Estimation of the Genetic Components of (Co)variance and Preliminary Genome-Wide Association Study for Reproductive Efficiency in Retinta Beef Cattle

Simple Summary Fertility is one of the most important traits for productivity in extensive beef production systems, since it has a major effect on the number of calves born and, as a result, the quantity of weaned calves produced per year. However, it is difficult to improve this trait under extensive conditions, mainly due to the lack of reliable and easy-to-obtain selection criteria. In this study, fertility was analyzed using reproductive efficiency, which was calculated as the deviation between the optimal and real parity number of females at each age. We demonstrated a high h2 value (0.30) using a classic repeatability model and a random regression model (ranging from 0.24 to 0.51), which suggests that the latter model can be recommended to improve fertility in beef breeds raised under extensive environmental conditions such as the Retinta. In addition, we performed the first GWAS analysis looking for SNP genetic markers associated with this character in cattle, which showed five markers significantly associated with the trait located on BTA4 and BTA28. Finally, the functional analysis revealed the presence of five candidate genes located within these regions, which were previously shown to be related to fertility in cattle and mice models. Abstract In this study, we analyzed the variation of reproductive efficiency, estimated as the deviation between the optimal and real parity number of females at each stage of the cow’s life, in 12,554 cows belonging to the Retinta Spanish cattle breed, using classical repeatability and random regression models. The results of the analyses using repeatability model and the random regression model suggest that reproductive efficiency is not homogeneous throughout the cow’s life. The h2 estimate for this model was 0.30, while for the random regression model it increased across the parities, from 0.24 at the first calving to 0.51 at calving number 9. Additionally, we performed a preliminary genome-wide association study for this trait in a population of 252 Retinta cows genotyped using the Axiom Bovine Genotyping v3 Array. The results showed 5 SNPs significantly associated with reproductive efficiency, located in two genomic regions (BTA4 and BTA28). The functional analysis revealed the presence of 5 candidate genes located within these regions, which were previously involved in different aspects related to fertility in cattle and mice models. This new information could give us a better understanding of the genetic architecture of reproductive traits in this species, as well as allow us to accurately select more fertile cows.

[1]  R. Schnabel,et al.  Genome-wide association and genotype by environment interactions for growth traits in U.S. Red Angus cattle , 2022, BMC Genomics.

[2]  L. G. Albuquerque,et al.  Integration analyses of structural variations and differential gene expression associated with beef fatty acid profile in Nellore cattle. , 2022, Animal genetics.

[3]  D. I. Perdomo-González,et al.  A genome-wide association study of mare fertility in the Pura Raza Español horse. , 2022, Animal : an international journal of animal bioscience.

[4]  G. Plastow,et al.  Integrative analyses of genomic and metabolomic data reveal genetic mechanisms associated with carcass merit traits in beef cattle , 2022, Scientific Reports.

[5]  M. Ramón,et al.  Fine-Scale Analysis of Runs of Homozygosity Islands Affecting Fertility in Mares , 2022, Frontiers in Veterinary Science.

[6]  M. Rolf,et al.  Genome-wide association study of beef bull semen attributes , 2022, BMC Genomics.

[7]  Á. Cánovas,et al.  Genome-wide association study for meat tenderness in beef cattle identifies patterns of the genetic contribution in different post-mortem stages. , 2022, Meat science.

[8]  L. Varona,et al.  Genetic inbreeding depression load for fertility traits in Pura Raza Española mares , 2021, Journal of animal science.

[9]  Huijiang Gao,et al.  Genome-Wide Association Study Based on Random Regression Model Reveals Candidate Genes Associated with Longitudinal Data in Chinese Simmental Beef Cattle , 2021, Animals : an open access journal from MDPI.

[10]  E. Peripolli,et al.  Genome-wide interaction study reveals epistatic interactions for beef lipid-related traits in Nellore cattle. , 2021, Animal genetics.

[11]  Huijiang Gao,et al.  Integration of selection signatures and multi-trait GWAS reveals polygenic genetic architecture of carcass traits in beef cattle. , 2021, Genomics.

[12]  Xiaoning Zhang,et al.  Predicted gene 31453 (Gm31453) and the gene encoding carboxypeptidase A5 (Cpa5) are not essential for spermatogenesis and male fertility in the mouse. , 2021, Reproduction, fertility, and development.

