Holsteins favor heifers, not bulls: biased milk production programmed during pregnancy as a function of fetal sex.
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.
Department of Human Evolutionary Biology, Harvard University, Cambridge, Massachusetts, United States of America ; Nutrition Laboratory, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, District of Columbia, United States of America ; Brain, Mind, and Behavior Unit, California National Primate Research Center, University of California Davis, Davis, California, United States of America.
Katie
K
Hinde
Department of Animal Sciences and Industry, Kansas State University, Manhattan, Kansas, United States of America.
Abigail J
AJ
Carpenter
Dairy Records Management Systems, Raleigh, North Carolina, United States of America.
John S
JS
Clay
Department of Animal Sciences and Industry, Kansas State University, Manhattan, Kansas, United States of America.
Barry J
BJ
Bradford
D000818:Animals; D002417:Cattle / Q000196:embryology / Q000502:physiology* / Q000523:psychology; D005260:Female; D007774:Lactation / Q000502:physiology*; D008297:Male; D008321:Mammary Glands, Animal / Q000378:metabolism*; D008892:Milk / Q000378:metabolism*; D010298:Parity; D011247:Pregnancy; D012098:Reproduction / Q000502:physiology; D012737:Sex Factors