Advertisement

Invited Review: Effect of early-life nutrition on the molecular and physiological regulation of puberty onset in the bull1

      ABSTRACT

      The advent of genomic selection has accentuated interest in procuring saleable semen from young genetically elite bulls as early in life as possible. However, the timing of availability of semen for commercial use will be determined by the age at which these young animals reach puberty and subsequent sexual maturity. Enhancing early-life nutrition stimulates the functionality of the hypothalamic–pituitary–testicular axis, mediated through complex biochemical interplay between metabolic and neuroendocrine signals and culminating in enhanced testicular growth, steroidogenesis, spermatogenesis, and ultimately, earlier onset of sexual maturation. Indeed, recent evidence indicates that the timing of sexual precocity, which is dictated by an early gonadotropin rise (8–20 wk of age) in the bull, is determined by prevailing metabolic status during calfhood and is not compensable even where prior undernutrition is followed by dietary augmentation. However, despite this, the precise neuronal mechanisms regulating these developmental processes remain to be elucidated for the bull. Although early-life nutrition clearly affects the sexual maturation process, there is little evidence for latent effects on postpubertal semen characteristics. Equally, postpubertal fertility, measured as in vitro fertilization and early embryogenesis, is not influenced by nutritional status during early life. Current efforts employing high throughput nucleic acid and proteomic sequencing and targeted immunofluorescence coupled with systems biology–based gene network analyses can provide further insight on how nutrition may mediate the biochemical interaction between neuroendocrine and testicular cellular processes. Such information can be harnessed to identify potential genomic targets as part of genomically assisted breeding programs as well as facilitate development of strategic nutritional regimens to optimize sexual maturation and subsequent semen availability from genetically elite young bulls.

      Key words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      LITERATURE CITED

        • Abele V.
        • Pelletier G.
        • Tremblay R.R.
        Radioautographic localization and regulation of the insulin receptors in rat testis.
        2884311
        J. Recept. Res. 1986; 6: 461-473
        • Acosta-Martínez M.
        PI3K: An attractive candidate for the central integration of metabolism and reproduction.
        Front. Endocrinol. 2011; 2: 110
        • Adam C.L.
        • Findlay P.A.
        • Moore A.H.
        Effects of insulin-like growth factor-1 on luteinizing hormone secretion in sheep.
        9615179
        Anim. Reprod. Sci. 1998; 50: 45-56
        • Allen C.C.
        • Alves B.R.
        • Li X.
        • Tedeschi L.O.
        • Zhou H.
        • Paschal J.C.
        • Riggs P.K.
        • Braga-Neto U.M.
        • Keisler D.H.
        • Williams G.L.
        • Amstalden M.
        Gene expression in the arcuate nucleus of heifers is affected by controlled intake of high- and low-concentrate diets.
        22266992
        J. Anim. Sci. 2012; 90: 2222-2232
        • Amann R.P.
        • DeJarnette J.M.
        Impact of genomic selection of AI dairy sires on their likely utilization and methods to estimate fertility: A paradigm shift.
        22153268
        Theriogenology. 2012; 77: 795-817
        • Amstalden M.
        Role of leptin in regulating the bovine hypothalamic-gonadotropic axis.
        Dept. Anim. Sci., Texas A&M Univ., College Station2003 (PhD Diss)
        • Amstalden M.
        • Alves B.R.C.
        • Liu S.
        • Cardoso R.C.
        • Williams G.L.
        Neuroendocrine pathways mediating nutritional acceleration of puberty: Insights from ruminant models.
        22654842
        Front. Endocrinol. (Lausanne). 2011; 2: 109
        • Amstalden M.
        • Garcia M.R.
        • Williams S.W.
        • Stanko R.L.
        • Nizielski S.E.
        • Morrison C.D.
        • Keisler D.H.
        • Williams G.L.
        Leptin gene expression, circulating leptin, and luteinizing hormone pulsatility are acutely responsive to short-term fasting in prepubertal heifers: Relationships to circulating insulin and insulin-like growth factor-1.
        10859251
        Biol. Reprod. 2000; 63: 127-133
        • Anderson R.A.
        • Zwain I.H.
        • Arroyo A.
        • Mellon P.L.
        • Yen S.S.
        The insulin-like growth factor system in the GT1-7 GnRH neuronal cell line.
