Monday, 16 June 2014

Forest Elephants in the Republic of Congo. What Species Were We Observing?

Opportunities to see the animals of the central African rainforests do not come every day. So the privilege of being able to visit groups of lowland gorillas and observe the other mammals, birds, reptiles and amphibians in the Congo Basin is an experience of a lifetime. In the middle of May we were with a group of ten clients of Naturetrek in the camps in the Republic of Congo run by Wilderness Safaris, Ngaga and Lango, 340 miles from Brazzaville, both in or adjacent to the Odzala-Kokoua National Park.

Lango Camp (the word ‘camp’ should be in inverted commas) is situated with views from the raised deck of Lango bai. Watching the bai as animals turn up is a delight, especially in the early morning when large flocks of African Green Pigeons fly overhead and African Grey Parrots appear from the forest to eat mud churned up by the elephants and buffalo. And by elephants I mean Forest Elephants and by buffalo, Forest Buffalo. Later in the day, solitary Bushbuck appeared and, just after our arrival, a Sitatunga.

This video shows what we saw at Lango Camp.

Talking about Forest Elephants with our guides, Justine, Alon and Adam, and the differences between forest and savanna elephants I knew that over the last century there had been arguments to and fro as to whether the Forest Elephant was a different species from the African Elephant. All the more recent books seemed to repeat the view that there was only one species of Elephant in Africa. I was also vaguely aware that the Forest Buffalo was not considered to be a separate species and that, recently, the Bushbuck had been split by somebody into two species.

Because when I actually saw Forest Elephants for the first time in the flesh and could appreciate that morphologically they were very different from the elephants we had seen in other parts of Africa, I resolved to look up their status in more detail when we got back.

Behaviourally too the Forest Elephant is very different. The nocturnal shrieks and cries that kept us awake as elephants gathered further down the bai were very different from the silence or low grumblings of other elephants. My natural tendency as a ‘lumper’ to think of one species of elephant in Africa was being shaken to the core at 2.00 am.

To cut a long story short, I am now convinced by the evidence available that the Forest Elephant is a separate species, that named by Matschie in 1900 as Loxodonta cyclotis. But in reading the papers, I was struck by the strange reluctance of many to accept this conclusion. IUCN still lumps all the elephants in Africa as Loxodonta africana.

Leaving aside the morphological differences and questions of gene flow between Forest and Savanna or Bush Elephants for the moment, the arguments that have arisen in the past 15 years or so have centred on genetic differences in populations of elephants in Africa. Different results were obtained using mitochondrial DNA (mtDNA) compared to nuclear DNA (nDNA).

The use of nuclear DNA to determine the phylogeny of elephants has been championed by Alfred L Roca’s group at the University of Illinois at Urbana-Champaign. Their first work was published in 2001 and showed a clear distinction between Forest and Savanna elephants. However, the single-species-in-Africa view continued as more work using mitochondrial DNA showed a number of geographically based clades. Nevertheless, continuing work by Roca’s group on nuclear DNA demonstrated that Forest and Savanna elephants were different and that mitochondrial DNA does not provide information on which the phylogeny of these species can be determined. In short, mitochondrial DNA provides a historical record of only the maternal line and with the introgression of genes by early hybridisation between separating lines during speciation or by later hybridisation leading to some fertile offspring, the mitochondrial DNA may bear no relation to the nuclear DNA of the species as a whole. As one paper (Rohland, Reich, Mallick, Meyer, Green, Georgiadis, Roca & Hofreiter, 2010) puts it:
…mtDNA represents just a single locus in the genome and need not represent the true species phylogeny since a single gene tree can differ from the consensus species tree of the taxa in question. Generalizing about species relationships based on mtDNA alone is especially problematic for the Elephantidae because their core social groups (‘‘herds’’) are matrilocal, with females rarely, if ever, dispersing across groups. This results in mtDNA genealogies in both African and Asian elephants that exhibit deeper divergence and/or different phylogeographic patterns than the nuclear genome.
Further strengthening of the case for two species in Africa came from work comparing these two elephants with the Asian Elephant and the relatively recently extinct Woolly Mammoth and American Mastodon.  Rohland et al. (2010) reported (with my emphasis in bold characters):
We have used a combination of modern DNA sequencing and targeted PCR amplification to obtain a large data set for comparing American mastodon, woolly mammoth, Asian elephant, African savanna elephant, and African forest elephant. We unequivocally establish that the Asian elephant is the sister species to the woolly mammoth. A surprising finding from our study is that the divergence of African savanna and forest elephants—which some have argued to be two populations of the same species—is about as ancient as the divergence of Asian elephants and mammoths. Given their ancient divergence, we conclude that African savanna and forest elephants should be classified as two distinct species.
And then, on the two African species (with references deleted):
Our study also infers a strikingly deep population divergence time between forest and savanna elephant, supporting morphological and genetic studies that have classified forest and savanna elephants as distinct species. The finding of deep nuclear divergence is important in light of findings from mtDNA, which indicate that the F-haplogroup is shared between some forest and savanna elephants, implying a common maternal ancestor within the last half million years. The incongruent patterns between the nuclear genome and mtDNA (‘‘cytonuclear dissociation’’) have been hypothesized to be related to the matrilocal behavior of elephantids, whereby males disperse from core social groups (‘‘herds’’) but females do not. If forest elephant female herds experienced repeated waves of migration from dominant savanna bulls, displacing more and more of the nuclear gene pool in each wave, this could explain why today there are some savanna herds that have mtDNA that is characteristic of forest elephants but little or no trace of forest DNA in the nuclear genome. In the future, it may be possible to distinguish between models of a single ancient population split between forest and savanna elephants, or an even older split with longer drawn out gene flow, by applying methods like Isolation and Migration (IM) models to data sets including more individuals.

