Genomic insights into the population history and adaptive traits of Latin American Criollo cattle.

Criollo cattle, the descendants of animals brought by Iberian colonists to the Americas, have been the subject of natural and human-mediated selection in novel tropical agroecological zones for centuries. Consequently, these breeds have evolved distinct characteristics such as resistance to diseases and exceptional heat tolerance. In addition to European taurine (Bos taurus) ancestry, it has been proposed that gene flow from African taurine and Asian indicine (Bos indicus) cattle has shaped the ancestry of Criollo cattle. In this study, we analysed Criollo breeds from Colombia and Venezuela using whole-genome sequencing (WGS) and single-nucleotide polymorphism (SNP) array data to examine population structure and admixture at high resolution. Analysis of genetic structure and ancestry components provided evidence for African taurine and Asian indicine admixture in Criollo cattle. In addition, using WGS data, we detected selection signatures associated with a myriad of adaptive traits, revealing genes linked to thermotolerance, reproduction, fertility, immunity and distinct coat and skin coloration traits. This study underscores the remarkable adaptability of Criollo cattle and highlights the genetic richness and potential of these breeds in the face of climate change, habitat flux and disease challenges. Further research is warranted to leverage these findings for more effective and sustainable cattle breeding programmes.

Genomic analysis for managing small and endangered populations: a case study in Tyrol Grey cattle.

Analysis of genomic data is increasingly becoming part of the livestock industry. Therefore, the routine collection of genomic information would be an invaluable resource for effective management of breeding programs in small, endangered populations. The objective of the paper was to demonstrate how genomic data could be used to analyse (1) linkage disequlibrium (LD), LD decay and the effective population size (NeLD); (2) Inbreeding level and effective population size (NeROH) based on runs of homozygosity (ROH); (3) Prediction of genomic breeding values (GEBV) using small within-breed and genomic information from other breeds. The Tyrol Grey population was used as an example, with the goal to highlight the potential of genomic analyses for small breeds. In addition to our own results we discuss additional use of genomics to assess relatedness, admixture proportions, and inheritance of harmful variants. The example data set consisted of 218 Tyrol Grey bull genotypes, which were all available AI bulls in the population. After standard quality control restrictions 34,581 SNPs remained for the analysis. A separate quality control was applied to determine ROH levels based on Illumina GenCall and Illumina GenTrain scores, resulting into 211 bulls and 33,604 SNPs. LD was computed as the squared correlation coefficient between SNPs within a 10 mega base pair (Mb) region. ROHs were derived based on regions covering at least 4, 8, and 16 Mb, suggesting that animals had common ancestors approximately 12, 6, and 3 generations ago, respectively. The corresponding mean inbreeding coefficients (F ROH) were 4.0% for 4 Mb, 2.9% for 8 Mb and 1.6% for 16 Mb runs. With an average generation interval of 5.66 years, estimated NeROH was 125 (NeROH>16 Mb), 186 (NeROH>8 Mb) and 370 (NeROH>4 Mb) indicating strict avoidance of close inbreeding in the population. The LD was used as an alternative method to infer the population history and the Ne. The results show a continuous decrease in NeLD, to 780, 120, and 80 for 100, 10, and 5 generations ago, respectively. Genomic selection was developed for and is working well in large breeds. The same methodology was applied in Tyrol Grey cattle, using different reference populations. Contrary to the expectations, the accuracy of GEBVs with very small within breed reference populations were very high, between 0.13-0.91 and 0.12-0.63, when estimated breeding values and deregressed breeding values were used as pseudo-phenotypes, respectively. Subsequent analyses confirmed the high accuracies being a consequence of low reliabilities of pseudo-phenotypes in the validation set, thus being heavily influenced by parent averages. Multi-breed and across breed reference sets gave inconsistent and lower accuracies. Genomic information may have a crucial role in management of small breeds, even if its primary usage differs from that of large breeds. It allows to assess relatedness between individuals, trends in inbreeding and to take decisions accordingly. These decisions would be based on the real genome architecture, rather than conventional pedigree information, which can be missing or incomplete. We strongly suggest the routine genotyping of all individuals that belong to a small breed in order to facilitate the effective management of endangered livestock populations.

Assessment of autozygosity in Nellore cows (Bos indicus) through high-density SNP genotypes.

The use of relatively low numbers of sires in cattle breeding programs, particularly on those for carcass and weight traits in Nellore beef cattle (Bos indicus) in Brazil, has always raised concerns about inbreeding, which affects conservation of genetic resources and sustainability of this breed. Here, we investigated the distribution of autozygosity levels based on runs of homozygosity (ROH) in a sample of 1,278 Nellore cows, genotyped for over 777,000 SNPs. We found ROH segments larger than 10 Mb in over 70% of the samples, representing signatures most likely related to the recent massive use of few sires. However, the average genome coverage by ROH (>1 Mb) was lower than previously reported for other cattle breeds (4.58%). In spite of 99.98% of the SNPs being included within a ROH in at least one individual, only 19.37% of the markers were encompassed by common ROH, suggesting that the ongoing selection for weight, carcass and reproductive traits in this population is too recent to have produced selection signatures in the form of ROH. Three short-range highly prevalent ROH autosomal hotspots (occurring in over 50% of the samples) were observed, indicating candidate regions most likely under selection since before the foundation of Brazilian Nellore cattle. The putative signatures of selection on chromosomes 4, 7, and 12 may be involved in resistance to infectious diseases and fertility, and should be subject of future investigation.

