Holsteins favor heifers, not bulls: Biased milk production programmed during pregnancy as a function of fetal sex

Katherine Hinde, Abigail J. Carpenter, John S. Clay, Barry J. Bradford

Research output: Contribution to journalArticle

52 Citations (Scopus)

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.

Original languageEnglish (US)
Article numbere86169
JournalPLoS One
Volume9
Issue number2
DOIs
StatePublished - Feb 3 2014
Externally publishedYes

Fingerprint

heifers
milk production
Lactation
bulls
Milk
lactation
pregnancy
parity (reproduction)
milk synthesis
Pregnancy
Parity
gender
fetus
Fetus
Dairies
dairy cows
milk
mammary glands
breasts
Human Mammary Glands

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Holsteins favor heifers, not bulls : Biased milk production programmed during pregnancy as a function of fetal sex. / Hinde, Katherine; Carpenter, Abigail J.; Clay, John S.; Bradford, Barry J.

In: PLoS One, Vol. 9, No. 2, e86169, 03.02.2014.

Research output: Contribution to journalArticle

Hinde, Katherine ; Carpenter, Abigail J. ; Clay, John S. ; Bradford, Barry J. / Holsteins favor heifers, not bulls : Biased milk production programmed during pregnancy as a function of fetal sex. In: PLoS One. 2014 ; Vol. 9, No. 2.
@article{d5563c28815e466f8257da5bcf7e5777,
title = "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.",
author = "Katherine Hinde and Carpenter, {Abigail J.} and Clay, {John S.} and Bradford, {Barry J.}",
year = "2014",
month = "2",
day = "3",
doi = "10.1371/journal.pone.0086169",
language = "English (US)",
volume = "9",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "2",

}

TY - JOUR

T1 - Holsteins favor heifers, not bulls

T2 - Biased milk production programmed during pregnancy as a function of fetal sex

AU - Hinde, Katherine

AU - Carpenter, Abigail J.

AU - Clay, John S.

AU - Bradford, Barry J.

PY - 2014/2/3

Y1 - 2014/2/3

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84895484089&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84895484089&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0086169

DO - 10.1371/journal.pone.0086169

M3 - Article

C2 - 24498270

AN - SCOPUS:84895484089

VL - 9

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 2

M1 - e86169

ER -