PictureLudwig Rütimeyer (1825-1895)
Almost all primates — a group of mammals that includes humans as well as apes, monkeys, tarsiers, lemurs, lorises, and bushbabies — live in warm and forested regions of either Asia, Africa, Madagascar, or South America. Primate species that have managed to survive in cold climates are exceedingly rare exceptions to a general pattern of tropical living that has persisted within the group since its members first appeared in the fossil record about 56 million years ago, at the beginning of the Eocene epoch (a division of the geological timescale that lasted about 22 million years, ending around 34 million years ago). This hasn't always been obvious; paleontologists have slowly pieced together the evidence for this conclusion over the last century and a half. So imagine the conundrum that the Swiss naturalist Ludwig Rütimeyer (1825-1895) faced in the mid-1800s when a fragmentary fossil of a primate — an upper jaw — was extracted from Eocene rocks in northern Switzerland, in an area known as Egerkingen. As far as he could tell, a fossil like this had never been found before, anywhere in the world. When Rütimeyer compared the upper molar teeth of the extinct species with those of living primates and other mammals, he discovered that they looked similar to those of howler monkeys (genus Alouatta), which live today in Central and South America. To a lesser extent, its teeth looked like those of some lemurs that live in Madagascar. Could it possibly be that he was looking at the remains of a monkey or lemur that had managed to carve out an existence north of the Swiss Alps?

PictureDarwinius masillae, from the middle Eocene of Germany
Rütimeyer was no doubt puzzled by the find, but was emboldened to identify the species as a primate by the earlier work of a famous English anatomist, Sir Richard Owen (1804-1892), who had inferred that an even more fragmentary fossil (a single tooth implanted in a jaw fragment) from Eocene rocks in southern England was that of a monkey (1,2). Owen named that specimen Macacus eocænus, implying that it was related to living macaque monkeys — some of which, such as the Japanese “snow monkey”, do live in areas with seasonally cold climates. But Owen was wrong; upon closer inspection the alleged fossil macaque turned out to be Hyracotherium, a tiny ancient relative of modern horses. Owen didn’t rectify his error until after Rütimeyer had prepared his description of the Swiss primate (3), which he placed in "die Klasse der Affen" (implying that it was a "monkey" of some sort) and named Caenopithecus lemuroides, hedging his bets about the species’ relationships by mixing references to both monkeys (-pithecus, from the Greek word for ape) and lemurs (lemuroides, Greek for “lemur-like”) in the name. Ironically, the remains of a fossil primate from the Eocene of France — a genus named Adapis — were known to science even before Rütimeyer was born, but both Rütimeyer and the famous paleontologist Georges Cuvier (1769-1832, who named Adapis in 1822) had failed to recognize it as such. Instead, they thought that it was related in some way to hoofed mammals — hence the name Adapis, which refers to the ancient Egyptian bull diety Apis. Rütimeyer’s task would have been so much simpler if Adapis had been correctly identified by Cuvier, or if he himself had made what seems, in hindsight, to be an obvious connection! Regardless, by identifying Caenopithecus as a primate, Rütimeyer became the first paleontologist to correctly identify a primate of Eocene age.

Thanks to paleontologists, we now know that primates lived all over the northern Hemisphere during the Eocene epoch — not only in Europe, but also in North America and Asia. From time to time, the ranges of lemur-like and tarsier-like primates must have even extended up into the Arctic (4). This isn’t because these species were able to tolerate cold climates, but rather because the world was considerably warmer at that time, due to higher concentrations of the “greenhouse” gas carbon dioxide in the atmosphere. As a result, there wasn’t such a big difference in temperature between the equator and the poles, so during particularly warm phases primates were able to move between Asia and North America in areas that are now often covered in snow.

