A novel lineage of the Capra genus discovered in the Taurus Mountains of Turkey using ancient genomics
- Smurfit Institute of Genetics, Trinity College Dublin, Ireland
- Department of Anthropology, University of North Carolina at Chapel Hill, United States
- Centre National de Recherche Scientifique / Muséum national d'Histoire naturelle, Archéozoologie, Archéobotanique, France
- University of Tehran, Bioarchaeology Laboratory, (Central Laboratory), Archaeozoology section, Islamic Republic of Iran
- School of History, Classics and Archaeology, University of Edinburgh, United Kingdom
- Department of Anthropology, University of Nevada, Las Vegas, United States
- Department of Archeology, Department of Prehistoric Archeology, Faculty of Letters, Ankara Hacı Bayram Veli University, Turkey
Figures
Figure 1 with 7 supplements
Direkli Cave caprids in geographic and genetic context.
(A) Elevation map of southwest Asia. Key sites are indicated, with C. caucasica and C. cylindricornis distributions from Gavashelishvili et al., 2018 displayed. MSL = metres above mean sea level. (B) Neighbour joining phylogeny of genomes >0.5 X and the lower coverage Tur2 (0.02 X) and Direkli16 (0.01 X) genomes using 625,495 transversion sites and pairwise IBS, rooted on Sheep (not shown, as well as a likely Barbary Sheep sample Falconeri1, see Methods). Node support from 100 replicates using 50 5 Mb regions sampled without replacement shown when <100. Pink = Direkli4, green = other genomes first reported here.
Figure 1—figure supplement 1
View of excavation area from SW, Direkli Cave (from Direkli Cave Excavation Archive, 2018).
Figure 1—figure supplement 2
Plan map of Direkli Cave showing location of Capra specimens sequenced in this study.
Figure 1—figure supplement 3
Probability density distribution of pairwise D statistics using 28 domestic C.
hircus and 20 wild C. aegagrus in the form D(Direkli4, H2; H3, Sheep). In all tests positive D statistics are obtained, implying an excess of ancestral variation in Direkli4 relative to C. hircus and C. aegagrus.
Figure 1—figure supplement 4
Substitution rates of C>T and G>A transitions for ancient and historic samples sequenced in the present study, relative to the 5’ and 3’ ends of DNA fragments.
Figure 1—figure supplement 5
NJ Phylogeny using sheep-aligned identity-by-state data, (A) with and (B) without the lower coverage Direkli16 sample.
96,930 and 110,672 transversion biallelic SNPs were used in each IBS calculation respectively. Node support values are displayed when <100.
Figure 1—figure supplement 6
MDS plot of sheep-aligned IBS data (A) underlying Figure 1—figure supplement 5 and (B) using ancients & historic samples only.
Insert plot gives a higher detailed view of the MDS region encapsulating the european ibex and tur specimen, including two “taurasian tur” (Direkli4 and Direkli16).
Figure 1—figure supplement 7
Distance-from-the-outgroup for modern and ancient/historic Capra genomes.
Distance values are obtained from sheep-aligned IBS statistics underlying Figure 1—figure supplement 5A.
Figure 2 with 5 supplements
Autosomal affinity and mtDNA profile of Direkli Cave caprids.
(A) D statistic test of affinity using specimens from Direkli Cave and a historic C.caucasica individual for reference. Positive values indicate sample X has greater affinity with the Tur-like Direkli4 genome; negative values indicate greater affinity with the C. aegagrus Direkli1-2. Error bars represent 3 standard errors, underlying site counts are presented in Supplementary file 1E. (B) ML phylogeny of mtDNA, abbreviated. Bootstrap node support values (100 replicates) are displayed when <100. The complete phylogeny including likely Barbary sheep Falconeri1 is displayed in Figure 2—figure supplement 1. T haplogroup is as defined by Daly et al., 2018 Low coverage sample Direkli17 is displayed in a highly reduced phylogeny Figure 2—figure supplement 2. C=collapsed. *=Direkli sample with discordant mtDNA and nuclear genome affinity.
Figure 2—figure supplement 1
ML phylogeny of mtDNA, uncollapsed.
Bootstrap node support values (100 replicates) are displayed when <100. Outgroup is Yak and not shown.
Figure 2—figure supplement 2
Reduced mtDNA ML phylogeny including Direkli17.
Direki17’s low number of called sites (1162) precluded inclusion in a larger phylogeny; Direkli1-2 and Direkli13 represent the ‘T’ clade, while Direkli4 and Direkli12 represent the ‘F’ clade. Bootstrap values (100 replicated) displayed at nodes.
