Sociality, Hierarchy, Health Comparative Biodemography: A Collection of Papers (2014) / Chapter Skim
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14 A Comparative Perspective on Reproductive Aging, Reproductive Cessation, Post-Reproductive Life, and Social Behavior--Peter T. Ellison and Mary Ann Ottinger
14 A Comparative Perspective on Reproductive Aging, Reproductive Cessation, Post-Reproductive Life, and Social Behavior--Peter T. Ellison and Mary Ann Ottinger
Pages 315-338
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From page 315... ...
Follicular depletion is widely considered to be the primary cause of the phenomenon of human menopause, as well as of cessation of ovarian function in other birds and mammals (Edson et al., 2009; Perheentupa and Huhtaniemi, 2009; Finch, 2013) , but the degree to which this imposes a constraint on evolution is not clear.
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From page 316... ...
Finally, we will return to questions of the evolutionary origins of human post-reproductive life in particular. MECHANISMS OF VERTEBRATE REPRODUCTIVE AGING Follicular Depletion in Females In all vertebrates, gonads develop embryologically from the genital ridge mesoderm and are populated by migrating primordial germ cells that give rise to mitotically competent oogonia and spermatogonia in females and males respectively.
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From page 317... ...
. This intriguing observation of persistent germinal stem cells may have important medical applications in the domain of assisted reproduction, but does not appear to have any effect on processes of reproductive aging or follicular depletion.
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From page 318... ...
. Given the finite supply of primordial follicles and the inexorable rate of attrition in that stock, the follicular supply in a bird or mammal that lives long enough will eventually drop below a threshold level necessary to supply a sufficient cohort of primary follicles for recruitment, and estrogen production by the primary follicles will drop below the levels necessary for
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From page 319... ...
. Because the primary follicular pool declines in size with age in an inexorable fashion due to the dwindling size of the primordial follicle stock, female fecundity in most species of birds and mammals begins to decline prior to the end of reproductive life (Holmes et al., 2003; Cohen, 2004; Finch and Holmes, 2010)
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From page 320... ...
. Fitness Value of Mechanisms of Female Reproductive Aging In most species of birds and mammals, the combination of initial primordial follicle supply, rate of follicular depletion, and balance of neuro endocrine feedback results in a reproductive lifespan in the wild that is at least as long as the natural lifespan.
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From page 321... ...
Age-related reproductive alterations become apparent in human males after the 5th decade in men, though they may begin much earlier, and include decreasing testosterone levels, loss of potency, increasing sperm abnormalities, and the potential for an increase in birth defects attributable to paternal age. Observations from the Massachusetts Male Aging Study show that total testosterone decreases 0.4-0.8 percent annually, while biologically active free testosterone levels decrease by 1.2-1.7 percent per year starting at the age of 50 (Plas et al., 2000; Henkel et al., 2005)
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From page 322... ...
Consequently, diminishing T levels precipitate a cascade that impacts the entire reproductive system, as well as impacting muscle function, bone density, and steroid hormone target tissues. Although declining testosterone levels do promote some increase in gonadotropin production, this change is not sufficient to prevent the agerelated decline in reproductive function.
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From page 323... ...
Reproductive termination in females can, for example, be defined anatomically, as follicular depletion below some threshold; endocrinologically, as a level of estrogen production insufficient to promote endometrial proliferation or to suppress gonadotropin production to a normal range; phenomenologically, as a cessation of menses, sexual swellings, estrus behavior, or other outward markers of ovarian cyclicity; or demographically, as a cessation of conceptions or births. Of these, only the anatomical definition can be applied in the present, but it is, of course, the most onerous, requiring histological examination of ovarian tissue.
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From page 324... ...
Generally, there is an assumption in the literature that data from captivity cannot be used to make inferences about reproductive cessation in the wild, but such data can speak to the existence and degree of phenotypic plasticity in reproductive and total lifespan. Because anatomical, endocrinological, or even phenomenological markers of reproductive termination are rarely available, most animal studies use age at last reproduction (e.g., egg laying, pregnancy, live birth)
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From page 325... ...
and Chinese hamsters (Chrisetelus griseus: Parkening, 1982) , regularly live for a significant period after reproductive cessation, even by the strictest anatomical definition, and are often used as models of follicular depletion.
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From page 326... ...
Post-Reproductive Life in Birds There are few examples of post-reproductive lifespan in wild birds, though relevant data are sparse and difficult to obtain. In captivity and in domestic species, post-reproductive life is more common.
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From page 327... ...
. Figure 14-3 Bitmapped Socioecological Correlates of Extended Post-Reproductive Life Because the only species with well-documented, extended, female postreproductive life in the "wild" are humans and a few toothed whales, some researchers have postulated that cooperative group living and the opportunity for older females to contribute behaviorally to the reproductive success of their offspring is an important correlate of extended female post-reproductive life (McAuliffe and Whitehead, 2005; Johnstone and Cant, 2010)
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From page 328... ...
The dynamics of follicular stocking and depletion are subject to natural selection, however, and have led to female reproductive lifespans that are at least co-terminous with natural lifespans in the vast majority of birds and mammals. The only notable exceptions in the wild are certain toothed whales.
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From page 329... ...
With respect to chimpanzees, humans, and wild populations in both captivity and domesticated, it is possible that increased fecundity at younger ages also reflects a more rapid depletion of the primordial follicular supply. Rates of human follicular depletion and ages at reproductive cessation are nevertheless quite close to those of chimpanzees and therefore presumably to the two species' last common ancestor (Jones et al., 2007)
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From page 330... ...
But the Chu and Lee hypotheses assume that the evolved characteristic in humans is an early termination of reproduction relative to its ancestral state, whereas it seems clear that the evolved characteristic is prevalent and extended postreproductive life, not premature reproductive cessation. It seems to us that the most appropriate starting point to posit for the current life history pattern would be the regular appearance of a phenotypic gap between female lifespan and reproductive cessation, a gap similar to that observed in contemporary captive populations of primates (Ellison, 2010)
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From page 331... ...
These changes would either have to increase the initial supply of primordial follicles or slow the rate of follicular depletion so that a sufficient follicular reserve would exist to support reproduction beyond the ordinary age of follicular exhaustion. For many evolutionary theorists, it seems clear that this path should lead to the highest adaptive peak, but it is not clear that its initial slope would be very steep.
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From page 332... ...
an attention to the selective pressures generated by this phenotypic gap and the potential for initial increases in fitness due to different responses rather than a comparison of ultimate fitness peaks. We conclude that the path of indirect reproductive effort may have provided the path of steepest initial ascent, and that the path of extended reproductive life may be compromised by insensitivity to changes in initial follicular supply and fitness tradeoffs associated with decreases in the rate of follicular depletion.
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From page 333... ...
Hence its fitness value must be high and tightly bound to the reproductive biology of birds and mammals, or it must be a pattern that is very difficult to change due to developmental constraint, or both. This pattern of female gamete production, involving both a finite primordial follicle supply and an ineluctable attrition in that supply with age, makes female post-reproductive life possible and even predictable, should a female live long enough.
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From page 334... ...
. Female post-reproductive lifespan: A general mammalian trait.
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From page 335... ...
. Hypoestrogenic "inactive phases" at the start of the menstrual cycle: Changes with age and reproductive stage, and relationship to follicular depletion.
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From page 336... ...
. Life history and reproductive biology of the short-fined pilot whale, Gloicephala macrorhyncus, off the Pacific coast of Japan.
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From page 337... ...
. Reproductive cessation in female mammals.
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From page 338... ...
. Pooled energy budget and human life history.
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