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 sex-biased 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.

Sex of offspring influences metabolism during early transition period in dairy cows

“…Serum protein patterns can provide information about dehydration in dairy cows during the peripartum period . Although Hinde et al (2014) reported that gestation of a daughter on the first parity increased milk production over the first two lactations, we have no data for cows in their third to fifth lactation in this study. Since dams of heifers showed a greater plasma dehydration than dams of bulls, it is possible that they also have greater milk production; however, further studies are necessary to validate this hypothesis.…”

“…Furthermore, this pattern difference could be explained by a long-term effect of fetal sex hormones on nitrogen metabolism. It is possible that male hormones divert proteins from catabolism to tissue formation in dams rather than in protein milk since lower milk yield for bulls is not compensated by higher protein and fat production (Hinde et al, 2014).…”

“…The number of days between calving and conception affects profitability in terms of breeding cost, increased risk of culling and replacement costs; hence, long days open reduce profitability (De Vries, 2004). Other studies have shown that a positive relationship between age at first calving and milk production (Müller et al, 2005), and a significant biological effect of sex-biased milk production in favour of daughters (Hinde et al, 2014) exists in Holstein dairy cows.…”

Epigenetics and developmental programming of welfare and production traits in farm animals

“…Although such responses fall out with the scope of this article, it is of note that in monotocous species, such as the cow, the fetus can influence maternal mammary development during pregnancy (e.g. fetal sex determines subsequent lactational performance of the gestating dam; Hinde et al 2014).…”

Postnatal consequences of assisted reproductive technologies in cattle

“…Also, while to the best of our knowledge, calves were managed similarly after birth regardless of reproductive technique, one cannot discount some unknown difference in management. For example, fetal sex can affect milk yield in the existing lactation (Hinde et al, 2014) and it is conceivable that sex ratio of pregnancies in first lactation varied between groups. Given that culture system affected the nature of developmental programming in mice (Fernández-Gonzalez et al, 2004;Donjacour et al, 2014;, the effect of being born using a specific reproductive technology might depend on the particular details of the techniques employed.…”