Figure 2—figure supplement 3
Capra body size estimates from archaeological assemblages, organized by region, time, and archaeological site.
Body weight estimates are based on Rivals, 2004 conversion formula of astragalus measurements to body weight (kg). The bezoar (Capra aegagrus) body size maximum of ~100 kg (Masseti, 2009) is highlighted to demonstrate the high upper range and variability observed at Direkli Cave and also Ksar Akil. Data from authors as well as the following: (Bökönyi, 1977; Hesse, 1978; Churcher, 1994; Horwitz, 2003; Açıkkol, 2006; Kersten, 1987). Data from Aşıklı Höyük (level 2) are used with permission of Hijlke Buitenhuis, Joris Peters and Nadja Pöllath.
Figure 2—figure supplement 4
D statistic of the form D(Abdul4, Test; Direkli4, Sheep), where Abdul4 is a Capra aegagrus from the 11th millennium BCE Zagros Mountains and Direkli4 is a Capra caucasica like genome from the Taurus Mountains.
Test individuals are restricted to Capra aegagrus/hircus. Significant (|Z|≥3) results are indicated in yellow; non-significant (|Z|<3) in blue. Positive D values indicate greater derived allele sharing between Direkli4 and the current H2 genome than between Direkli4 and Abdul4; negative indicates greater allele sharing between Direkli4 and Abdul4. These tests indicate that a Late Pleistocene C.aegagrus from Armenia (Hovk-1), from Direkli Cave, and modern bezoar from northwest Iran have elevated Direkli4 derived allele sharing, as well as domestic Capra hircus from west Eurasia and Europe.
Figure 2—figure supplement 5
D statistic of the form D(Abdul4, Test; Direkli4, Sheep), where Abdul4 is a Capra aegagrus from the 11th millennium BCE Zagros Mountains and Direkli4 is a Capra caucasica like genome from the Taurus Mountains.
Test individuals exclude Capra aegagrus/hircus. Significant (|Z|≥3) results are indicated in yellow; non-significant (|Z|<3) in blue. Positive D values indicate greater derived allele sharing between Direkli4 and the current H2 genome than between Direkli4 and Abdul4; negative indicates greater allele sharing between Direkli4 and Abdul4.
Figure 3 with 22 supplements
Extended D calculation and application to Direkli4 specific allele sharing.
(A) Extended D statistic. To control for gene flow with the Capra genus, we condition on variants derived in Direkli4 (H3) and a genome X (H2), but ancestral in other populations (here: Sheep, non-bezoar Capra genomes, bezoar from Direkli Cave, and other bezoar). Values are calculated relative to a set of Neolithic goat from the Zagros Mountains, and normalized similarly to the D statistic. (B) Extended D statistic values for Direkli4 using transversions, (C) plotted through time. Each symbol is a test genome, with shape denoting time period. Black borders indicates a |Z| score ≥3, using 1000 bootstrap replicates and 5 Mb blocks.
Figure 3—figure supplement 1
Extended D statistic in the form {Aceramic Neolithic Zagros, X/H2, Direkli4 (H3), Direkli Wild + Other Wild + Capra, Sheep}, using both transitions and transversions.
Fill color indicates extended D value measuring excess of Direkli4-specific alleles in H2, relative to Aceramic Neolithic Zagros goat. ‘+’ demarcates different populations in which the ancestral allele (relative to the derived Direkli4 allele) must be observed and fixed. Black borders indicate a Z score ≥ |3|.
Figure 3—figure supplement 2
Extended D, rotating H3 through Capra genus genomes, first tranche of H3 genomes.
Figure 3—figure supplement 3
Extended D, rotating H3 through Capra genus genomes, second tranche of H3 genomes.
Figure 3—figure supplement 4
Distribution of Direkli4-specific variants also present at >0%,≤10% in wild genomes, expressed as a proportion of the total number of these variants in the tested domestic genomes.
The majority of ‘shared Direkli4’ variants are observed with Tur1, particularly for modern European and African goats. Modern European and African goats also show ‘Direkli4’ allele sharing with the historic-era Capra cylindricornis Caucasus1, while ancient European goats show allele sharing with ancient Turkish wild Direkli1-2.
Figure 3—figure supplement 5
Treemix results for m=5, using 223,772 transversion variants ascertained on sheep, k=1000.
Support values for nodes are indicated when <100 (50 bootstrap replicates).
Figure 3—figure supplement 6
Residuals for Treemix m=5.
