PictureA mouse lemur (Microcebus) in
Madagascar. Image by Blanchard
Lemurs, including species such as the mouse lemur in the image to the right, are a diverse group of primates that is now restricted to Madagascar and a few nearby islands. But the common ancestor that lemurs shared with the other extant "strepsirrhine" primates — the lorises and bushbabies — probably lived in the early Eocene, ~50-56 million years ago (and possibly even earlier) on what was then "Afro-Arabia", an isolated continent made up of the conjoined African and Arabian tectonic plates (1). An ancient ancestor of Asia's modern lorises presumably migrated from Arabia much later, perhaps during the early Miocene (~16-~23 million years ago), as that plate's eastern margin slowly made contact with the conjoined Asian and Indian plates (2). At least this seems to be the most likely scenario given the evidence that we have available; the early evolution of strepsirrhines is still shrouded in mystery, presumably because Afro-Arabia's Eocene fossil record has been so poorly sampled. 

PictureJaw of Djebelemur, an early relative of strepsirrhines
from Tunisia. Modified from Marivaux et al. (3).
Regardless, most of the potential close fossil relatives of the living strepsirrhines (a group that is also known as the "toothcombed" primates, for the comb-like shape of their lower incisor and canine teeth) are from Africa. Included among these early African species is a tiny primate named Djebelemur, from an early Eocene site in Tunisia [image to the left (ref. 3)]. The only known remains of Djebelemur — jaws, teeth, ankle bones, and ear bones — are all consistent with it being a strepsirrhine, and yet it lacks the toothcomb, suggesting that it is not the common ancestor of the living species, but rather an extinct side branch. Also present at sites of a similar age in Algeria are remains of other tiny strepsirrhines known as azibiids (Azibius and Algeripithecus). The ankle bones of Azibius closely resemble those of Djebelemur, but the arrangement of cusps and crests on its teeth is remarkably specialized for a species of such great antiquity (3).

But where did these early African strepsirrhine primates come from? Are they the descendants of a much more ancient Afro-Arabian lineage, or are they immigrants from some nearby landmass? The closest relatives of strepsirrhines are the tarsiers and anthropoids (monkeys, apes, humans), followed more distantly by two orders of non-primate mammals — flying lemurs and treeshrews. All of these groups have early fossil records in Asia, and on this basis it has been argued that the "stem lineage" of strepsirrhines (that is, the long line of successive ancestral populations that ultimately gave rise to the most recent common ancestor of lemurs, lorises, and bushbabies) probably also traces back to Asia (1). To be fair, though, not everybody agrees on this scenario. And there are, in fact, no known Djebelemur-like primates on either the Asian plate or on the Indian plate in the early Eocene (when those two tectonic plates were first coming into contact).

PictureA lower jaw of Anchomomys from Egerkingen,
Switzerland, held in the collections of
the Naturhistorisches Museum Basel.
Instead, the non-African fossil species whose teeth most closely resemble those of Djebelemur are anchomomyins — a group of tiny primates that lived in the middle and late Eocene of Europe, and that also lacked toothcombs. Anchomomys was first described in 1916, by the Swiss paleontologist Hans Stehlin (4), based on fragmentary jaws from middle Eocene sites in the Egerkingen area of Switzerland (which I discussed in an earlier post), but since that time teeth of several close relatives have been discovered, most recently in northeast Spain (5-7). Traditionally, anchomomyins have been linked to other fossil primates known from the Eocene of Europe, such as middle Eocene Europolemur and Protoadapis (8), but they are odd in being considerably smaller than their alleged relatives, and in having no older relatives that conclusively link them to other European species.

PictureA calcaneus bone of Anchomomys
compared to that of a mouse lemur
Mirza and an older strepsirrhine relative,
Asiadapis. Note the elongation of the
calcaneus in Anchomomys and Mirza.
One reason why anchomomyins have remained so mysterious over the course of the last century is that they have long been known only from partial jaws and isolated teeth. However early in the 1990s, work led by the Spanish paleontologist Salvador Moyà-Solà, at a ~42 million-year-old site called "Sant Jaume de Frontanyà-3C" in northeastern Spain, resulted in the recovery of numerous postcranial bones of a species named Anchomomys frontanyensis (9). Surprisingly, these fossils showed that, unlike its purported European relatives, Anchomomys was characterized by elongation of the end of the calcaneus bone (see image to the left) — a feature that is today seen only in small leaping prosimians, including bushbabies and some lemurs. In a recently published paper in Journal of Human Evolution (10) that I co-authored with lead author Judit Marigó, as well as Imma Roig, Moyà-Solà, and Doug Boyer, the ankle bones of Anchomomys are described in detail for the first time, and the information from these bones is incorporated into an analysis of relationships among early primates.

