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Maternal aging affects life performance of progeny in a Holstein dairy cow model

Published online by Cambridge University Press:  01 August 2014

S. Astiz ,
A. Gonzalez-Bulnes ,
F. Sebastian ,
O. Fargas ,
I. Cano  and
P. Cuesta
S. Astiz*
Affiliation:
Dpto. Reproducción Animal (INIA), Madrid, Spain
A. Gonzalez-Bulnes
Affiliation:
Dpto. Reproducción Animal (INIA), Madrid, Spain
F. Sebastian
Affiliation:
Granja SAT More, Camino Alcublas, Bétere, Valencia, Spain
O. Fargas
Affiliation:
VAPL S.L., Tona, Barcelona, Spain
I. Cano
Affiliation:
Informatics Department for Research Support, Complutense University of Madrid, Avda de la Complutense s/n, Madrid, Spain
P. Cuesta
Affiliation:
Informatics Department for Research Support, Complutense University of Madrid, Avda de la Complutense s/n, Madrid, Spain
*
*Address for correspondence: S. Astiz, Dpto. Reproducción Animal (INIA), Avda. Puerta de Hierro s/n, 28040 Madrid, Spain. (Email [email protected])
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Abstract

The development and life performance of 404 high-producing Holstein dairy cows was studied from birth onwards and during two lactations. The management, environment and parental genetics of the cows were known in detail. Cluster analysis identified four performance ‘types’: high-yielding (HY) cows and persistently high-yielding (PHY) cows, which accounted for 33% of the animals; medium-yielding (MY) cows, 41%; and low-yielding (LY) cows, 26%. Prenatal determinants of the life performance of the progeny were analyzed. Developmental and environmental factors were excluded as determinants of performance (including birth weight, level of passive immunity transfer, growth rate, age at first parturition and reproductive efficiency). Life performance did show minor seasonal effects, with more HY cows but less PHY being born during the cold season (90.1% in HY; 58.3% in PHY v. 81.5%). Instead, the single most important factor influencing life performance of daughters was maternal age. HY cows were born from the youngest mothers (1.89±1.14 parturitions, 3.12±1.42-year old), whereas LY cows were born from the oldest (2.72±1.80 parturitions, 3.97±2.01-year old; P<0.001). Life performance of the dams did not differ among clusters. In addition, metabolic parameters (fat and protein yield) were found to correlate significantly with yields between the first and second lactations (milk yield: r=0.357; fat yield: r=0.211; protein yield: r=0.277; P<0.0001), suggesting the influence of the individual. These results suggest that under optimal health, nutritional and environmental conditions, maternal aging is an important determinant of the life performance of progeny and argue for the need to identify conditions that contribute to health and disease in progeny according to the Developmental Origin of Health and Disease or DOHaD concept. Our findings may help the development of novel management guidelines for dairy farms.

Keywords

dairy cow modeldevelopmental programmingenvironmentmaternal ageperformance
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 5 , Issue 5 , October 2014 , pp. 374 - 384
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2014 

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References

1.George, EM, Granger, JP. Mechanisms and potential therapies for preeclampsia. Curr Hypertens Rep. 2011; 13, 269–275.CrossRefGoogle ScholarPubMed
2.Parraguez, VH, Urquieta, B, De los Reyes, M, et al.Steroidogenesis in sheep pregnancy with intrauterine growth retardation by high-altitude hypoxia: effects of maternal altitudinal status and antioxidant treatment. Reprod Fertil Dev. 2013; 25, 639–645.CrossRefGoogle ScholarPubMed