Some genomes have unmodeled affinity with Direkli4: Neolithic Serbian genomes from Blagotin; wild Late Pleistocene bezoar (Capra aegagrus) from Direkli Cave; Alpine Ibex (Capra ibex); Pyrenean ibex (Capra pyrenaica); Moroccan goat; and the outgroup Sheep. Populations which have lower genetic affinity with Direkli4 than the model predicts: the markhor (Capra falconeri); Siberian ibex (Capra sibirica); and Nubian ibex (Capra nubiana). X-axis labels are colored by their residual with Direkli4.
Figure 3—figure supplement 7
Orientagraph model and residuals for m=4, using 104,550 transversion variants and k=1000.
Residual x-axis labels are colored by their residual with Direkli4.
Figure 3—figure supplement 8
ADMIXTOOLS2.
Maier et al., 2022 automated graph exploration for m=2 (two admixture events), using 223,772 biallelic variants ascertained in sheep and presenting the best fitting graph as measured by log likelihood score (–0.5). Graphs which fit the data ‘as good as’ the above graph are available at https://osf.io/3ecqd/, along with the best fitting graph for m=3. Abbreviations used for populations defined in Supplementary file 1C: ETa = Direkli Cave bezoar (Epipaleolithic Taurus), DIR4=Direkli4, NSe = Neolithic Serbia, NEI = Neolithic East Iran, Tur1=Tur1. Sheep was used as the outgroup.
Figure 3—figure supplement 9
Clustered heatmap of IBS data for ARS1 1:104,150,173–104,349,720.
Sheep and lower coverage Nubiana1, Caucasus1 are removed.
Figure 3—figure supplement 10
Clustered heatmap of IBS data for ARS1 2:24,324,410–24,369,675.
Sheep and lower coverage Nubiana1, Caucasus1 are removed.
Figure 3—figure supplement 11
Clustered heatmap of IBS data for ARS1 13:66,710,508–66,749,824.
Sheep and lower coverage Nubiana1, Caucasus1 are removed.
Figure 3—figure supplement 12
Clustered heatmap of IBS data for ARS1 1:118,433,695–118,469,862.
Sheep and lower coverage Nubiana1, Caucasus1 are removed.
Figure 3—figure supplement 13
Clustered heatmap of IBS data for ARS1 6:20,670,803–20,728,594.
Sheep and lower coverage Nubiana1, Caucasus1 are removed.
Figure 3—figure supplement 14
Clustered heatmap of IBS data for ARS1 6–75,470,180-75,509,529.
Sheep and lower coverage Nubiana1, Caucasus1 are removed.
Figure 3—figure supplement 15
Clustered heatmap of IBS data for ARS1 7:24,370,068–24,409,932.
Sheep and lower coverage Nubiana1, Caucasus1 are removed.
Figure 3—figure supplement 16
Clustered heatmap of IBS data for ARS1 11:66,897,539–66,929,689.
Sheep and lower coverage Nubiana1, Caucasus1 are removed.
Figure 3—figure supplement 17
Clustered heatmap of IBS data for ARS1 11:78,464,458–78,495,561.
Sheep and lower coverage Nubiana1, Caucasus1 are removed.
Figure 3—figure supplement 18
Clustered heatmap of IBS data for ARS1 19:13,575,349–13,629,669.
Sheep and lower coverage Nubiana1, Caucasus1 are removed.
Figure 3—figure supplement 19
Clustered heatmap of IBS data for ARS1 29:4,557,144–4,627,040.
Sheep and lower coverage Nubiana1, Caucasus1 are removed.
Figure 3—figure supplement 20
Clustered heatmap of IBS data for ARS1 29:46,175,547–46,301,705.
Sheep and lower coverage Nubiana1, Caucasus1 are removed.
Figure 3—figure supplement 21
NJ trees of IBS data of introgressed regions, tranche 1.
Outgroups (Sheep) are not shown.
Figure 3—figure supplement 22
NJ trees of IBS data of introgressed regions, tranche 2.
Outgroups (Sheep) are not shown.