        10567861
        Neuroendocrinology. 1999; 70: 353-359
        • Aravindakshan J.P.
        • Honaramooz A.
        • Bartlewski P.M.
        • Beard A.P.
        • Pierson R.A.
        • Rawlings N.C.
        Pattern of gonadotropin secretion and ultrasonographic evaluation of developmental changes in the testis of early and late maturing bull calves.
        11051319
        Theriogenology. 2000; 54: 339-354
        • Arrieta-Cruz I.
        • Gutiérrez-Juárez R.
        The role of circulating amino acids in the hypothalamic regulation of liver glucose metabolism.
        27422516
        Adv. Nutr. 2016; 7: 790S-797S
        • Bagu E.T.
        • Madgwick S.
        • Duggavathi R.
        • Bartlewski P.M.
        • Barrett D.M.
        • Huchkowsky S.
        • Cook S.J.
        • Rawlings N.C.
        Effects of treatment with LH or FSH from 4 to 8 weeks of age on the attainment of puberty in bull calves.
        Theriogenology. 2004; 62: 861-873
        • Berndtson W.E.
        • Igboeli G.
        • Pickett B.W.
        Relationship of absolute numbers of Sertoli cells to testicular size and spermatogenesis in young beef bulls.
        3818487
        J. Anim. Sci. 1987; 64: 241-246
        • Bondy C.A.
        • Lee W.H.
        Patterns of insulin-like growth factor and IGF receptor gene expression in the brain: Functional implications.
        Ann. N. Y. Acad. Sci. 1993; 692: 33-43
        • Brito L.F.
        • Barth A.D.
        • Rawlings N.C.
        • Wilde R.E.
        • Crews Jr., D.H.
        • Boisclair Y.R.
        • Ehrhardt R.A.
        • Kastelic J.P.
        Effect of feed restriction during calfhood on serum concentrations of metabolic hormones, gonadotropins, testosterone, and on sexual development in bulls.
        17641099
        Reproduction. 2007; 134 (a): 171-181
        • Brito L.F.
        • Barth A.D.
        • Rawlings N.C.
        • Wilde R.E.
        • Crews Jr., D.H.
        • Mir P.S.
        • Kastelic J.P.
        Effect of improved nutrition during calfhood on serum metabolic hormones, gonadotropins, and testosterone concentrations, and on testicular development in bulls.
        17029677
        Domest. Anim. Endocrinol. 2007; 33 (b): 460-469
        • Brito L.F.
        • Barth A.D.
        • Rawlings N.C.
        • Wilde R.E.
        • Crews Jr., D.H.
        • Mir P.S.
        • Kastelic J.P.
        Effect of nutrition during calfhood and peripubertal period on serum metabolic hormones, gonadotropins and testosterone concentrations, and on sexual development in bulls.
        16677793
        Domest. Anim. Endocrinol. 2007; 33 (c): 1-18
        • Brito L.F.C.
        • Barth A.D.
        • Rawlings N.C.
        • Wilde R.E.
        • Crews D.J.
        • Mir P.S.
        • Kastelic J.P.
        Circulating metabolic hormones during the peripubertal period and their association with testicular development in bulls.
        17845606
        Reprod. Domest. Anim. 2007; 42 (d): 502-508
        • Bruning J.C.
        • Gautam D.
        • Burks D.J.
        • Gillette J.
        • Schubert M.
        • Orban P.C.
        • Klein R.
        • Krone W.
        • Muller-Wieland D.
        • Kahn C.R.
        Role of brain insulin receptor in control of body weight and reproduction.
        11000114
        Science. 2000; 289: 2122-2125
        • Burgus R.
        • Butcher M.
        • Ling N.
        • Monahan M.
        • Rivier J.
        • Fellows R.
        • Amoss M.
        • Blackwell R.
        • Vale W.
        • Guillemin R.
        Molecular structure of the hypothalamic factor (LRF) of ovine origin monitoring the secretion of pituitary gonadotropic hormone of luteinization (LH).
        5002981
        C. R. Acad. Sci. Hebd. Seances Acad. Sci. D. 1971; 273: 1611-1613
        • Byrne C.J.
        • Fair S.
        • English A.M.
        • Cirot M.
        • Staub C.
        • Lonergan P.
        • Kenny D.A.
