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Somatic maintenance/reproduction tradeoffs and human evolution

Published online by Cambridge University Press:  25 July 2022

Kristen Hawkes*
Affiliation:
Department of Anthropology, University of Utah, Salt Lake City, UT 84112, USA hawkes@anthro.utah.edu

Abstract

The authors propose that many morbidities higher in women than men are adaptations protecting survival, selected because survival has been especially crucial to mothers' reproductive success. Following their lead, I pursue variation in tradeoffs between reproduction and survival recognized by Darwin that were likely central to the evolution of many traits that distinguish us from our great ape cousins.

Type
Open Peer Commentary
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Benenson, Webb, and Wrangham's (BWW) extension of Campbell's (Reference Campbell1999) staying alive theory (SAT) is a welcome elaboration of likely sex differences in fitness-related tradeoffs. Both the Origin (Reference Darwin1859) and Descent (Reference Darwin1871) show Darwin's own recognition of variation in tradeoffs that account for astonishing diversity in the living world. He lacked tools to understand how inheritance works but still saw enormous phenotypic consequences of sexual reproduction's “one mother, one father for each offspring” foundation. That foundation is now usually called the Fisher condition, as Fisher (Reference Fisher1930) combined Mendelian inheritance with natural selection to show that each sex contributes half the ancestry of future generations. Although it is fertile females – not males – limiting the number of babies, offspring sex ratios are usually near even because two haploid gametes, ovum and sperm, form each diploid zygote. If males are rare, the average reproductive success of rare males is higher than the female average. Then mothers tending to produce more males average more grandchildren, erasing the male rarity.

The Fisher condition also explains why sex ratios in the fertile ages determine which strategies dominate mating competition. Campbell (Reference Campbell1999) countered textbook claims that with typical sex roles males compete while females care: males are ardent, females coy. She cited Hrdy (Reference Hrdy1979, Reference Hrdy1981, Reference Hrdy and Bleier1986), Smuts (Reference Smuts, Smuts, Cheney, Seyfarth, Wrangham and Struhsaker1987, Reference Smuts1995), and Wrangham (Reference Wrangham1980) for evidence of libidinous and competitive female primates, with different resources limiting fitness for each sex: food and safety for females, paternities for males. Those differences contributed to Campbell's SAT and BWW's extension here.

Variations in tradeoffs between reproduction and survival were taken up by Williams' (Reference Williams1957) field-defining paper that explained why natural selection results in differing rates of aging across the living world. Williams (Reference Williams1966) later modeled costs to survival imposed by current reproduction showing selection favors a “normal reaction” adjusted to the actor's age and sex by fitness gains expected from additional allocation to current reproduction or to survival instead. Williams called the likely fitness value of the latter residual reproductive value (more on reproductive value in Hawkes, Reference Hawkes2020a).

These tradeoffs are important for all sexual reproducers but their distinctive importance in human evolution is the topic here. Darwin saw phenotypic evidence of our phylogenetic closeness to great apes, now confirmed by genetics placing us all in the same hominid family. In all living hominids female fertility usually ends before age 50 – but great ape females age faster than women and usually die while still cycling. Humans differ in our postmenopausal longevity, later maturity, yet faster rate of baby production. A grandmother hypothesis to explain those distinctive traits uses ethnographic observations of grandmothers' foraging subsidies (Blurton Jones, Reference Blurton Jones2016; Hawkes, O'Connell, & Blurton Jones, Reference Hawkes, O'Connell and Blurton Jones1997, Reference Hawkes, O'Connell and Blurton Jones2018) and theory developed to explain the broad variation in female mammal life histories (Charnov, Reference Charnov1991, Reference Charnov1993; Hawkes, O'Connell, Blurton Jones, Alvarez, & Charnov, Reference Hawkes, O'Connell, Blurton Jones, Alvarez and Charnov1998; O'Connell, Hawkes, & Blurton Jones, Reference O'Connell, Hawkes and Blurton Jones1999). In two-sex agent-based models of that hypothesis, grandmothers' subsidies propel the evolution of a great ape-like life history to a human-like one (Kim, Coxworth, & Hawkes, Reference Kim, Coxworth and Hawkes2012, Reference Kim, McQueen, Coxworth and Hawkes2014, Reference Kim, McQueen and Hawkes2019). Increased longevity also shifts the sex ratio in the fertile ages from the female-bias typical of mammals to the male-bias in humans as proportions of both post-fertile women and older still-fertile men expand (Coxworth, Kim, McQueen, & Hawkes, Reference Coxworth, Kim, McQueen and Hawkes2015). When mating sex ratios are female-biased, males pursuing multiple mates gain more paternities; with the bias reversed, claiming and guarding a mate against other males wins more paternities (Loo, Chan, Hawkes, & Kim, Reference Loo, Chan, Hawkes and Kim2017a; Loo, Hawkes, & Kim, Reference Loo, Hawkes and Kim2017b; Loo, Weight, Hawkes, & Kim, Reference Loo, Weight, Hawkes and Kim2020; Loo, Rose, Hawkes, & Kim, Reference Loo, Rose, Hawkes and Kim2021; Rose, Hawkes, & Kim, Reference Rose, Hawkes and Kim2019; Schacht & Bell, Reference Schacht and Bell2016).