[13]  H. Deng,et al.  Zp4 is completely dispensable for fertility in female rats† , 2021, Biology of Reproduction.

[14]  A. Molina,et al.  Use of Principal Component Analysis to Combine Genetic Merit for Heat Stress and for Fat and Protein Yield in Spanish Autochthonous Dairy Goat Breeds , 2021, Animals : an open access journal from MDPI.

[15]  A. Molina,et al.  Selection Criteria for Improving Fertility in Spanish Goat Breeds: Estimation of Genetic Parameters and Designing Selection Indices for Optimal Genetic Responses , 2021, Animals : an open access journal from MDPI.

[16]  G. Murdoch,et al.  Genome-Wide Association Analyses of Fertility Traits in Beef Heifers , 2021, Genes.

[17]  P. Chevret,et al.  ZP4 Is Present in Murine Zona Pellucida and Is Not Responsible for the Specific Gamete Interaction , 2021, Frontiers in Cell and Developmental Biology.

[18]  D. Kenny,et al.  Genome-wide association study of economically important traits in Charolais and Limousin beef cows. , 2020, Animal : an international journal of animal bioscience.

[19]  F. Silva,et al.  Alternative bayesian models for genetic evaluation of biometrical, physical, and morphological reproductive traits in nelore bulls , 2020 .

[20]  Darius J. Devlin,et al.  Knockout of serine-rich single-pass membrane protein 1 (Ssmem1) causes globozoospermia and sterility in male mice† , 2020, Biology of Reproduction.

[21]  Kohske Takahashi,et al.  Welcome to the Tidyverse , 2019, J. Open Source Softw..

[22]  D. Berry,et al.  Genomic Regions Associated With Gestation Length Detected Using Whole-Genome Sequence Data Differ Between Dairy and Beef Cattle , 2019, Front. Genet..

[23]  A. Molina,et al.  Genetic effects of season on the preweaning growth of beef cattle: A first approach to Retinta calves , 2019, Revista Colombiana de Ciencias Pecuarias.

[24]  M. Avilés,et al.  ZP4 confers structural properties to the zona pellucida essential for embryo development , 2019, eLife.

[25]  R. Wellmann Optimum contribution selection for animal breeding and conservation: the R package optiSel , 2019, BMC Bioinformatics.

[26]  K. Larson,et al.  Effect of calving period on beef cow longevity and lifetime productivity in western Canada , 2018, Translational animal science.

[27]  A. Molina,et al.  Breeding beef cattle for an extended productive life: Evaluation of selection criteria in the Retinta breed , 2017 .

[28]  Yixuan Fan,et al.  Effects of NRF1 on steroidogenesis and apoptosis in goat luteinized granulosa cells. , 2017, Reproduction.

[29]  J. Sinsheimer,et al.  Genetic analysis of hyperemesis gravidarum reveals association with intracellular calcium release channel (RYR2) , 2017, Molecular and Cellular Endocrinology.

[30]  L. G. Albuquerque,et al.  Principal component analysis of breeding values for growth and reproductive traits and genetic association with adult size in beef cattle. , 2016, Journal of animal science.

[31]  B. Tychon,et al.  Modeling heat stress under different environmental conditions. , 2016, Journal of dairy science.

[32]  J. Pryce,et al.  Genetics and genomics of reproductive performance in dairy and beef cattle. , 2014, Animal : an international journal of animal bioscience.

[33]  D. Berry,et al.  Genetics of reproductive performance in seasonal calving beef cows and its association with performance traits. , 2014, Journal of animal science.

[34]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[35]  O. González-Recio,et al.  Reaction norm of fertility traits adjusted for protein and fat production level across lactations in Holstein cattle. , 2013, Journal of dairy science.

[36]  L. G. Albuquerque,et al.  Phenotypic plasticity of composite beef cattle performance using reaction norms model with unknown covariate. , 2013, Animal : an international journal of animal bioscience.

[37]  J. Bogstad,et al.  Specific genes are selectively expressed between cumulus and granulosa cells from individual human pre-ovulatory follicles. , 2012, Molecular human reproduction.