        Plane of nutrition before and after 6 months of age in Holstein-Friesian bulls: I. Effects on performance, body composition, age at puberty, and postpubertal semen production.
        29428748
        J. Dairy Sci. 2018; 101 (a): 3447-3459
        • Byrne C.J.
        • Fair S.
        • English A.M.
        • Urh C.
        • Sauerwein H.
        • Crowe M.A.
        • Lonergan P.
        • Kenny D.A.
        Plane of nutrition before and after 6 months of age in Holstein-Friesian bulls: II. Effects on metabolic and reproductive endocrinology and identification of physiological markers of puberty and sexual maturation.
        29397166
        J. Dairy Sci. 2018; 101 (b): 3460-3475
        • Cailleau J.
        • Vermeire S.
        • Verhoeven G.
        Independent control of the production of insulin-like growth factor I and its binding protein by cultured testicular cells.
        2157618
        Mol. Cell. Endocrinol. 1990; 69: 79-89
        • Calikoglu A.S.
        • Karayal A.F.
        • D’Ercole A.J.
        Nutritional regulation of IGF-I expression during brain development in mice.
        11158513
        Pediatr. Res. 2001; 49: 197-202
        • Cannarella R.
        • Condorelli R.A.
        • La Vignera S.
        • Calogero A.E.
        Effects of the insulin-like growth factor system on testicular differentiation and function: A review of the literature.
        29195026
        Andrology. 2018; 6: 3-9
        • Cánovas A.
        • Reverter A.
        • DeAtley K.L.
        • Ashley R.L.
        • Colgrave M.L.
        • Fortes M.R.S.
        • Islas-Trejo A.
        • Lehnert S.
        • Porto-Neto L.
        • Rincón G.
        • Silver G.A.
        • Snelling W.M.
        • Medran J.F.
        • Thomas M.G.
        Multi-tissue omics analyses reveal molecular regulatory networks for puberty in composite beef cattle.
        PLoS One. 2014; 9: e102551
        • Cardoso R.C.
        • Alves B.R.
        • Sharpton S.M.
        • Williams G.L.
        • Amstalden M.
        Nutritional programming of accelerated puberty in heifers: Involvement of pro-opiomelanocortin neurones in the arcuate nucleus.
        25944025
        J. Neuroendocrinol. 2015; 27: 647-657
        • Chandolia R.K.
        • Evans A.C.
        • Rawlings N.C.
        Effect of inhibition of increased gonadotrophin secretion before 20 weeks of age in bull calves on testicular development.
        9068415
        J. Reprod. Fertil. 1997; 109: 65-71
        • Chouzouris T.M.
        • Dovolou E.
        • Dafopoulos K.
        • Georgoulias P.
        • Vasileiou N.G.
        • Fthenakis G.C.
        • Anifandis G.
        • Amiridis G.S.
        Ghrelin suppresses the GnRH-induced preovulatory gonadotropin surge in dairy heifers.
        27329156
        Theriogenology. 2016; 86: 1615-1621
        • Coulter G.H.
        • Carruthers T.D.
        • Amann R.P.
        • Kozub G.C.
        Testicular development, daily sperm production and epididymal sperm reserves in 15-mo-old Angus and Hereford bulls: Effects of bull strain plus dietary energy.
        3818488
        J. Anim. Sci. 1987; 64: 254-260
        • Daftary S.S.
        • Gore A.C.
        Developmental changes in hypothalamic insulin-like growth factor-1: Relationship to gonadotropin-releasing hormone neurons.
        12697712
        Endocrinology. 2003; 144: 2034-2045
        • Dance A.
        • Kastelic J.
        • Thundathil J.
        A combination of insulin-like growth factor I (IGF-I) and FSH promotes proliferation of prepubertal bovine Sertoli cells isolated and cultured in vitro.
        27700982
        Reprod. Fertil. Dev. 2017; 29: 1635-1641
        • Dance A.
        • Thundathil J.
        • Blondin P.
        • Kastelic J.
        Enhanced early-life nutrition of Holstein bulls increases sperm production potential without decreasing postpubertal semen quality.
        27114168
        Theriogenology. 2016; 86: 687-694
        • Dance A.
        • Thundathil J.
        • Wilde R.
        • Blondin P.
        • Kastelic J.
        Enhanced early-life nutrition promotes hormone production and reproductive development in Holstein bulls.
