Whole mitochondrial genomes unveil the impact of domestication on goat matrilineal variability

Colli et al. BMC Genomics (2015) 16:1115 DOI 10.1186/s12864-015-2342-2 RESEARCH ARTICLE Open Access Whole mitochondrial genomes unveil the impact of domestication on goat matrilineal variability Licia Colli1,2†, Hovirag Lancioni3†, Irene Cardinali3, Anna Olivieri4, Marco Rosario Capodiferro3,4, Marco Pellecchia1, Marcin Rzepus1,5, Wahid Zamani6,7, Saeid Naderi8, Francesca Gandini4,9, Seyed Mohammad Farhad Vahidi10, Saif Agha11, Ettore Randi12,13, Vincenza Battaglia4, Maria Teresa Sardina14, Baldassare Portolano14, Hamid Reza Rezaei15, Petros Lymberakis16, Frédéric Boyer6, Eric Coissac6, François Pompanon6, Pierre Taberlet6, Paolo Ajmone Marsan1,2 and Alessandro Achilli3,4* Abstract Background: The current extensive use of the domestic goat (Capra hircus) is the result of its medium size and high adaptability as multiple breeds. The extent to which its genetic variability was influenced by early domestication practices is largely unknown. A common standard by which to analyze maternally-inherited variability of livestock species is through complete sequencing of the entire mitogenome (mitochondrial DNA, mtDNA). Results: We present the first extensive survey of goat mitogenomic variability based on 84 complete sequences selected from an initial collection of 758 samples that represent 60 different breeds of C. hircus, as well as its wild sister species, bezoar (Capra aegagrus) from Iran. Our phylogenetic analyses dated the most recent common ancestor of C. hircus to ~460,000 years (ka) ago and identified five distinctive domestic haplogroups (A, B1, C1a, D1 and G). More than 90 % of goats examined were in haplogroup A. These domestic lineages are predominantly nested within C. aegagrus branches, diverged concomitantly at the interface between the Epipaleolithic and early Neolithic periods, and underwent a dramatic expansion starting from ~12–10 ka ago. Conclusions: Domestic goat mitogenomes descended from a small number of founding haplotypes that underwent domestication after surviving the last glacial maximum in the Near Eastern refuges. All modern haplotypes A probably descended from a single (or at most a few closely related) female C. aegagrus. Zooarchaelogical data indicate that domestication first occurred in Southeastern Anatolia. Goats accompanying the first Neolithic migration waves into the Mediterranean were already characterized by two ancestral A and C variants. The ancient separation of the C branch (~130 ka ago) suggests a genetically distinct population that could have been involved in a second event of domestication. The novel diagnostic mutational motifs defined here, which distinguish wild and domestic haplogroups, could be used to understand phylogenetic relationships among modern breeds and ancient remains and to evaluate whether selection differentially affected mitochondrial genome variants during the development of economically important breeds. Keywords: Goat mitochondrial genome, mtDNA haplogroups, Domestication, Origin of Capra hircus, Capra aegagrus * Correspondence: † Equal contributors 3 Dipartimento di Chimica, Biologia e Biotecnologie, Università di Perugia, Perugia 06123, Italy 4 Dipartimento di Biologia e Biotecnologie “L. Spallanzani”, Università di Pavia, Pavia 27100, Italy Full list of author information is available at the end of the article © 2015 Colli et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Colli et al. BMC Genomics (2015) 16:1115 Background The domestic goat (Capra hircus), which counts a worldwide population of more than 800,000,000 specimens and about 1200 breeds described (http://dad.fao.org), is among the “big five” livestock species defined by the Food and Agriculture Organization (FAO) [1] and is an invaluable source of milk, meat, skin and fiber for poor small holders and shepherds in developing countries and marginal areas [2]. On the basis of bone morphological changes associated with progressive taming [3], zooarchaeology suggests that goat domestication began about 11,000 years (ka) ago in an area stretching from the high Euphrates valleys in Southeastern Anatolia (Turkey) to the Zagros Mountains in Central Iran [4, 5] and located within the natural distribution of the wild ancestor species, the bezoar Capra aegagrus [6, 7]. This event is now considered as the final outcome of a gradual change from hunting to management of wild captive animals [3, 5, 8]. Due to their high rusticity and adaptability to harsh environments, goats represented a key resource during the Neolithic agricultural revolution and for the human migration waves that spread Neolithic culture out of the Fertile Crescent [9]. Previous studies of mitochondrial control-region haplotypes described six highly divergent haplogroups (Hg.s) in domestic goats: A, B, C [10], D [11], F [12] and G [13]. An additional haplogroup, named E, has been described by Joshi et al. [9] on the basis of two highly divergent control-region haplotypes. This was recognized as a sub-clade of haplogroup A when compared to a larger dataset [13]. The reported weak geographical structuring of goat mitochondrial variability was often interpreted as a consequence of the frequent transportation of goats along terrestrial and maritime routes of migration and commerce, probably during the early domestication phases [7, 10, 14, 15]. A subsequent comparison with wild stocks confirmed the presence of all “domestic” haplogroups in the current C. aegagrus populations, which could result from early translocations of animals and/or feralization before the worldwide spread of goats [7]. The haplogroup A is largely predominant (>90 %) among domestic goats, but rare (6 %) in the bezoar and never observed in the Iranian Zagros Mountains. The probable origin of haplogroup A occurred in Eastern Anatolia, where it is still present among wild populations, and its presence in Eastern Iran probably is the result of a subsequent feralization of domestic goats. The most frequent haplogroup in wild populations is C (39 %) detected in most of the bezoar distribution area and more common in Southern Zagros/Central Iranian Plateau. The evidence that C control-region haplotypes from Pakistan are the farthest from the domestic-related ones [7] disproved the Indus Valley domestication Page 2 of 12 hypothesis suggested by archaeological remains from Mehrgarh (Baluchistan, Pakistan) [5]. Haplogroup F is still found in wild populations (from Northern Caucasus (...truncated)