Complete Columbian mammoth mitogenome suggests interbreeding with woolly mammoths

BackgroundLate Pleistocene North America hosted at least two divergent and ecologically distinct species of mammoth: the periglacial woolly mammoth (Mammuthus primigenius) and the subglacial Columbian mammoth (Mammuthus columbi). To date, mammoth genetic research has been entirely restricted to woolly mammoths, rendering their genetic evolution difficult to contextualize within broader Pleistocene paleoecology and biogeography. Here, we take an interspecific approach to clarifying mammoth phylogeny by targeting Columbian mammoth remains for mitogenomic sequencing.ResultsWe sequenced the first complete mitochondrial genome of a classic Columbian mammoth, as well as the first complete mitochondrial genome of a North American woolly mammoth. Somewhat contrary to conventional paleontological models, which posit that the two species were highly divergent, the M. columbi mitogenome we obtained falls securely within a subclade of endemic North American M. primigenius.ConclusionsThough limited, our data suggest that the two species interbred at some point in their evolutionary histories. One potential explanation is that woolly mammoth haplotypes entered Columbian mammoth populations via introgression at subglacial ecotones, a scenario with compelling parallels in extant elephants and consistent with certain regional paleontological observations. This highlights the need for multi-genomic data to sufficiently characterize mammoth evolutionary history. Our results demonstrate that the use of next-generation sequencing technologies holds promise in obtaining such data, even from non-cave, non-permafrost Pleistocene depositional contexts.

[1]  A. Lister,et al.  The pattern and process of mammoth evolution in Eurasia , 2005 .

[2]  Adrian W. Briggs,et al.  Analysis of one million base pairs of Neanderthal DNA , 2006, Nature.

[3]  S. O’Brien,et al.  Patterns of molecular genetic variation among African elephant populations , 2002, Molecular ecology.

[4]  Alexander F. Auch,et al.  Metagenomics to Paleogenomics: Large-Scale Sequencing of Mammoth DNA , 2006, Science.

[5]  R. Sukumar,et al.  Social organization of the Asian elephant (Elephas maximus) in southern India inferred from microsatellite DNA , 2005, Journal of Ethology.

[6]  M. Slatkin,et al.  Proboscidean Mitogenomics: Chronology and Mode of Elephant Evolution Using Mastodon as Outgroup , 2007, PLoS biology.

[7]  M. Hofreiter,et al.  Next Generation Sequencing of Ancient DNA: Requirements, Strategies and Perspectives , 2010, Genes.

[8]  C. Groves,et al.  Do Loxodonta cyclotis and L. africana interbreed , 2000 .

[9]  P. Tassy,et al.  The Proboscidea : evolution and palaeoecology of elephants and their relatives , 1996 .

[10]  D. Madsen,et al.  The Columbian mammoth, Mammuthus columbi, from the Wasatch Mountains of central Utah , 1993, Journal of Paleontology.

[11]  F. Allendorf,et al.  The problems with hybrids: setting conservation guidelines , 2001 .

[12]  M. Naresh,et al.  Studies of collagen in bone and dentin matrix of a Columbian mammoth (late Pleistocene) of central Utah. , 1992, Matrix.

[13]  C. Harington Mammoths, Bison and Time in North America , 1984 .

[14]  A. Berta Pleistocene Mammals of North America , 1981 .

[15]  L. Agenbroad North American Proboscideans: Mammoths: The state of Knowledge, 2003 , 2005 .

[16]  A. Aubrey,et al.  New insights from old bones: DNA preservation and degradation in permafrost preserved mammoth remains , 2009, Nucleic acids research.

[17]  P. Arctander,et al.  Population genetic structure of the African elephant in Uganda based on variation at mitochondrial and nuclear loci: evidence for male‐biased gene flow , 1999, Molecular ecology.

[18]  Alice Dorottya Domokos BIOINFORMATICS AND COMPUTATIONAL BIOLOGY , 2008 .

[19]  V. J. Maglio Origin and evolution of the Elephantidae , 1973 .

[20]  Mike Walker,et al.  Quaternary Dating Methods , 2005 .

[21]  D. O’Rourke,et al.  Phylogeographic analysis of the mid-Holocene Mammoth from Qagnaxˆ Cave, St. Paul Island, Alaska , 2009 .

[22]  Aakrosh Ratan,et al.  Intraspecific phylogenetic analysis of Siberian woolly mammoths using complete mitochondrial genomes , 2008, Proceedings of the National Academy of Sciences.

