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

Colli L, Lancioni H, Cardinali I, Olivieri A, Capodiferro MR, Pellecchia M, Rzepus M, Zamani W, Naderi S, Gandini F, Vahidi SM, 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 - BMC Genomics (2015)

Bottom Line: Zooarchaelogical data indicate that domestication first occurred in Southeastern Anatolia.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.

View Article: PubMed Central - PubMed

Affiliation: Institute of Zootechnics, Università Cattolica del S. Cuore, Piacenza, 29122, Italy. licia.colli@unicatt.it.

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.

No MeSH data available.


Related in: MedlinePlus

Bayesian Skyline Plot showing the goat population size trend with a generation time of 4.5 years [60]. The Y axis indicates the effective number of females. The thick solid line is the median estimate and the grey shading shows the 95 % highest posterior density limits. The time axis is limited to 100 ka, beyond that time the curve remains linear
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Fig2: Bayesian Skyline Plot showing the goat population size trend with a generation time of 4.5 years [60]. The Y axis indicates the effective number of females. The thick solid line is the median estimate and the grey shading shows the 95 % highest posterior density limits. The time axis is limited to 100 ka, beyond that time the curve remains linear

Mentions: A Bayesian Skyline Plot (BSP) analysis was carried out to assess population expansions. The overall BSP points to a steep increase of the female effective population size about 12–10 ka ago (Fig. 2). This analysis was performed on the complete molecule after establishing six different partitions (1st, 2nd and 3rd codon positions, RNA genes, HVS-I and other control-region segments). The same partitions were also considered to perform ML analyses on the entire mitogenome. The final outcomes were an overall mutational rate of 3.95 × 10−8 substitutions per nucleotide per year (1 mutation every 1522 years) on the entire molecule and 1.57 × 10−8 substitutions per nucleotide per year (or 1 mutation every 4120 years) on the coding region alone. Both analyses revealed that the molecular clock could not be rejected (p-values > 0.05) when employing the complex GTR/REV model. A clear sign of purifying selection is apparent when calculating the non-synonymous/synonymous ratio, i.e. (ɷ) = 0.190 (Table 3). As expected, this ratio is significantly lower (p-value < < 0.001; Fisher’s exact test) in the deep portion of the tree and the comparison among domestic branches reveals slightly significant differences (χ2 p-value = 0.026) (Table 3); in particular the ɷ ratio of A is much higher than previously reported (ɷ = 0.049) [17]. Similarly, age values of younger clades are much higher when considering the entire panel of mutations rather than those based on synonymous changes only (Fig. 3), probably because the effect of purifying selection is incomplete and all the negatively selectable characters are still included [29].Fig. 2


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

Colli L, Lancioni H, Cardinali I, Olivieri A, Capodiferro MR, Pellecchia M, Rzepus M, Zamani W, Naderi S, Gandini F, Vahidi SM, 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 - BMC Genomics (2015)

Bayesian Skyline Plot showing the goat population size trend with a generation time of 4.5 years [60]. The Y axis indicates the effective number of females. The thick solid line is the median estimate and the grey shading shows the 95 % highest posterior density limits. The time axis is limited to 100 ka, beyond that time the curve remains linear
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4696231&req=5

Fig2: Bayesian Skyline Plot showing the goat population size trend with a generation time of 4.5 years [60]. The Y axis indicates the effective number of females. The thick solid line is the median estimate and the grey shading shows the 95 % highest posterior density limits. The time axis is limited to 100 ka, beyond that time the curve remains linear
Mentions: A Bayesian Skyline Plot (BSP) analysis was carried out to assess population expansions. The overall BSP points to a steep increase of the female effective population size about 12–10 ka ago (Fig. 2). This analysis was performed on the complete molecule after establishing six different partitions (1st, 2nd and 3rd codon positions, RNA genes, HVS-I and other control-region segments). The same partitions were also considered to perform ML analyses on the entire mitogenome. The final outcomes were an overall mutational rate of 3.95 × 10−8 substitutions per nucleotide per year (1 mutation every 1522 years) on the entire molecule and 1.57 × 10−8 substitutions per nucleotide per year (or 1 mutation every 4120 years) on the coding region alone. Both analyses revealed that the molecular clock could not be rejected (p-values > 0.05) when employing the complex GTR/REV model. A clear sign of purifying selection is apparent when calculating the non-synonymous/synonymous ratio, i.e. (ɷ) = 0.190 (Table 3). As expected, this ratio is significantly lower (p-value < < 0.001; Fisher’s exact test) in the deep portion of the tree and the comparison among domestic branches reveals slightly significant differences (χ2 p-value = 0.026) (Table 3); in particular the ɷ ratio of A is much higher than previously reported (ɷ = 0.049) [17]. Similarly, age values of younger clades are much higher when considering the entire panel of mutations rather than those based on synonymous changes only (Fig. 3), probably because the effect of purifying selection is incomplete and all the negatively selectable characters are still included [29].Fig. 2

Bottom Line: Zooarchaelogical data indicate that domestication first occurred in Southeastern Anatolia.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.

View Article: PubMed Central - PubMed

Affiliation: Institute of Zootechnics, Università Cattolica del S. Cuore, Piacenza, 29122, Italy. licia.colli@unicatt.it.

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.

No MeSH data available.


Related in: MedlinePlus