        25497791
        J. Dairy Sci. 2015; 98: 987-998
        • D’Elia A.
        • Tell G.
        • Paron I.
        • Pellizzari L.
        • Lonigro R.
        • Damante G.
        Missense mutations of homeoboxes: A review.
        Hum. Mutat. 2001; 18: 361-374
        • Dias M.M.
        • Canovas A.
        • Mantilla-Rojas C.
        • Riley D.G.
        • Luna-Nevarez P.
        • Coleman S.J.
        • Speidel S.E.
        • Enns R.M.
        • Islas-Trejo A.
        • Medrano J.F.
        • Moore S.S.
        • Fortes M.R.
        • Nguyen L.T.
        • Venus B.
        • Diaz I.S.
        • Souza F.R.
        • Fonseca L.F.
        • Baldi F.
        • Albuquerque L.G.
        • Thomas M.G.
        • Oliveira H.N.
        SNP detection using RNA-sequences of candidate genes associated with puberty in cattle.
        10.4238/gmr16019522
        Genet. Mol. Res. 2017; 16
        • English A.M.
        • Byrne C.J.
        • Cormican P.
        • Waters S.M.
        • Fair S.
        • Kenny D.A.
        Effect of early calf-hood nutrition on the transcriptional regulation of the hypothalamic-pituitary-testicular axis in Holstein-Friesian bull calves.
        Sci. Rep. 2018; (In press)
        • English A.M.
        • Kenny D.
        • Byrne C.J.
        • Sauerwein H.
        • Urh C.
        • Crowe M.A.
        • Staub C.
        • Waters S.
        • Fair S.
        Role of early life nutrition on the hypothalamic-pituitary-testicular axis of the bull.
        10.1530/REP-17-0671
        29967283
        Reproduction. 2018; (b)
        • English A.M.
        • Waters S.M.
        • Cormican P.
        • Byrne C.J.
        • Fair S.
        • Kenny D.A.
        Effect of early calf-hood nutrition on the transcriptomic profile of subcutaneous adipose tissue in Holstein-Friesian bulls.
        29690861
        BMC Genomics. 2018; 19 (c): 281-293
        • Evans A.C.
        • Davies F.J.
        • Nasser L.F.
        • Bowman P.
        • Rawlings N.C.
        Differences in early patterns of gonadotrophin secretion between early and late maturing bulls, and changes in semen characteristics at puberty.
        16727648
        Theriogenology. 1995; 43: 569-578
        • Evans A.C.
        • Pierson R.A.
        • Garcia A.
        • McDougall L.M.
        • Hrudka F.
        • Rawlings N.C.
        Changes in circulating hormone concentrations, testes histology and testes ultrasonography during sexual maturation in beef bulls.
        16727903
        Theriogenology. 1996; 46: 345-357
        • Fortes M.R.S.
        • Reverter A.
        • Kelly M.
        • McCulloch R.
        • Lehnert S.A.
        Genome-wide association study for inhibin, luteinizing hormone, insulin-like growth factor 1, testicular size and semen traits in bovine species.
        Andrology. 2013; 1: 644-650
        • Franca L.R.
        • Hess R.A.
        • Dufour J.M.
        • Hofmann M.C.
        • Griswold M.D.
        The Sertoli cell: One hundred fifty years of beauty and plasticity.
        26846984
        Andrology. 2016; 4: 189-212
        • Guan Y.
        • Liang G.
        • Hawken P.A.
        • Meachem S.J.
        • Malecki I.A.
        • Ham S.
        • Stewart T.
        • Guan L.L.
        • Martin G.B.
        Nutrition affects Sertoli cell function but not Sertoli cell numbers in sexually mature male sheep.
        25515817
        Reprod. Fertil. Dev. 2014; 28: 1152-1163
        • Harstine B.
        • Cruppe L.
        • Abreu F.
        • Rodrigues A.
        • Premanandan C.
        • DeJarnette J.
        • Day M.
        Impact of a timed-release FSH treatment from 2 to 6 months of age in bulls I: Endocrine and testicular development of beef bulls.
        28965026
        Theriogenology. 2018; 105 (a): 142-149
        • Harstine B.R.
        • Cruppe L.H.
        • Abreu F.M.
        • Rodrigues A.D.
        • DeJarnette J.M.
        • Day M.L.