[23]  S. Pääbo,et al.  Multiplexed DNA Sequence Capture of Mitochondrial Genomes Using PCR Products , 2010, PloS one.

[24]  S. Salzberg,et al.  Versatile and open software for comparing large genomes , 2004, Genome Biology.

[25]  W. Moore INFERRING PHYLOGENIES FROM mtDNA VARIATION: MITOCHONDRIAL‐GENE TREES VERSUS NUCLEAR‐GENE TREES , 1995, Evolution; international journal of organic evolution.

[26]  Alexei J Drummond,et al.  Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. , 2005, Molecular biology and evolution.

[27]  Adam M. Phillippy,et al.  Comparative genome assembly , 2004, Briefings Bioinform..

[28]  P. Tassy,et al.  Advances in proboscidean taxonomy & classification, anatomy & physiology, and ecology & behavior , 2005 .

[29]  A. Rambaut,et al.  BEAST: Bayesian evolutionary analysis by sampling trees , 2007, BMC Evolutionary Biology.

[30]  Ben Shneiderman,et al.  Hawkeye: an interactive visual analytics tool for genome assemblies , 2007, Genome Biology.

[31]  B. MacFadden,et al.  Calibration of mammoth (Mammuthus) dispersal into North America using rare earth elements of Plio-Pleistocene mammals from Florida , 2009, Quaternary Research.

[32]  B. Deagle,et al.  Quantification of damage in DNA recovered from highly degraded samples – a case study on DNA in faeces , 2006, Frontiers in Zoology.

[33]  K. Lidén,et al.  Temporal genetic change in the last remaining population of woolly mammoth , 2010, Proceedings of the Royal Society B: Biological Sciences.

[34]  M. Schatz,et al.  Genome assembly forensics: finding the elusive mis-assembly , 2008, Genome Biology.

[35]  S. Pääbo,et al.  Genetic analyses from ancient DNA. , 2004, Annual review of genetics.

[36]  Edward M. Rubin,et al.  Genomic Sequencing of Pleistocene Cave Bears , 2005, Science.

[37]  S. O’Brien,et al.  Cytonuclear genomic dissociation in African elephant species , 2005, Nature Genetics.

[38]  N. Georgiadis,et al.  Genetic Evidence for Two Species of Elephant in Africa , 2001, Science.

[39]  A. Lister,et al.  The Origin and Evolution of the Woolly Mammoth , 2001, Science.

[40]  Newton E. Morton,et al.  Génétique des populations humaines , 1975 .

[41]  D. Simberloff,et al.  Extinction by hybridization and introgression , 1996 .

[42]  Eric S. Lander,et al.  Sequencing the nuclear genome of the extinct woolly mammoth , 2008, Nature.

[43]  R. Sukumar,et al.  Range-wide mtDNA phylogeography yields insights into the origins of Asian elephants , 2009, Proceedings of the Royal Society B: Biological Sciences.

[44]  Ian Barnes,et al.  Multiplex amplification of the mammoth mitochondrial genome and the evolution of Elephantidae , 2006, Nature.

[45]  S. Salzberg,et al.  Phymm and PhymmBL: Metagenomic Phylogenetic Classification with Interpolated Markov Models , 2009, Nature Methods.

[46]  C. Groves,et al.  Living African elephants belong to two species: Loxodonta africana (Blumenbach, 1797) and Loxodonta cyclotis (Matschie, 1900) , 2000 .

[47]  D. Posada jModelTest: phylogenetic model averaging. , 2008, Molecular biology and evolution.

[48]  R. Macphee :Mammoths: Giants of the Ice Age. , 2008 .

[49]  H. Poinar,et al.  Time dependency of molecular rates in ancient DNA data sets, a sampling artifact? , 2009, Systematic biology.

[50]  J. Southon,et al.  Out of America: Ancient DNA Evidence for a New World Origin of Late Quaternary Woolly Mammoths , 2008, Current Biology.

[51]  Swapan Mallick,et al.  Genomic DNA Sequences from Mastodon and Woolly Mammoth Reveal Deep Speciation of Forest and Savanna Elephants , 2010, PLoS biology.

[52]  R. Debruyne A case study of apparent conflict between molecular phylogenies: the interrelationships of African elephants , 2005, Cladistics : the international journal of the Willi Hennig Society.

[53]  Mark George Thomas,et al.  Genetic Structure and Extinction of the Woolly Mammoth, Mammuthus primigenius , 2007, Current Biology.

[54]  Philip L. F. Johnson,et al.  Targeted Investigation of the Neandertal Genome by Array-Based Sequence Capture , 2010, Science.