Phylogeography of the woolly mammoth (Mammuthus primigenius) in the Minusinsk Depression of southern Siberia in the Late Pleistocene
https://doi.org/10.18699/vjgb-24-63
Abstract
To date, a number of studies have been published on the phylogenetics of woolly mammoths (Mammuthus primigenius), ranging from analyses of parts of the mitochondrial genome to studies of complete nuclear genomes. However, until recently nothing was known about the genetic diversity of woolly mammoths in southern Siberia, in the Minusinsk Depression in particular. Within the framework of this effort, libraries for high-throughput sequencing of seven bone samples of woolly mammoths were obtained, two-round enrichment using biotinylated probes of modern mtDNA of Elephas maximus immobilised on magnetic microspheres and sequencing with subsequent bioinformatic analysis were carried out. Phylogenetic reconstructions showed the presence of all studied mammoths in clade I, which expanded its range. The assignment of mammoth mitotypes in the Minusinsk Depression to different clusters within clade I may indicate a sufficiently high diversity of their gene pool. Phylogeographic reconstructions revealed a genetic proximity of mitochondrial lineages of Late Pleistocene mammoths of the Minusinsk Depression and other regions of eastern Siberia and estimated their divergence time in the range of 100–150 thousand years ago, which indicates active migrations of woolly mammoths over vast territories of eastern Siberia in the late Middle Pleistoceneearly Late Pleistocene.
About the Authors
S. A. ModinaRussian Federation
Novosibirsk
M. A. Kusliy
Russian Federation
Novosibirsk
D. G. Malikov
Russian Federation
Novosibirsk
A. S. Molodtseva
Russian Federation
Novosibirsk
References
1. Barnes I., Shapiro B., Lister A., Kuznetsova T., Sher A., Guthrie D., Thomas M. Genetic structure and extinction of the woolly mammoth, Mammuthus primigenius. Curr. Biol. 2007;17(12):1072-1075. DOI 10.1016/j.cub.2007.05.035
2. Briggs A.W., Good J.M., Green R.E., Krause J., Maricic T., Stenzel U., Lalueza-Fox C., Rudan P., Brajkovic D., Kucan Z., Gusic I., Schmitz R., Doronichev V.B., Golovanova L.V., Rasilla M., For-tea J., Rosas A., Paabo S. Targeted retrieval and analysis of five neandertal MtDNA genomes. Science. 2009;325(5938):318-321. DOI 10.1126/science.1174462
3. Brotherton P., Endicott P., Sanchez J.J., Beaumont M., Barnett R., Austin J., Cooper A. Novel high-resolution characterization of ancient DNA reveals C > U-type base modification events as the sole cause of post mortem miscoding lesions. Nucleic Acids Res. 2007;35(17): 5717-5128. DOI 10.1093/nar/gkm588
4. Capelli C., MacPhee R.D.E., Roca A.L., Brisighelli F., Georgiadis N., O’Brien S.J., Greenwood A.D. A nuclear DNA phylogeny of the woolly mammoth (Mammuthus primigenius). Mol. Phylogen. Evol. 2006;40(2):620-627. DOI 10.1016/j.ympev.2006.03.015
5. Carpenter M.L., Buenrostro J.D., Valdiosera C., Schroeder H., Allentoft M.E., Sikora M., Rasmussen M., Gravel S., Guillén S., Nekhrizov G., Leshtakov K., Dimitrova D., Theodossiev N., Pettener D., Luiselli D., Sandoval K., Moreno-Estrada A., Li Y., Wang J., Gilbert M.T.P., Willerslev E., Greenleaf W.J., Bustamante C.D. Pulling out the 1 %: whole-genome capture for the targeted enrichment of ancient DNA sequencing libraries. Am. J. Hum. Genet. 2013;93(5): 852-864. DOI 10.1016/j.ajhg.2013.10.002
6. Dabney J., Knapp M., Glocke I., Gansauge M.T., Weihmann A., Nickel B., Valdiosera C., Garcia N., Paabo S., Arsuaga J.L., Meyer M. Complete mitochondrial genome sequence of a middle pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc. Natl. Acad. Sci. USA. 2013;110(39):15758-15763. DOI 10.1073/pnas.1314445110