        Impact of a timed-release FSH treatment from 2 to 6 months of age in bulls II: Endocrinology, puberty attainment, and mature sperm production in Holstein bulls.
        28965025
        Theriogenology. 2018; 105 (b): 135-141
        • Harstine B.R.
        • Maquivar M.
        • Helser L.A.
        • Utt M.D.
        • Premanandan C.
        • DeJarnette J.M.
        • Day M.L.
        Effects of dietary energy on sexual maturation and sperm production in Holstein bulls.
        26115263
        J. Anim. Sci. 2015; 93: 2759-2766
        • Henry B.A.
        • Clarke I.J.
        Adipose tissue hormones and the regulation of food intake.
        18601708
        J. Neuroendocrinol. 2008; 20: 842-849
        • Hu J.
        • Zhang Z.
        • Shen W.J.
        • Azhar S.
        Cellular cholesterol delivery, intracellular processing and utilization for biosynthesis of steroid hormones.
        Nutr. Metab. (Lond.). 2010; 7: 47
        • Jin J.M.
        • Yang W.X.
        Molecular regulation of hypothalamus-pituitary-gonads axis in males.
        Gene. 2014; 555: 15-25
        • Kastelic J.P.
        • Rizzoto G.
        • Thundathil J.
        Review: Testicular vascular cone development and its association with scrotal thermoregulation, semen quality and sperm production in bulls.
        Animal. 2018; 12: s133-s141
        • Kenny D.A.
        • Byrne C.J.
        The effect of nutrition on timing of pubertal onset and subsequent fertility in the bull.
        29554994
        Animal. 2018; 12: s36-s44
        • Kenny D.A.
        • Heslin J.
        • Byrne C.J.
        Early onset of puberty in cattle: Implications for gamete quality and embryo survival.
        29539307
        Reprod. Fertil. Dev. 2017; 30: 101-117
        • Konig S.
        • Simianer H.
        • Willam A.
        Economic evaluation of genomic breeding programs.
        19109296
        J. Dairy Sci. 2009; 92: 382-391
        • Langfelder P.
        • Horvath S.
        WGCNA: An R package for weighted correlation network analysis.
        BMC Bioinformatics. 2008; 9: 559
        • Levine J.E.
        • Pau K.Y.
        • Ramirez V.D.
        • Jackson G.L.
        Simultaneous measurement of luteinizing hormone-releasing hormone and luteinizing hormone release in unanesthetized, ovariectomized sheep.
        6751794
        Endocrinology. 1982; 111: 1449-1455
        • Liron J.
        • Fernández M.
        • Prando A.
        • Baldo A.
        • Giovambattista G.
        Hypothalamus transcriptome during the early rise in LH secretion related to puberty age in bull calves.
        Proc. 36th Int. Soc. Anim. Genet., Dublin, Ireland2017 (Page 184 in)
        • Lunstra D.D.
        • Ford J.J.
        • Echternkamp S.E.
        Puberty in beef bulls: Hormone concentrations, growth, testicular development, sperm production and sexual aggressiveness in bulls of different breeds.
        566747
        J. Anim. Sci. 1978; 46: 1054-1062
        • Matsuo H.
        • Baba Y.
        • Nair R.M.
        • Arimura A.
        • Schally A.V.
        Structure of the porcine LH- and FSH-releasing hormone. I. The proposed amino acid sequence.
        4936338
        Biochem. Biophys. Res. Commun. 1971; 43: 1334-1339
        • McLachlan R.I.
        • Wreford N.G.
        • Robertson D.M.
        • Kretser D.M.
        Hormonal control of spermatogenesis.
        Trends Endocrinol. Metab. 1995; 6: 95-101
        • Orth J.M.
        The role of follicle-stimulating hormone in controlling Sertoli cell proliferation in testes of fetal rats.
        Endocrinology. 1984; 115: 1248-1255
        • Peters S.O.
        • Kizilkaya K.
        • Garrick D.J.
        • Fernando R.L.
        • Reecy J.M.
        • Weaber R.L.
        • Silver G.A.
        • Thomas M.G.
        Heritability and Bayesian genome-wide association study of first service conception and pregnancy in Brangus heifers.
        23148252
        J. Anim. Sci. 2013; 91: 605-612
        • Pitetti J.L.
        • Calvel P.
        • Zimmermann C.
        • Conne B.
