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

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Hinde, Katie ^a,d,e   Carpenter, Abigail J ^b   Clay, John S ^c   Bradford, Barry J ^b  

^a HARVARD UNIVERSITY   (United States)

^b KANSAS STATE UNIVERSITY   (United States)

^c Dairy Records Management Systems   (United States)

^d SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; DAIRY CATTLE; DAUGHTER; FAT CONTENT; FEMALE; HEIFER; HOLSTEIN CATTLE; LACTATION; MALE; MILK PRODUCTION; MOTHER CHILD RELATION; NONHUMAN; PARITY; PREGNANCY; PROTEIN CONTENT; SEX DIFFERENCE; SON; ANIMAL; BOVINAE; EMBRYOLOGY; METABOLISM; MILK; PHYSIOLOGY; PSYCHOLOGY; REPRODUCTION; SECRETION (PROCESS); UDDER;

ANIMALS; CATTLE; FEMALE; LACTATION; MALE; MAMMARY GLANDS, ANIMAL; MILK; PARITY; PREGNANCY; REPRODUCTION; SEX FACTORS;

EID: 84895484089     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086169     Document Type: Article

References (96)

1. Clark AB (1978) Sex ratio and local resource competition in a prosimian primate. Science 201(4351): 163-165.
2. Silk JB (1983) Local resource competition and facultative adjustment of sex ratios in relation to competitive abilities. Am Nat 121(1): 56-66.
3. Simpson MJ, Simpson AE (1982) Birth sex ratios and social rank in rhesus monkey mothers. Nature 300(5891): 440-441. (Pubitemid 13182905)
4. Emlen ST, Emlen JM, Levin SA (1986) Sex-ratio selection in species with helpers-at-the-nest. Am Nat 127(1): 1-8.
5. Silk JB, Brown GR (2008) Local resource competition and local resource enhancement shape primate birth sex ratios. Proc Biol Sci 275(1644): 1761-1765. (Pubitemid 351839886)
6. Shibata F, Kawamichi T (2009) Female-biased sex allocation of offspring by an Apodemus mouse in an unstable environment. Behav Ecol Sociobiol 63(9): 1307-1317.
7. Leimar O (1996) Life-history analysis of the Trivers and Willard sex-ratio problem. Behav Ecol 7(3): 316-325.
8. Smith JM (1980) A new theory of sexual investment. Behav Ecol Sociobiol 7(3): 247-251.
9. Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179(4068): 90-92.
10. Cockburn A, Legge S, Double MC (2002) in Sex Ratios: Concepts and Research Methods, ed Hardy ICW (Cambridge University Press, Cambridge), 266-286.
11. Cameron EZ (2004) Facultative adjustment of mammalian sex ratios in support for the Trivers-Willard hypothesis: evidence for a mechanism. Proc R Soc Lond B 271: 1723-1728.
12. Hewison AJ, Gaillard JM (1999) Successful sons or advantaged daughters? The Trivers-Willard model and sex-biased maternal investment in ungulates. Trends Ecol Evol 14(6): 229-234. (Pubitemid 29235005)
13. Sheldon BC, West SA (2004) Maternal dominance, maternal condition, and offspring sex ratio in ungulate mammals. Am Nat 163(1): 40-54. (Pubitemid 38231545)
14. Pélabon C, Gaillard JM, Loison A, Portier C (1995) Is sex-biased maternal care limited by total maternal expenditure in polygynous ungulates? Behav Ecol Sociobiol 37(5): 311-319. (Pubitemid 3005370)
15. Cameron EZ (1998) Is suckling behaviour a useful predictor of milk intake? A review. Anim Behav 56(3): 521-532.
16. Hogg JT, Hass CC, Jenni DA (1992) Sex-biased maternal expenditure in Rocky Mountain bighorn sheep. Behav Ecol Sociobiol 31(4): 243-251. (Pubitemid 23401862)
17. Byers JA, Moodie JD (1990) Sex-specific maternal investment in pronghorn, and the question of a limit on differential provisioning in ungulates. Behav Ecol Sociobiol 26(3): 157-164.
