Systematic Paleontology

Order Primates Linnaeus, 1758

Suborder Euprimates Hoffstetter, 1977

Family Notharctidae Trouessart, 1879

Subfamily Cercamoniinae Gingerich, 1975

Darwinius new genus

The limb proportions of Europolemur kelleri Franzen, 2000a, E. koenigswaldi Franzen, 1988, and the North American Notharctus osborni Gregory, 1920, are similar, whereas the limbs of E. klatti Weigelt, 1933, from Geiseltal are unknown. The dentition of E. kelleri, E. koenigswaldi and E. klatti (type species) correspond so well, that there is no doubt that they belong to the same genus. Radiographs demonstrate that all species of Europolemur match each other in possessing unicuspid but two-rooted P 2 /P 2 , while that of Godinotia neglecta and that of Darwinius masillae are small, straight and one-rooted, almost remnants in the maxilla ( Fig. 3 ). The type specimen of G. neglecta from Geiseltal clearly differs from E. kelleri, E. koenigswaldi, and D. masillae in having very gracile limb bones ( Figs. 1 – 3 ). The postcranial skeleton of E. klatti is little known save for an isolated astragalus, calcaneum, and atlas, the species determination of which is uncertain [22: 50, 62–65, fig. 2.20] .

When Franzen described the counterpart specimen (plate B) and assigned it to Godinotia neglecta from Geiseltal [1] , the permanent dentition of the Messel specimen was only represented by a fragmentary left M 1 and an incomplete forelimb and lower leg without hands and feet. He therefore did not recognize the difference of limb proportions, basing his determination mainly on the similar degree of reduction of the antemolar dentition. In 1994 similarities of the dentition led him to assign Geiseltal and Messel specimens to the genus Caenopithecus described by Rütimeyer in1862 from Egerkingen γ [18] , [27] . Now that the completely preserved right side of the Messel specimen (plate A) is known and described herein, it is clear that Darwinius masillae n.gen., n.sp. differs considerably from the type specimen of Godinotia neglecta in the postcranial skeleton and in particular, the limb proportions. Moreover, its dentition is clearly different from that of Europolemur koenigswaldi as well as E. kelleri from Messel and it differs from that of Caenopithecus lemuroides from Egerkingen in lacking a mesostyle on the upper molars.

Differs from Cercamonius brachyrhynchus (Stehlin, 1912), from Prajous (Quercy Phosphorite deposits) in having a mandibular ramus that is mesially not as deep, a trigonid of M 1 that is mesiodistally longer, and a talonid of M 1–2 that is larger and broader. M 1 and M 2 have a separate metastylid cusp not seen in Cercamonius.

Differs from Caenopithecus lemuroides Rütimeyer, 1862 (Egerkingen γ [26] ) in being smaller and having upper molars that lack a mesostyle (postcranial skeleton of Caenopithecus is unknown except for an isolated talus; see below).

M 1 and M 2 display a well developed hypocone but no mesostyle. A metaconule is lacking. The M 1 and M 2 show a small trigonid and a very broad talonid. In the permanent dentition, P 1 /P 1 have been lost whereas P 2 /P 2 are unicuspid and uniradical, especially reduced in the maxilla. The lower segments of the anterior and posterior limbs are conspicuously short and robust. The phalanges are elongated. A toilet or grooming claw is not present. Molars of Darwinius masillae are distinct in morphology and intermediate in size between those of contemporary species of Periconodon and Europolemur.

Description

Rostrum and orbit. Nasale: The anterior parts of the nasals are not preserved. The ventral suture with the premaxilla is about one-third of the length of the suture with the maxilla and lachrymal (or median process of maxilla, see below). Following the impressions, the right nasal extends mesially to above I2 whereas the left ends above the border between I1 and I2. The right nasal contains three similar sized slit-like nasal foramina. The most caudal one is situated above the anterior rim of the orbit. The most mesial one occurs above the tip of the deciduous upper canine. Premaxilla: The suture between the two premaxillae is recognizable between the central incisors. The right premaxilla contains two permanent incisors (Figs. 4–5). The bone is almost triangular and has a long caudal suture with the maxilla, as well as a straight, upwardly-directed suture with the premaxilla of the left side. Above there is also a dorsomesial suture with the right nasal. The bone reaches distally to above upper dC1. PPT PowerPoint slide