Tables
Table 1
Sample provenance and sequencing summary.
| Sample | Morphological Species | Origin | Age | Sex† | Nuclear Cov. ‡ | mtDNA Cov. |
|---|---|---|---|---|---|---|
| Direkli4 | Capra spc. | E4/8 A, Direkli Cave, Turkey | 12,164–11,864 cal BCE (2σ) | M | 2.59 | 642.23 |
| Direkli9 | Capra spc. | B6/5, Direkli Cave, Turkey | Est. 12,100–8,900 BCE* | M | 0.0003 | 9.5 |
| Direkli12 | Capra spc. | B13/4 A, Direkli Cave, Turkey | Est. 12,100–8,900 BCE | M | 0.07 | 44.06 |
| Direki13 | Capra spc. | B13/7B, Direkli Cave, Turkey | Est. 12,100–8,900 BCE | M | 0.0055 | 76.99 |
| Direkli14 | Capra spc. | D3/7, Direkli Cave, Turkey | Est. 12,100–8,900 BCE | M | 0.0005 | 13.24 |
| Direkli15 | Capra spc. | B6/5, Direkli Cave, Turkey | Est. 12,100–8,900 BCE | F | 0.0002 | 24.21 |
| Direkli16 | Capra spc. | B8/7, Direkli Cave, Turkey | Est. 12,100–8,900 BCE | F | 0.01 | 15.11 |
| Direkli17 | Capra spc. | E5/5, Direkli Cave, Turkey | Est. 12,100–8,900 BCE | F | 0.0001 | 0.0845 |
| Caucasus1 | Capra caucasica | Tamara Fort, Kazbegi, Georgia | 4th-21st c. CE, probably 5th-15th c. CE | M | 0.55 | 64.63 |
| Caucasus2 | Capra caucasica | Tamara Fort, Kazbegi, Georgia | 4th-21st c. CE, probably 5th-15th c. CE | M | 0.0021 | 379.71 |
| Caucasus3 | Capra caucasica | Tamara Fort, Kazbegi, Georgia | 4th-21st c. CE, probably 5th-15th c. CE | M | 0.004 | 464.51 |
| Falconeri1 | Capra falconeri hepteneri § | Unknown, via Parc de la Haute-Touche | 20th Century CE | M | 0.58 | 72.11 |
| Falconeri2 | Capra falconeri | Born at MNHN Zoo, Paris | 20th Century CE | M | 0.06 | 45.78 |
| Ibex1 | Capra ibex | Unknown | 20th Century CE | F | 3.93 | 179.03 |
| Ibex2 | Capra ibex | Pointe de Calabre, Savoie | 20th Century CE | M | 0.05 | 21.4 |
| Sibirica1 | Capra sibirica | Born at MNHN Zoo, Paris | 20th Century CE | M | 0.04 | 163.16 |
| Sibirica2 | Capra sibirica | Born at MNHN Zoo, Paris | 20th Century CE | F | 1.48 | 205.78 |
| Tur2 | Capra cylindricornis | Unknown, via Vincennes Zoo | 20th Century CE | F | 0.02 | 4.96 |
| Walie1 | Capra walie | Born at MNHN Zoo, Paris | 20th Century CE | M | 0.75 | 103.12 |
| Pyrenaica2 | Capra pyrenaica | Unknown | 20th Century CE | M | 0.16 | 51.2 |
| Nubiana1 | Capra nubiana | Unknown | 20th Century CE | M | 1.25 | 211.32 |
-
*
Estimated ages for Direkli material is based on calibrated ages from the cave stratigraphy.
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†
M=Male, F=Female.
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‡
Cov. = coverage.
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§
Falconeri1, a likely Barbary sheep (see Materials and methods).
Additional files
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Supplementary file 1
Additional data tables.
(A) Sample information. (B) Bias of D statistic tests involving Direkli4. (C) Published samples used in the present study. (D) Sample sequencing statistics. (E) Direkli1-2 (bezoar)-Direkli4 (tur-like) relative affinity measured using D(Direkli1-2, Direkli4; X, Sheep). (F) Published mtDNA sequences included in ML phylogeny. (G) Direkli4-Abdul4 relative affinity measured using D(X, Abdul4; Direkli4, Sheep). (H) Ganjdareh3-Direkli4 relative affinity measured using D(X, Ganjdareh3; Direkli4, Sheep). (I) Direkli4-Tur1 (west Caucasian tur) relative affinity measured using D(Direkli4, Tur1; X, Sheep). (J) Extended D statistic, Direkli4 set as H3 (“Direkli4-specific alleles”). (L) Extended D statistic, Direkli4 set as H3, sheep-ascertained. (M) Correlation of extended D values. (N) Extended D values, rotating H3 among different wild Capra genomes.
- https://cdn.elifesciences.org/articles/82984/elife-82984-supp1-v1.xlsx
-
Transparent reporting form
- https://cdn.elifesciences.org/articles/82984/elife-82984-transrepform1-v1.pdf
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A novel lineage of the Capra genus discovered in the Taurus Mountains of Turkey using ancient genomics
eLife 11:e82984.
https://doi.org/10.7554/eLife.82984
