Mitochondrial evidence of introgression among North American mammoths

Hendrik Poinar and colleagues have a new paper in Frontiers in Ecology and Evolution that reports new mitochondrial genomes from 67 North American mammoth specimens. These include specimens attributed to three mammoth species defined by paleontologists, the Columbian mammoth (Mammuthus columbi), the Jefferson mammoth (M. jeffersoni) and the pygmy mammoth (M. exilis), which they add to pre-existing data from permafrost-preserved woolly mammoths (M. primigenius). This dataset enabled them for the first time to generate a picture of the diversity of this ancient extinct lineage extending into temperate latitudes of North America.

Mammoth tooth detail
Mammoth tooth. Photo credit: James St. John CC-BY

What they found is that the mitochondrial clades exhibit many instances of non-correspondence with mammoth species as recognized by paleontologists. The paper’s discussion of mammoth phylogenetic hypotheses is extensive but a bit cloudy. The main issue is the relationship of Columbian and woolly mammoths. Columbian mammoths were endemic in North America and evolved sometime early in the Pleistocene. Woolly mammoths seem to have evolved relatively recently from the steppe mammoth M. trogontherii, inhabited northern parts of Siberia and Beringia, but reached south of the ice sheets in North America only within the past 125,000 years. After that time, they both coexisted in parts of North America.

Paleontologists have previously hypothesized hybridization between these mammoth species, looking both at skeletal and genetic evidence. Mammoth systematics has relied heavily upon molar morphology, and the number of lamellar plates of the molars is a main diagnostic criterion. Individual mammoths varied in the number of these enamel plates; Columbian mammoths had an average of 18-20 lamellar plates in their molars similar to steppe mammoths, while woolly mammoths tended to have more plates, at a higher density. The woolly mammoth morphology appeared first in Siberia and spread into Europe some 200,000 years ago. Some paleontologists had already suggested that Jefferson’s mammoth is an ecotype within the eastern United States that resulted from hybridization between Columbian and woolly mammoths.

An earlier mitochondrial study by Enk and colleagues (2011) found that two Columbian mammoths had mtDNA types that nest within the variability known for woolly mammoths, this despite the fact that Columbian mammoths were in North America long before the first woolly mammoths appeared in Eurasia. This finding seemed to point to a recent introgression of woolly mammoth mtDNA types into Columbian mammoth populations. What remained was the question of whether this introgression might represent a widespread replacement of Columbian mammoth mtDNA by the woolly mammoth haplogroup, or whether they had just sampled hybrids by chance.

The current study adds dozens of specimens of Columbian and Jefferson mammoths, and these form a fairly clear picture in comparison to the woolly mammoths. Woolly mammoths of Siberia and Beringia belong to three mtDNA clades, which share a common mtDNA ancestor sometime in the Early to Middle Pleistocene. Two of these are quite divergent and relatively rarely found within the sample studied here. One of the clades is very diverse and includes woolly mammoths from Siberia, Beringia, and North America south of the icen sheets. This clade, which the study denotes as “clade 1”, also includes the Columbian and Jefferson mammoths.

The figure from the paper that shows this phylogeny is large and complicated, too much to try to include here – it’s a whole page multi-pane figure with three distinct color schemes and legends describing them. It has geographic, phylogenetic and taxonomic information all mixed together, and while it is a great figure, it’s probably crying out for a better visualization method. So I’m leaving it out of this post.

There is structure within the mtDNA clade that includes both Columbian and woolly mammoths. The Columbian mammoths are all part of a single branch, and the sister of this branch includes mtDNA lineages mostly found in woolly mammoths of eastern North America, along with some Beringian woolly mammoths. Jefferson mammoths are scattered across both these branches. To the extent that the Jefferson mammoths are morphologically intermediate and suggestive of hybridization between woolly and Columbian mammoth populations, their highly diverse mtDNA suggests that they were likely the result of multiple introgression events. In the earlier paper by Eck and colleagues (2011), they compare this situation to forest and savanna African elephants, which have multiple instances of mtDNA introgression as well.

I’m never in favor of interpreting too much on the basis of the single mtDNA phylogeny. The paper agrees that nuclear DNA will be necessary to resolve how introgression and hybridization have really affected the mammoth populations.

