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

Licia Colli, Hovirag Lancioni, Irene Cardinali, Anna Olivieri, Marco Rosario Capodiferro, Marco Pellecchia, Marcin Rzepus, Wahid Zamani, Saeid Naderi, Francesca Gandini, Seyed Mohammad Farhad Vahidi, Saif Agha, Ettore Randi, Vincenza Battaglia, Maria Teresa Sardina, Baldassare Portolano, Hamid Reza Rezaei, Petros Lymberakis, Frédéric Boyer, Eric Coissac & 4 others François Pompanon, Pierre Taberlet, Paolo Ajmone Marsan, Alessandro Achilli

Research output: Contribution to journalArticle

28 Citations (Scopus)

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.

LanguageEnglish
Article number1115
JournalBMC Genomics
Volume16
Issue number1
DOIs
Publication statusPublished - 29 Dec 2015

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Mitochondrial Genome
Goats
Haplotypes
Bezoars
Livestock
Iran
Domestication
Mitochondrial DNA
Population

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Colli, L., Lancioni, H., Cardinali, I., Olivieri, A., Capodiferro, M. R., Pellecchia, M., ... Achilli, A. (2015). Whole mitochondrial genomes unveil the impact of domestication on goat matrilineal variability. BMC Genomics, 16(1), [1115]. https://doi.org/10.1186/s12864-015-2342-2
Colli, Licia ; Lancioni, Hovirag ; Cardinali, Irene ; Olivieri, Anna ; Capodiferro, Marco Rosario ; Pellecchia, Marco ; Rzepus, Marcin ; Zamani, Wahid ; Naderi, Saeid ; Gandini, Francesca ; Vahidi, Seyed Mohammad Farhad ; Agha, Saif ; Randi, Ettore ; Battaglia, Vincenza ; Sardina, Maria Teresa ; Portolano, Baldassare ; Rezaei, Hamid Reza ; Lymberakis, Petros ; Boyer, Frédéric ; Coissac, Eric ; Pompanon, François ; Taberlet, Pierre ; Ajmone Marsan, Paolo ; Achilli, Alessandro. / Whole mitochondrial genomes unveil the impact of domestication on goat matrilineal variability. In: BMC Genomics. 2015 ; Vol. 16, No. 1.
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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.",
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author = "Licia Colli and Hovirag Lancioni and Irene Cardinali and Anna Olivieri and Capodiferro, {Marco Rosario} and Marco Pellecchia and Marcin Rzepus and Wahid Zamani and Saeid Naderi and Francesca Gandini and Vahidi, {Seyed Mohammad Farhad} and Saif Agha and Ettore Randi and Vincenza Battaglia and Sardina, {Maria Teresa} and Baldassare Portolano and Rezaei, {Hamid Reza} and Petros Lymberakis and Fr{\'e}d{\'e}ric Boyer and Eric Coissac and Fran{\cc}ois Pompanon and Pierre Taberlet and {Ajmone Marsan}, Paolo and Alessandro Achilli",
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Colli, L, Lancioni, H, Cardinali, I, Olivieri, A, Capodiferro, MR, Pellecchia, M, Rzepus, M, Zamani, W, Naderi, S, Gandini, F, Vahidi, SMF, Agha, S, Randi, E, Battaglia, V, Sardina, MT, Portolano, B, Rezaei, HR, Lymberakis, P, Boyer, F, Coissac, E, Pompanon, F, Taberlet, P, Ajmone Marsan, P & Achilli, A 2015, 'Whole mitochondrial genomes unveil the impact of domestication on goat matrilineal variability', BMC Genomics, vol. 16, no. 1, 1115. https://doi.org/10.1186/s12864-015-2342-2

Whole mitochondrial genomes unveil the impact of domestication on goat matrilineal variability. / Colli, Licia; Lancioni, Hovirag; Cardinali, Irene; Olivieri, Anna; Capodiferro, Marco Rosario; Pellecchia, Marco; Rzepus, Marcin; Zamani, Wahid; Naderi, Saeid; Gandini, Francesca; Vahidi, Seyed Mohammad Farhad; Agha, Saif; Randi, Ettore; Battaglia, Vincenza; Sardina, Maria Teresa; Portolano, Baldassare; Rezaei, Hamid Reza; Lymberakis, Petros; Boyer, Frédéric; Coissac, Eric; Pompanon, François; Taberlet, Pierre; Ajmone Marsan, Paolo; Achilli, Alessandro.

In: BMC Genomics, Vol. 16, No. 1, 1115, 29.12.2015.

Research output: Contribution to journalArticle

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T1 - Whole mitochondrial genomes unveil the impact of domestication on goat matrilineal variability

AU - Colli, Licia

AU - Lancioni, Hovirag

AU - Cardinali, Irene

AU - Olivieri, Anna

AU - Capodiferro, Marco Rosario

AU - Pellecchia, Marco

AU - Rzepus, Marcin

AU - Zamani, Wahid

AU - Naderi, Saeid

AU - Gandini, Francesca

AU - Vahidi, Seyed Mohammad Farhad

AU - Agha, Saif

AU - Randi, Ettore

AU - Battaglia, Vincenza

AU - Sardina, Maria Teresa

AU - Portolano, Baldassare

AU - Rezaei, Hamid Reza

AU - Lymberakis, Petros

AU - Boyer, Frédéric

AU - Coissac, Eric

AU - Pompanon, François

AU - Taberlet, Pierre

AU - Ajmone Marsan, Paolo

AU - Achilli, Alessandro

PY - 2015/12/29

Y1 - 2015/12/29

N2 - 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.

AB - 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.

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KW - Origin of Capra hircus

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Colli L, Lancioni H, Cardinali I, Olivieri A, Capodiferro MR, Pellecchia M et al. Whole mitochondrial genomes unveil the impact of domestication on goat matrilineal variability. BMC Genomics. 2015 Dec 29;16(1). 1115. https://doi.org/10.1186/s12864-015-2342-2