Offspring of primiparous mothers do not experience greater mortality or poorer growth: Revisiting the conventional wisdom with archival records of Rhesus Macaques

Abstract

Female mammals often begin to reproduce before achieving somatic maturity and therefore face tradeoffs between allocating energy to reproduction or their own continued development. Constraints on primiparous females are associated with greater reproductive failure, and first-born infants often have slower growth and greater mortality and morbidity than infants born to multiparous females. Effects of early life investment may persist even after weaning when juveniles are no longer dependent on maternal care and mother’s milk. We investigated the long-term consequences of birth order in a large sample of rhesus macaques, Macaca mulatta, assigned to the outdoor breeding colony at the California National Primate Research Center (N=2724). A joint model for growth and mortality over the first three years of life allowed us to explicitly connect growth rates to survival. As expected, males are born heavier and grow faster relative to females. However, contrary to expectations, later-born males face substantially lower survival probability during their first three years, whereas first-born males survive at greater rates similar to both first-born and later-born females. Primiparous mothers are less likely to conceive during the subsequent breeding season, suggesting that their reproductive costs are greater than those of multiparous mothers. We speculate that compensatory tactics, both behavioral and physiological, of first-born offspring and their mothers, as well as the novel ecology of the captive environment, underlie these findings. The results presented here provide new insights into how maternal and infant life history tradeoffs may influence developmental trajectories even after the period of maternal dependence.

Faster reproductive rates trade off against offspring growth in wild chimpanzees

“…Body size is a strong predictor of infant and juvenile survival in a wide range of animals, including some lizards (80), fish (81), birds (82,83), rodents (84,85), pinnipeds (86,87), deer (88,89), and primates (90). Although these effects are often attributable to predation, similar effects are seen in humans, for which both low birthweight and poor growth compromise long-term health and well-being (91)(92)(93)(94).…”

Age at reproductive debut: Developmental predictors and consequences for lactation, infant mass, and subsequent reproduction in rhesus macaques (Macaca mulatta)

“…As mammalian females typically provide the behavioral care and physiological investment that shape offspring development, the age of “reproductive debut” (Wallin et al, 1983; Engstrom 1978; Vigil and Geary 2006) is intimately tied to the somatic capacity of the mother to rear her young (Altmann 1986). Typically younger and smaller than their multiparous counterparts, primiparous mothers have fewer embodied resources to allocate to more biological imperatives —maintenance, development, and reproduction— while rearing proportionately larger offspring (Hinde, 2009; Nuñez et al, 2015; Lu et al, 2016). Reproductive debut during somatic growth, termed adolescent pregnancy, brings these tradeoffs into particularly stark contrast, as mothers apportion investment between their own continued development and toward supporting the development of their offspring (Nuñez et al 2015; Altmann 1986).…”

“…Typically younger and smaller than their multiparous counterparts, primiparous mothers have fewer embodied resources to allocate to more biological imperatives —maintenance, development, and reproduction— while rearing proportionately larger offspring (Hinde, 2009; Nuñez et al, 2015; Lu et al, 2016). Reproductive debut during somatic growth, termed adolescent pregnancy, brings these tradeoffs into particularly stark contrast, as mothers apportion investment between their own continued development and toward supporting the development of their offspring (Nuñez et al 2015; Altmann 1986). Given these constraints, primiparity has been associated with higher mortality, greater morbidity, and slower growth for the offspring (see Nowak et al, 2000; guinea pig, Cavia porcellus : Künkele 2000; bighorn ewe, Ovis canadensis Festa-Bianchet et al, 1995; mountain gorillas, Gorilla beringei : Robbins et al 2006; baboon, Papio spp : Smuts and Nicolson, 1989; rhesus macaque, Macaca mulatta : Mas Rivera & Bercovitch 2008; but see Nuñez et al, 2015).…”

“…Reproductive debut during somatic growth, termed adolescent pregnancy, brings these tradeoffs into particularly stark contrast, as mothers apportion investment between their own continued development and toward supporting the development of their offspring (Nuñez et al 2015; Altmann 1986). Given these constraints, primiparity has been associated with higher mortality, greater morbidity, and slower growth for the offspring (see Nowak et al, 2000; guinea pig, Cavia porcellus : Künkele 2000; bighorn ewe, Ovis canadensis Festa-Bianchet et al, 1995; mountain gorillas, Gorilla beringei : Robbins et al 2006; baboon, Papio spp : Smuts and Nicolson, 1989; rhesus macaque, Macaca mulatta : Mas Rivera & Bercovitch 2008; but see Nuñez et al, 2015). Poorer offspring outcomes of primiparous mothers can be due to the lack of maternal behavioral experience or reduced efficiency (rhesus macaque: Bercovitch et al, 2000; sheep, Ovis aries : Dwyer, 2008; rat, Rattus morvegicus : Künkele and Kenagy, 1997; mouse, Mus musculus : Lopatina et al, 2011) and/or limited somatic reserves and physiological ability to sustain gestation and lactation (African elephant, Loxodonta africana , Moss, 2001; human, Homo sapiens : Fraser et al, 1995; Friede et al, 1987).…”

“…Parturition timing within the season is additionally related to age of reproductive debut: young primiparous mothers who conceive later during the breeding season benefit from several additional months of growth critical for their ability to sustain pregnancy and lactation (Antarctic fur seal: Lunn et al, 1994; bonnet macaque: Silk, 1989; rhesus macaque: Wilson et al, 1983). In turn, birth timing within the season is likely to influence infant survival in relation to resources available for weaning transitions and social competition (lion-tailed macaque, Macaca silenus : Clarke et al, 1992; gray mouse lemur, Microcebus murinus : Radespiel and Zimmermann, 2001; bonnet macaque: Silk, 1989; red-bellied lemur, Eulemur rubriventer : Tecot, 2010; or see Nuñez et al, 2015). Among captive rhesus macaques, Small and Smith (1986) reported no influence of birth timing on survival but found that late birth is associated with both a larger infant and slower growth.…”