18. Stěhulová I, Špinka M, Šárová R, Máchová L, Kněz R, et al. (2013) Maternal behaviour in beef cows is individually consistent and sensitive to cow body condition, calf sex and weight. Appl Anim Behav Sci 144(3-4): 89-97.
19. Bercovitch FB (2002) Sex-biased parental investment in primates. Int J Primatol 23(4): 905-921.
20. Brown GR (2001) Sex-biased investment in nonhuman primates: can Trivers & Willard's theory be tested? Anim Behav 61(4): 683-694.
21. Clutton-Brock TH, Albon SD, Guinness FE (1981) Parental investment in male and female offspring in polygynous mammals. Nature 289(5797): 487-489.
22. Cameron EZ, Stafford KJ, Linklater WL, Veltman CJ (1999) Suckling behaviour does not measure milk intake in horses, Equus caballus. Anim Behav 57(3): 673-678. (Pubitemid 29245146)
23. Landete-Castillejos T, García A, López-Serrano FR, Gallego L (2005) Maternal quality and differences in milk production and composition for male and female Iberian red deer calves (Cervus elaphus hispanicus). Behav Ecol Sociobiol 57(3): 267-274. (Pubitemid 40167471)
24. Koskela E, Mappes T, Niskanen T, Rutkowska J (2009) Maternal investment in relation to sex ratio and offspring number in a small mammal-a case for Trivers and Willard theory? J Anim Ecol 78(5): 1007-1014.
25. Hinde K (2007) First-time macaque mothers bias milk composition in favor of sons. Curr Biol 17(22): R958-R959.
26. Hinde K (2009) Richer milk for sons but more milk for daughters: Sex-biased investment during lactation varies with maternal life history in rhesus macaques. Am J Hum Biol 21(4): 512-519.
27. Fujita M, Roth E, Lo YJ, Hurst C, Vollner J, et al. (2012) In poor families, mothers' milk is richer for daughters than sons: A test of Trivers-Willard hypothesis in agropastoral settlements in Northern Kenya. Am J Phys Anth 149(1): 52-59.
28. Powe CE, Knott CD, Conklin-Brittain N. (2010) Infant sex predicts breast milk energy content. Am J Human Biol 22(1): 50-54.
29. Thakkar SK, Giuffrida F, Cristina CH, De Castro CA, Mukherjee R, et al. (2013) Dynamics of human milk nutrient composition of women from Singapore with a special focus on lipids. Am J Hum Biol early view: doi: 10.1002/ajhb.22446.
30. Quinn EA (2013) No evidence for sex biases in milk macronutrients, energy, or breastfeeding frequency in a sample of filipino mothers. Am J Phys Anth 152(2): 209-16.
31. Robert KA, Braun S (2012) Milk composition during lactation suggests a mechanism for male biased allocation of maternal resources in the tammar wallaby (Macropus eugenii). PloS One 7(11): e51099.
32. Trivers RL (1974) Parent-offspring conflict. Am Zool 14(1): 249-264.
33. Godfray HCJ (1995) Evolutionary theory of parent- offspring conflict. Nature 376(6536): 133-138.
34. Hinde K, Milligan LA (2011) Primate milk: proximate mechanisms and ultimate perspectives. Evol Anthropol 20(1): 9-23.
35. Neville MC, Anderson SM, McManaman JL, Badger TM, Bunik M, et al. (2012) Lactation and neonatal nutrition: defining and refining the critical questions. J Mammary Gland Biol 17(2): 167-188.
36. Akers RM (2002) Lactation and the mammary gland (Iowa State Press, Ames).
37. Rudolph MC, McManaman JL, Hunter L, Phang T, Neville MC (2003) Functional development of the mammary gland: use of expression profiling and trajectory clustering to reveal changes in gene expression during pregnancy, lactation, and involution. J Mammary Gland Biol 8(3): 287-307. (Pubitemid 39137512)
