PictureA boomslang, Dispholidus typus (Colubridae)
in Tanzania. Photo by William Warby.
Presumably humans have always had a complex relationship with snakes; some cultures revere and worship them, others see them as evil, and the estimated one-third of the population that suffers from ophiophobia (fear of snakes) simply want nothing to do with them. Love them or hate them, there is just something about their shape and movement that freaks us out, and we are remarkably good at detecting snakes (or just snake-like objects) in our peripheral vision and amongst camouflage (1, 2). These and other observations underpin the controversial hypothesis that past predation by snakes has, over the course of tens of millions of years of evolution, played a key selective role in shaping parts of the primate brain that relate to visual threat detection (3). It has even been argued that perhaps “venomous snakes were such an important selective pressure favoring greater visual specialization in primates that they were ultimately responsible for the emergence of anthropoids” (Isbell, ref. 3, p. 12). It is true that snakes eat non-human primates (at least occasionally), and we all know stories about humans who have been bit by snakes, but what do we really know about the snakes that lived alongside the earliest members of the primate group that now includes monkeys, apes, and humans? Until very recently, almost nothing.

Today Africa is home to some of the deadliest venomous snakes on Earth, all of which belong to a large group known as Colubroidea, a superfamily that includes most living snake species. The majority of colubroids are non-venomous, but counted among its members are undeniably scary venomous African species such as puff adders (genus Bitis, a member of the family Viperidae), boomslangs (Dispholidus, a member of the family Colubridae, seen in the picture above), and elapids such as cobras (genus Naja) and mambas (genus Dendroaspis). The ancestral lineage that gave rise to all living colubroids probably originated in Asia very early in the Cenozoic, but colubroids have since undergone a remarkable diversification and are now found on all continents aside from Antarctica.

There is growing evidence that anthropoids probably also arose in Asia early in the Cenozoic, but, at some point in the Eocene, an ancestral population of anthropoids made it across the ancient Tethys Sea onto the then-isolated Afro-Arabian landmass (see for instance Seiffert (ref. 4), among others). The group subsequently diversified into parapithecoids (an extinct side branch), platyrrhines (the New World monkeys), and catarrhines (the Old World monkeys, apes, and humans). The fossil evidence for this phase in our shared evolutionary history with other anthropoids is best-documented in an area of northern Egypt known as the Fayum Depression, where there are multiple fossil sites that range from 37 to 29 million years in age. However, snake fossils are rare at the Fayum sites, and in fact the only species that have been described, way back in 1901 -- the giant madtsoiid Gigantophis garstini and the palaeophiid Pterosphenus schweinfurthi (both non-colubroid) -- were found in near-shore marine deposits that do not preserve anthropoid fossils (5). In light of this, for the last 115 years we had no evidence that the earliest African anthropoids lived alongside colubroids at all.

PictureSearching for fossil snakes and monkeys,
among other species, at BQ-2.
Photo by Hesham Sallam.
Thanks to more recent paleontological work in the Paleogene of Egypt and Tanzania, we finally know more about the early African record of Colubroidea. And, of particular significance for Isbell's hypothesis, we know more about snakes whose fossil remains occur right alongside those of the oldest undoubted African anthropoids. In a recent paper (6) in Journal of Vertebrate Paleontology that I co-authored with snake expert Jacob McCartney of SUNY Geneseo, a diverse snake fauna from the 37 million-year-old Fayum Birket Qarun Locality 2 ("BQ-2", image to the left) is described. BQ-2 has also yielded remains of several primates: the early anthropoid Biretia, the adapiform Afradapis, the lorisiforms Karanisia and Saharagalago, and the enigmatic possible anthropoid Nosmips (ref. 4; in addition to a few additional species, including anthropoids, that have not yet been described). This is the only example, from the entire Eocene epoch (34-56 million years ago) of Africa, of snakes and primates co-occurring at the same locality.

So what can be said of relevance to the "Snake Detection Theory" in light of what has been found at BQ-2? A key piece of Isbell's hypothesis is that early anthropoids lived alongside venomous snakes. The BQ-2 snake fauna provides no positive support for that hypothesis. Only one colubroid snake is present, the new genus and species Renenutet enmerwer, and it accounts for about 15% of the recovered snake remains, but it cannot be assigned to a particular lineage of colubroids -- instead it is simply a generalized species that can only be excluded from certain colubroid groups with venomous members (elapids, viperids) based on the absence of the specialized features that are seen in those groups. This shouldn't be taken to mean that there weren't potential primate predators in the BQ-2 snake fauna. Also present was the enormous Gigantophis, adults of which might have been 9-11 meters long, and the fauna is dominated by booids (which probably would have been similar to living medium-sized boas or pythons). Also present, strangely enough, is a tropidophiid -- a group that is now represented solely by the "dwarf boas" of the New World (West Indies, Central and South America; see image below), but that is also known from older fossil members in Europe. Perhaps tropidophiids can be added to the small list of land animals (including platyrrhine anthropoids and caviomorph rodents) that somehow dispersed across the South Atlantic, from Africa to South America, during the Eocene.