3.Parraguez, VH, Urquieta, B, Pérez, L, et al.Fertility in a high-altitude environment is compromised by luteal dysfunction: the relative roles of hypoxia and oxidative stress. Reprod Biol Endocrinol. 2013; 11, 24, doi:10.1186/1477-7827-11-24.CrossRefGoogle Scholar
4.Momand, JR, Xu, G, Walter, CA. The paternal age effect: a multifaceted phenomenon. Biol Reprod. 2013; 88, 108, doi:10.1095/biolreprod.112.103440.CrossRefGoogle ScholarPubMed
5.Sandovici, I, Smith, NH, Nitert, MD, et al.Maternal diet and aging alter the epigenetic control of a promoter-enhancer interaction at the Hnf4a gene in rat pancreatic islets. Proc Natl Acad Sci USA 2011; 108, 5449–5454.CrossRefGoogle ScholarPubMed
6.Adkins, RM, Thomas, F, Tylavsky, FA, et al.Parental ages and levels of DNA methylation in the newborn are correlated. BMC Med Genet. 2011; 12, 47, doi:10.1186/1471-2350-12-47.CrossRefGoogle ScholarPubMed
7.Wiener-Megnazi, Z, Auslender, R, Dirnfeld, M. Advanced paternal age and reproductive outcome. Asian J Androl. 2012; 14, 69–76.CrossRefGoogle ScholarPubMed
8.Stene, LC, Gale, EA. The prenatal environment and type 1 diabetes. Diabetologia. 2013; 56, 1888–1897.CrossRefGoogle ScholarPubMed
9.Huang, L, Sauve, R, Birkett, N, et al.Maternal age and risk of stillbirth: a systematic review. CMAJ. 2008; 178, 165–172.CrossRefGoogle ScholarPubMed
10.Mills, M, Rindfuss, RR, McDonald, P, et al.Why do people postpone parenthood? Reasons and social policy incentives. Human Reprod Update. 2011; 17, 848–860.CrossRefGoogle ScholarPubMed
11.Wong-Taylor, LA, Lawrence, A, Cowen, S, et al.Maternal and neonatal outcomes of spontaneously conceived pregnancies in mothers over 45 years: a review of the literature. Arch Gynecol Obstet. 2012; 285, 1161–1166.CrossRefGoogle Scholar
12.McMillen, IC, Adam, CL, Mühlhäusler, BS. Early origins of obesity: programming the appetite regulatory system. J Physiol. 2005; 565, 9–17.CrossRefGoogle ScholarPubMed
13.Nijland, MJ, Ford, SP, Nathanielsz, PW. Prenatal origins of adult disease. Curr Opin Obstet Gynecol. 2008; 20, 132–138.CrossRefGoogle ScholarPubMed
14.Reynolds, LP, Borowicz, PP, Caton, JS, et al.Developmental programming: the concept, large animal models, and the key role of uteroplacental vascular development. J Anim Sci. 2010; 88, E61–E72.CrossRefGoogle ScholarPubMed
15.Gonzalez-Bulnes, A, Ovilo, C. Genetic basis, nutritional challenges and adaptive responses in the prenatal origin of obesity and type-2 diabetes. Curr Diabetes Rev. 2012; 8, 144–154.CrossRefGoogle ScholarPubMed
16.Gonzalez-Bulnes, A, Pallares, P, Ovilo, C. Ovulation, implantation and placentation in females with obesity and metabolic disorders: life in the balance. Endocr Metab Immune Disord Drug Targets. 2011; 11, 285–301.CrossRefGoogle ScholarPubMed
17.Wu, G, Bazer, FW, Wallace, JM, et al.Board-invited review: intrauterine growth retardation: implications for the animal sciences. J Anim Sci. 2006; 84, 2316–2337.CrossRefGoogle ScholarPubMed
18.Barry, JS, Anthony, RV. The pregnant sheep as a model for human pregnancy. Theriogenology. 2008; 69, 55–67.CrossRefGoogle Scholar
19.VanRaden, PM. Invited review: selection on net merit to improve lifetime profit. J Dairy Sci. 2004; 87, 3125–3131.CrossRefGoogle ScholarPubMed
20.Pritchard, T, Coffey, M, Mrode, R, et al.Understanding the genetics of survival in dairy cows. J Dairy Sci. 2013; 96, 3296–3309.CrossRefGoogle ScholarPubMed
21.Ferguson, JD, Skidmore, A. Reproductive performance in a select sample of dairy herds. J Dairy Sci. 2013; 96, 1269–1289.CrossRefGoogle Scholar
22.Astiz, S, Fargas, O. Pregnancy per AI differences between primiparous and multiparous high-yield dairy cows after using Double Ovsynch or G6G synchronization protocols. Theriogenology. 2013; 79, 1065–1070.CrossRefGoogle ScholarPubMed
