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On the origin and diversification of Podolian cattle breeds: testing scenarios of European colonization using genome-wide SNP data

BACKGROUND: During the Neolithic expansion, cattle accompanied humans and spread from their domestication centres to colonize the ancient world. In addition, European cattle occasionally intermingled with both indicine cattle and local aurochs resulting in an exclusive pattern of genetic diversity....

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Autores principales: Senczuk, Gabriele, Mastrangelo, Salvatore, Ajmone-Marsan, Paolo, Becskei, Zsolt, Colangelo, Paolo, Colli, Licia, Ferretti, Luca, Karsli, Taki, Lancioni, Hovirag, Lasagna, Emiliano, Marletta, Donata, Persichilli, Christian, Portolano, Baldassare, Sarti, Francesca M., Ciani, Elena, Pilla, Fabio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8173809/
https://www.ncbi.nlm.nih.gov/pubmed/34078254
http://dx.doi.org/10.1186/s12711-021-00639-w
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author Senczuk, Gabriele
Mastrangelo, Salvatore
Ajmone-Marsan, Paolo
Becskei, Zsolt
Colangelo, Paolo
Colli, Licia
Ferretti, Luca
Karsli, Taki
Lancioni, Hovirag
Lasagna, Emiliano
Marletta, Donata
Persichilli, Christian
Portolano, Baldassare
Sarti, Francesca M.
Ciani, Elena
Pilla, Fabio
author_facet Senczuk, Gabriele
Mastrangelo, Salvatore
Ajmone-Marsan, Paolo
Becskei, Zsolt
Colangelo, Paolo
Colli, Licia
Ferretti, Luca
Karsli, Taki
Lancioni, Hovirag
Lasagna, Emiliano
Marletta, Donata
Persichilli, Christian
Portolano, Baldassare
Sarti, Francesca M.
Ciani, Elena
Pilla, Fabio
author_sort Senczuk, Gabriele
collection PubMed
description BACKGROUND: During the Neolithic expansion, cattle accompanied humans and spread from their domestication centres to colonize the ancient world. In addition, European cattle occasionally intermingled with both indicine cattle and local aurochs resulting in an exclusive pattern of genetic diversity. Among the most ancient European cattle are breeds that belong to the so-called Podolian trunk, the history of which is still not well established. Here, we used genome-wide single nucleotide polymorphism (SNP) data on 806 individuals belonging to 36 breeds to reconstruct the origin and diversification of Podolian cattle and to provide a reliable scenario of the European colonization, through an approximate Bayesian computation random forest (ABC-RF) approach. RESULTS: Our results indicate that European Podolian cattle display higher values of genetic diversity indices than both African taurine and Asian indicine breeds. Clustering analyses show that Podolian breeds share close genomic relationships, which suggests a likely common genetic ancestry. Among the simulated and tested scenarios of the colonization of Europe from taurine cattle, the greatest support was obtained for the model assuming at least two waves of diffusion. Time estimates are in line with an early migration from the domestication centre of non-Podolian taurine breeds followed by a secondary migration of Podolian breeds. The best fitting model also suggests that the Italian Podolian breeds are the result of admixture between different genomic pools. CONCLUSIONS: This comprehensive dataset that includes most of the autochthonous cattle breeds belonging to the so-called Podolian trunk allowed us not only to shed light onto the origin and diversification of this group of cattle, but also to gain new insights into the diffusion of European cattle. The most well-supported scenario of colonization points to two main waves of migrations: with one that occurred alongside with the Neolithic human expansion and gave rise to the non-Podolian taurine breeds, and a more recent one that favoured the diffusion of European Podolian. In this process, we highlight the importance of both the Mediterranean and Danube routes in promoting European cattle colonization. Moreover, we identified admixture as a driver of diversification in Italy, which could represent a melting pot for Podolian cattle. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12711-021-00639-w.
