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).maternal depletion ͉ menopause ͉ reproductive effort ͉ biodemography ͉ life-history tradeoff T he idea that reproduction confers fitness costs and benefits is central to evolutionary life-history theory, and evidence for reproductive costs has been found in a variety of species (1-3), including humans (4, 5). The evidence in humans is mixed (6) and controversial (7,8), and so more studies would help to solve this important question. Also, it is widely assumed that women have higher costs of reproduction than men because of enduring pregnancy, childbirth, and lactation, but evidence is lacking. Studies on women show that high parity and low birth spacing are associated with reduced health (9), postreproductive survival (10-13), and offspring quality (14, 15). There are only a few studies on men, and they suggest that men incur no fitness costs for reproduction (16,17). Taken together, the evidence supports the idea that women incur greater reproductive costs than men. However, the studies on men were mainly conducted on aristocrats and industrial societies, and men in most societies probably have not been so sheltered from the costs of reproduction. Thus, more studies are needed, especially large, longitudinal studies on couples living in preindustrial societies. Our aim was to examine the fitness costs of reproduction for husbands versus wives in an historical, 19th-century population in North America facing resource limitations, because a previous study suggested that both sexes in this population incurred fitness costs for reproduction (12).Determining the relative costs of reproduction for the sexes is relevant to understanding the evolution of some puzzling aspects of human physiology and behavior. For example, menopa...

What do men want? Re-examining whether men benefit from higher fertility than is optimal for women

“…While women often experience higher physiological and parenting costs to reproduction, men pay reproductive costs in terms of acquiring and keeping mates, and may also engage in parenting. The last is associated with slight mortality increases after parenthood [32]. As further evidence that these are significant costs, it is worth noting that age-specific mortality is higher for males than females, and particularly higher for young men in part because they engage in high-risk forms of intra-sexual competition [41].…”

“…Several authors have argued that a man should favour larger families because the cost of producing each offspring is lower for him than for a woman [10,32]. However, differential costs do not mean that men and women necessarily have different optimal fertility strategies (but see the electronic supplementary material for how it can affect sexual conflicts of interest).…”

“…To our knowledge, no paper on humans shows that different reproductive rates within a relationship are optimal for men versus women. Penn et al [32] purport to show greater fitness costs for women than for men of greater fertility in a pre-industrial North American population. However, the actual consequence of reproduction reported is parity-specific parental mortality, rather than fitness [32].…”

“…Penn et al [32] purport to show greater fitness costs for women than for men of greater fertility in a pre-industrial North American population. However, the actual consequence of reproduction reported is parity-specific parental mortality, rather than fitness [32]. Given the low parental mortality rates reported in this study, even the negative effect of dying on number of grandchildren and its effect on geometric mean fitness over evolutionary time do not seem to outweigh the fitness benefits of having an extra child in this population for both men and women, although these should be calculated more directly from the data.…”

Survival costs of reproduction vary with age in North American red squirrels

“…It has been suggested that under unfavourable environmental conditions, such fitness costs of reproduction may be more pronounced (Reznick 1985;. Unfavourable conditions might originate from high density ( FestaBianchet et al 1998), a high level of aggressive interactions (Lindströ m 2001), low food availability (Davis et al 2005;Penn & Smith 2007) or harsh weather ( Tavecchia et al 2005).…”