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larger image TIFF original image Download: Figure 5. Map of deciduous and permanent teeth of the right side in the skull of Darwinius masillae, new genus and species. Deciduous dI 2 has not yet been shed, and dC1/dC 1 , dP3/dP 3 , and dP4/dP 4 are still functional. Permanent teeth that are fully erupted include I1/I 1 , P2/P 2 , and M1/M 1 (P2 is present on plate B [1). Erupting teeth include I2/I 2 and M2/M 2 . Crowns of M3/M 3 are fully formed but lack roots. Crowns of P3/P 3 and P4/P 4 are partially formed, with P4/P 4 notably more developed than P3/P 3 . The crown of C1 appears to be fully formed, while that of C 1 is less mineralized. Judging from the stage of crown formation, premolars erupted in the sequence P2/P 2 – P4/P 4 – P3/P 3 , as in Cantius (Gingerich and Smith, in prep.), Notharctus [23, pl. LII: 9], and Europolemur [16, pl.III: 3]. https://doi.org/10.1371/journal.pone.0005723.g005 Maxilla: The bone forms a large part of the face. It contains the canine, two deciduous premolars, P2 and three molars (Fig. 4). The maxilla is very flattened and damaged and hard to distinguish from the other bones. The anterior border is located above the precanine diastema. Its suture with the premaxilla is steep and curving caudally into the suture with the nasal. There might be a median process of the maxilla dorsal to the lachrymal as seen in Lemur, but this cannot be decided from the X-ray photographs or CT scans. In the intraorbital part of the maxilla, there is a large intraorbital foramen. The mesial opening of the infraorbital channel is very small and situated above the metacone of dP4. Lachrymal: The lachrymal bone is crushed. There seems to be a substantial facial part, but most of the bone lies within the orbit. The lachrymal foramen is not visible. Frontal: The frontal bone forms the medial and upper half of the posterior border of the orbit. Mesially, it has a suture with the nasal and lachrymal. There is a well-defined ethmoidal foramen. The processus jugalis is robust and meets the processus frontalis of the jugal halfway. Together the two bones form the postorbital bar. Jugal: The mesiodorsal beginning of the zygomatic arch as well as the ventral border of the orbit is situated above the metacone of dP4. The zygomatic arch is mesially low and slender. The jugal size increases considerably distally until the divergence of the processus frontalis. Behind this the jugal narrows to about half of its former height. This is also the width of the postorbital bar. Squamosum: The bone forms the posterior half of the zygomatic arch and ends caudally in the fossa glenoidalis.

Auditory region. Squamosum: Caudally of the rather massive processus postglenoidalis there is a deep porus acusticus, which is not surrounded by an external meatus. The squamosum forms the dorsal roof of the meatus. Petrosum: The bulla tympanica has completely collapsed. However, the posterior and dorsal part is visible. The bulla of the left side is preserved on plate B, where the dorsal half of the annulus tympanicus is clearly seen on the X-ray photograph [1: fig. 5].

Braincase. Part of the left parietal and frontal is visible above the well exposed sutura sagittalis. Because of compaction, the skull appears higher than it was originally. A crista sagittalis was not developed. The rather voluminous braincase ends distally at the crista nuchalis. Caudoventrally, the in situ planum nuchale is turned up and crushed. The following bones form the dorsal and lateral parts of the braincase: Frontal: As usual, the bone forms the mesial part of the braincase. Parietal: The bone makes up most of the lateral side of the braincase. It is both deep and wide. Mesially, the parietal meets the frontal bone and caudally it has a long suture with the dorsal part of the occipital. It ends posterolaterally at the nuchal crest. Occipital: The dorsal extension of the occipital bone (protuberantia occipitalis externa) is wedged between the parietals as a triangular plate. On the caudal end of the skull, the dorsal rim of the foramen magnum is visible. The atlas is visible to the right of the foramen magnum, pressed against the occipital plane.