One important conclusion of our study is that the astragalus (or talus) bones of Anchomomys differ very little from those of Azibius and Djebelemur. Another important conclusion is that our analyses of primate relationships place anchomomyins closer to azibiids, Djebelemur, and living strepsirrhines than to any European species. This result raises the intriguing possibility that African strepsirrhines might be derived from a much older anchomomyin-like ancestor that lived on the Iberian Peninsula in the earliest Eocene. This part of the strepsirrhine family tree is, however, still poorly resolved, and instability in the placement of anchomomyins relative to African species leaves open the possibility that movement was not from Europe to Africa, but rather from Africa to Europe -- that is, perhaps anchomomyins might be derived from the early African radiation of non-toothcombed strepsirrhines that also gave rise to azibiids and Djebelemur.

Another possibility that must be entertained is that our phylogenetic results are entirely due to convergent evolution in the teeth and ankle bones of these early primates, which might have occurred if similar habitats were available to small proto-strepsirrhines in northwestern Africa and the Iberian Peninsula during the Eocene. Interestingly, a distantly related group of small primates known as microchoerines — remains of which have also been found in Spain alongside those of Anchomomys -- also evolved particularly long calcaneus bones, which (by analogy with living primates) presumably facilitated acrobatic leaping between trees. Selection pressures clearly favored the evolution of leaping adaptations in multiple primate lineages that were present in Europe during the Eocene. 

Digital models of the Anchomomys tarsal bones can be viewed (with registration) on MorphoSource, where they can be compared with models of astragali and calcanei belonging to hundreds of other living and extinct primate species.

References (with links to the original papers, if available):

(1) Seiffert E.R. 2012. Early primate evolution in Afro-Arabia. Evolutionary Anthropology 21: 239-253.

(2) Seiffert E.R. 2007. Early evolution and biogeography of lorisiform strepsirrhines. American Journal of Primatology 69: 27-35.

(3) Marivaux L., Ramdarshan A., Essid E.M., Marzougui W., Ammar H.K., Lebrun R., Marandat B., Merzeraud G., Tabuce R., Vianey-Liaud M. 2013. Djebelemur, a tiny pre-tooth-combed primate from the Eocene of Tunisia: A glimpse into the origin of crown strepsirhines. PLoS ONE 8: e80778.

(4) Stehlin H.G. 1916. Die Säugetiere des schweizerischen Eocaens. Critischer Catalog der Materialen. Siebenter Teil, zweite Hälfte: Caenopithecus--Necrolemur--Microchoerus--Nannopithex--Anchomomys--Periconodon--Amphichiromys--Heterochiromys —Nachträge zu Adapis —Schlussbetrachtungen zu den PrimatenAbhandlung der Schweizerischen Paläontologischen Gesellschaft 41 :1299–1552.

(5) Marigó J., Minwer-Barakat R., and Moyà-Solà S. 2010. New Anchomomyini (Adapoidea, Primates) from the Mazaterón Middle Eocene locality (Almazán Basin, Soria, Spain). Journal of Human Evolution 58:353-361. 

(6) Marigó J., Minwer-Barakat R., and Moyà-Solà S. 2011. New Anchomomys (Adapoidea, Primates) from the Robiacian (Middle Eocene) of northeastern Spain. Taxonomic and evolutionary implications. Journal of Human Evolution 60:665-672.

(7) Marigó J., Minwer-Barakat R., and Moyà-Solà S. 2013. Nievesia sossisensis, a new anchomomyin (Adapiformes, Primates) from the early late Eocene of the southern Pyrenees (Catalonia, Spain). Journal of Human Evolution 64:473–485.

(8) Godinot M. 1998. A summary of adapiform systematics and phylogeny. Folia Primatologica 69 (Suppl. 1): 218-249.

(9) Moyà-Solà S, and Köhler M. 1993. Middle Bartonian locality with Anchomomys (Adapidae, Primates) in the Spanish Pyrenees - preliminary report. Folia Primatologica 60:158-163. 

(10) Marigó J., Roig I., Seiffert E.R., Moyà-Solà S., and Boyer D.M. 2016. Astragalar and calcaneal morphology of the middle Eocene primate Anchomomys frontanyensis: Implications for early primate evolution. Journal of Human Evolution 91:122-143.

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.