23.Sova, AD, Leblanc, SJ, McBride, BW, et al.Associations between herd-level feeding management practices, feed sorting, and milk production in freestall dairy farms. J Dairy Sci. 2013; 6, 4759–4770.CrossRefGoogle Scholar
24.de Graaf, T, Dwinger, RH. Estimation of milk production losses due to sub-clinical mastitis in dairy cattle in Costa Rica. Prev Vet Med. 1996; 26, 3–4.CrossRefGoogle Scholar
25.Rajala-Schultz, PJ, Gröhn, YT, McCulloch, CE, et al.Effects of clinical mastitis on milk yield in dairy cows. J Dairy Sci. 1999; 82, 1213–1220.CrossRefGoogle ScholarPubMed
26.Wilson, DJ, Grohn, YT, Bennett, GJ, et al.Milk production change following clinical mastitis and reproductive performance compared among J5 vaccinated and control dairy cattle. J Dairy Sci. 2008; 91, 3869–3879.CrossRefGoogle ScholarPubMed
27.Morris, MJ, Kaneko, K, Walker, SL, et al.Influence of lameness on follicular growth, ovulation, reproductive hormone concentrations and estrus behavior in dairy cows. Theriogenology. 2011; 76, 658–668.CrossRefGoogle ScholarPubMed
28.Pavlenko, A, Bergsten, C, Ekesbo, I, et al.Influence of digital dermatitis and sole ulcer on dairy cow behaviour and milk production. Animal. 2011; 5, 1259–1269.CrossRefGoogle ScholarPubMed
29.De Vliegher, S, Fox, LK, Piepers, S, et al.Invited review: mastitis in dairy heifers: nature of the disease, potential impact, prevention, and control. J Dairy Sci. 2012; 95, 1025–1040.CrossRefGoogle ScholarPubMed
30.Eicher, SD, Lay, DC Jr, Arthington, JD, et al.Effects of rubber flooring during the first 2 lactations on production, locomotion, hoof health, immune functions, and stress. J Dairy Sci. 2013; 96, 3639–3651.CrossRefGoogle ScholarPubMed
31.Fulwider, WK, Grandin, T, Garrick, DJ, et al.Influence of free-stall base on tarsal joint lesions and hygiene in dairy cows. J Dairy Sci. 2007; 90, 3559–3566.CrossRefGoogle ScholarPubMed
32.Sakaguchi, M. Practical aspects of the fertility of dairy cattle. J Reprod Dev. 2011; 57, 17–33.CrossRefGoogle ScholarPubMed
33.Jacobs, JA, Siegford, JM. Invited review: the impact of automatic milking systems on dairy cow management, behavior, health, and welfare. J Dairy Sci. 2012; 95, 2227–2247.CrossRefGoogle ScholarPubMed
34.Collier, RJ, Annen-Dawson, EL, Pezeshki, A. Effects of continuous lactation and short dry periods on mammary function and animal health. Animal. 2012; 6, 403–414.CrossRefGoogle ScholarPubMed
35.Tao, S, Dahl, GE. Invited review: heat stress effects during late gestation on dry cows and their calves. J Dairy Sci. 2013; 96, 4079–4093.CrossRefGoogle ScholarPubMed
36.Davis Rincker, LE, Vandehaar, MJ, Wolf, CA, et al.Effect of intensified feeding of heifer calves on growth, pubertal age, calving age, milk yield, and economics. J Dairy Sci. 2011; 94, 3554–3567.CrossRefGoogle ScholarPubMed
37.Bach, A. Ruminant nutrition symposium optimizing performance of the offspring: nourishing and managing the dam and postnatal calf for optimal lactation, reproduction, and immunity. J Anim Sci. 2012a90, 1835–1845.CrossRefGoogle ScholarPubMed
38.Eaglen, SA, Coffey, MP, Woolliams, JA, et al.Direct and maternal genetic relationships between calving ease, gestation length, milk production, fertility, type, and lifespan of Holstein-Friesian primiparous cows. J Dairy Sci. 2013; 96, 4015–4025.CrossRefGoogle ScholarPubMed
39.Funston, RN, Larson, DM, VonNahme, KA. Effects of maternal nutrition on conceptus growth and offspring performance: implications for beef cattle production. J Anim Sci. 2010; 88, E205–E215.CrossRefGoogle ScholarPubMed
40.Hinde, K, Carpenter, AJ, Clay, JS, et al.Holsteins favor heifers, not bulls: biased milk production programmed during pregnancy as a function of fetal sex. PLoS One. 2014; 9, e86169.CrossRefGoogle Scholar
