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.



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