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Blue Turns to Gray: Paleogenomic Insights into the Evolutionary History and Extinction of the Blue Antelope (Hippotragus leucophaeus) - PubMed

  • ️Sat Jan 01 2022

Blue Turns to Gray: Paleogenomic Insights into the Evolutionary History and Extinction of the Blue Antelope (Hippotragus leucophaeus)

Elisabeth Hempel et al. Mol Biol Evol. 2022.

Abstract

The blue antelope (Hippotragus leucophaeus) is the only large African mammal species to have become extinct in historical times, yet no nuclear genomic information is available for this species. A recent study showed that many alleged blue antelope museum specimens are either roan (Hippotragus equinus) or sable (Hippotragus niger) antelopes, further reducing the possibilities for obtaining genomic information for this extinct species. While the blue antelope has a rich fossil record from South Africa, climatic conditions in the region are generally unfavorable to the preservation of ancient DNA. Nevertheless, we recovered two blue antelope draft genomes, one at 3.4× mean coverage from a historical specimen (∼200 years old) and one at 2.1× mean coverage from a fossil specimen dating to 9,800-9,300 cal years BP, making it currently the oldest paleogenome from Africa. Phylogenomic analyses show that blue and sable antelope are sister species, confirming previous mitogenomic results, and demonstrate ancient gene flow from roan into blue antelope. We show that blue antelope genomic diversity was much lower than in roan and sable antelope, indicative of a low population size since at least the early Holocene. This supports observations from the fossil record documenting major decreases in the abundance of blue antelope after the Pleistocene-Holocene transition. Finally, the persistence of this species throughout the Holocene despite low population size suggests that colonial-era human impact was likely the decisive factor in the blue antelope's extinction.

Keywords: Holocene; South Africa; ancient DNA; diversity; extinction; paleogenome.

© The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.

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Figures

<sc>Fig.</sc> 1.
Fig. 1.

Blue antelope distribution and specimens. (A) Historical distribution (light purple at the southern tip) and Quaternary fossil occurrences of blue antelope (Skead 1980; Kerley et al. 2009; modified from Avery 2019). Fossil sites: EBC = Elands Bay Cave, DK1 = Die Kelders Cave 1, BNK1 = Byneskranskop 1, BPA = Boomplaas Cave, NBC = Nelson Bay Cave, KRM1/1A = Klasies River Mouth 1/1A (base map:

https://www.naturalearthdata.com

, prepared in QGIS v2.18 [

https://qgis.org

]). (B) Historical mounted skin of a young male blue antelope (Hippotragus leucophaeus) from the Swedish Museum of Natural History, Stockholm, Sweden (NRM 590107); arrow indicates area sampled for aDNA extraction. (C) Fossil lower left deciduous fourth premolar (NBC RB4 D3) of a blue antelope from Nelson Bay Cave (curated at Iziko Museums of South Africa, Cape Town, South Africa); scale is one centimeter; arrows indicate areas sampled for aDNA extraction. Photo credits: NBC RB4 D3: J.T. Faith, courtesy: Archaeology Unit, Iziko Museums of South Africa; NRM 590107: Hempel, Bibi, et al. (2021).

<sc>Fig.</sc> 2.
Fig. 2.

Phylogenetic analysis. Dated phylogenetic tree computed using nuclear and mitochondrial data from the three Hippotragus species. The tree topology was inferred using a data set that excluded transition-only sites, under the multispecies coalescent model using ASTRAL v4.10 (Rabiee et al. 2019), whereas the timescale was inferred using MCMCtree v4.9 (dos Reis and Yang 2011). Node annotations below age credibility interval bars show the respective credibility interval's range in Ma, whereas the branch label shows support values (bootstrap, local posterior probability, gene concordance factor, and site-concordance factor). Branch support is calculated on an unrooted tree; in this case with four taxa, so the support is for the separation between two pairs of taxa as represented by that single internal branch. The scimitar-horned oryx was used as outgroup (Humble et al. 2020). Roan and sable antelope raw data are from Gonçalves et al. (2021) and Koepfli et al. (2019). Photo credits: NBC RB4 D3: J.T. Faith, courtesy: Archaeology Unit, Iziko Museums of South Africa; roan antelope: Charles J. Sharp, wikimedia commons, CC-BY 4.0; sable antelope: Paulmaz, wikimedia commons, CC-BY 3.0; scimitar-horned oryx: E. Hempel.

<sc>Fig.</sc> 3.
Fig. 3.

Gene flow analyses for the three Hippotragus species. (A) D values and Z-scores of D statistics for the fossil (NBC RB4 D3) and historical (NRM 590107) blue antelope specimens showing significant gene flow between blue and roan antelope demonstrated by positive D values; analysis performed with Dstat (transversions only version,

https://github.com/jacahill/Admixture

). A Z-score > |3| is regarded as significant. (B) Tested topology for D statistics according to the 20 kb sliding window multispecies coalescent and the neighbor joining phylogenies (fig. 2 and supplementary fig. S3, Supplementary Material online) with blue antelope in position 2. The green double arrow indicates gene flow between blue and roan antelope with unknown directionality. (C) Percentages of tree topologies in the 100 kb sliding window tree analysis. In every combination, more windows show a closer affinity between roan and blue antelope than between roan and sable antelope. Topologies in category “other” were so rare that they are not visible in the figure. Roan antelope: 10954, He108 (Gonçalves et al. 2021); sable antelope: SB2152, HN216 (Koepfli et al. 2019); blue antelope: NBC RB4 D3, NRM 590107. Photo credits: NBC RB4 D3: J.T. Faith, courtesy: Archaeology Unit, Iziko Museums of South Africa; NRM 590107: Hempel, Bibi, et al. (2021); roan antelope: Charles J. Sharp, wikimedia commons, CC-BY 4.0; sable antelope: Paulmaz, wikimedia commons, CC-BY 3.0; scimitar-horned oryx: E. Hempel.

<sc>Fig.</sc> 4.
Fig. 4.

Gene flow direction analysis. (A) Expected outcome of changes in genetic distances for gene flow (green arrow) from roan into blue antelope and blue into roan antelope. Dashed red lines illustrate the expected distances between roan and sable antelope. (B) Genetic distances between roan and sable antelope as a proportion of the tree length performed with WindowTrees v1.0.0 (

https://github.com/achimklittich/WindowTrees

). Photo credits: see fig. 3.

<sc>Fig.</sc> 5.
Fig. 5.

Nuclear diversity analysis. Species-wide nuclear diversity of the three Hippotragus species computed from pairwise comparisons (data normalized by dividing by the number of sites used in the analysis — 2,243,953 sites; genomes for heterozygosity subsampled to 4.26× mean coverage, the lowest mean coverage in the roan/sable antelope data set). Each dot represents a pairwise comparison. Lines represent means. Heterozygosity was not estimated for the blue antelope due to low coverage and aDNA damage. Photo credits: see fig. 3.

<sc>Fig.</sc> 6.
Fig. 6.

Species distribution and fossil sites. Historical distribution and Holocene and Pleistocene fossil sites of blue, sable, and roan antelope in southern Africa. The distributions of the roan and sable antelope further north are not shown (base map:

https://www.naturalearthdata.com

, prepared in QGIS v2.18 (

https://qgis.org

; du Plessis 1969; Kerley et al. 2009; modified from Avery 2019). Photo credits: see fig. 3.

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