tural. Fortunately, anthropologists’ preoccupation with framework one prefers, understanding the extent and variation, our willingness (even eagerness) to work out- causes of variation in ovarian functioning is fundamental side the confines of our own populations, and our capacity to ascertaining the proximate and remote determinants of for adapting laboratory methods to remote field sites pre- human reproductive patterns. disposes us better than most to undertake the fascinating Many investigators, particularly those concerned with and necessary task of discovering the nature and extent the role of energetics in reproduction, have focused on of variation in human reproductive functioning. measuring ovarian functioning, ‘‘the ‘linchpin’ of the For the most part, contemporary biological anthropolo- female reproductive system, with steroid levels being the gists investigate human reproductive variation within a most useful, readily detectable reflection of ovarian func- somewhat fuzzy framework that has come to be known tion’’ (Ellison, 1990, p 936). Proponents of this approach as human reproductive ecology (HRE). Reflecting differ- presume that variation in measures of ovarian function- ent intellectual traditions, there are several definitions ing is associated with variation in fecundity and have of this field of inquiry (e.g., Campbell and Wood, 1994; been less concerned with measuring fertility, considered Hill and Hurtado, 1996; Morbeck et al., 1997; Winter- by some to ‘‘provide for second-order inferences only’’ halder and Smith, 2000; Ellison, 2001; Leslie and Little, (Ellison, 1990, p 934). 2003). For the purpose of the present discussion, I define On the other hand, fertility differentials are at the HRE as: the study of the mechanisms that link variation heart of demographic frameworks, which delineate a fi- in reproductive traits with variation in local habitats. nite set of proximate determinants by which all the Habitats comprise the physical, biological, and social potential causes of variation in fertility must exert their conditions that an individual must accommodate and effects. Wood and Weinstein (1988), Campbell and Wood exploit for survival and reproduction. I emphasize ‘‘local (1988), and Wood (1990, 1994a) have developed a model habitats’’ because these are the contexts within which of the proximate determinants of natural fertility natural selection acts on individuals and because human (PDNF; Table 1, Fig. 1 [middle panel]). Ovarian hormone ‘‘biological uniformitarianism,’’ the assumption that all levels are not a PDNF but might influence several humans respond in a similar manner to comparable PDNF including ovarian cycle length and the proportion stimuli across varied habitats, is demonstrably incorrect of cycles that are ovulatory. A sensitivity analysis of the (Leslie and Little, 2003). potential contribution to fertility differentials of each Mechanisms subsumes both physiological and behav- fecundability factor in this model suggested that varia- ioral processes that modulate reproductive traits. These tion in the frequency
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