Impacts of residual feed intake and pre-natal diet on reproductive potential of bulls
Chinju Johnson A , Carolyn Fitzsimmons B C , Marcos Colazo D , Changxi Li B C , John Kastelic A and Jacob Thundathil A E
+ Author Affiliations
- Author Affiliations
A Department of Production Animal Health, Faculty of Veterinary Medicine, University of Calgary, Calgary, AB T2N 4N1, Canada.
B Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, T6G 2P5, Canada.
C Agriculture and Agri-Food Canada, Lacombe Research and Development Centre, 6000 C & E Trail, Lacombe, AB, T3 L 1W1, Canada.
D Alberta Agriculture and Forestry, Livestock Research and Extension Branch, Edmonton, T6H 5T6, Canada.
E Corresponding author. Email: jthundat@ucalgary.ca
Animal Production Science 59(10) 1827-1836 https://doi.org/10.1071/AN18301
Submitted: 11 May 2018 Accepted: 12 February 2019 Published: 28 June 2019
Abstract
Our objective was to determine effects of genetic potential for residual feed intake (RFI) and pre-natal diet on post-natal growth and reproductive development of bulls. Twenty-five bull calves with a divergent potential for RFI were produced by mating purebred Angus heifers (60) categorised as high or low RFI and inseminated with semen from high or low RFI bulls. From 30 to 150 days of gestation, half the heifers (balanced for RFI across treatments) in each RFI category were fed to gain 0.7 or 0.5 kg/day (~100% and 75% of recommended feed intake; designated normal- and low-diet, respectively). Birthweights of bull calves (n = 25) did not differ significantly among treatment groups (P ≥ 0.1). However, there was a tendency (P < 0.1) for a maternal diet * time interaction for bull weights, with bulls from low pre-natal diet fed heifers growing faster between 10 and 16 months of age than bulls from normal pre-natal diet fed heifers. Furthermore, high-RFI bulls had a larger scrotal circumference (P < 0.01) and attained puberty (P < 0.05) earlier than low-RFI bulls. Other testes measures, including paired testes volume, epididymal sperm reserves, daily sperm production and total sperm production, were not significantly different among treatment groups (P ≥ 0.1). High RFI bulls tended (P < 0.1) to have better average sperm motility than low RFI bulls. However, sperm morphology, viability and chromatin damage were not different (P ≥ 0.1). In summary, young beef bulls with low RFI had smaller testis, delayed onset of puberty (~1.7 months) and tended to exhibit lower progressive motility compared with high RFI bulls. Pre-natal diet had no direct influence on male reproductive development, nor did it interact with RFI of bulls.
Additional keywords: feed efficiency, maternal diet, puberty, RFI.
References
Alberta Agriculture and Forestry (2018) Available at https://www.agric.gov.ab.ca [Verified 10 October 2018]Amann RP, Kavanaugh JF, Griel LC, Voglmayr JK (1974) Sperm production of Holstein bulls determined from testicular spermatid reserves, after cannulation of rete testis or vas deferens, and by daily ejaculation. Journal of Dairy Science 57, 93–99.
| Sperm production of Holstein bulls determined from testicular spermatid reserves, after cannulation of rete testis or vas deferens, and by daily ejaculation.Crossref | GoogleScholarGoogle Scholar | 4810488PubMed |
Arthur PF, Archer JA, Johnston DJ, Herd RM, Richardson EC, Parnell PF (2001) Genetic and phenotypic variance and covariance components for feed intake, feed efficiency, and other postweaning traits in Angus cattle. Journal of Animal Science 79, 2805–2811.
| Genetic and phenotypic variance and covariance components for feed intake, feed efficiency, and other postweaning traits in Angus cattle.Crossref | GoogleScholarGoogle Scholar | 11768108PubMed |
Awda BJ, Miller SP, Montanholi YR, Vander Voort G, Caldwell T, Buhr MM, Swanson KC (2013) The relationship between feed efficiency traits and fertility in young beef bulls. Canadian Journal of Animal Science 93, 185–192.
| The relationship between feed efficiency traits and fertility in young beef bulls.Crossref | GoogleScholarGoogle Scholar |
Bailey TL, Hudson RS, Powe TA, Riddell MG, Wolfe DF, Carson RL (1998) Caliper and ultrasonographic measurements of bovine testicles and a mathematical formula for determining testicular volume and weight in vivo. Theriogenology 49, 581–594.
