Assessment of genetic diversity and population structure of U.S. Polypay sheep from breed origins to future genomic selection

Authors: Wilson, Carrie - Welsh; PETERSEN, JESSICA - University Of Nebraska; BRITO, LUIZ - Purdue University; Freking, Bradley - Brad; NILSON, SARA - University Of Nebraska; Taylor, Joshua - Bret; Murphy, Thomas - Tom; LEWIS, RONALD - University Of Nebraska

Submitted to: Frontiers in Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/16/2024
Publication Date: 8/5/2024
Citation: Wilson, C.S., Petersen, J.L., Brito, L.F., Freking, B.A., Nilson, S.M., Taylor, J.B., Murphy Jr, T.W., Lewis, R.M. 2024. Assessment of genetic diversity and population structure of U.S. Polypay sheep from breed origins to future genomic selection. Frontiers in Genetics. Volume 15. https://doi.org/10.3389/fgene.2024.1436990.
DOI: https://doi.org/10.3389/fgene.2024.1436990

Interpretive Summary: Knowledge of past and present genetic diversity within a breed is critical for the design and optimization of breeding programs as well as the development of strategies for the conservation of genetic resources. The Polypay sheep breed was developed at the U.S. Sheep Experiment Station (USSES) in 1968 with the goal of improving productivity in Western U.S. range flocks. It has since flourished in the more intensively managed production systems throughout the U.S. Genetic diversity of the breed has yet to be documented. Therefore, the primary objective of this study was to perform a comprehensive evaluation of the genetic diversity and population structure of the U.S. Polypay using both pedigree- and genomic-based methods. Pedigree data from 193 Polypay flocks participating in the National Sheep Improvement Program (NSIP) were combined with pedigree records from USSES (n = 162,997) tracing back to the breed’s origin. A subset (n=1,856) of these pedigreed sheep from 32 flocks born from 2011 to 2023 were genotyped with the GGP Ovine 50K BeadChip containing 51,867 single nucleotide polymorphisms (SNP). Pedigree-based inbreeding for the full population was 2.2% with a rate of inbreeding of 0.215% per generation. Pedigree-based and genomic inbreeding measures ranged from 1.3% to 5.1% for the genotyped population. The effective population size ranged from 41 to 249 for the pedigree-based methods and 118 for the genomic-based estimate. Population substructure was evident based on the Fixation Index (FST), principal component analysis, and model-based population structure. These analyses provided evidence of differentiation from the foundation flock (USSES). Overall, the Polypay breed exhibited substantial genetic diversity and the presence of population substructure that provides a basis for the implementation of genomic selection in the breed.

Technical Abstract: Knowledge of past and present genetic diversity within a breed is critical for the design and optimization of breeding programs as well as the development of strategies for the conservation of genetic resources. The Polypay sheep breed was developed at the U.S. Sheep Experiment Station (USSES) in 1968 with the goal of improving productivity in Western U.S. range flocks. It has since flourished in the more intensively managed production systems throughout the U.S. Genetic diversity of the breed has yet to be documented. Therefore, the primary objective of this study was to perform a comprehensive evaluation of the genetic diversity and population structure of the U.S. Polypay using both pedigree- and genomic-based methods. Pedigree data from 193 Polypay flocks participating in the National Sheep Improvement Program (NSIP) were combined with pedigree records from USSES (n = 162,997) tracing back to the breed’s origin. A subset (n=1,856) of these pedigreed sheep from 32 flocks born from 2011 to 2023 were genotyped with the GGP Ovine 50K BeadChip containing 51,867 single nucleotide polymorphisms (SNP). Four subgroups were used for the pedigree-based analyses: 1) the current generation of animals born in 2020 to 2022 (n = 20,701), 2) the current generation with a minimum of 4 generations of known ancestors (n = 12,685), 3) only genotyped animals (n = 1,856), and 4) the sires of the current generation (n = 509). Pedigree-based inbreeding for the full population was 2.2% with a rate of inbreeding of 0.215% per generation. Pedigree-based inbreeding, Wright’s inbreeding, and genomic inbreeding based on runs of homozygosity were 2.9%, 1.3%, and 5.1%, respectively, for the genotyped population. The effective population size ranged from 41 to 249 for the pedigree-based methods and 118 for the genomic-based estimate. The ratio of the effective number of founders to the effective number of ancestors was 1.9, providing evidence of genetic bottlenecks in the population. The top 10 marginal contributors to the population came from 8 flocks and contributed 20.3% of the current gene pool. Fifty percent of the variation was explained by 79 ancestors. The NSIP estimated breeding values (EBV) for 4 traits (weaning weight, maternal weaning weight, number of lambs born, and number of lambs weaned) and the U.S. Maternal Index showed a wide range among sires of the current generation. The SNP available for the genomic analyses were highly polymorphic (3.2% monomorphic). Expected and observed heterozygosity levels were 0.409 and 0.403, respectively. Runs of homozygosity (ROH) were concentrated in the smallest ROH class (1 to 6 Mb), which is indicative of historical inbreeding or breed founder effects rather than recent inbreeding. Linkage disequilibrium (LD) among markers was low and decreased with increasing SNP distance. The average LD (r2) and average distance between adjacent markers after quality control was 0.09 and 0.07 Mb, respectively. Population substructure was evident based on the Fixation Index (FST), principal component analysis, and model-based population structure. These analyses provided evidence of differentiation from the foundation flock (USSES). Overall, the Polypay breed exhibited substantial genetic diversity and the presence of population substructure that provides a basis for the implementation of genomic selection in the breed.