41.Robinson, J, Sinclair, K, Mcevoy, T. Nutritional effects on fetal growth. Anim Sci. 1999; 68, 315–331.CrossRefGoogle Scholar
42.Berry, DP, Lonergan, P, Butler, ST, et al.Negative influence of high maternal milk production before and after conception on offspring survival and milk production in dairy cattle. J Dairy Sci. 2012; 91, 329–337.CrossRefGoogle Scholar
43.González-Recio, O, Ugarte, E, Bach, A. Trans-generational effect of maternal lactation during pregnancy: a Holstein cow model. PLoS One. 2012; 7, e51816.CrossRefGoogle ScholarPubMed
44.Schillo, KK, Hall, JB, Hileman, SM. Effects of nutrition and season on the onset of puberty in the beef heifer. J Anim Sci. 1992; 70, 3994–4005.CrossRefGoogle ScholarPubMed
45.Hoffman, PC. Optimum body size of Holstein replacement heifers. J Anim Sci. 1997; 75, 836–845.CrossRefGoogle ScholarPubMed
46.Brickell, JS, Wathes, DC. A descriptive study of the survival of Holstein-Friesian heifers through to third calving on English dairy farms. J Dairy Sci. 2011; 94, 1831–1838.CrossRefGoogle ScholarPubMed
47.National Research Council. Nutrient Requirements of Dairy Cattle, 7th rev edn, 2001. National Academy Press: Washington, DC.Google Scholar
48.Bello, NM, Steibel, JP, Erskine, RJ, et al.Optimizing ovulation to first GnRH improved outcomes to each hormonal injection of Ovsynch in lactating dairy cows. J Dairy Sci. 2006; 89, 3413–3424.CrossRefGoogle ScholarPubMed
49.Hartigan, JA. Clustering Algorithms. 1975. John Wiley & Sons Inc.: New York.Google Scholar
50.Lebart, L, Morineau, A, Piron, M. Statistique Exploratoire Multidimensionnelle. 1995. Dunod: Paris.Google Scholar
51.Elvira, L, Hernandez, F, Cuesta, P, et al.Factors affecting the lactation curves of intensively managed sheep based on a clustering approach. J Dairy Res. 2013; 4, 1–9.Google Scholar
52.Cardenas, CS. Segmentation of bovine lactation curves, during the first third of lactation via cluster and lineal discriminant analysis. Agro Sur. 2009; 37, 126–133.Google Scholar
53.Hargrove, GL, Salazar, JJ, Legates, JE. Relationships among first lactation and lifetime measurements in a dairy population. J Dairy Sci. 1969; 52, 651–656.CrossRefGoogle Scholar
54.Jairath, LK, Hayes, JF, Cue, R. Correlation between FIrst lactation and lifetime performance traits of Canadian Holsteins. J Dairy Sci. 1995; 78, 438–448.CrossRefGoogle ScholarPubMed
55.Togashi, K, Lin, CY. Genetic improvement of total milk yield and total lactation persistency of the first three lactations in dairy cattle. J Dairy Sci. 2008; 91, 2836–2843.CrossRefGoogle ScholarPubMed
56.Swali, A, Wathes, DC. Influence of the dam and sire on size at birth and subsequent growth, milk production and fertility in dairy heifers. Theriogenology. 2006; 66, 1173–1184.CrossRefGoogle ScholarPubMed
57.Weaver, DM, Tyler, JW, VanMetre, DC, et al.Passive transfer of colostral immunoglobulins in calves. J Vet Inter Med. 2000; 14, 569–577.CrossRefGoogle ScholarPubMed
58.Windeyer, MC, Leslie, KE, Godden, SM, et al.The effects of viral vaccination of dairy heifer calves on the incidence of respiratory disease, mortality, and growth. J Dairy Sci. 2012; 95, 6731–6739.CrossRefGoogle ScholarPubMed
59.Donovan, GA, Dohoo, IR, Montgomery, DM. Association between passive immunity and morbidity and mortality in dairy heifers in Florida, USA. Prev Vet Med. 1998; 34, 31–46.CrossRefGoogle ScholarPubMed
60.Gulliksen, SM, Lie, KI, Loken, T, et al.Calf mortality in Norwegian dairy herds. J Dairy Sci. 2009; 92, 2782–2795.CrossRefGoogle ScholarPubMed
61.Trotz-Williams, LA, Leslie, KE, Peregrine, AS. Passive immunity in Ontario dairy calves and investigation of its association with calf management practices. J Dairy Sci. 2008; 91, 3840–3849.CrossRefGoogle ScholarPubMed
