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The importance of distinguishing mathematical and biological plausibility

Posted by aacohen1 on 15 Jun 2013 at 20:53 GMT

As two researchers who have worked on the evolutionary theory of menopause/post-fertile lifespan (PFL) (refs below) and one who has been asked by the popular press for comments, we read this article with great interest. The article demonstrates the mathematical feasibility of an influence of male mate preference on female PFL; however we wish to stress that this is not the same as explaining the origin of the menopause. In fact we argue that this model has a low likelihood and is biologically implausible due to its restrictive assumptions. Here we outline our three major concerns regarding the model specification and ensuing conclusions.

First, it appears quite likely to us that the causality is reversed here. There is a clear reason to expect that declining fertility in older women would lead to male mating preferences for younger women, and not the other way around. Anderson (1986) showed that males in most primates prefer females of higher parity (i.e., generally older) and Muller, Thompson et al. (2006) showed that male chimpanzees prefer older females. While this is not in itself inconsistent with the findings presented by Morton et al., the question arises as to why humans would be (apparently) unique in having a male preference for younger mates. The most obvious and plausible answer is that declining fertility with age in human females (and particularly a complete lack of fertility at older ages) strongly favoured selection in human males for a preference for younger females.

Given that (a) this is the obvious explanation for the evolution human male mate preferences, and (b) there are several other plausible scenarios for the evolution of menopause/ PFL, including those proposed by us, we feel there is a particularly high burden on Morton et al. to either show that the other theories are not viable, or to show that male preference for younger mates could not have evolved as a result of human female PFL. The article does not address either of these questions; it simply demonstrates mathematical feasibility. The authors may be correct that there is a potential for such effects, but if so they are likely to be minor, after-the-fact adjustments in the length of PFL, not a major reason for why it evolved. Proof of this would require a different model, one designed to show that existing PFL could be modified through mate preference in a feedback loop where both PFL and mating preferences, of both sexes, are free to evolve.

Second, the model proposed assumes that mutations are free to act in a highly age-specific manner. For example, a mutation could arise that would have an effect on fertility just in a specific 5-year age range. This is not consistent with what is known about most mutations and their effects. There is no known internal biological clock that could be used by genes to trigger highly specific age effects; rather, most age effects are likely due to trajectories of function that change as the whole biological context changes with age. Indeed, the human female decline in fecund ability is a long gradual process, with menopause occurring after fecundability has reached zero (Holman and Wood 2001). While a few relatively age-specific genes are known to exist (e.g., Huntington’s chorea), the paucity of such examples suggests that this is a poor model for how evolution works.

The consequence of this for the model is important. A large change in fertility at, say, age 55 is not likely to be independent of fertility at age 25 – rather, a drop in late fertility is almost certainly accompanied by earlier declines, either in the form of a more rapid drop off or an earlier start to reproductive decline (Cohen 2004). This implies that the costs of a decline in late fertility are substantially underestimated by the model, and that the effect of male preference is over-estimated.

Third, the authors, in conflating menopause (the age related cessation of cycling) with post-fertile survival, address the wrong trait. As has been pointed out many times in the literature on this subject, human females are not unique in having an age beyond which they generally become infertile, nor are they unique in having the ability, provided with the right environment, to live beyond that age. Rather, they are unique among primates in frequently surviving to and well beyond infertile ages. It is therefore the pattern of age specific survival, rather than age-specific fertility, that is a derived human trait requiring a sociobiological explanation (Levitis, Burger et al. 2013).

We believe that together these points show the risks of pursuing mathematical plausibility outside a context of biological plausibility and likelihood, and we hope the authors will undertake appropriate analyses to address these questions. Lastly, we would like to note that most post-menopausal women across the spectrum of human societies continue to have husbands/partners/lovers, indicating that a potential for longer reproduction would be present for most women if there were no menopause.

Alan A. Cohen
Université de Sherbrooke
Sherbrooke, QC, Canada

Daniel A. Levitis
Max-Planck Odense Center on the Biodemography of Aging
University of Southern Denmark

Max Burton-Chellew
Oxford University
Oxford UK

Anderson, C.M. 1986. Female age: Male preference and reproductive success in primates. International Journal of Primatology. 7:305-326.

Cohen, A.A. 2004. Female post-reproductive life span: A general mammalian trait. Biological Reviews 79: 733–750.

Levitis D.A., Lackey, L.B. 2011. A measure for describing and comparing postreproductive life span as a population trait. Methods in Ecology and Evolution 2: 446-453.

Holman, D. J. and J. W. Wood (2001). Pregnancy loss and fecundability in women. Reproductive Ecology and Human Evolution. New York: Aldine de Gruyter. P. T. Ellison. New Brunswick, Trasaction Publishers: 15-38.

Levitis, D., et al. (2013). The Human Postfertile Life Span in Comparative Evolutionary Context. Evolutionary Anthropology 22(2): 66-79.

Muller, M. N., et al. (2006). Male chimpanzees prefer mating with old females. Current Biology 16(22): 2234-2238.

No competing interests declared.