The problems inherent in using mitochondrial DNA have been stressed recently by Jerry Coyne in his blog, Why Evolution is True, in relation to the evolution of the Brown Bear and the Polar Bear in which conclusions drawn from mitochondrial DNA have been shown to confuse rather than illuminate. This is a screen grab from his blog:

This entry can be found at:

IUCN still persists in lumping all the elephants in Africa into one species. However, in a hard-hitting paragraph in the discussion of their paper, Ishida, Oleksyk, Georgiadis, David, Zhao, Stephens, Kolokotronis & Roca (2011) state the case clearly and why it is important for practical conservation:
“Mitochondrial essentialism” and the conservation of Africa's elephantsGiven that mtDNA haplotypes among elephants are an unreliable indicator of overall genetic similarity it is unfortunate that mtDNA alone continues to be used as a guide to elephant genealogical affinities. This “mitochondrial essentialism,” the continuing use of mtDNA to partition populations and species, among elephants where morphological and nuclear markers have established that mtDNA patterns may be inaccurate or misleading, might lead to adverse results for elephant conservation, as the following examples illustrate: If mtDNA data were used as the sole basis for elephant taxonomy and population structure, elephants in the Guinean forest block could be recommended for translocation to the deserts of Mali, on the grounds that their mtDNA similarity implies that they must be genetically similar. Likewise, relying on mtDNA to infer population structure would mean that savanna elephants from Tanzania could be moved west into the Congolian tropical forest, since forest and savanna elephants in these regions share similar F clade mtDNAs. Either of these translocations would be inappropriate, since even while carrying mtDNA from the same haplogroup, individuals in forest and savanna locations are very different in nuclear genotypes, belong to different species, and are thus unlikely to thrive when moved to the wrong habitats. Although the examples are extreme, it may be equally troublesome that mtDNA-based misinterpretations of African elephant taxonomy constitute an unacknowledged potential hindrance to their proper conservation by convincing conservation groups to “continue to treat African elephants as a single species”.
Although studies based solely on mitochondrial DNA appear to be useless in this and many other cases, there is a bonus as Roca and his colleagues have both pointed out and actually worked on: the use of both nuclear and mitochondrial genetic markers can more accurately determine the geographical source of poached ivory.

But now we come full circle. The Forest Elephant was described as a new species by Professor Dr (Georg Friedrich) Paul Matschie (1861-1926) in 1900. Unfortunately, Matschie, who somehow rose to be Director of the Berlin Museum in 1924, was treated as a joke by fellow professionals. An anti-Darwinian mystic, he described a new species or subspecies from pretty well every specimen that fell under his gaze. Mammalian taxonomy seems to have suffered mightily as a result of his activities. His antics and those of his protégé are described, unfortunately briefly, by Colin Groves and the late Peter Grubb in their book, Ungulate Taxonomy (Johns Hopkins University Press, 2011). The ultimate splitter caused a lumping backlash. (Groves and Grubb, incidentally were responsible for the morphological work that resurrected the two-species-in-Africa idea in 2000.) I have the suspicion that Matchie’s involvement in erecting Loxodonta cyclotis may have been one of the reasons why there was such opposition to the possibility of the existence of a separate Forest Elephant in the last century. So, sadly, it appears that Matschie, for once, was right. Maybe right for the wrong reasons but right.

For those wanting more information, these papers and the references therein contain the story as it stands at the moment.

Roca AL,  Georgiadis N,  Pecon-Slattery J, O’Brien SJ (2001) Genetic Evidence for Two Species of Elephant in Africa. Science 293, 1473-1477
Ishida Y, Oleksyk TK, Georgiadis NJ, David VA, Zhao K, Stephens RM, Koloktronis, S-O, Roca AL (2011) Reconciling Apparent Conflicts between Mitochondrial and Nuclear Phylogenies in African Elephants. PLoS ONE 6(6): e20642. doi:10.1371/journal.pone.0020642
Roca AL, Georgiadis N, O’Brien SJ (2004) Cytonuclear genomic dissociation in African elephant species. Nature Genetics 37 96-104
Ishida Y, Demeke Y, Van Coeverden de Groot PJ, Georgiadis NJ, Leggett KEA, Fox VE, Roca AL. Distinguishing Forest and Savanna African Elephants Using Short Nuclear DNA Sequences. Journal of Heredity 2011 610-616
Rohland N, Reich D, Mallick S, Meyer M, Green RE, Georgiadis NJ, Roca AL, Hofreiter M. (2010) Genomic DNA Sequences from Mastodon and Woolly Mammoth Reveal Deep Speciation of Forest and Savanna Elephants. PLoS Biol 8(12): e1000564. doi:10.1371/journal.pbio.1000564