We also now know that Europe was home to quite a diverse group of primates during the Eocene. Some of these primates, known as “adapiforms” (including species of Adapis, Caenopithecus, and the relatively well-known, and relatively complete, Darwinius, to the right, known by many as “Ida”) are, in my opinion, probably distant relatives of lemurs and lorises, while another group of small and bug-eyed leaping primates, known as “omomyiforms”, might have been related to the bizarre tarsiers that are found today on various islands in southeast Asia. But adapiforms have long been a problem group for primate paleontologists, because, as
Rütimeyer first discovered, they combine monkey-like and lemur-like features (omomyiforms are just as controversial due to their combination of lemur-like and tarsier-like features, but that is a story for another day). Those who accepted Rütimeyer's identification of Caenopithecus as a primate were similarly perplexed by its genealogical position; for instance, in his review of the paltry primate fossil record that existed by 1872, Charles Forsyth-Major (1843-1923) echoed Rütimeyer's confusion about Caenopithecus, noting that "...Cænopithecus is to a certain extent intermediate between the Lemuridae and the Simiadæ..." (5, p. 160); similar observations have repeatedly been made about Caenopithecus and other adapiforms up to the present day (most recently, and notably, about Darwinius).

The work that I have undertaken with my collaborators on the relationships of early primates, taking into account most of the evidence that is now available from the Eocene record of primate evolution, nevertheless suggests that there were no monkeys in Europe during the Eocene, and that, based on its teeth and jaws, Caenopithecus was (despite having some monkey-like features) probably more closely related to lemurs and lorises than to monkeys, apes, and humans (though not all agree, see. ref. 6). If our results are correct, then Rütimeyer was right about Caenopithecus being a primate, but probably for the wrong reasons — the strong similarity of its teeth to those of howler monkeys was entirely the result of convergent evolution, an evolutionary phenomenon in which distantly related species acquire similar adaptations due to their similar lifestyles (a famous example are the wings of bats and birds, which were not present in their common ancestor).

PictureA howler monkey chomping on a leaf.

Photo by Steve Jurvetson.
In the case of Caenopithecus, it appears that, like howler monkeys, this species regularly used its molar teeth to chew up leaves. Leaves can be tough and difficult to slice through, so primate lineages whose distant ancestors depended on leaves for their survival typically have evolved (through the process of natural selection) long and tall crests on their molars that act somewhat like small scissors when food is being compressed between them. Caenopithecus’ molar tooth crests coincidentally came to look a lot like those of the howler monkeys via natural selection, but their common ancestor didn’t have such specialized tooth crests; in fact, the ancestor of living howler monkeys probably didn’t appear on Earth until about 30 million years after Caenopithecus individuals were living and dying in northern Switzerland around 44 million years ago — and furthermore it seems very likely that howler monkeys have only ever lived in Central and South America. Whatever the basis for his conclusions, Rütimeyer’s identification of Caenopithecus as a primate — notably only three years after Darwin published The Origin of Species — set in motion important debates about the existence of primates in the ancient rocks of Europe, and the evolutionary and/or climatic changes that might have allowed such primates to have existed so far north of their modern distributions.

PictureCaenopithecus maxilla described by Stehlin in 1916
In 1916, over half a century after Rütimeyer first described Caenopithecus, another Swiss paleontologist named Hans Stehlin (1870-1941) brought to light additional fossils of this mysterious species (7). By that time, paleontologists working in the western United States had documented several additional Eocene primate species, and four years earlier Stehlin had written a monograph on Adapis, clearly establishing, once and for all, that it was a primate. With the new and more complete Caenopithecus fossils, he was able to show that it differed from Adapis in some important ways — for instance, Caenopithecus only had six molar and premolar teeth on each side of the jaw, whereas Adapis had seven (humans typically have four or five, depending on whether our “wisdom” teeth have erupted, or have been removed by a dentist). In Caenopithecus, the first premolar behind its fang-like canine tooth was peculiar and unlike that of Adapis in being very small, almost vestigial. Stehlin argued that Adapis showed the greatest anatomical similarity to living lemurs, and should not be aligned with "higher primates", but he could not make sense of Caenopithecus' odd combination of features. Caenopithecus probably seemed even more distinctive to Stehlin than it should have, because he mistakenly identified a foot bone from Egerkingen — an astragalus (or talus) bone, which connects the shin bone (tibia) to the rest of the foot — as belonging to Caenopithecus, but it was actually that of a very distantly related carnivorous mammal, called a “creodont” (8), that lived in the same time and place as Caenopithecus (and possibly preyed upon it). And that was the end of the story for Caenopithecus — the fossils from Egerkingen showed what its jaws and teeth looked like, but for the last century we’ve known nothing else about paleontology’s “first" Eocene primate.