| Caliper and ultrasonographic measurements of bovine testicles and a mathematical formula for determining testicular volume and weight in vivo.Crossref | GoogleScholarGoogle Scholar | 10732037PubMed |
Barker DJP (1990) The fetal and infant origins of adult disease. British Medical Journal 301, 1111
Barth AD, Oko AJ (Eds) (1989) ‘Abnormal morphology of bovine spermatozoa.’ (Iowa State University Press: Ames, IA)
Basarab JA, Price MA, Aalhus JL, Okine EK, Snelling WM, Lyle KL (2003) Residual feed intake and body composition in young growing cattle. Canadian Journal of Animal Science 83, 189–204.
| Residual feed intake and body composition in young growing cattle.Crossref | GoogleScholarGoogle Scholar |
Basarab JA, McCartney D, Okine EK, Baron VS (2007) Relationships between progeny residual feed intake and dam productivity traits. Canadian Journal of Animal Science 87, 489–502.
| Relationships between progeny residual feed intake and dam productivity traits.Crossref | GoogleScholarGoogle Scholar |
Basarab JA, Colazo MG, Ambrose DJ, Novak S, McCartney D, Baron VS (2011) Residual feed intake adjusted for backfat thickness and feeding frequency is independent of fertility in beef heifers. Canadian Journal of Animal Science 91, 573–584.
| Residual feed intake adjusted for backfat thickness and feeding frequency is independent of fertility in beef heifers.Crossref | GoogleScholarGoogle Scholar |
Berry DP (2008) Improving feed efficiency in cattle with residual feed intake. In ‘Recent advances in animal nutrition’. (Ed. P Garnsworthy) pp. 67–99. (University of Nottingham Press: Nottingham, UK)
Bottje WG, Carstens GE (2009) Association of mitochondrial function and feed efficiency in poultry and livestock species. Journal of Animal Science 87, E48–E63.
| Association of mitochondrial function and feed efficiency in poultry and livestock species.Crossref | GoogleScholarGoogle Scholar | 19028862PubMed |
Brito LFC, Barth AD, Rawlings NC, Wilde RE, Crews DH, Mir PS, Kastelic JP (2007) Effect of improved nutrition during calfhood on serum metabolic hormones, gonadotropins, and testosterone concentrations, and on testicular development in bulls. Domestic Animal Endocrinology 33, 460–469.
| Effect of improved nutrition during calfhood on serum metabolic hormones, gonadotropins, and testosterone concentrations, and on testicular development in bulls.Crossref | GoogleScholarGoogle Scholar |
Chen L, Schenkel F, Vinsky M, Crews DH, Li C (2013) Accuracy of predicting genomic breeding values for residual feed intake in Angus and Charolais beef cattle. Journal of Animal Science 91, 4669–4678.
Crowley JJ, Evans RD, McHugh N, Kenny DA, McGee M, Crews DH, Berry DP (2011) Genetic relationships between feed efficiency in growing males and beef cow performance. Journal of Animal Science 89, 3372–3381.
| Genetic relationships between feed efficiency in growing males and beef cow performance.Crossref | GoogleScholarGoogle Scholar | 21680792PubMed |
Da Silva P, Aitken PR, Rhind SM, Racey PA, Wallace JM (2002) Impact of maternal nutrition during pregnancy on pituitary gonadotrophin gene expression and ovarian development in growth-restricted and normally grown late gestation sheep fetuses. Reproduction (Cambridge, England) 123, 769–777.
| Impact of maternal nutrition during pregnancy on pituitary gonadotrophin gene expression and ovarian development in growth-restricted and normally grown late gestation sheep fetuses.Crossref | GoogleScholarGoogle Scholar |
Dance A, Thundathil JC, Wilde R, Blondin P, Kastelic J (2015) Enhanced early-life nutrition promotes hormone production and reproductive development in Holstein bulls. Journal of Dairy Science 98, 987–998.
| Enhanced early-life nutrition promotes hormone production and reproductive development in Holstein bulls.Crossref | GoogleScholarGoogle Scholar | 25497791PubMed |
Dance A, Thundathil JC, Blondin P, Kastelic J (2016) Enhanced early-life nutrition of Holstein bulls increases sperm production potential without decreasing postpubertal semen quality. Theriogenology 86, 687–694.
| Enhanced early-life nutrition of Holstein bulls increases sperm production potential without decreasing postpubertal semen quality.Crossref | GoogleScholarGoogle Scholar | 27114168PubMed |
Darżynkiewicz Z, Traganos F, Sharpless T, Melamed MR (1975) Thermal denaturation of DNA in situ as studied by acridine orange staining and automated cytofluorometry. Experimental Cell Research 90, 411–428.