That being said, the mtDNA in this case is provocative for more than the apparent mixing represented by the Jefferson mammoths. The mtDNA clade that includes both Columbian and some woolly mammoths seems younger than the origin of Columbian mammoths. The paper goes into substantial detail about why it is difficult to get accurate estimates of the time of mtDNA common ancestors, largely because the “tips” of the branches are separated in part by slightly deleterious mutations that would not persist over very much evolutionary time, so the deeper “roots” of the tree reflect a relatively slower rate of substitutions. But some problem remains even if the age of this clade is somewhat older than the rates suggested in this paper. The paper suggests two possible resolutions. Less likely, the authors propose that the Columbian mammoths had their mitochondrial genomes completely replaced by a woolly-mammoth-derived mtDNA clade sometime after the arrival of woolly mammoths

More likely, the authors propose that mtDNA introgression went the opposite direction, with woolly mammoths taking a North American clade and invading Eurasia with it. They support this by observing that mammoths carrying the clade 1 seem to have included the latest survivors in Eurasia, as if this successful lineage of mammoths had reinvaded and supplanted the earlier, more diverse mammoths belonging to clades 2 and 3. Possibly these woolly mammoths carried adaptive traits with origins in North America that helped them to spread; or maybe they simply exploited an opening left by the decline of woolly mammoths in Eurasia during the later part of the last Ice Age. It is even conceivable that the mtDNA itself was a target of selection, comparison to the phylogeography of nuclear loci would help to settle this.

This scenario is not quite as good a fit to the mtDNA phylogeny; it would require some incomplete lineage sorting to explain why Columbian mammoths are nested within the woolly mammoth clade 1 instead of having the most basal clade 1 subclade. But it fits within the evidence of dynamic replacement of mtDNA within the population of Eurasia.

And it raises interesting possibilities. Woolly mammoths originated from steppe mammoths by reducing body size, shortening the skull, and increasing the number and density of enamel plates in the molars. By the late Middle Pleistocene, they had supplanted steppe mammoths across Eurasia.

In North America, the Columbian mammoth was in many respects the ecological equivalent of the steppe mammoth; so much so that some paleontologists consider them a geographic continuation of the same species lineage. When woolly mammoths re-encountered this species in the Late Pleistocene, they evidently had no reproductive barrier and may have picked up many adaptive traits.

Poinar and colleagues consider what these scenarios mean for taxonomic practice within the mammoths:

Are columbi and primigenius still to be regarded as “good” species if they were capable of introgressing despite a possible million-year difference in their divergence times from trogontherii ancestors? Or is this lengthy difference illusory, because mammoths on both sides of the Bering Strait experienced dynamic population histories of immigrations, contractions, expansions, introgressions and replacements [13; 14; 18], a now well-established finding that throws into question traditional species designations. This point also applies to making assumptions about unidirectional change in morphological attributes, a highly unlikely proposition now that hybridization between supposedly long-separate lineages of North American mammoths has been adequately demonstrated.

From my point of view, all these estimates of timing of population separation and contact seem familiar. The establishment of the Columbian mammoth population in the Early to Middle Pleistocene ran along the same approximate timescale as the differentiation of African and Eurasian archaic human lineages, including the Neandertals and Denisovans. The introduction of woolly mammoths into North America occurred around the same time that modern humans may have been introduced to Asia. The back-migration of North American mtDNA lineages into Eurasian mammoths occurred around the same time that modern humans were dispersing into Australasia and northward into Siberia and Europe.

Reference

Poinar H, MacPhee R, Enk J, Devault A, Widga C, Saunders J, Szpak P, Southon J, Rouillard J-M, Shapiro B, Golding B, Zazula G, Froese D, Fisher D. Mammuthus Population Dynamics in Late Pleistocene North America: Divergence, Phylogeography and Introgression. Frontiers in Ecology and Evolution (in press) doi:10.3389/fevo.2016.00042

Enk, J., Devault, A., Debruyne, R., King, C. E., Treangen, T., O’Rourke, D., ... & Poinar, H. (2011). Complete Columbian mammoth mitogenome suggests interbreeding with woolly mammoths. Genome biology, 12(5), R51. doi:10.1186/gb-2011-12-5-r51