PictureView of the Egerkingen area in 2011
In 2011 I met with colleagues in Switzerland to see if there was any chance that the Egerkingen sites could be reopened for excavation, with the hope that some day we might learn more about Caenopithecus and the other adapiform and omomyiform primates that lived alongside it. Unfortunately, the prospects for future work at Egerkingen are not particularly good — the tall and steep rock faces that yielded the fossils are now used primarily by local rock climbers, and the paleontologically interesting fissures are either gone or largely exhausted. However when I visited the museum that both Rütimeyer and Stehlin worked at, the Naturhistorisches Museum Basel, and looked through the old Egerkingen collections, I was surprised to find four primate foot bones, about the size that one would expect for a Caenopithecus individual, that had never been formally described. They were particularly interesting to me because the primate astragalus bone from Egerkingen looked very similar to one that has been discovered in late Eocene rocks in Egypt several years earlier (9), and that probably belonged to a close relative of Caenopithecus that my colleagues and I had named Afradapis in 2009 (10). With the realization that the astragalus bone (and three other calcaneus, or “heel”, bones) from Egerkingen probably belonged to Caenopithecus, we appeared to have our first new information about this enigmatic primate in almost a century...and conveniently didn’t even have to excavate to find them!

Together with my co-authors Doug Boyer, of Duke University, and Loïc Costeur, of the Naturhistorisches Museum Basel, we have just described these fossils (11) in the journal PeerJ. The “new” remains of Caenopithecus provide some interesting clues about its lifestyle that we didn’t have before.

PictureA slow-moving African loris (genus Perodicticus)
Using three-dimensional digital models of the bones, which we constructed by CT-scanning the specimens, we used quantitative approaches to compare their shapes with those of other living and extinct primates (if you are interested, these models can be downloaded, viewed, and manipulated here, on MorphoSource, an extraordinarily useful digital library of CT-scanned bones that was created by my co-author Doug Boyer). We found that while the bones of Caenopithecus are quite unique when compared with those of other early primates, they do show some specializations that are similar to those of the slow lorises — prosimian primates that (as their name would suggest) typically move very slowly and cautiously, and do not leap at all. This raises some interesting questions, because slow lorises have diets made up largely of insects or fruits, but recall that Caenopithecus had the teeth of a leaf-eater. So Caenopithecus might have moved through the trees somewhat like a loris, but perhaps for very different reasons. For instance, lorises are active at night, and their stealthy movement through the darkness appears to be part of a strategy to avoid being detected by both potential insect prey, and by potential predators (such as mammalian carnivores and birds), but the leaves that Caenopithecus liked to eat obviously couldn’t have run away, so there would have been no need to sneak up on them.

Picture3D models of the Caenopithecus bones
Given that Caenopithecus was a leaf eater, perhaps the cautious movement that we envision for Caenopithecus would have been related more to a need to safely move through complex networks of small leaf-bearing twigs that exist at the ends of larger branches, without slipping and falling to the forest floor. The joint surfaces of Caenopithecus’ ankle bones suggest that its feet were very mobile, and, by analogy with the foot bone anatomy of some living lemurs, we inferred that a deep groove on the base of the astragalus bone might have helped to constrain the line of action of the tendon of an important toe-flexing muscle, and help to maintain the mechanical advantage of that muscle when the foot is pointed away from the shin, as would have happened if a Caenopithecus individual suspended itself under a branch, holding on exclusively by one or both feet (thereby freeing up the hands to grab leaves or fruit). In fact, these kinds of movements are commonly observed in a primate group mentioned before — the howler monkeys — which also eat lots of leaves; this would be yet another example of convergent evolution between Caenopithecus and howler monkeys. Howler monkeys also use their prehensile tails to hang from branches, but we don't know if Caenopithecus had such capabilities.