| Thermal denaturation of DNA in situ as studied by acridine orange staining and automated cytofluorometry.Crossref | GoogleScholarGoogle Scholar |
Dickerson G (1970) Efficiency of animal production – Molding the biological components. Journal of Animal Science 30, 849–859.
| Efficiency of animal production – Molding the biological components.Crossref | GoogleScholarGoogle Scholar |
Du M, Tong J, Zhao J, Underwood KR, Zhu M, Ford SP, Nathanielsz PW (2010) Fetal programming of skeletal muscle development in ruminant animals. Journal of Animal Science 88, E51–E60.
| Fetal programming of skeletal muscle development in ruminant animals.Crossref | GoogleScholarGoogle Scholar | 19717774PubMed |
Evenson D, Jost L, Gandour D, Rhodes L, Stanton B, Clausen OP, Angelis P, Coico R, Daley A, Becker K, Yopp T (1995) Comparative sperm chromatin structure assay measurements on epiillumination and orthogonal axes flow cytometers. Cytometry 19, 295–303.
| Comparative sperm chromatin structure assay measurements on epiillumination and orthogonal axes flow cytometers.Crossref | GoogleScholarGoogle Scholar | 7796694PubMed |
Fontoura ABP, Montanholi YR, Diel De Amorim M, Foster RA, Chenier T, Miller SP (2016) Associations between feed efficiency, sexual maturity and fertility-related measures in young beef bulls. Animal 10, 96–105.
| Associations between feed efficiency, sexual maturity and fertility-related measures in young beef bulls.Crossref | GoogleScholarGoogle Scholar |
Fox TJ, Carstens GE, Brown EG, White MB, Woods SA, Welsh TH, Holloway JW, Warrington BG, Randel RD, Forrest DW, Lunt DK (2004) Net feed intake of growing bulls and relationships with performance, fertility and ultrasound composition traits. In ‘Beef cattle research in Texas’. pp. 117–120. (Department of Animal Science, Texas A&M University: College Station, TX)
Grazul-Bilska A, Caton J, Arndt W, Burchill K, Thorson C, Borowczyk E, Bilski JJ, Redmer DA, Reynolds DA, Vonnahme KA (2009) Cellular proliferation and vascularization in ovine fetal ovaries: effects of undernutrition and selenium in maternal diet. Reproduction (Cambridge, England) 137, 699–707.
| Cellular proliferation and vascularization in ovine fetal ovaries: effects of undernutrition and selenium in maternal diet.Crossref | GoogleScholarGoogle Scholar |
Herd RM, Arthur PF (2014) Physiological basis for residual feed intake. Journal of Animal Science 87, E64–E71.
| Physiological basis for residual feed intake.Crossref | GoogleScholarGoogle Scholar |
Kasimanickam R, Nebel RL, Peeler ID, Silvia WL (2006) Breed differences in competitive indices of Holstein and Jersey bulls and their association with sperm DNA fragmentation index and plasma membrane integrity. Theriogenology 66, 1307–1315.
| Breed differences in competitive indices of Holstein and Jersey bulls and their association with sperm DNA fragmentation index and plasma membrane integrity.Crossref | GoogleScholarGoogle Scholar | 16797065PubMed |
Kastelic JP (2014) Understanding and evaluating bovine testes. Theriogenology 81, 18–23.
| Understanding and evaluating bovine testes.Crossref | GoogleScholarGoogle Scholar | 24274406PubMed |
Kennedy BW, Van der Werf JH, Meuwissen TH (1993) Genetic and statistical properties of residual feed intake. Journal of Animal Science 71, 3239–3250.
| Genetic and statistical properties of residual feed intake.Crossref | GoogleScholarGoogle Scholar | 8294275PubMed |
Koch RM, Swiger LA, Chambers D, Gregory KE (1963) Efficiency of feed use in beef cattle. Journal of Animal Science 22, 486–494.
| Efficiency of feed use in beef cattle.Crossref | GoogleScholarGoogle Scholar |
Krishnakumar S, Whiteside DP, Elkin B, Thundathil JC (2011) Evaluation of an animal protein-free semen extender for cryopreservation of epididymal sperm from North American bison (Bison bison). Theriogenology 76, 252–260.
| Evaluation of an animal protein-free semen extender for cryopreservation of epididymal sperm from North American bison (Bison bison).Crossref | GoogleScholarGoogle Scholar | 21550101PubMed |
Krishnakumar S, Whiteside D, Dance A, Elkin B, Thundathil JC (2013) Effect of chilling duration on post-thaw characteristics of sperm from the North American bison (Bison bison). Reproduction in Domestic Animals 48, 636–642.