38. Sternlicht MD, Kouros-Mehr H, Lu P, Werb Z (2006) Hormonal and local control of mammary branching morphogenesis. Differentiation 74(7): 365-381. (Pubitemid 44215408)
39. Daly SE, Hartmann PE (1995) Infant demand and milk supply. Part 1: Infant demand and milk production in lactating women. J Hum Lact 11(1): 21-26.
40. Rattray PV, Garrett WN, East NE, Hinman N (1974) Growth, development and composition of the ovine conceptus and mammary gland during pregnancy. J Anim Sci 38(3): 613-626.
41. Hayden TJ, Thomas CR, Forsyth IA (1979) Effect of number of young born (litter size) on milk yield of goats: role for placental lactogen. J Dairy Sci 62(1): 53-57.
42. Ajmone-Marsan P, Garcia JF, Lenstra JA (2010) On the origin of cattle: how aurochs became cattle and colonized the world. Evol Anthropol 19(4): 148-157.
43. Grigson C (1978) The craniology and relationships of four species of Bos: the relationship between Bos primigenius Boj. and B. taurus L. and its implications for the phylogeny of the domestic breeds. J Archaeological Sci 5(2): 123-152.
44. Minick JA, Buchanan DS, & Rupert SD (2001) Milk production of crossbred daughters of high-and low-milk EPD Angus and Hereford bulls. J Animal Sci 79(6): 1386-1393. (Pubitemid 33620412)
45. Rutledge JJ, Robison OW, Ahlschwede WT, Legates JE (1971). Milk yield and its influence on 205-day weight of beef calves. J Animal Sci 33(3): 563-567.
46. Christian LL, Hauser ER, Chapman AB (1965). Association of preweaning and postweaning traits with weaning weight in cattle. J Animal Sci 24(3): 652-659.
47. Loor JJ, Bionaz M, Invernizzi G (2011) in Systems Biology and Livestock Science, eds Pas MF, Woelders H, Bannink A (Wiley-Blackwell, Oxford, UK), 215-245.
48. Rowson A, Daniels KM, Ellis SE, Hovey RC (2012) Growth and development of the mammary glands of livestock: a veritable barnyard of opportunities. Semin Cell Dev Biol 23(5): 557-566.
49. Silva del Río N, Stewart S, Rapnicki P, Chang YM, Fricke PM (2007) An observational analysis of twin births, calf sex ratio, and calf mortality in Holstein dairy cattle. J Dairy Sci 90(3): 1255-1264. (Pubitemid 350045452)
50. Lemay DG, Lynn DJ, Martin WF, Neville MC, Casey TM, et al. (2009) The bovine lactation genome: insights into the evolution of mammalian milk. Genome Biology 10: R43.
51. González-Recio O, Ugarte E, Bach A (2012) Trans-generational effect of maternal lactation during pregnancy: a Holstein cow model. PloS One 7(12): e51816.
52. Lang SL, Iverson SJ, Bowen WD (2012) Primiparous and multiparous females differ in mammary gland alveolar development: implications for milk production. J Exp Biol 215(16): 2904-2911.
53. Anderson RR, Sheffield LG (1983) Growth of guinea pig mammary glands through their first six lactations. J Dairy Sci 66(1): 29-34.
54. Miller N, Delbecchi L, Petitclerc D, Wagner GF, Talbot BG, et al. (2006) Effect of stage of lactation and parity on mammary gland cell renewal. J Dairy Sci 89(12): 4669-4677. (Pubitemid 46118368)
55. Wiggans GR (1991) National genetic improvement programs for dairy cattle in the United States. J Anim Sci 69(9): 3853-3860.
56. VanRaden PM (1997) Lactation yields and accuracies computed from test day yields and (co)variances by best prediction. J Dairy Sci 80(11): 3015-3022.