PictureThe recently extinct lemur Babakotia
The foot bones of Caenopithecus are also somewhat similar to (but less specialized than) those of a recently extinct large “sloth” lemur from Madagascar, named Babakotia, that also ate leaves and probably spent much of its time hanging under branches by its arms and legs (12). As in the case of the howler monkeys, the last common ancestor of Caenopithecus and Babakotia wouldn’t have had this lifestyle, and so this would be yet another example of convergent evolution. It is fascinating to think that a much more ancient, and much smaller, ancestor of Babakotia might have closely resembled a species like Caenopithecus lemuroides due solely to similar selection pressures that were operating entirely independently in Europe and Madagascar. These recurring patterns in the primate fossil record serve as a reminder of just how strongly our evolutionary paths have been shaped by the combination of constraints imposed externally (by life in the trees and the foods that exists in those trees) and internally (by the genetic and developmental constraints on anatomy that we inherited from the ancient last common ancestor of all primates); we should not be surprised to find that similar evolutionary “solutions” to survival have occurred time and time again over the course of the last 56 million years.

The ankle bones of primates are also of interest for determining relationships, because some features of the astragalus and calcaneus consistently sort living species onto different sides of the primate family tree. For instance, the orientation of the joint between the fibula and astragalus
seems to be one of only a few reliable skeletal indicators of whether an early fossil primate is a member of the strepsirrhine group (lemurs, lorises, bushbabies, and their early relatives) or the haplorhine group (humans, apes, monkeys, tarsiers, and their early relatives) (13, 14). In Caenopithecus this joint shows a very pronounced flare, as in strepsirrhines (which appear to be specialized in this feature). When we re-evaluated the relationships of Caenopithecus taking the new foot bones into account, we found that it is a distant relative of strepsirrhines, and probably a close relative of Adapis (see below)
— which, you might recall, was actually the first fossil primate ever discovered (of any age), but wasn't recognized as such until late in the 19th century. However even as early as 1873, the French paleontologist Paul Gervais (1816-1879) had argued that perhaps Caenopithecus and Adapis were very close relatives (if not members of the same genus), so it isn't a new idea...but it's still remarkable, in hindsight, that Cuvier and Rütimeyer didn't recognize the anatomical evidence for this connection.

The position of "adapiforms" in the primate family tree, based on the results of our analyses
And the relationships among the adapiforms, based on this most recent genealogical estimate that we provide (greatly simplified in the picture above), bring us to another interesting issue —  which is that the closest relative (or "sister taxon") of Caenopithecus is Afradapis, a younger form (about 37 million years old) from Egypt. This might not seem so odd given the current arrangement of the continents, but throughout the Eocene, Africa was separated from both Europe and Asia by a vast sea that paleontologists call "Tethys" (the ancient, and much larger, precursor of the modern-day Mediterranean). If Afradapis' close relatives, such as Adapis, Caenopithecus, and Darwinius, are all found in Europe and are descended from an ancestor that lived there as well, the adapiform family tree implies that somehow an ancestor of Afradapis managed to cross the Tethys Sea to get to Africa, most likely from Europe but perhaps from Asia (the Eocene record of which is not as well-sampled by paleontologists, and still holds many mysteries). It is an inescapable, but perplexing, conclusion that primates have made these improbable sea voyages multiple times, probably by floating on rafts of vegetation that were washed out to sea by strong storms or tsunamis — it's the only way to explain lemurs' presence in Madagascar, and somehow monkeys made an even more impressive journey across the Atlantic Ocean from Africa to South America (though those continents were much closer at the time; have a look at this recent post for a good discussion of the problem). Looking back into the fossil record, we see that members of several other extinct groups, including adapiforms and our own monkey-like ancestors, probably also crossed the Tethys, but perhaps taking advantage of island chains that have since been erased from the geological record as the conjoined African and Arabian continental plates slowly moved to the northeast and smushed into Asia (thereby closing off the Tethys, and forming the Zagros Mountains).

