Camelus knoblochi genome reveals the complex evolutionary history of Old World camels

Extant Old World camels (genus Camelus) contributed to the economic and cultural exchanges between the East and West for thousands of years. 1 Almathen F. Charruau P. Mohandesan E. Mwacharo J.M. Orozco-terWengel P. Pitt D. Abdussamad A.M. Uerpmann M. Uerpmann H.P. de Cupere B. et al. Ancient and modern DNA reveal dynamics of domestication and cross-continental dispersal of the dromedary. Proc. Natl. Acad. Sci. USA. 2016; 113: 6707-6712https://doi.org/10.1073/pnas.1519508113 Crossref PubMed Scopus (102) Google Scholar ,2 Ming L. Yuan L. Yi L. Ding G. Hasi S. Chen G. Jambl T. Hedayat-Evright N. Batmunkh M. Badmaevna G.K. et al. Whole-genome sequencing of 128 camels across Asia reveals origin and migration of domestic Bactrian camels. Commun. Biol. 2020; 3: 1https://doi.org/10.1038/s42003-019-0734-6 Crossref PubMed Scopus (54) Google Scholar Although many remains have been unearthed, 3 Peters J. von den Driesh A. The two-humped camel (Camelus bactrianus): new light on its distribution, management and medical treatment in the past. J. Zool. 1997; 242: 651-679https://doi.org/10.1111/j.1469-7998.1997.tb05819.x Crossref Scopus (47) Google Scholar ,4 Cakırlar C. Berthon R. Caravans, camel wrestling and cowrie shells: towards a social zooarchaeology of camel hybridization in anatolia and adjacent regions. Anthropozoologica. 2014; 49: 237-252https://doi.org/10.5252/az2014n2a06 Crossref Scopus (12) Google Scholar ,5 Berthon R. Mashkour M. Burger P. Cakırlar C. Domestication, diffusion and hybridization of the Bactrian camel. 2020 Crossref Google Scholar we know neither whether the prevalent hybridization observed between extant Camelus species 2 Ming L. Yuan L. Yi L. Ding G. Hasi S. Chen G. Jambl T. Hedayat-Evright N. Batmunkh M. Badmaevna G.K. et al. Whole-genome sequencing of 128 camels across Asia reveals origin and migration of domestic Bactrian camels. Commun. Biol. 2020; 3: 1https://doi.org/10.1038/s42003-019-0734-6 Crossref PubMed Scopus (54) Google Scholar ,6 Burger P.A. The history of Old World camelids in the light of molecular genetics. Trop. Anim. Health Prod. 2016; 48: 905-913https://doi.org/10.1007/s11250-016-1032-7 Crossref PubMed Scopus (47) Google Scholar ,7 Felkel S. Wallner B. Chuluunbat B. Yadamsuren A. Faye B. Brem G. Walzer C. Burger P.A. A first Y-chromosomal haplotype network to investigate male-driven population dynamics in domestic and wild Bactrian camels. Front. Genet. 2019; 10: 423https://doi.org/10.3389/fgene.2019.00423 Crossref PubMed Scopus (12) Google Scholar also occurred between extinct lineages and the ancestors of extant Camelus species nor why some populations became extinct while others survived. To investigate these questions, we generated paleogenomic and stable isotope data from an extinct two-humped camel species, Camelus knoblochi. We find that in the mitochondrial phylogeny, all C. knoblochi form a paraphyletic group that nests within the diversity of modern, wild two-humped camels (Camelus ferus). In contrast, they are clearly distinguished from both wild and domesticated (Camelus bactrianus) two-humped camels on the nuclear level. Moreover, the divergence pattern of the three camel species approximates a trifurcation, because the most common topology is only slightly more frequent than the two other possible topologies. This mito-nuclear phylogenetic discordance likely arose due to interspecific gene flow between all three species, suggesting that interspecific hybridization is not exclusive to modern camels but a recurrent phenomenon throughout the evolutionary history of the genus Camelus. These results suggest that the genomic complexity of Old World camels' evolutionary history is underestimated when considering data from only modern species. Finally, we find that C. knoblochi populations began declining prior to the last glacial maximum and, by integrating palaeoecological evidence and stable isotope data, suggest that this was likely due to failure to adapt to a changing environment.