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

Abstract

Mammalian females pay high energetic costs for reproduction, the greatest of which is imposed by lactation. The synthesis of milk requires, in part, the mobilization of bodily reserves to nourish developing young. Numerous hypotheses have been advanced to predict how mothers will differentially invest in sons and daughters, however few studies have addressed sexbiased milk synthesis. Here we leverage the dairy cow model to investigate such phenomena. Using 2.39 million lactation records from 1.49 million dairy cows, we demonstrate that the sex of the fetus influences the capacity of the mammary gland to synthesize milk during lactation. Cows favor daughters, producing significantly more milk for daughters than for sons across lactation. Using a sub-sample of this dataset (N = 113,750 subjects) we further demonstrate that the effects of fetal sex interact dynamically across parities, whereby the sex of the fetus being gestated can enhance or diminish the production of milk during an established lactation. Moreover the sex of the fetus gestated on the first parity has persistent consequences for milk synthesis on the subsequent parity. Specifically, gestation of a daughter on the first parity increases milk production by ,445 kg over the first two lactations. Our results identify a dramatic and sustained programming of mammary function by offspring in utero. Nutritional and endocrine conditions in utero are known to have pronounced and long-term effects on progeny, but the ways in which the progeny has sustained physiological effects on the dam have received little attention to date.

Bioactive factors in milk across lactation: Maternal effects and influence on infant growth in rhesus macaques (Macaca mulatta)

“…However, our results provide further evidence that the “biological recipe” of milk has the potential to differ for sons and daughters, as shown in previously for macro‐constituents and calcium concentration in rhesus monkey milk [Hinde, ; Hinde et al, ]. If the developmental trajectory or priorities differ for sons and daughters, either in the interest of their own or their mother's reproductive success, we can predict that natural selection will shape milk composition and/or infant receptor expression and nutrient assimilation to be sex‐differentiated [Hinde, ; Hinde et al, , ].…”

“…Nutritional status of mothers during pregnancy and lactation affects both the composition of breast milk as well as the overall volume of milk produced per day [Robyn et al, ], although these effects are not necessarily mediated by differences in maternal body mass index [Gambian women, Prentice and Prentice, ]. The “biological recipe” of milk synthesized for sons can differ from milk synthesized for daughters [macaques, Hinde, ; humans, Fujita et al, ; Powe et al, ; Thakkar et al, but not always—see Quinn ] and likely reflects, in part, divergent developmental priorities and trajectories [Hinde et al, ].…”

Milk ejection patterns remain consistent during the first and second lactations

“…It is not known how or whether this physiological process is a result of programming, but it appears to be established before the second lactation. Animal studies suggest that some aspects of maternal milk production and offspring feeding behavior and growth are actually programmed during pregnancy (Cowley et al, ; Hinde, Carpenter, Clay, & Bradford, ). This occurs through genetic imprinting; Grb 10 appears to influence both maternal milk production and milk consumption by the offspring.…”

Steroid hormone concentrations in milk predict sex‐specific offspring growth in a nonhuman primate

“…For example, milk production and quality in rhesus macaques vary with maternal parity and offspring sex (Hinde, ), and mothers rearing daughters produced milk with higher calcium content (Hinde et al, ). Additionally, even when milk synthesis does not seem to differ between sons and daughters, the magnitude and windows of sensitivity to milk constituents can differ between sons and daughters (Hinde, Carpenter, Clay, & Bradford, ). Sex differences may therefore extend to milk hormones and their effects on the pace of early postnatal growth.…”

“…Sex differences may therefore extend to milk hormones and their effects on the pace of early postnatal growth. Indeed, the effects of milk GCs on other offspring outcomes such as temperament (Grey, Davis, Sandman, & Glynn, ; Hinde et al, ; Sullivan et al, ) and social and cognitive functioning (Dettmer et al, ) have been found to vary as a function of infant sex.…”