Finally, the four errors that have been mentioned so far, all made by very skilled anatomists and paleontologists, nicely demonstrate how knowledge in paleontology often advances by taking two steps forward and one step back. If people like Cuvier, Owen, Rütimeyer, and Stehlin (and so many others) all made mistakes when analyzing the early fossil primates of Europe, we have to wonder…what were we wrong about in our study? There are a few obvious possibilities. Perhaps we have attributed the foot bones to the wrong species, and they actually belong to another adapiform from Egerkingen named Leptadapis priscus. We think this is unlikely, though, because remains of Caenopithecus are far more abundant in the Egerkingen sites, and furthermore the ankle bones are very different from those of Leptadapis priscus’ close relatives. Maybe the evolutionary trees that we present have incorrect groupings; in fact this would not be surprising, because we have so little information from the fossil species that are included, and anatomy isn't always a reliable guide to relationships (again, due to convergent evolution). And fortunately we avoided at least one embarrassing oversight thanks to the process of peer review — unbeknownst to us, one of the world's experts on primate foot bones, Marian Dagosto (now of Northwestern University), actually briefly described and figured the Caenopithecus tarsals in her unpublished doctoral dissertation, which was completed in 1986. One of the reviewers of our paper caught the omission and we are glad that we were able to give her due credit in the final version of our manuscript; fortunately she had come to very similar conclusions about the functional and evolutionary implications of the fossils, which is reassuring. Only time will tell what conclusions of our study will turn out to be inaccurate once more evidence has been collected, but we can be pretty confident that we didn’t get everything right; it would be foolish to think otherwise.

References (with links to the original papers):

(1) Owen R. 1839. Description of the fossil mentioned in the preceding letter. The Magazine of Natural History 3: 446-448.

(2) Owen R. 1846. A History of British Fossil Mammals and Birds. London: John Van Voorst, 561 pp.

(3) Rütimeyer L. 1862. Eocäne Säugethiere aus dem Gebiet des schweizerischen Jura. Neue Denkschriften der Allgemeinen Schweizerischen Gesellschaft für die Gesammten Naturwissenschaften 19:1–98.

(4) Smith T., Rose K.D., and Gingerich P.D. 2006. Rapid Asia–Europe–North America geographic dispersal of earliest Eocene primate Teilhardina during the Paleocene–Eocene Thermal Maximum. Proceedings of the National Academy of Sciences, U.S.A. 103: 11223–11227.

Forsyth Major C.I. 1872. Note on some fossil monkeys found in Italy, preceded by a review of the fossil Quadrumana in general. The Annals and Magazine of Natural History 10: 153-166.

(6) Franzen J.L., Gingerich P.D., Habersetzer J., Hurum J. H., von Koenigswald W., and Smith B.H. 2009. Complete primate skeleton from the Middle Eocene of Messel in Germany: morphology and paleobiology. PLoS ONE 4: e5723.

(7) 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 Primaten. Abhandlung der Schweizerischen Paläontologischen Gesellschaft 41 :1299–1552.

(8) Decker R.L. and Szalay F.S. 1974. Origins and function of the pes in the Eocene Adapidae
(Lemuriformes, Primates). In: Jenkins, F.A., ed. Primate Locomotion. New York: Academic Press,

(9) Boyer D.M., Seiffert E.R., and Simons E.L. 2010. Astragalar morphology of Afradapis, a large adapiform primate from the earliest late Eocene of Egypt. American Journal of Physical Anthropology 143 :383-402.

(10) Seiffert E.R., Perry J.M.G., Simons E.L., and Boyer D.M. (2009) Convergent evolution of anthropoid-like adaptations in Eocene adapiform primates. Nature 461: 1118-1121.

(11) Seiffert E.R., Costeur L., and Boyer D.M. (2015) Primate tarsal bones from Egerkingen, Switzerland, attributable to the middle Eocene adapiform Caenopithecus lemuroides. PeerJ.

(12) Jungers W.L., Godfrey L.R., Simons E.L., Chatrath P.S., and Rakotosamimanana, B. 1991. Phylogenetic and functional affinities of Babakotia (Primates), a fossil lemur from northern Madagascar. Proceedings of the National Academy of Sciences 88: 9082–9086.

(13) Gebo DL. 1988. Foot morphology and locomotor adaptation in Eocene primates. Folia Primatologica 50:3–41.

(14) Boyer D.M. and Seiffert E.R. 2013.  Patterns of astragalar fibular facet orientation in extant and fossil primates and their evolutionary implications. American Journal of Physical Anthropology 151:420-447.



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