Genomic data as the "hitchhiker's guide" to cattle adaptation: tracking the milestones of past selection in the bovine genome.

The bovine species have witnessed and played a major role in the drastic socio-economical changes that shaped our culture over the last 10,000 years. During this journey, cattle "hitchhiked" on human development and colonized the world, facing strong selective pressures such as dramatic environmental changes and disease challenge. Consequently, hundreds of specialized cattle breeds emerged and spread around the globe, making up a rich spectrum of genomic resources. Their DNA still carry the scars left from adapting to this wide range of conditions, and we are now empowered with data and analytical tools to track the milestones of past selection in their genomes. In this review paper, we provide a summary of the reconstructed demographic events that shaped cattle diversity, offer a critical synthesis of popular methodologies applied to the search for signatures of selection (SS) in genomic data, and give examples of recent SS studies in cattle. Then, we outline the potential and challenges of the application of SS analysis in cattle, and discuss the future directions in this field.

Assessing signatures of selection through variation in linkage disequilibrium between taurine and indicine cattle.

BACKGROUND: Signatures of selection are regions in the genome that have been preferentially increased in frequency and fixed in a population because of their functional importance in specific processes. These regions can be detected because of their lower genetic variability and specific regional linkage disequilibrium (LD) patterns. METHODS: By comparing the differences in regional LD variation between dairy and beef cattle types, and between indicine and taurine subspecies, we aim at finding signatures of selection for production and adaptation in cattle breeds. The VarLD method was applied to compare the LD variation in the autosomal genome between breeds, including Angus and Brown Swiss, representing taurine breeds, and Nelore and Gir, representing indicine breeds. Genomic regions containing the top 0.01 and 0.1 percentile of signals were characterized using the UMD3.1 Bos taurus genome assembly to identify genes in those regions and compared with previously reported selection signatures and regions with copy number variation. RESULTS: For all comparisons, the top 0.01 and 0.1 percentile included 26 and 165 signals and 17 and 125 genes, respectively, including TECRL, BT.23182 or FPPS, CAST, MYOM1, UVRAG and DNAJA1. CONCLUSIONS: The VarLD method is a powerful tool to identify differences in linkage disequilibrium between cattle populations and putative signatures of selection with potential adaptive and productive importance.

Genome-wide mapping of loci explaining variance in scrotal circumference in Nellore cattle.

The reproductive performance of bulls has a high impact on the beef cattle industry. Scrotal circumference (SC) is the most recorded reproductive trait in beef herds, and is used as a major selection criterion to improve precocity and fertility. The characterization of genomic regions affecting SC can contribute to the identification of diagnostic markers for reproductive performance and uncover molecular mechanisms underlying complex aspects of bovine reproductive biology. In this paper, we report a genome-wide scan for chromosome segments explaining differences in SC, using data of 861 Nellore bulls (Bos indicus) genotyped for over 777,000 single nucleotide polymorphisms. Loci that excel from the genome background were identified on chromosomes 4, 6, 7, 10, 14, 18 and 21. The majority of these regions were previously found to be associated with reproductive and body size traits in cattle. The signal on chromosome 14 replicates the pleiotropic quantitative trait locus encompassing PLAG1 that affects male fertility in cattle and stature in several species. Based on intensive literature mining, SP4, MAGEL2, SH3RF2, PDE5A and SNAI2 are proposed as novel candidate genes for SC, as they affect growth and testicular size in other animal models. These findings contribute to linking reproductive phenotypes to gene functions, and may offer new insights on the molecular biology of male fertility.

Genome-wide association study for birth weight in Nellore cattle points to previously described orthologous genes affecting human and bovine height.

BACKGROUND: Birth weight (BW) is an economically important trait in beef cattle, and is associated with growth- and stature-related traits and calving difficulty. One region of the cattle genome, located on Bos primigenius taurus chromosome 14 (BTA14), has been previously shown to be associated with stature by multiple independent studies, and contains orthologous genes affecting human height. A genome-wide association study (GWAS) for BW in Brazilian Nellore cattle (Bos primigenius indicus) was performed using estimated breeding values (EBVs) of 654 progeny-tested bulls genotyped for over 777,000 single nucleotide polymorphisms (SNPs). RESULTS: The most significant SNP (rs133012258, PGC = 1.34 × 10-9), located at BTA14:25376827, explained 4.62% of the variance in BW EBVs. The surrounding 1 Mb region presented high identity with human, pig and mouse autosomes 8, 4 and 4, respectively, and contains the orthologous height genes PLAG1, CHCHD7, MOS, RPS20, LYN, RDHE2 (SDR16C5) and PENK. The region also overlapped 28 quantitative trait loci (QTLs) previously reported in literature by linkage mapping studies in cattle, including QTLs for birth weight, mature height, carcass weight, stature, pre-weaning average daily gain, calving ease, and gestation length. CONCLUSIONS: This study presents the first GWAS applying a high-density SNP panel to identify putative chromosome regions affecting birth weight in Nellore cattle. These results suggest that the QTLs on BTA14 associated with body size in taurine cattle (Bos primigenius taurus) also affect birth weight and size in zebu cattle (Bos primigenius indicus).