Richer milk for sons but more milk for daughters: Sex‐biased investment during lactation varies with maternal life history in rhesus macaques

Abstract

Lactation represents the greatest postnatal energetic expenditure for human and non-human primate females, and the ability to sustain the costs of lactation is influenced by a mother's physical condition. This is especially true for young mothers that initiate reproduction shortly after adolescence. These mothers have fewer bodily reserves available for lactation and face tradeoffs between reproduction and their own growth. Milk synthesis among captive rhesus macaques (Macaca mulatta) was investigated at the California National Primate Research Center from 2005 to 2007 (N = 114). Rhesus macaques produced low energy density milk typical of the primate order, but there was substantial individual variation among mothers in both milk energy density and yield. As a consequence, the available milk energy (AME), the product of milk energy density and milk yield, to support infant growth, development, and activity, varied tenfold among mothers. Primiparous mothers (N = 40) had fewer bodily resources, as measured by mass and body mass index, available for lactation than did multiparous mothers (N = 74) and showed poorer lactational performance. Mothers of sons produced milk of higher energy density, especially primiparous mothers, but lower milk yield, such that AME was the same for sons and daughters. Although AME from the mother was the same for sons and daughters, there was significant sexual dimorphism in infant mass. These data indicate that selection has likely favored sex-specific regulation of growth and development that is not necessarily contingent on greater maternal investment.

Holsteins Favor Heifers, Not Bulls: Biased Milk Production Programmed during Pregnancy as a Function of Fetal Sex

“…Although bST was able to overwhelm sex-biased milk synthesis among multiparous cows, significant sex-bias remained among primiparous cows whose mammary glands had functionally developed for the first time in the context of the fetal sex of the first gestation. The magnitude of sex bias is strongest among first parity rhesus monkeys [25][26] and possibly humans [28][29] and Tamar wallabies [31] in which primiparous females have been disproportionately represented in published studies. The effect of fetal sex may diminish to some extent among multiparous females due to the aggregate effects on mammary gland architecture of sequential gestations of different fetal sexes.…”

“…Notably, investigations of sexually dimorphic developmental trajectories, however, overwhelmingly essentialize the role of the mother and sex-biased allocation of maternal resources. More often overlooked are sexually differentiated mechanisms within offspring that influence utilization and assimilation of early life nutrition and environmental signals [26,[95][96]. Consideration of progenyspecific adaptations as well as biased maternal effort will contribute to a better understanding of the ontogeny of sexual dimorphism.…”

“…Post-natally, local regulation of milk synthesis is maintained by milk removal via offspring suckling [36,39] but maternal rejection can prevent or limit milk intake [18]. As a result, sex-biased milk synthesis may reflect differential cellular capacity in the mammary gland, programmed via hormonal signals from the fetal-placental unit, or post-natally through sex-biased nursing behavior [26]. There has been only one study that has investigated mechanisms underlying sex-biased milk synthesis.…”

“…Suckling behavior, however, is not useful for estimating milk energy transfer as verified by experimental use of radio-labeled isotopes in Equus caballus [22]. Direct evidence for sex-biased milk synthesis among nondomesticated species has now been reported in ungulates (Cervus elaphus hispanicus, [23]), rodents (Myodes glareolus [24]), primates (Macaca mulatta [25][26]; Homo sapiens [27][28][29], but see also [30] for exception), and marsupials (Macropus eugenii, [31]). Drawing systematic conclusions from the studies to date, however, is challenging in part because most have been limited by relatively small sample sizes or report milk composition without accounting for milk yield.…”

Field and laboratory methods in human milk research

“…Researchers have only begun to define normal milk variation across populations and how it influences the postnatal period and beyond (Neville et al, 2012). Many of the emerging questions in human biology are linked to lactation, from unique aspects of primate Milligan and Bazinet, 2008) and human life histories (Fujita et al, 2011), parental investment (Fujita et al, 2012;Hinde, 2009;Powe et al, 2010), and developmental programming (de Moura et al, 2008;Hinde and Capitano, 2010;Miralles et al, 2006;Newburg et al, 2010;Palou et al, 2009;Pico et al, 2007;Prentice, 2005;Quinn, 2011;Quinn et al, 2012;Savino et al, 2009;Stocker and Cawthorne, 2008;Weyerman et al, 2007). In addition, lactation is implicated in human evolutionary biology, including the evolution of large brains and body fat (Kuzawa, 1998;Martin, 1981), childhood (Bogin, 1999;Konner, 2010;Sellen, 2007), reproductive timing (Al-Sahab et al, 2011) and the developmental origins of adult metabolism (Kuzawa and Quinn, 2009;Wells, 2003).…”