Genome wide analysis of the world's sheep breeds reveals high levels of historic mixture and strong recent selection

Authors: KIJAS, JAMES - Commonwealth Scientific And Industrial Research Organisation (CSIRO); LENSTRA, JOHANNES - Utrecht University; PORTO NETO, LAERCIO - Commonwealth Scientific And Industrial Research Organisation (CSIRO); MCCULLOCH, RUSSELL - Commonwealth Scientific And Industrial Research Organisation (CSIRO); WHAN, VICKI - Commonwealth Scientific And Industrial Research Organisation (CSIRO); GIETZEN, KIMBERLY - Illumina, Inc; PAIVA, SAMUEL - Embrapa Genetic Resources; GILL, CLARE - Texas A&M University; BARENDSE, WILLIAM - Commonwealth Scientific And Industrial Research Organisation (CSIRO); CIANI, ELENA - University Of Bari; RAADSMA, HERMAN - University Of Sydney; MCEWAN, JOHN - Agresearch; DALRYMPLE, BRIAN - Commonwealth Scientific And Industrial Research Organisation (CSIRO); Heaton, Michael - Mike

Submitted to: PLoS Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/28/2011
Publication Date: 2/7/2012
Citation: Kijas, J.W., Lenstra, J.A., Porto Neto, L., Mcculloch, R., Whan, V., Gietzen, K., Paiva, S., Gill, C., Barendse, W., Ciani, E., Raadsma, H., Mcewan, J., Dalrymple, B., Heaton, M.P., et al. 2012. Genome wide analysis of the world's sheep breeds reveals high levels of historic mixture and strong recent selection. PLoS Biology. 10(2): e1001258. DOI:10.1371/journal.pbio.1001258.

Interpretive Summary: Domesticated animals offer the opportunity to explore the genetic consequences of domestication and selection. Sheep present an appealing example as they have been adapted to thrive in a diversity of environments, which opens the possibility to detect selection in response to environmental variables. In addition, animal husbandry practice and hundreds of years of selective breeding have created populations for the specialized production of milk, fiber or meat. This opens the possibility to identify production genes and elucidate the biological mechanisms driving phenotypic change. To investigate diversity, population history and to perform a genome-wide scan for selection signals, we developed and genotyped approximately 50,000 single nucleotide polymorphisms in a diverse collection of 74 ovine breeds sampled from across the species range. Strong recent selection was detected in key regions of the sheep genome. The regions under selection contained genes for coat pigmentation, skeletal morphology, body size, growth and reproduction and we demonstrate the strongest selection signal (genome wide) has occurred in response to breeding for the absence of horns. We also present a detailed view of the genetic relationship between breeds and link it with migration following domestication and human movements throughout history. Improvements to the rate of genetic gain achieved within the livestock industry are essential to sustain food production in the context of a growing global population with an increasing appetite for protein. Increasing genetic gain through genomic selection and the identification of elite breeding candidates has the undesirable potential to reduce genetic diversity and leave populations less robust to the challenges of disease. Our results indicate that the levels of genetic diversity and effective population size contained in modern sheep breeds is such that strong selection response can be expected to continue without threatening breed viability. This can be contrasted to dairy cattle where inbreeding and viability are of increasing concern.

Technical Abstract: Through their domestication and subsequent selection, sheep have been adapted to thrive in a diverse range of environments. To characterize the genetic consequence of both domestication and selection, we genotyped 49,034 single nucleotide polymorphisms in 2,819 animals from a diverse collection of 74 sheep breeds. We find the majority of sheep populations contain high SNP diversity and have retained an effective population size much higher than most cattle or dog breeds, suggesting domestication occurred from a broad genetic base. Extensive haplotype sharing and generally low divergence time between breeds reveal frequent genetic exchange has occurred during the development of modern breeds. A scan of the genome for selection signals revealed 31 regions containing genes for coat pigmentation, skeletal morphology, body size, growth and reproduction. We demonstrate the strongest selection signal has occurred in response to breeding for the absence of horns. The high density map of genetic variability presented provides the first in-depth view of the genetic history for this important livestock species.