All of this follows ancestral grandmothers' subsidies adjusting the fitness maximizing tradeoffs between somatic maintenance and current reproduction. More somatic allocation results in more grandmothering subsidies, shortening birth intervals. Ancestral mothers' bearing next babies sooner poses survival challenges for their previous infants recognized by Hrdy (Reference Hrdy2009; see also Hawkes, Reference Hawkes2014). She saw the precocious social responsiveness that makes human babies so engaging as an adaptive consequence of those challenges. Added to the maturity delaying effects of lower adult mortality, slower neural maturation expands final brain size and also proportion neocortex across the mammals (Finlay & Darlington, Reference Finlay and Darlington1995; Workman, Charvet, Clancy, Darlington, & Finlay, Reference Workman, Charvet, Clancy, Darlington and Finlay2013). The combination of earlier weaning with slower neural maturation would have wired distinctive priorities for shared understanding in ancestral infancy (Finlay, Reference Finlay2019; Finlay & Uchiyama, Reference Finlay, Uchiyama and Kaas2017; Hawkes, Reference Hawkes2020b; Hawkes & Finlay, Reference Hawkes and Finlay2018).

BWW suggest their SAT's relevance to the male–female health-survival paradox: Where data are available, women's longevity is almost always greater than men's even though morbidities are higher in women than men (Alberts et al., Reference Alberts, Archie, Gesquiere, Altmann, Vaupel, Christensen, Weinstein and Lane2014). If the morbidities BWW explore are actually protective that could resolve the paradox. If increased longevity was favored in our lineage as ancestral grandmothering displaced the independent mothering of other great apes, our postmenopausal life stage also had consequences for sexual selection (O'Connell, Hawkes, Lupo, & Blurton Jones, Reference O'Connell, Hawkes, Lupo and Blurton Jones2002). More fertile old men competed for paternities (Coxworth et al., Reference Coxworth, Kim, McQueen and Hawkes2015) with preferences for mating younger females that distinguish men from chimpanzees (Muller, Emery Thompson, & Wrangham, Reference Muller, Emery Thompson and Wrangham2006, Reference Muller, Blurton Jones, Colchero, Emery Thompson, Enigk, Feldblum and Pusey2020). Ethnography shows older men usually hold substantial advantages over younger ones (Collier & Rosaldo, Reference Collier, Rosaldo, Ortner and Whitehead1981; Hawkes, Reference Hawkes and Diehl2000; Marlowe & Berbesque, Reference Marlowe and Berbesque2012; Rodseth, Reference Rodseth2013). That alters males' fitness tradeoffs between current reproduction and somatic maintenance. Formal two-sex models of the grandmother hypothesis expose sexual conflict over longevity (Chan, Hawkes, & Kim, Reference Chan, Hawkes and Kim2016, Reference Chan, Hawkes and Kim2017; Kim et al., Reference Kim, Coxworth and Hawkes2012, Reference Kim, McQueen, Coxworth and Hawkes2014) with male advantages for greater longevity pushing the compromise longevity higher than an equilibrium without males (Hawkes, Reference Hawkes2020a).

If BWW's expansion of SAT brings more attention to the evolution of human postmenopausal longevity, more attention to consequences for paternity competition might follow. Yet the topic of sexual selection in human evolution can seem unwelcome where broader gender identities are now celebrated. Expanded appreciation of sexual fluidity can make Darwin's recognition of “competition among the males for possession of the females” seem to glorify toxic masculinity and obscure gender diversity. Yet Darwin's theory of natural selection including sexual selection is central to understanding human evolution. It helps explain pervasive conflicts of interest – and our distinct appetite for shared understanding, an appetite that inflates antagonisms – but can also defuse them.

Acknowledgments

I'm grateful to Megan Mullineaux and Jim O'Connell for insights and editorial advice.

Financial support

No special funding supported preparation of this comment.

Conflict of interest

I have no conflict of interest.

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