7. Debruyne R., Chu G., King C.E., Bos K., Kuch M., Schwarz C., Szpak P., Gröcke D.R., Matheus P., Zazula G., Guthrie D., Froese D., Buigues B., Marliave C., Flemming C., Poinar D., Fisher D., Southon J., Tikhonov A.N., MacPhee R.D.E., Poinar H.N. Out of America: ancient DNA evidence for a new world origin of late quaternary woolly mammoths. Curr. Biol. 2008;18(17):1320-1326. DOI 10.1016/j.cub.2008.07.061
8. Gilbert M.T.P., Tomsho L.P., Rendulic S., Packard M., Drautz D.I., Sher A., Tikhonov A., Dalen L., Kuznetsova T., Kosintsev P., Campos P.F., Higham T., Collins M.J., Wilson A.S., Shidlovskiy F., Buigues B., Ericson P.G.P., Germonpre M., Gotherstrom A., Iacumin P., Nikolaev V., Nowak-Kemp M., Willerslev E., Knight J.R., Irzyk G.P., Perbost C.S., Fredrikson K.M., Harkins T.T., Sheridan S., Miller W., Schuster S.C. Whole-genome shotgun sequencing of mitochondria from ancient hair shafts. Science. 2007;317(5846):1927-1930. DOI 10.1126/science.1146971
9. Greenwood A.D., Capelli С., Possnert G., Paabo S. Nuclear DNA sequences from late Pleistocene megafauna. Mol. Biol. Evol. 1999; 16(11):1466-1473. DOI 10.1093/oxfordjournals.molbev.a026058
10. Horn S. Target enrichment via DNA hybridization capture. In: Shapiro B., Hofreiter M. (Eds.) Ancient DNA. Methods in molecular biology. Vol. 840. Humana Press, 2012;177-188. DOI 10.1007/978-1-61779-516-9_21
11. Krause J., Dear P.H., Pollack J.L., Slatkin M., Spriggs H., Barnes I., Lister A.M., Ebersberger I., Pääbo S., Hofreiter M. Multiplex amplification of the mammoth mitochondrial genome and the evolution of elephantidae. Nature. 2006;439(7077):724-727. DOI 10.1038/nature04432
12. Kusliy M.A., Vorobieva N.V., Tishkin A.A., Makunin A.I., Druzhkova A.S., Trifonov V.A., Iderkhangai T.O., Graphodatsky A.S. Traces of Late Bronze and Early Iron age Mongolian horse mitochondrial lineages in modern populations. Genes. 2021;12(3):412. DOI 10.3390/genes12030412
13. Malikov D.G. Large Mammals of the Middle-Late Neopleistocene of the Minusinsk Depression, Stratigraphic Significance and Palaeozoogeography. Cand. geol. and mineral. sci. diss. Tomsk, 2015 (in Russian)
14. Malikov D.G., Svyatko S.V., Pyryaev A.N., Kolobova K.A., Ovchinnikov I.Yu., Malikova E.L. New data on the distribution and isotopic characteristics of woolly mammoth remains, Mammuthus primigenius (Proboscidea, Elephantidae), in the Late Pleistocene of the Minusinsk Depression (South Siberia). Zoologičeskij Žurnal = Journal of Zoology. 2023;102(8):924-938. DOI 10.31857/S004451342308007X (in Russian)
15. Maricic T., Whitten M., Pääbo S. Multiplexed DNA sequence capture of mitochondrial genomes using PCR products. PLoS One. 2010; 5(11):e14004. DOI 10.1371/journal.pone.0014004
16. Maschenko E.N., Potapova O.R., Vershinina A., Shapiro B., Streletskaya I.D., Vasiliev A.A., Oblogov G.E., Kharlamova A.S., Potapov E., Plicht J., Tikhonov A.N., Serdyuk N.V., Tarasenko K.K. The Zhenya mammoth (Mammuthus primigenius (Blum.)): taphonomy, geology, age, morphology and ancient DNA of a 48,000 year old frozen mummy from western Taimyr, Russia. Quat. Int. 2007;445: 104-134. DOI 10.1016/j.quaint.2017.06.055
17. Meyer M., Kircher M. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb. Protoc. 2010;2010(6):pdb.prot5448-pdb.prot5448
18. Miller W., Drautz D.I., Ratan A., Pusey B., Qi J., Lesk A.M., Tomsho L.P., Packard M.D., Zhao F., Sher A., Tikhonov A., Raney B., Patterson N., Lindblad-Toh K., Lander E.S., Knight J.R., Irzyk G.P., Fredrikson K.M., Harkins T.T., Sheridan S., Pringle T., Schuster S.C. Sequencing the nuclear genome of the extinct woolly mammoth. Nature. 2008;456(7220):387-390. DOI 10.1101/pdb.prot5448
19. Nasimovich A.A. African Elephant. Moscow: Nauka Publ., 1975 (in Russian)
