Whole genome structural analysis of Caribbean hair sheep reveals quantitative link to West African ancestry

Abstract

Hair sheep of Caribbean origin have become an important part of the U.S. sheep industry. Their lack of wool eliminates a number of health concerns and drastically reduces the cost of production. More importantly, Caribbean hair sheep demonstrate robust production performance even in the presence of drug-resistant gastrointestinal nematodes, a rising concern to the industry. Despite the growing importance of hair sheep in the Americas their genetic origins have remained speculative. Prior to this report no genetic studies were able to identify a unique geographical origin of hair sheep in the New World. Our study clarifies the African and European ancestry of Caribbean hair sheep. Whole-genome structural analysis was conducted on four established breeds of hair sheep from the Caribbean region. Using breeds representing Africa and Europe we establish an objective measure indicating Caribbean hair sheep are derived from Iberian and West African origins. Caribbean hair sheep result from West African introgression into established ecotypes of Iberian descent. Genotypes from 47,750 autosomal single nucleotide polymorphism markers scored in 290 animals were used to characterize the population structure of the St. Croix, Barbados Blackbelly, Morada Nova, and Santa Ines. Principal components, admixture, and phylogenetic analyses results correlate with historical patterns of colonization and trade. These patterns support co-migration of these sheep with humans.

Fig 1. Principal components analysis.

A. Multi-Dimensional Scaling (MDS) plot of the pair-wise Identity by State distances among the 27 breeds used in this study. The Iberian Group is indicated by a dashed circle and contains the New World Breeds: Navajo Churro, Brazilian Creole, Gulf Coast Native, and St Elizabeth. The Spanish and Australian Merino are indistinguishable in this group, as well as the Spanish Churra, Ojalada, Rosa Aragonesa, Castellana, and the Italian Bergamesca. Dashed lines indicate breeds of known admixture: (1)- The Dorper is a composite breed of the Dorset Horn and Blackhead Somali (Menz/Maasai used as substitutes). (2)- The Australian Poll Dorset was developed by inserting the poll gene into the Dorset Horn by crossing with Corriedale and Ryeland, a breed similar to the Australian Suffolk. B. MDS plot of Components 01 vs 02 after outlier removal. Component 1 clearly separates the West African Djallonké and the four Caribbean Hair sheep from the East African group: Menz, Maasai, and Afrikaaner. PC02 separates the Hair sheep from the European breeds leaving the Caribbean Hair sheep in a quadrant alone with the West African Djallonké. The Dorper is approximately 70% East African admixture and clusters with this group. All of the European breeds cluster in or near the Iberian Group along with the New World wool breeds. C. MDS plot of Components 02 vs 03 after outlier removal. As in the above plot PC02 divides East and West African breeds. PC03 further separates the British from the Iberian.

Fig 2. Admixture analysis of 29 breeds used in this study.

Breeds are separated into blocks. Lines within each block represent individuals within the breed. Graphs for K = 3–14 show the admixture ratio of each theoretical population [K] within the individuals in a block. Groups are indicated at the top. Caribbean hair sheep are inscribed by dashed lines. Norduz is included with the African group for simplicity.

Fig 3. Tree topology with six migration events inferred by Treemix.

Drift parameter is shown at the bottom and weights of inferred gene flow shown at the top in modified Newick format.

Fig 4. Historical and geographical corroboration of the results of whole genome structural analysis.

Map indicates migration routes of British (olive) and Iberian (Orange) colonization and locations of New World and hair sheep breeds used in this study; Navajo Churro (CHO), Gulf Coast native (GCN), St. Elizabeth (STE), St. Croix (STX), Barbados Blackbelly (BBB), Brazilian Creole (BZC), Morada Nova (MNV), Santa Ines (STI). Red arrows indicate routes and relative magnitude of the Trans-Atlantic Slave Trade taken from Galloway. Gray ovals (Barbados and Parambuco) indicate regions of heavy sugar production and centers of slave importation. Green highlighted African nations indicate range and distribution of the West African Djallonké sheep (FAO).