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spelling pubmed-81738092021-06-03 On the origin and diversification of Podolian cattle breeds: testing scenarios of European colonization using genome-wide SNP data Senczuk, Gabriele Mastrangelo, Salvatore Ajmone-Marsan, Paolo Becskei, Zsolt Colangelo, Paolo Colli, Licia Ferretti, Luca Karsli, Taki Lancioni, Hovirag Lasagna, Emiliano Marletta, Donata Persichilli, Christian Portolano, Baldassare Sarti, Francesca M. Ciani, Elena Pilla, Fabio Genet Sel Evol Research Article BACKGROUND: During the Neolithic expansion, cattle accompanied humans and spread from their domestication centres to colonize the ancient world. In addition, European cattle occasionally intermingled with both indicine cattle and local aurochs resulting in an exclusive pattern of genetic diversity. Among the most ancient European cattle are breeds that belong to the so-called Podolian trunk, the history of which is still not well established. Here, we used genome-wide single nucleotide polymorphism (SNP) data on 806 individuals belonging to 36 breeds to reconstruct the origin and diversification of Podolian cattle and to provide a reliable scenario of the European colonization, through an approximate Bayesian computation random forest (ABC-RF) approach. RESULTS: Our results indicate that European Podolian cattle display higher values of genetic diversity indices than both African taurine and Asian indicine breeds. Clustering analyses show that Podolian breeds share close genomic relationships, which suggests a likely common genetic ancestry. Among the simulated and tested scenarios of the colonization of Europe from taurine cattle, the greatest support was obtained for the model assuming at least two waves of diffusion. Time estimates are in line with an early migration from the domestication centre of non-Podolian taurine breeds followed by a secondary migration of Podolian breeds. The best fitting model also suggests that the Italian Podolian breeds are the result of admixture between different genomic pools. CONCLUSIONS: This comprehensive dataset that includes most of the autochthonous cattle breeds belonging to the so-called Podolian trunk allowed us not only to shed light onto the origin and diversification of this group of cattle, but also to gain new insights into the diffusion of European cattle. The most well-supported scenario of colonization points to two main waves of migrations: with one that occurred alongside with the Neolithic human expansion and gave rise to the non-Podolian taurine breeds, and a more recent one that favoured the diffusion of European Podolian. In this process, we highlight the importance of both the Mediterranean and Danube routes in promoting European cattle colonization. Moreover, we identified admixture as a driver of diversification in Italy, which could represent a melting pot for Podolian cattle. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12711-021-00639-w. BioMed Central 2021-06-02 /pmc/articles/PMC8173809/ /pubmed/34078254 http://dx.doi.org/10.1186/s12711-021-00639-w Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Senczuk, Gabriele
Mastrangelo, Salvatore
Ajmone-Marsan, Paolo
Becskei, Zsolt
Colangelo, Paolo
Colli, Licia
Ferretti, Luca
Karsli, Taki
Lancioni, Hovirag
Lasagna, Emiliano
Marletta, Donata
Persichilli, Christian
Portolano, Baldassare
Sarti, Francesca M.
Ciani, Elena
Pilla, Fabio
On the origin and diversification of Podolian cattle breeds: testing scenarios of European colonization using genome-wide SNP data
title On the origin and diversification of Podolian cattle breeds: testing scenarios of European colonization using genome-wide SNP data
title_full On the origin and diversification of Podolian cattle breeds: testing scenarios of European colonization using genome-wide SNP data
title_fullStr On the origin and diversification of Podolian cattle breeds: testing scenarios of European colonization using genome-wide SNP data
title_full_unstemmed On the origin and diversification of Podolian cattle breeds: testing scenarios of European colonization using genome-wide SNP data
title_short On the origin and diversification of Podolian cattle breeds: testing scenarios of European colonization using genome-wide SNP data
title_sort on the origin and diversification of podolian cattle breeds: testing scenarios of european colonization using genome-wide snp data
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8173809/
https://www.ncbi.nlm.nih.gov/pubmed/34078254
http://dx.doi.org/10.1186/s12711-021-00639-w
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