[38]  M. Stephens,et al.  Genome-wide Efficient Mixed Model Analysis for Association Studies , 2012, Nature Genetics.

[39]  O. Vangen,et al.  A bio-economic model for calculating economic values of traits for intensive and extensive beef cattle breeds , 2012 .

[40]  Milt G. Thomas,et al.  Reproductive Traits and Their Heritabilities in Beef Cattle , 2009 .

[41]  R. Lôbo,et al.  Genetic associations between accumulated productivity, and reproductive and growth traits in Nelore cattle , 2008 .

[42]  E. C. Mattos,et al.  Genetic analysis of average annual productivity of Nellore breeding cows (COWPROD). , 2008, Genetics and molecular research : GMR.

[43]  E. C. Mattos,et al.  Genetic parameters for productive life traits and reproductive efficiency traits at 6 years in Nellore cattle. , 2008, Genetics and molecular research : GMR.

[44]  Manuel A. R. Ferreira,et al.  PLINK: a tool set for whole-genome association and population-based linkage analyses. , 2007, American journal of human genetics.

[45]  K. Togashi,et al.  Improvement of lactation milk and persistency using the eigenvectors of the genetic covariance matrix between lactation stages , 2007 .

[46]  K. Togashi,et al.  Selection for milk production and persistency using eigenvectors of the random regression coefficient matrix. , 2006, Journal of dairy science.

[47]  D. Réale,et al.  Ontogeny of Additive and Maternal Genetic Effects: Lessons from Domestic Mammals , 2005, The American Naturalist.

[48]  F. Goyache,et al.  Genetic analysis of days open in beef cattle , 2005 .

[49]  R. T. F. Freitas,et al.  Parâmetros genéticos de longevidade e produtividade de fêmeas da raça Nelore , 2004 .

[50]  M. Fernández-Perea,et al.  Economic weights for a selection index in Avileña purebred beef cattle , 2004 .

[51]  P. Carnier,et al.  Definition of a breeding goal for the Piemontese breed: economic and biological values and their sensitivity to production circumstances. , 2004 .

[52]  Laura Leung,et al.  Deficiency of the Nrf1 and Nrf2 Transcription Factors Results in Early Embryonic Lethality and Severe Oxidative Stress* , 2003, Journal of Biological Chemistry.

[53]  J. Díez,et al.  Genetic relationships between calving date, calving interval, age at first calving and type traits in beef cattle , 2002 .

[54]  G. Jong,et al.  Selection and phenotypic plasticity in evolutionary biology and animal breeding , 2002 .

[55]  Robin Thompson,et al.  ASREML user guide release 1.0 , 2002 .

[56]  E. Groeneveld,et al.  Variance component estimation on female fertility traits in beef cattle , 2001 .

[57]  G. Simm,et al.  Breeding objectives for beef cattle in Ireland , 2001 .

[58]  H. N. Oliveira,et al.  Estimativas de (Co)variâncias entre características de reprodução e de crescimento em fêmeas de um rebanho Nelore , 2000 .

[59]  J. Gibson,et al.  Economic values for beef production traits from a herd level bioeconomic model , 1998 .

[60]  J. Dekkers,et al.  Comparison of possible covariates for use in a random regression model for analyses of test day yields. , 1997, Journal of dairy science.

[61]  R. Bourdon,et al.  Within-herd genetic analyses of stayability of beef females. , 1995, Journal of animal science.

[62]  F. Swanepoel,et al.  Interrelationship among cow size, lifetime cow fertility, milk production and pre-weaning calf growth in sub-tropically adapted beef cattle , 1994 .

[63]  T. Meuwissen,et al.  Computing inbreeding coefficients in large populations , 1992, Genetics Selection Evolution.

[64]  S. Newman,et al.  Developing breeding objectives for australian beef cattle production , 1989 .

[65]  D. Falconer Introduction to quantitative genetics. 1. ed. , 1984 .

[66]  R. Bourdon,et al.  Genetic, environmental and phenotypic relationships among gestation length, birth weight, growth traits and age at first calving in beef cattle. , 1982, Journal of animal science.

[67]  H. Grüneberg,et al.  Introduction to quantitative genetics , 1960 .