| Effect of chilling duration on post-thaw characteristics of sperm from the North American bison (Bison bison).Crossref | GoogleScholarGoogle Scholar | 23279606PubMed |
Littell RC, Henry RC, Ammerman CB (1998) Statistical analysis of repeated measures data using SAS procedures. Journal of Animal Science 76, 1216–1231.
| Statistical analysis of repeated measures data using SAS procedures.Crossref | GoogleScholarGoogle Scholar | 9581947PubMed |
Lunstra DD (1982) Testicular Development and Onset of Puberty in Beef Bulls. Beef Research Program Progress Report No. 1. US Meat Animal Research Center ARM-NC-21, Clay Center, Nebraska.
Lunstra DD, Ford JJ, Echternkamp SE (1978) Puberty in beef bulls: hormone concentrations, growth, testicular development, sperm production and sexual aggressiveness in bulls of different breeds. Journal of Animal Science 46, 1054–1062.
| Puberty in beef bulls: hormone concentrations, growth, testicular development, sperm production and sexual aggressiveness in bulls of different breeds.Crossref | GoogleScholarGoogle Scholar | 566747PubMed |
Mao F, Chen L, Vinsky MD, Okine EK, Wang Z, Basarab JA, Crews DH, Li C (2013) Phenotypic and genetic relationships of feed efficiency with growth performance, ultrasound and carcass merit traits in Angus and Charolais steers. Journal of Animal Science 91, 2067–2076.
| Phenotypic and genetic relationships of feed efficiency with growth performance, ultrasound and carcass merit traits in Angus and Charolais steers.Crossref | GoogleScholarGoogle Scholar | 23463551PubMed |
Meyer AM, Caton JS, Hess BW, Ford SP, Reynolds LP (2012) Epigenetics and effects on the neonate that may impact feed efficiency. In ‘Feed efficiency in the beef industry’. (Ed. RA Hill) pp. 199–223. (Wiley-Blackwell: Oxford, UK)
Montanholi Y, Swanson K, Schenkel F, Mcbride B, Caldwell T, Miller S (2009) On determination of residual feed intake and associations of infrared thermography with efficiency and ultrasound traits in beef bulls. Livestock Science 125, 22–30.
| On determination of residual feed intake and associations of infrared thermography with efficiency and ultrasound traits in beef bulls.Crossref | GoogleScholarGoogle Scholar |
Moore SS, Mujibi FD, Sherman EL (2009) Molecular basis for residual feed intake in beef cattle. Journal of Animal Science 87, E41–E47.
| Molecular basis for residual feed intake in beef cattle.Crossref | GoogleScholarGoogle Scholar | 18952728PubMed |
Moore SS, Johnston DJ, Graser HU, Herd R (2005) Genetic and phenotypic relationships between insulin-like growth factor I (IGF-I) and net feed intake, fat, and growth traits in Angus beef cattle. Australian Journal of Agricultural Research 56, 211–218.
Price PL, Nayigihugu V, Du M, Means WJ, Paisley SI, Hess BW (2009) Feedlot performance and carcass characteristics of steers and heifers whose dams were nutrient restricted from early to mid-gestation. Journal of Animal Science 87, 71
Rae MT, Kyle CE, Miller DW, Hammond AJ, Brooks AN, Rhind SM (2002) The effects of undernutrition, in utero, on reproductive function in adult male and female sheep. Animal Reproduction Science 72, 63–71.
| The effects of undernutrition, in utero, on reproductive function in adult male and female sheep.Crossref | GoogleScholarGoogle Scholar | 12106966PubMed |
Ramsey R, Doye D, Ward C, McGrann J, Falconer L, Bevers S (2005) Factors affecting beef cow-herd costs, production, and profits. Journal of Agricultural and Applied Economics 37, 91–99.
| Factors affecting beef cow-herd costs, production, and profits.Crossref | GoogleScholarGoogle Scholar |
Rawlings N, Evans A, Chandolia R, Bagu E (2008) Sexual maturation in the bull. Reproduction in Domestic Animals 43, 295–301.
| Sexual maturation in the bull.Crossref | GoogleScholarGoogle Scholar | 18638138PubMed |
Richardson EC, Herd RM (2004) Biological basis for variation in residual feed intake in beef cattle. 2. Synthesis of results following divergent selection. Australian Journal of Experimental Agriculture 44, 431–440.