The dwarf boa Tropidophis melanurus, in Cuba. Picture by Jerry Oldenettel.
The presence of a generalized colubroid in the late Eocene of Africa raises a number of questions that are difficult to answer given available material, most obvious of which is -- where does Renenutet fall in colubroid phylogeny? The molecular phylogeny of snakes published by Pyron et al. (7) is consistent with an Asian origin of Colubroidea, and multiple independent dispersals of colubroids into Africa, but when did these different dispersals occur? Some might have been relatively recent, but one diverse group that could be of ancient African origin is Lamprophiidae -- a family that Renenutet cannot be excluded from, or included in, based on vertebral morphology. The recent "tip-dating" analysis of Hsiang et al. (8) suggested an Eocene divergence of lamprophiids from elapids, perhaps close in time to the deposition of BQ-2, but the Pyron et al. phylogeny suggests that the common ancestor of that clade was Asian, not African. This result is again not necessarily consistent with the presumed coexistence of anthropoids and venomous snakes in the Eocene of Africa.

But even if there were no venomous snakes in Africa during the Eocene or the early Oligocene, that period of isolation might have been short-lived (in geological terms). Thanks to the work of McCartneyNancy Stevens, and Patrick O'Connor, we now know that 12 million years after the deposition of BQ-2, at about 25 million years ago in the late Oligocene, there was a more diverse colubroid fauna present in Tanzania (9). The fossil snakes that they described were found in the Rukwa Rift Basin, which has also yielded the oldest fossil remains of apes (Hominoidea) and Old World monkeys (Cercopithecoidea). Notably, included among the Rukwa colubroids is a member of the family Elapidae, living members of which have hollow fangs that are used to inject venom (though note that the fossils from Tanzania are, like most fossil snakes, only known from vertebrae, so we don't know if these species had hollow fangs). In contrast to the BQ-2 fauna, these discoveries provide positive evidence that the earliest hominoids and cercopithecoids likely coexisted with venomous snakes in the late Oligocene of Tanzania, though they have not yet been documented to co-occur at the same sites.

As always, we need more fossils (and ideally much more complete fossils), from different parts of Africa and different time periods, to more thoroughly test the hypothesis that early African anthropoids co-existed with venomous snakes; it is, after all, a huge continentAnd clearly it is time for a taxonomically broad analysis of divergence dates within Colubroidea (ideally including fossils and using the same "tip-dating" methods employed by Hsiang et al.), with attention paid to the time and place of origin of venom delivery in the various colubroid lineages that evolved that adaptation. It may well be that there is little reason to expect that venom delivery had evolved in any colubroid family by the Eocene. Another key question would be whether diurnal arboreal anthropoids would have regularly encountered these venomous snakes at all -- Hsiang et al. (8) found that elapids and colubrids were likely to have been ancestrally diurnal, but were they ancestrally arboreal or terrestrial?

References (with links to the original papers):

(1) Lean Q.V., Isbell L.A., Matsumoto J., Nguyena M., Horia E., Maiorc R.S., Tomazc C., Trana A.H., Ono T., and Nishijoa H. 2013. Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes. Proceedings of the National Academy of Sciences, U.S.A. 110: 19000–19005.

(2) Soares S.C., Lindström B., Esteves F., and Öhman A. 2014. The hidden snake in the grass: Superior detection of snakes in challenging attentional conditions. PLoS ONE 9: e114724.

(3) Isbell L.A. 2006. Snakes as agents of evolutionary change in primate brains. Journal of Human Evolution 51: 1-35.
(4) Seiffert E.R. 2012. Early primate evolution in Afro-ArabiaEvolutionary Anthropology 21: 239-253.

(5) Andrews C.W. 1901. Preliminary note on some recently discovered extinct vertebrates from Egypt (Part II). Geological Magazine 8: 436-444.

(6) McCartney J.M. and Seiffert E.R. 2016. A late Eocene snake fauna from the Fayum Depression, Egypt. Journal of Vertebrate Paleontology e1029580.

(7) Pyron R.A., Burbrink F.T., and Wiens J.J. 2013. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology 13: 1-53.

(8) Hsiang A.Y., Field D.J., Webster T.H., Behlke A.D.B., Davis M.B., Racicot R.A., and Gauthier J.A. 2015. The origin of snakes: revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record. BMC Evolutionary Biology 15: 1-22.

(9) McCartney J.M., Stevens N.J., and O'Connor P.M. 2014. The earliest colubroid-dominated snake fauna from Africa: Perspectives from the late Oligocene Nsungwe Formation of southwestern Tanzania. PLoS ONE 9: e90415.


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