20. Pääbo S., Poinar H., Serre D., Jaenicke-Despres V., Hebler J., Rohland N., Kuch M., Krause J., Vigilant L., Hofreiter M. Genetic analyses from ancient DNA. Annu. Rev. Genet. 2004;38:645-679. DOI 10.1146/annurev.genet.37.110801.143214
21. Palkopouloue E., Mallick S., Skoglund P., Enk J., Rohland N., Li H., Omrak A., Vartanyan S., Poinar H., Götherström A., Reich D., Dalén L. Complete genomes reveal signatures of demographic and genetic declines in the woolly mammoth. Curr. Biol. 2015;25(10): 1395-1400. DOI 10.1016/j.cub.2015.04.007
22. Payne J.L., Finnegan S. The effect of geographic range on extinction risk during background and mass extinction. Proc. Natl. Acad. Sci. USA. 2007;104(25):10506-10511. DOI 10.1073/pnas.0701257104
23. Poinar H.N., Schwarz C., Qi J., Shapiro B., MacPhee R.D.E., Buigues B., Tikhonov A., Huson D.H., Tomsho L.P., Auch A., Rampp M., Miller W., Schuster S.C. Metagenomics to paleogenomics: large-scale sequencing of mammoth DNA. Science. 2006;311(5759):392-394. DOI 10.1126/science.1123360
24. Reich D., Green R.E., Kircher M., Krause J., Patterson N., Durand E.Y., Viola B., Briggs A.W., Stenzel U., Johnson P.L.F., Maricic T., Good J.M., Marques-Bonet T., Alkan C., Fu Q., Mallick S., Li H., Meyer M., Eichler E.E., Stoneking M., Richards M., Talamo S., Shunkov M.V., Derevianko A.P., Hublin J.J., Kelso J., Slatkin M., Pääbo S. Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature. 2010;468(7327):1053-1060. DOI 10.1038/nature09710
25. Rogaev E.I., Moliaka Y.K., Malyarchuk B.A., Kondrashov F.A., Derenko M.V., Chumakov I., Grigorenko A.P. Complete mitochondrial genome and phylogeny of pleistocene mammoth Mammuthus primigenius. PLoS Biol. 2006;4(3):e73. DOI 10.1371/journal.pbio.0040073
26. Thalmann O., Shapiro B., Cui P., Schuenemann V.J., Sawyer S.K., Greenfield D.L., Germonpré M.B., Sablin M.V., López-Giráldez F., Domingo-Roura X., Napierala H., Uerpmann H.P., Loponte D.M., Acosta A.A., Giemsch L., Schmitz R.W., Worthington B., Buikstra J.E., Druzhkova A.S., Graphodatsky A.S., Ovodov N.D., Wahlberg N., Freedman A.H., Schweizer R.M., Koepfli K.P., Leonard J.A., Meyer M., Krause J., Pääbo S., Green R.E., Wayne R.K. Complete mitochondrial genomes of ancient canids suggest a European origin of domestic dogs. Science. 2013;342(6160):871-874. DOI 10.1126/science.1243650
27. Van der Valk T., Pečnerová P., Díez-del-Molino D., Bergström A., Oppenheimer J., Hartmann S., Xenikoudakis G., Thomas J.A., Dehasque M., Sağlıcan E., Fidan F.R., Barnes I., Liu S., Somel M., Heintzman P.D., Nikolskiy P., Shapiro B., Skoglund P., Hofreiter M., Lister A.M., Götherström A., Dalén L. Million-year-old DNA sheds light on the genomic history of mammoths. Nature. 2021; 591(7849):265-269. DOI 10.1038/s41586-021-03224-9
28. Vorobieva N.V., Makunin A.I., Druzhkova A.S., Kusliy M.A., Trifonov V.A., Popova K.O., Polosmak N.V., Molodin V.I., Vasiliev S.K., Shunkov M.V., Graphodatsky A.S. High genetic diversity of ancient horses from the Ukok Plateau. Plos One. 2020;15(11):e0241997. DOI 10.1371/journal.pone.0241997
29. Vorontsov A.A. Regularities of the formation of volcanics of the Minusinsk Basin in the Devonian (according to geological and isotopic-geochemical data). In: Proceedings of the All-Russia Meeting “Modern Problems of Geochemistry”. Irkutsk, 2012;36-39 (in Russian)
30. Wall J., Wittemyer G., Klinkenberg B., LeMay V., Douglas-Hamilton I. Characterizing properties and drivers of long distance movements by elephants (Loxodonta africana) in the Gourma, Mali. Biol. Conserv. 2013;157:60-68. DOI 10.1016/j.biocon.2012.07.019
31. Yang H., Golenberg E.M., Shoshani J. Phylogenetic resolution within the Elephantidae using fossil DNA sequence from the American mastodon (Mammut americanum) as an outgroup. Proc. Natl. Acad. Sci. USA. 1996;93(3):1190-1194. DOI 10.1073/pnas.93.3.1190