Sex differences in survival costs of reproduction in a promiscuous primate

Abstract

In sexually promiscuous mammals, female reproductive effort is mainly expressed through gestation, lactation, and maternal care, whereas male reproductive effort is mainly manifested as mating effort. In this study, we investigated whether reproduction has significant survival costs for a seasonally breeding, sexually promiscuous species, the rhesus macaque, and whether these costs occur at different times of the year for females and males, namely in the birth and the mating season, respectively. The study was conducted with the rhesus macaque population on Cayo Santiago, Puerto Rico. Data on 7,402 births and 922 deaths over a 45-year period were analyzed. Births were concentrated between November and April, while conceptions occurred between May and October. As predicted, female mortality probability peaked in the birth season whereas male mortality probability peaked in the mating season. Furthermore, as the onset of the birth season gradually shifted over the years in relation to climatic changes, there was a concomitant shift in the seasonal peaks of male and female mortality. Taken together, our findings provide the first evidence of sex differences in the survival costs of reproduction in nonhuman primates and suggest that reproduction has significant fitness costs even in environments with abundant food and absence of predation.

Oxidative stress as an indicator of the costs of reproduction among free-ranging rhesus macaques

“…In rhesus macaques, direct male competition is less pronounced than in many polygynous primates, yet male mortality peaks during the breeding season (Hoffman et al, 2008) and energy availability appears to constrain mating effort (Higham et al, 2011). Genetic data reveal significant, though moderate, reproductive skew, with lifetime reproductive success better predicted by variation in reproductive rate than longevity (Dubuc et al, 2014).…”

“…Genetic data reveal significant, though moderate, reproductive skew, with lifetime reproductive success better predicted by variation in reproductive rate than longevity (Dubuc et al, 2014). Because of constraints imposed by the timing of trapping, both males and females were sampled during the latter part of the birth season, when lactating females were experiencing high reproductive costs (Hoffman et al, 2008). The fact that oxidative damage remained higher in males Regression line is for illustrative purposes.…”

“…Male rhesus macaques have a shorter life span than females (Clutton-Brock and Isvaran, 2007), thus males are expected to exhibit higher levels of oxidative damage than females. However, since males experience higher mortality during the mating season while female mortality is higher during the birth season (Hoffman et al, 2008), sex differences in oxidative damage may depend on the time period in which oxidative stress is measured.…”

Experimental demonstration of the growth rate–lifespan trade-off

“…As a result of the treatment differences in compensation, the size of the fish within each experiment converged; the significant length differences among temperature-treatment groups found at the end of period 1 had disappeared after 15 weeks at the ambient temperature in the winter experiment and after 12 weeks in the spring experiment (figure 1). While there was no overall effect of photoperiod treatment on compensatory growth rate ( 23, p , 0.001) influenced compensatory growth: males grew slower than females, and growth rate was faster in fish that were smaller at the end of the temperature manipulation period (see [11,12] for more detailed statistical analysis).…”

“…Sex differences in survival linked to differences in reproductive costs have been found in a diverse range of other species [23][24][25], but in this study there was no evidence in either sex of any trade-off between reproduction and survival; this is almost certainly because we did not manipulate reproductive effort, and so fish were able to allocate resources to reproduction according to their current state or condition, leading to positive relationships between reproduction and survival indicative of quality differences among individuals [26]. Relevant to this is the fact that while manipulated growth rates (i.e.…”