LETTER

REPLY TO MITTEROECKER AND FISCHER:

Developmentalsolutionstotheobstetricaldilemma LETTER are not Gouldian spandrels

Marcia S. Ponce de Le ´ona,1, Alik Huseynova, and Christoph P. E. Zollikofera

In our study on human pelvic development (1), we pro- a long postreproductive lifespan indicates the exis- pose two hypotheses explaining the narrowing of the tence of such evolutionary-selective mechanisms. female pelvis during postreproductive life. Hypothesis Second, the concept of biological spandrels (5) is 1 proposes ultimate, evolutionary causes, reflecting helpful to categorize phenotypic features into main selective pressures acting on postreproductive life. products and by-products of natural selection, thus cau- Hypothesis 2 proposes proximate, developmental tioning against adaptationist overinterpretation of sin- causes, reflecting reduced estrogen levels during post- gle features. However, this presupposes an omniscient reproductive life. observer who knows which structure has been selected Mitteroecker and Fischer (2) replicate one part of our for which function. In the case of the human pelvis, we study—that concerning adult pelvic development—with are doubly ignorant. Since the falsification of Wash- an independent dataset, taking into account age effects burn’s obstetrical dilemma hypothesis (6–8), we have on pelvic shape variation not considered in their earlier had to rethink how obstetric, locomotor, and other con- study (3). (Note that the smoothing functions used in our straints actually govern the evolution of the female and study only serve for visual guidance, not for statistical the male pelvis. In addition, we do not yet understand testing.) Rather than testing our hypotheses (1) with new which mechanisms of sex-biased autosomal gene ex- data, however, Mitteroecker and Fischer (2) discard the pression govern human pelvic development. first hypothesis and interpret postreproductive pelvic Third, we do not propose that postreproductive narrowingasanevolutionarysideeffect.Herewereit- narrowing evolved specifically “as an adaptation to erate that further research and new data are required to changing obstetric needs” (2). Rather, our hypothesis actually test both hypotheses. 1 proposes that it evolved under selective pressures First, Mitteroecker and Fischer (2) argue that be- acting on postreproductive life (1). Based on the cur- cause postreproductive females had a small inclusive rently available data, we propose that humans evolved fitness, and were rare during human evolution, their a developmental mechanism that regulates female pelvic phenotype was fitness-irrelevant. This argument pelvic shape change via changes in estrogen levels is not valid. A long postreproductive lifespan is gener- (which themselves represent a physiological marker ally acknowledged to be one of the hallmarks of mod- of fertility). According to this hypothesis, both the pu- ern human evolution (4), so we need to explain why and bertal widening and postmenopausal narrowing of the how it evolved. It is likely that the “longevity pheno- female pelvis are based on the same evolved mecha- type” is the result of selection on a large number of nism of hormone-mediated developmental plasticity. postreproductive physiological and morphological fea- Designating pelvic widening as the evolutionary main tures. The contribution of each single feature to this effect and narrowing as a side effect is premature un- phenotype may be small, and the initially few postre- less we understand the fitness functions of pelvic mor- productive individuals might have had a small inclusive phology in both sexes, and how they change during fitness. However, the fact that modern humans do have an individual’s lifetime.

1 Huseynov A, et al. (2016) Developmental evidence for obstetric adaptation of the human female pelvis. Proc Natl Acad Sci USA 113(19):5227–5232. 2 Mitteroecker P, Fischer B (2016) Adult pelvic shape change is an evolutionary side effect. Proc Natl Acad Sci USA, 10.1073/ pnas.1607066113. 3 Fischer B, Mitteroecker P (2015) Covariation between human pelvis shape, stature, and head size alleviates the obstetric dilemma. Proc Natl Acad Sci USA 112(18):5655–5660.

aAnthropological Institute and Museum, University of Zurich, 8057 Zurich, Switzerland Author contributions: M.S.P.d.L. and C.P.E.Z. designed research; M.S.P.d.L. and C.P.E.Z. performed research; A.H. analyzed data; and M.S.P.d.L. and C.P.E.Z. wrote the paper. The authors declare no conflict of interest. 1To whom correspondence should be addressed. Email: [email protected].

www.pnas.org/cgi/doi/10.1073/pnas.1607209113 PNAS Early Edition | 1of2 Downloaded by guest on September 23, 2021 4 Hawkes K, O’Connell JF, Jones NG, Alvarez H, Charnov EL (1998) Grandmothering, menopause, and the evolution of human life histories. Proc Natl Acad Sci USA 95(3):1336–1339. 5 Gould SJ, Lewontin RC (1979) The spandrels of San Marco and the Panglossian paradigm: A critique of the adaptationist programme. Proc R Soc Lond B Biol Sci 205(1161):581–598. 6 Washburn SL (1960) Tools and human evolution. Sci Am 203:63–75. 7 Dunsworth HM, Warrener AG, Deacon T, Ellison PT, Pontzer H (2012) Metabolic hypothesis for human altriciality. Proc Natl Acad Sci USA 109(38):15212–15216. 8 Warrener AG, Lewton KL, Pontzer H, Lieberman DE (2015) A wider pelvis does not increase locomotor cost in humans, with implications for the evolution of childbirth. PLoS One 10(3):e0118903.

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