57. Norman HD, Hutchison JL, Miller RH (2010) Use of sexed semen and its effect on conception rate, calf sex, dystocia, and stillbirth of Holsteins in the United States. J Dairy Sci 93(8): 3880-3890.
58. Garner DL, Seidel Jr GE (2008) History of commercializing sexed semen for cattle. Theriogenology 69(7): 886-895.
59. Chilliard Y (1988) Long-term effects of recombinant bovine somatotropin (rBST) on dairy cow performances. Ann Zootech 37(3): 159-180.
60. Bauman DE, Vernon RG (1993) Effects of exogenous bovine somatotropin on lactation. Annu Rev Nutr 13(1): 437-461. (Pubitemid 23227792)
61. Gianola D, Tyler WJ (1974) Influences on birth weight and gestation period of Holstein-Friesian cattle. J Dairy Sci 57(2): 235-240.
62. Dematawena CMB, Berger PJ (1997) Effect of dystocia on yield, fertility, and cow losses and an economic evaluation of dystocia scores for Holsteins. J Dairy Sci 80(4): 7 54-761.
63. Rutherford JN (2013) in Building Babies: Primate Development in Proximate and Ultimate Perspective, eds Clancy KBH, Hinde K, Rutherford JN (Springer, New York), 27-53.
64. Akers RM (2006) Major advances associated with hormone and growth factor regulation of mammary growth and lactation in dairy cows. J Dairy Sci 89(4): 1222-1234.
65. Plath-Gabler A, Gabler C, Sinowatz F, Berisha B, Schams D (2001) The expression of the IGF family and GH receptor in the bovine mammary gland. J Endocrinol 168(1): 39-48. (Pubitemid 32099351)
66. Johnson TL, Tomanek L, Peterson DG (2013) A proteomic analysis of the effect of growth hormone on mammary alveolar cell-T (MAC-T) cells in the presence of lactogenic hormones. Dom Anim Endocrinol 44(1): 26-35.
67. Rose MT, Weekes TEC, Rowlinson P (2004) Individual variation in the milk yield response to bovine somatotropin in dairy cows. J Dairy Sci 87(7): 2024-2031. (Pubitemid 38978803)
68. Williams GC (1966) Adaptation and natural selection (Princeton University Press, Princeton, NJ).
69. Cameron EZ, Linklater WL, Stafford KJ, Minot EO (2000) Aging and improving reproductive success in horses: declining residual reproductive value or just older and wiser? Behav Ecol Sociobiol 47(4): 243-249. (Pubitemid 30199584)
70. Olynk NJ, Wolf CA (2007) Expected net present value of pure and mixed sexed semen artificial insemination strategies in dairy heifers. J Dairy Sci 90(5): 2569-2576. (Pubitemid 350045380)
71. Ribeiro E, Galvão K, Thatcher W, Santos J (2012) Economic aspects of applying reproductive technologies to dairy herds. Anim Reprod 9(3): 370-387.
72. De Vries A, Overton M, Fetrow J, Leslie K, Eicker S, et al. (2008) Exploring the impact of sexed semen on the structure of the dairy industry. J Dairy Sci 91(2): 847-856. (Pubitemid 351455810)
73. Moore T (2012) Review: Parent-offspring conflict and the control of placental function. Placenta 33(Suppl.): S33-S36.
74. Aschenbach JR, Kristensen NB, Donkin SS, Hammon HM, Penner GB (2010) Gluconeogenesis in dairy cows: The secret of making sweet milk from sour dough. IUBMB Life 62(12): 869-877.
75. Klisch K, Mess A (2007) Evolutionary differentiation of cetartiodactyl placentae in the light of the viviparity-driven conflict hypothesis. Placenta 28(4): 353-360. (Pubitemid 46505936)
76. Baur R (1981) Morphometric data and questions concerning placental transfer. Placenta 2(S): 35-44.
77. Yang MY, Fortune JE (2008) The capacity of primordial follicles in fetal bovine ovaries to initiate growth in vitro develops during mid-gestation and is associated with meiotic arrest of oocytes. Biol Repro 78(6): 1153-1161. (Pubitemid 351749297)