62.Gardner, RW, Smith, LW, Park, RL. Feeding and management of dairy heifers for optimal lifetime productivity. J Dairy Sci. 1988; 71, 996–999.CrossRefGoogle ScholarPubMed
63.Khan, MA, Weary, DM, von Keyserlingk, MA. Invited review: effects of milk ration on solid feed intake, weaning, and performance in dairy heifers. J Dairy Sci. 2011; 94, 1071–1081.CrossRefGoogle ScholarPubMed
64.Soberon, F, Raffrenato, E, Everett, RW, et al.Preweaning milk replacer intake and effects on long-term productivity of dairy calves. J Dairy Sci. 2012; 95, 783–793.CrossRefGoogle ScholarPubMed
65.Bach, A. Associations between several aspects of heifer development and dairy cow survivability to second lactation. J Dairy Sci. 2012; 94, 1052–1057.CrossRefGoogle Scholar
66.Lin, CY, McAllister, AJ, Batra, TR, et al.Effects of early and late breeding of heifers on multiple lactation performance of dairy cows. J Dairy Sci. 1988; 71, 2735–2743.CrossRefGoogle Scholar
67.Ettema, JF, Santos, JE. Impact of age at first calving on lactation, reproduction, health and income in first-parity Holsteins on commercial farms. J Dairy Sci. 2004; 87, 2730–2742.CrossRefGoogle ScholarPubMed
68.Nilforooshan, MA, Edriss, MA. Effect of age at first calving on some productivity and longevity traits in Iranian Holsteins of the Isfahan province. J Dairy Sci. 2004; 87, 2130–2135.CrossRefGoogle ScholarPubMed
69.Haworth, GM, Tranter, WP, Chuck, JN, Cheng, Z, Wathes, DC. Relationships between age at first calving and first lactation milk yield, and lifetime productivity and longevity in dairy cows. Vet Rec. 2008; 162, 643–647.CrossRefGoogle ScholarPubMed
70.Tao, S, Dahl, GE. Invited review: heat stress effects during late gestation on dry cows and their calves. J Dairy Sci. 2013; 96, 1–15.CrossRefGoogle ScholarPubMed
71.Brotherstone, S, Goddard, M. Artificial selection and maintenance of genetic variance in the global dairy cow population. Philos Trans R Soc Lond B Biol Sci. 2005; 360, 1479–1488.CrossRefGoogle ScholarPubMed
72.Deng, F, Tao, FB, Liu, DY, et al.Effects of growth environments and two environmental endocrine disruptors on children with idiopathic precocious puberty. Eur J Endocrinol. 2012; 166, 803–809.CrossRefGoogle ScholarPubMed
73.Shiotsuki, L, Silva, JA 2nd, Tonhati, H, Albuquerque, LG. Genetic associations of sexual precocity with growth traits and visual scores of conformation, finishing, and muscling in Nelore cattle. J Anim Sci. 2009; 87, 1591–1597.CrossRefGoogle ScholarPubMed
74.Deardorff, J, Berry-Millett, R, Rehkopf, D, et al.Maternal pre-pregnancy BMI, gestational weight gain, and age at menarche in daughters. Matern Child Health J. 2013; 17, 1391–1398.CrossRefGoogle ScholarPubMed
75.Kern, S, Ackermann, M, Stearns, SC, et al.Decline in offspring viability as a manifestation of aging in Drosophila melanogaster. Evolution. 2010; 55, 1822–1831.Google Scholar
76.Hamel, S, Craine, JM, Towne, EG. Maternal allocation in bison: co-occurrence of senescence, cost of reproduction, and individual quality. Ecol Appl. 2012; 22, 1628–1639.Google ScholarPubMed
77.Hanson, M, Godfrey, KM, Lillycrop, KA, et al.Developmental plasticity and developmental origins of non-communicable disease: theoretical considerations and epigenetic mechanisms. Prog Biophys Mol Biol. 2011; 106, 272–280.CrossRefGoogle ScholarPubMed
78.Stene, LC, Gale, EA. The prenatal environment and type 1 diabetes. Diabetologia. 2013; 56, 1888–1897.CrossRefGoogle ScholarPubMed
79.Kenny, LC, Lavender, T, McNamee, R, et al.Advanced maternal age and adverse pregnancy outcome: evidence from a large contemporary cohort. PLoS One. 2013; 8, e56583.CrossRefGoogle ScholarPubMed
80.Nelson, SM, Telfer, EE, Anderson, RA. The ageing ovary and uterus: new biological insights. Human Reprod Update. 2013; 19, 67–83.CrossRefGoogle ScholarPubMed