Genomic signatures of ancient rendezvous and separation in elephant evolution

Evidence from various levels of the tree of life is showing that we’ve been picturing ancient encounters between related species all wrong and admixture events are probably more common than expected. Even rendezvous among primates, caniforms, and majestic proboscideans often turned from afternoon tea to a wild party, and the outcomes are clearly written in the genetic code.
Or maybe not so clearly. Only now, with complete nuclear genomes, we are beginning to understand the extent of admixture in evolutionary history.
Obviously, great excitement was provoked by the discoveries of Neanderthal introgression into modern humans (Green et al. 2010), as well as by admixture in our primate relatives, chimpanzees and bonobos (de Manuel et al. 2016). However, analyses of admixture in non-primate species also revealed intriguing patterns.
The ancestry of two species of North American wolves, representing admixture between grey wolves and coyotes (vonHoldt et al. 2016), has been stirring up questions about how admixed species should be treated in conservation policies. The admixed populations might play an important role in changing environments, for example in times of rapid climate change. This was likely the case with polar bear admixture into brown bears, which seems to be linked with climate fluctuations at the end of the last ice age (Cahill et al. 2018).

“Thus admixture resulting from climate-related habitat redistribution is likely to have long-term and widespread evolutionary consequences, and may be an important mechanism for generating and maintaining diversity.” (Cahill et al. 2018)

Admixture and isolation in elephants and their relatives

Now proboscideans joined the party and a new study by Palkopoulou et al. (2018) showed that “both gene flow and isolation have been central in the evolution of elephantids”.
Palkopoulou and colleagues generated new high-coverage genomes for the Asian elephant, African savanna and forest elephants, and low- to medium-coverage genomes for the woolly mammoth, American mastodon, and Columbian mammoth. Moreover, they generated first data, including one low-coverage and one 15X-coverage genome, of the straight-tusked elephant (Palaeoloxodon antiquus), which lived ~120,000 years ago in Europe.

Already last June, the research team published a mitogenome paper (Meyer et al. 2017) heralding the arrival of a big proboscidean study. Based on the mitogenomes, the researchers surprisingly concluded that the straight-tusked elephant, which was assumed to be most closely related to the Asian elephant, is actually closer to African forest elephants.

Straight-tusked elephant: A genomic composite

As usual, the complete nuclear genome showed something rather different. The authors concluded that a simple phylogenetic tree does not capture the relationships fully, and instead they used a fitted admixture graph that incorporates gene flow. And they found that rather than being a sister lineage to forest elephants, the straight-tusked elephant is a composite of three components: lineages ancestral to African elephants, woolly mammoths, and extant forest elephants.
While the largest genetic component was derived from a basal African elephant lineage, almost 40% of its ancestry originated from (a lineage related to) forest elephants, explaining why a simple neighbor-joinging tree places them together. On the other hand, a 6 to 10% introgression from a lineage related to mammoths, early after their split from the Asian elephant, would explain the morphological similarities.
The straight-tusked elephant seems to have split from the common ancestor with the African elephant lineage about at the same time as is the split of mammoths and the Asian elephant, probably somewhere on the higher end of the ~2 to 6 million-year range.

Separate households of savanna and forest elephants

What is also interesting about this study is the contrasting story of savanna and forest elephants, and their lack of admixture. There has been an ongoing debate about the relationship and systematic position of these two types of African elephants. For almost 20 years, scientists had evidence based on DNA indicating that they represent separate lineages. However, hybridization is well-documented in areas where they meet, and not only the hybrids survive, but they are also fertile (Mondol et al. 2015).

Using D-statistics to analyze two savanna and two forest elephants, Palkopoulou and colleagues found that the pairs of elephants are mutually symmetrically related, meaning that their genomes show no evidence of admixture after their lineages split approximately 609,000 years ago.
In other words, even though savanna and forest elephants hybridize in the contact zone, this hybridization does not affect the genomic make-up beyond its borders. And this might be precisely the piece of evidence that shifts the weights in favor of officially accepting two species of elephants in Africa. In turn, this has profound consequences for conservation because it matters whether there are 400,000 African elephants, or 300,000 savanna and 100,000 forest elephants left.
And the best way to conclude this post is with a quote by Palkopoulou for Tech Times that I very much liked:

“I hope that this study can create an appreciation for the rich evolutionary history of elephants and emphasize the need for protecting the only three elephant species that still walk the planet today, who are all under imminent risk of extinction from poaching and habitat loss.”

References
Cahill JA, Heintzman PD, Harris K, et al. (2018) Genomic evidence of widespread admixture from polar bears into brown bears during the last ice age. Molecular Biology and Evolution, msy018. DOI: https://doi.org/10.1093/molbev/msy018
de Manuel M, Kuhlwilm M, Frandsen P, et al. (2016) Chimpanzee genomic diversity reveals ancient admixture with bonobos. Science 354, 477-481. DOI: 10.1126/science.aag2602
Green RE, Krause J, Briggs AW, et al. (2010) A Draft Sequence of the Neandertal Genome. Science 328, 710-722. DOI: 10.1126/science.1188021
Meyer M, Palkopoulou E, Baleka S, et al. (2017) Palaeogenomes of Eurasian straight-tusked elephants challenge the current view of elephant evolution. Elife 6. DOI: 10.7554/eLife.25413
Mondol S, Moltke I, Hart J, et al. (2015) New evidence for hybrid zones of forest and savanna elephants in Central and West Africa. Molecular Ecology 24, 6134-6147. DOI: 10.1111/mec.13472
Palkopoulou E, Lipson M, Mallick S, et al. (2018) A comprehensive genomic history of extinct and living elephants. Proceedings of the National Academy of Sciences. DOI: https://doi.org/10.1073/pnas.1720554115
vonHoldt BM, Cahill JA, Fan ZX, et al. (2016) Whole-genome sequence analysis shows that two endemic species of North American wolf are admixtures of the coyote and gray wolf. Science Advances 2, no. 7, e1501714. DOI: 10.1126/sciadv.1501714.