78. Nilsson EE, Skinner MK (2009) Progesterone regulation of primordial follicle assembly in bovine fetal ovaries. Molecular Cell Endocrinol 313(1): 9-16.
79. Anand-Ivell R, Hiendleder S, Viñoles C, Martin GB, Fitzsimmons C, et al. (2011) INSL3 in the ruminant: a powerful indicator of gender- and genetic-specific feto-maternal dialogue. PloS one 6(5): e19821.
80. Capellini I (2012) The evolutionary significance of placental interdigitation in mammalian reproduction: contributions from comparative studies. Placenta 33(10): 763-768.
81. Carlsen SM, Jacobsen G, Vanky E (2010). Mid-pregnancy androgen levels are negatively associated with breastfeeding. Acta Obstet Gynecol Scand 89(1): 87-94.
82. Foote RH (1977) Sex ratios in dairy cattle under various conditions. Theriogenology 8(6): 349-356.
83. Meier S, Williams YJ, Burke CR, Kay JK, Roche JR (2010). Short communication: Feed restriction around insemination did not alter birth sex ratio in lactating dairy cows. J Dairy Sci 93(11): 5408-5412.
84. Roche JR, Lee JM, Berry DP (2006) Pre-conception energy balance and secondary sex ratio-partial support for the Trivers-Willard hypothesis in dairy cows. J Dairy Sci 89(6): 2119-2125. (Pubitemid 44365801)
85. Hohenbrink S, Meinecke-Tillmann S (2012) Influence of social dominance on the secondary sex ratio and factors affecting hierarchy in Holstein dairy cows. J Dairy Sci 95(10): 5694-5701.
86. Hinde K, Foster AB, Landis LM, Rendina D, Oftedal OT, et al. (2013) Daughter dearest: Sex-biased calcium in mother's milk among rhesus macaques. Am J Phys Anth 51(1): 144-150.
87. Blomquist GE (2009) Trade-off between age of first reproduction and survival in a female primate. Biol Letters 5(3): 339-342.
88. Martin JG, Festa-Bianchet M (2012) Determinants and consequences of age of primiparity in bighorn ewes. Oikos 121(5): 752-760.
89. Willisch CS, Biebach I, Koller U, Bucher T, Marreros N, et al. (2012) Male reproductive pattern in a polygynous ungulate with a slow life-history: the role of age, social status and alternative mating tactics. Evol Ecol 26(1): 187-206.
90. Festa-Bianchet M (2012) The cost of trying: weak interspecific correlations among life-history components in male ungulates. Can J Zool 90(9): 1072-1085.
91. Bercovitch FB, Widdig A, Nürnberg P (2000) Maternal investment in rhesus macaques (Macaca mulatta): reproductive costs and consequences of raising sons. Behav Ecol Sociobiol 48(1): 1-11. (Pubitemid 30411219)
92. Windig JJ, Calus MPL, Beerda B, Veerkamp RF (2006) Genetic correlations between milk production and health and fertility depending on herd environment. J Dairy Sci 89(5): 1765-1775. (Pubitemid 44365866)
93. González-Recio O, Ugarte E, Bach A (2012) Trans-generational effect of maternal lactation during pregnancy: a Holstein cow model. PLoS One. 7(12): e51816.
94. Berry DP, Lonergan P, Butler ST, Cromie AR, Fair T, et al. (2008) Negative influence of high maternal milk production before and after conception on offspring survival and milk production in dairy cattle. J Dairy Sci 91(1): 329-337. (Pubitemid 351455848)
95. Badyaev AV (2002) Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecol Evol 17(8): 369-378.
96. Aiken CE, Ozanne SE (2013) Sex differences in developmental programming models. Reproduction 145(1): R1-R13.