The trade-off between number and size of offspring in humans and other primates

Abstract

Life-history theory posits a fundamental trade-off between number and size of offspring that structures the variability in parental investment across and within species. We investigate this 'quantity-quality' trade-off across primates and present evidence that a similar trade-off is also found across natural-fertility human societies. Restating the classic Smith-Fretwell model in terms of allometric scaling of resource supply and offspring investment predicts an inverse scaling relation between birth rate and offspring size and a (-1/4) power scaling between birth rate and body size. We show that these theoretically predicted relationships, in particular the inverse scaling between number and size of offspring, tend to hold across increasingly finer scales of analyses (i.e. from mammals to primates to apes to humans). The advantage of this approach is that the quantity-quality trade-off in humans is placed into a general framework of parental investment that follows directly from first principles of energetic allocation.

Figure 1

The allometry of birth rates across eutherian mammals on log–log axes. In Smith–Fretwell notation, this relationship is equivalent to regressing C on R·I⁻¹ from equation (1.3). Mammals and apes scale as approximately the −¼ power of body size. The ‘other primates’ include strepsirhines and haplorhines as both clades show similar scaling. Natural-fertility human societies are the only sample here where fertility increases with body size.

Figure 2

Energy-corrected fertility rate as a function of weaning mass for primates on log–log axes. In Smith–Fretwell notation, this relationship is C·R⁻¹ regressed on I. The slopes are close to −1 (apes: −0.90±0.43; other haplorhines −0.89±0.23). While there is some uncertainty in the data for five smaller haplorhines, their removal has little effect on the scaling (−0.88±0.36). These primate lines are downshifted (i.e. lower intercept) in comparison to the trade-off in other mammals (Charnov & Ernest 2006). Size at age 3 is shown for humans.

Figure 3

Independent contrasts (n=32) of the trade-off between energy-corrected fertility rate and weaning size (both on log-scale) for primates (humans excluded and no data for strepsirhines). In the Smith–Fretwell model, this is C·R⁻¹ regressed on I. The slope of this relationship that is constrained through the origin is −0.71±0.20 across primates (dotted line), but one particular contrast (Miopithecus talapoin and Cercopithecus, right-most side of graph) has considerable leverage and upon removal the slope is −0.94±0.22 (solid line).

Figure 4

Energy-corrected fertility rate as a function of offspring size at age 5 across natural-fertility human societies. Axes are not logged; the fits are power equations. Following the Smith–Fretwell model, this graph is C·R⁻¹ regressed on I. Dashed line is the ordinary least-squares fit with an exponent of −0.56±0.51. However, given that error is probably present in our estimates of offspring size, RMA regression may be more appropriate (solid line, exponent=−1.15±0.86). Similar results are found for size at age 10.