Differential fitness costs of reproduction between the sexes

Abstract

Natural selection does not necessarily favor maximal reproduction because reproduction imposes fitness costs, reducing parental survival, and offspring quality. Here, we show that parents in a preindustrial population in North America incurred fitness costs from reproduction, and women incurred greater costs than men. We examined the survivorship and reproductive success (Darwinian fitness) of 21,684 couples married between 1860 and 1895 identified in the Utah Population Database. We found that increasing number of offspring (parity) and rates of reproduction were associated with reduced parental survivorship, and significantly more for mothers than fathers. Parental mortality resulted in reduced survival and reproduction of offspring, and the mothers' mortality was more detrimental to offspring than the fathers'. Increasing family size was associated with lower offspring survival, primarily for later-born children, indicating a tradeoff between offspring quantity versus quality. Also, we found that the costs of reproduction increased with age more for women than men. Our findings help to explain some puzzling aspects of human reproductive physiology and behavior, including the evolution of menopause and fertility declines associated with improvements in women's status (demographic transitions).

Fig. 1.

Survivorship of mothers (a) and fathers (b) during the first year after the last child's birth by parity. The greatest relative mortality risk for women in relation to men occurred at low levels of completed family size [relative risk for mortality of 3.05 (P < 0.001) for those with 1–3 children; detail of results in SI Table 2]. This effect occurs because the mortality risk was high for first- or second-time mothers but very low for comparable fathers. If women survived their early reproductive years, their absolute mortality risk increased with additional children, but it rose more sharply for men (in part because men's mortality risks generally rise quicker with age than women's during middle adulthood), although risks of paternal mortality never exceed those for maternal mortality; those with a completed family size of 4–6, 7–11, 12 or 13, and 14 or more children had relative risks for mortality (between women and men) of 2.65, 2.18, 2.34 (all P < 0.001), and 2.74 (P = 0.016), respectively, in relation to those with 1–3 children. These sex differences have been adjusted for year of marriage, age at first birth, age at last birth, and child mortality.

Fig. 2.

Age-specific proportions of parents who died within one year after the last birth by sex.

Fig. 3.

Child survivorship by sibship size (up to age 18).

Fig. 4.

Child survivorship by birth order (to age 18).