| Biological basis for variation in residual feed intake in beef cattle. 2. Synthesis of results following divergent selection.Crossref | GoogleScholarGoogle Scholar |
Schoonmaker J, Eastridge M (2013) Effect of maternal nutrition on calf health and growth. In ‘Proceedings of the 22nd tri-state dairy nutrition conference’, Fort Wayne, IN. pp. 63–80. (Michigan State University: East Lansing, MI)
Shaffer KS, Turk P, Wagner WR, Felton EED (2011) Residual feed intake, body composition, and fertility in yearling beef heifers. Journal of Animal Science 89, 1028–1034.
| Residual feed intake, body composition, and fertility in yearling beef heifers.Crossref | GoogleScholarGoogle Scholar | 21112981PubMed |
Shojaei H, Kroetsch T, Wilde R, Blondin P, Kastelic JP, Thundathil JC (2012) Moribund sperm in frozen-thawed semen, and sperm motion end points post-thaw and post-swim-up, are related to fertility in Holstein AI bulls. Theriogenology 77, 940–951.
| Moribund sperm in frozen-thawed semen, and sperm motion end points post-thaw and post-swim-up, are related to fertility in Holstein AI bulls.Crossref | GoogleScholarGoogle Scholar | 22137769PubMed |
Sullivan TM, Micke GC, Greer RM, Perry VEA (2010) Dietary manipulation of Bos indicus heifers during gestation affects the prepubertal reproductive development of their bull calves. Animal Reproduction Science 118, 131–139.
| Dietary manipulation of Bos indicus heifers during gestation affects the prepubertal reproductive development of their bull calves.Crossref | GoogleScholarGoogle Scholar | 19671489PubMed |
Susan M (2006) The economics of feed efficiency – the case for RFI. Available at http://www1.agric.gov.ab.ca/$department/deptdocs.nsf/all/beef14854 [Verified 8 May 2018]
Susan M (2016) Beef Cattle Research Council – genetic improvements in feed efficiency. Available at http://www.beefresearch.ca/research-topic.cfm/genetic-improvements-in-feed-efficiency-57 [Verified 4 December 2018]
Symonds M, Sebert S, Budge H (2010) Nutritional regulation of fetal growth and implications for productive life in ruminants. Animal 4, 1075–1083.
| Nutritional regulation of fetal growth and implications for productive life in ruminants.Crossref | GoogleScholarGoogle Scholar | 22444610PubMed |
Trenkle A, Willham RL (1977) Beef production efficiency. Science 198, 1009–1015.
| Beef production efficiency.Crossref | GoogleScholarGoogle Scholar | 17779672PubMed |
Underwood KR (2007) Gestational nutrient restriction effects on steer carcass and muscle characteristics. Master’s Thesis, University of Wyoming, Laramie.
Walker J, Perry G, Daly R, Olson K (2009) Bull management and nutrition. In ‘Proceedings range beef cow symposium XXI’, paper 277, 1–3 December 2009, Casper, Wyoming. (University of Nebraska-Lincoln: Lincoln, NE)
Wang Z, Colazo MJ, Basarab JA, Goonewardene LA, Ambrose DJ, Marques E, Plastow G, Miller SP, Moore SS (2012) Impact of selection for residual feed intake on breeding soundness and reproductive performance of bulls on pasture-based multisire mating. Journal of Animal Science 90, 2963–2969.
| Impact of selection for residual feed intake on breeding soundness and reproductive performance of bulls on pasture-based multisire mating.Crossref | GoogleScholarGoogle Scholar | 22585812PubMed |
Westhuizen RR, Westhuizen J, Schoeman SJ (2004) Genetic relationship between feed efficiency and profitability traits in beef cattle. South African Journal of Animal Science 34, 50–52.
Wu G, Bazer FW, Wallace JM, Spencer TE (2006) Board-invited review: intrauterine growth retardation: implications for the animal sciences. Journal of Animal Science 84, 2316–2337.
| Board-invited review: intrauterine growth retardation: implications for the animal sciences.Crossref | GoogleScholarGoogle Scholar | 16908634PubMed |
Zhu MJ, Du M, Hess BW, Means WJ, Nathanielsz PW, Ford SP (2007) Maternal nutrient restriction upregulates growth signaling pathways in the cotyledonary artery of cow placentomes. Placenta 28, 361–368.
| Maternal nutrient restriction upregulates growth signaling pathways in the cotyledonary artery of cow placentomes.Crossref | GoogleScholarGoogle Scholar | 16822544PubMed |