        • Papaioannou M.D.
        • Aubry F.
        • Cederroth C.R.
        • Urner F.
        • Fumel B.
        • Crausaz M.
        • Docquier M.
        • Herrera P.L.
        • Pralong F.
        • Germond M.
        • Guillou F.
        • Jegou B.
        • Nef S.
        An essential role for insulin and IGF-1 receptors in regulating Sertoli cell proliferation, testis size, and FSH action in mice.
        23518924
        Mol. Endocrinol. 2013; 27: 814-827
        • Quennell J.H.
        • Mulligan A.C.
        • Tups A.
        • Liu X.
        • Phipps S.J.
        • Kemp C.J.
        • Herbison A.E.
        • Grattan D.R.
        • Anderson G.M.
        Leptin indirectly regulates gonadotropin-releasing hormone neuronal function.
        19179437
        Endocrinology. 2009; 150: 2805-2812
        • Raetzman L.T.
        • Ward R.
        • Camper S.A.
        Lhx4 and Prop1 are required for cell survival and expansion of the pituitary primordia.
        Development. 2002; 129: 4229-4239
        • Ramaswamy S.
        • Weinbauer G.F.
        Endocrine control of spermatogenesis: Role of FSH and LH/testosterone.
        26413400
        Spermatogenesis. 2015; 4: e996025
        • Rawlings N.
        • Evans A.C.O.
        • Chandolia R.K.
        • Bagu E.T.
        Sexual maturation in the bull.
        Reprod. Domest. Anim. 2008; 43: 295-301
        • Rawlings N.C.
        • Evans A.C.O.
        Androgen negative feedback during the early rise in LH-secretion in bull calves.
        7616157
        J. Endocrinol. 1995; 145: 243-249
        • Roa J.
        • Tena-Sempere M.
        Connecting metabolism and reproduction: Roles of central energy sensors and key molecular mediators.
        Mol. Cell. Endocrinol. 2014; 397: 4-14
        • Rodriguez R.E.
        • Wise M.E.
        Ontogeny of pulsatile secretion of gonadotropin-releasing hormone in the bull calf during infantile and pubertal development.
        2642416
        Endocrinology. 1989; 124: 248-256
        • Schwartz M.W.
        • Woods S.C.
        • Porte Jr., D.
        • Seeley R.J.
        • Baskin D.G.
        Central nervous system control of food intake.
        10766253
        Nature. 2000; 404: 661-671
        • Scully K.M.
        • Rosenfeld M.G.
        Pituitary development: Regulatory codes in mammalian organogenesis.
        Science. 2002; 295: 2231-2235
        • Sinowatz F.
        • Amselgruber W.
        Postnatal development of bovine Sertoli cells.
        Anat. Embryol. (Berl.). 1986; 174: 413-423
        • Subiran N.
        • Casis L.
        • Irazusta J.
        Regulation of male fertility by the opioid system.
        Mol. Med. 2011; 17: 846-853
        • Vigier B.
        • Picard J.Y.
        • Tran D.
        • Legeai L.
        • Josso N.
        Production of anti-Mullerian hormone: Another homology between Sertoli and granulosa cells.
        6546716
        Endocrinology. 1984; 114: 1315-1320
        • Villalpando I.
        • Lira E.
        • Medina G.
        • Garcia-Garcia E.
        • Echeverria O.
        Insulin-like growth factor 1 is expressed in mouse developing testis and regulates somatic cell proliferation.
        18367630
        Exp. Biol. Med. (Maywood). 2008; 233: 419-426
        • Wang G.
        • Hardy M.P.
        Development of Leydig cells in the insulin-like growth factor-I (IGF-I) knockout mouse: Effects of IGF-I replacement and gonadotropic stimulation.
        14585811
        Biol. Reprod. 2004; 70: 632-639
        • Wang Z.
        • Wang Y.
        • Wang N.
        • Wang J.
        • Wang Z.
        • Vallejos C.E.
        • Wu R.
        Towards a comprehensive picture of the genetic landscape of complex traits.
        22930650
        Brief. Bioinform. 2014; 15: 30-42
        • Wolf F.R.
        • Almquist J.O.
        • Hale E.B.
        Prepuberal behavior and puberal characteristics of beef bulls on high nutrient allowance.
        14313741
        J. Anim. Sci. 1965; 24: 761-765