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. 2009 Apr 24;324(5926):532-6.
doi: 10.1126/science.1170587.

Revealing the history of sheep domestication using retrovirus integrations

Bernardo Chessa  1 , Filipe Pereira, Frederick Arnaud, Antonio Amorim, Félix Goyache, Ingrid Mainland, Rowland R Kao, Josephine M Pemberton, Dario Beraldi, Michael J Stear, Alberto Alberti, Marco Pittau, Leopoldo Iannuzzi, Mohammad H Banabazi, Rudovick R Kazwala, Ya-Ping Zhang, Juan J Arranz, Bahy A Ali, Zhiliang Wang, Metehan Uzun, Michel M Dione, Ingrid Olsaker, Lars-Erik Holm, Urmas Saarma, Sohail Ahmad, Nurbiy Marzanov, Emma Eythorsdottir, Martin J Holland, Paolo Ajmone-Marsan, Michael W Bruford, Juha Kantanen, Thomas E Spencer, Massimo Palmarini
Affiliations

Revealing the history of sheep domestication using retrovirus integrations

Bernardo Chessa et al. Science. .

Abstract

The domestication of livestock represented a crucial step in human history. By using endogenous retroviruses as genetic markers, we found that sheep differentiated on the basis of their "retrotype" and morphological traits dispersed across Eurasia and Africa via separate migratory episodes. Relicts of the first migrations include the Mouflon, as well as breeds previously recognized as "primitive" on the basis of their morphology, such as the Orkney, Soay, and the Nordic short-tailed sheep now confined to the periphery of northwest Europe. A later migratory episode, involving sheep with improved production traits, shaped the great majority of present-day breeds. The ability to differentiate genetically primitive sheep from more modern breeds provides valuable insights into the history of sheep domestication.

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Figures

Fig. 1
Fig. 1
Worldwide distribution of insertionally polymorphic enJSRVs. Distribution of the insertionally polymorphic enJSRV loci analysed in this study in 65 sheep populations representing local breeds from the old world. (A) Frequencies of each enJSRV locus in each population are represented by a vertical bar and arranged in a descending order. Insertion frequencies were obtained using the software Arlequin 3.11 (27) treating the absence of a specific enJSRV provirus as a recessive allele. (B) Locations of sheep populations sampled. (C-F). Interpolation maps displaying the spatial distribution of estimated enJSRVs frequencies. The geographical variation was visualized using the ‘Spatial Analyst Extension’ of ArcView GIS 3.2 software (ESRI, Redlands, CA, USA; http://www.esri.com). Interpolated map values were calculated employing the inverse distance–weighted with 12 nearest neighbours and a power of two, and interpolation surfaces were divided into 13 classes with higher insertion frequencies indicated by darkest shading. The central point of the sampling area was used as geographic coordinates for each population (Table S1).
Fig. 2
Fig. 2
Combination of enJSRV proviruses (retrotypes) in the domestic sheep. Pie charts in the figure represent the frequency of each retrotype in the 65 populations tested. Each sheep tested was assigned a retrotype on the basis of the combination of insertionally polymorphic enJSRV proviruses present in their genome. Retrotypes were defined R0 to R14 as follows: RO = no insertionally polymorphic enJSRVs; R1 = enJSRV-7; R2 = enJSRV-18; R3 = enJS5F16; R4 = enJSRV-7 + enJSRV-18; R5 = enJSRV-7 + enJS5F16; R6 = enJSRV-18 + enJS5F16; R7 = enJSRV-7 + enJSRV-18+ enJS5F16; R8 = enJSRV-8; R9 =enJS5F16 + enJSRV-8; R10 = enJSRV-7 + enJS5F16 + enJSRV-8; R11 = enJSRV-18 + enJSRV-8; R12 = enJSRV-18 + enJS5F16 + enJSRV-8; R13 = enJSRV-7 + enJSRV-18 + enJSRV-8; R14 = enJSRV-7 + enJSRV-18 + enJS5F16 + enJSRV-8. Each retrotype is represented with a different colour (and pattern) as indicated in the figure. Numbers beside each pie chart indicate each of the 65 populations tested as indicated in Table S1. Note that most of the populations in South-West Asia, Central Asia, Southern Europe and Africa possess R2 (i.e. presence of enJSRV-18 only, shown in green) as the predominant retrotype. Around the Mediterranean basin there is also a high proportion of R4 given by the contemporary presence of enJSRV-7 and enJSRV-18 (shown in yellow). The primitive breeds are characterized by a high proportion of animals with R0 (no insertionally polymorphic proviruses, shown in white) or R1 (presence of enJSRV-7 only, shown in red). A ‘Nordic’ retrotype R3 (shown in blue) was characterized by a low frequency of enJSRV-18 and a high frequency of enJS5F16; Nordic populations also had a relatively high frequency of sheep with none of the insertionally polymorphic proviruses tested.
Fig. 3
Fig. 3
Genetic distances between sheep populations on the basis of enJSRVs insertion frequencies. (A) Multidimensional (MDS) scaling plot computed from the matrix of Nei’s unbiased genetic distances (TFPGA 1.3 software) (28). The dominant nature of the enJSRVs as genetic markers was considered in all analyses. The matrix of interpopulation distances was summarized in two dimensions by use of MDS analysis as implemented by the STATISTICA ‘99 software package (StatSoft Inc., Tulsa, OK, USA). Each triangle represents one of the 65 populations tested. Note that in the graph only those populations outside the main cluster (enclosed within the square with the broken line and including the great majority of breeds from Africa, Asia and Europe) have been named. (B) Tri-dimensional plot summarising data obtained by principal component analysis (PCA) of the insertionally polymorphic enJSRV proviruses in the 65 sheep populations tested using the Proc Factor of the statistical package SAS/STAT® (SAS Institute Inc, Cary NC) according to the recommendations by Cavalli-Sforza et al. (29). Four factors, accounting for 86.66% of variation, with eigenvalue ≥ 1 were identified. Factor 1 (on the X-axis), explained 30.09% of variation and can be interpreted as the ‘Northern Sea factor’, distinguishing between a group of populations formed from some UK and continental European (including Denmark and Texel) sheep populations and the others. Factor 2 (on the Y-axis), explaining 23.58% of variation separating the Texel population from the rest. Factor 3 (on the Z-axis), explained 22.92% of variation and can be interpreted as the ‘primitive breed factor’, distinguishing between the group of populations formed by the mouflon and Scandinavian populations (including the Hebridean, Orkney and Soay populations) from the rest. Note that to increase the clarity of the figure, the populations that form the main cluster have not been named.
Fig. 4
Fig. 4
Morphological characteristics of primitive breeds. Breeds identified in this study as remnants of the first sheep migrations possess morphological characteristics (such as darker coarser fleece, moulting coat, frequent presence of horns in females), similar to wilder sheep and the Mouflon. (A) Urial sheep; (B) Cyprus Mouflon; (C) Mediterranean Mouflon; (D) Orkney sheep; (E) Soay sheep; (F) Gute sheep; (G) Åland sheep; (H) Icelandic sheep; (I) Hebridean sheep.
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Comment in

  • Genetics. It's a bull's market.
    Lewin HA. Lewin HA. Science. 2009 Apr 24;324(5926):478-9. doi: 10.1126/science.1173880. Science. 2009. PMID: 19390037 No abstract available.

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