Lower jaw. The right ramus mandibularis is exposed laterally, with the teeth visible in buccal view. In contrast to adapid skulls [28], its height increases mesially, but not as much as it seems on its left counterpart [1: 293, fig. 4]. In addition, the mesial outline of the mandible is not as steep as it is on the left side (plate B). Both may result from damage during preparation. The micro-CT shows that the symphysis was fused ventrally but still open dorsally, due to the juvenile age of the individual (see below). The angular area increases caudally, where it extends into a well developed, caudally-protruding processus angularis. Some flat bony fragments located ventral and caudal to the processus angularis seem to belong to the hyoids. The processus articularis is still articulated with the fossa glenoidalis, which is situated about 6 mm above the occlusal surface of the mandibular cheek teeth. The coronoid process appears dorsal to the arcus zygomaticus, but it is not fully exposed making description impossible. There is only one foramen mentale appearing below P 2 in the middle of the corpus.

Dentition. The dentition of Darwinius masillae shows the holotype to be a juvenile, and imaging reveals a host of developing teeth within the face and jaw (Fig. 5). Much of the face preserves natural occlusion of upper and lower teeth. Studies of higher primates show that teeth generally begin eruption sometime after roots begin to mineralize, emerging through bone and gum before roots are complete [28]. In this light, images of Darwinius crown and root development reveal a coherent, readable pattern, in which we see: (1) fainter, less dense deciduous crowns with long roots; (2) developing permanent molars with densely mineralized crowns and incomplete roots; and (3) mineralizing crowns of the replacing permanent teeth (I1/I 1 -P4/P 4 ), largely, but not entirely, buried within the face. Basically, the entire permanent dentition was mineralizing while the deciduous dentition had only begun to be shed. Deciduous teeth: In the mandible, it appears that the central deciduous incisors (dI 1 ) have been shed and replaced. Much smaller second deciduous incisors (dI 2 ) remain in the mandible, on right and left sides. We cannot positively identify any upper deciduous incisors, which may have been shed. Clearly, upper and lower deciduous canines are in place. All four deciduous third and fourth premolars (dP3/dP 3 and dP4/dP 4 ) are erupted and in occlusion. All the deciduous teeth have long roots, consistent with circumnatal emergence. At the second premolar position we see only a single tooth generation in the mandible and maxilla, and, after more extensive comparison, conclude that dP 2 was probably shed at an early age. Permanent molars: All three permanent molars can be seen in the dentary. The first permanent molar in the dentary, M 1 , is fully erupted, occluding in normal position with M1. The long, but open roots of M 1 suggest that it was probably erupted for some time (weeks or possibly months). The mandibular second molar, M 2 , is just erupting, and its roots are less developed. The upper second molar, M2, is displaced but lacks sufficient root development for eruption. Third molars, M3/M 3 , had no roots mineralized, and these crowns were probably still covered by soft tissues. Replacement teeth: The first permanent incisor is the most advanced of the replacement teeth; this tooth is fully erupted with root length mineralized perhaps ⅔ or ¾ of final adult length. The tooth labeled I 1 is permanent because it is much larger than dI 2 and it has a denser crown. Development of I 2 is well underway, but it is significantly behind I 1 . In the premaxilla, we can see four incisor teeth. The right side is clearest: here, the I1 (with its labial edge slightly broken) is erupted, with a long root (¾ or more mineralized). The more caniniform right I2 shows root development of about ⅔. Radiographs also show a well developed incisor from the left side that is more difficult to identify (it may be I1 or possibly I2; one of these teeth is missing in either case). Maxillary permanent incisors were at or near emergence. The developing lower canine crown, C 1 , is substantial, but probably no more than half its eventual size. The massive upper permanent canine crown is probably caught at its maximum width, as mineralization was just outlining flanges at the base of the crown, indicating that a wide but not extremely tall crown was forming. The second premolar is represented by a tiny maxillary tooth, P2, on plate B, and a small mandibular tooth, P 2 , on both plates A and B. The mandibular tooth has a more densely mineralized crown, casting a denser shadow on radiographs and allying it with other permanent teeth. Root development is long and clearly advanced over that of the remaining permanent premolars. The crown of P 4 is less than ½ formed, but noticeably advanced over that of P 3 ; crowns of P4 and P3 can be identified in radiographs, with P4 again much advanced over P3.

Molar morphology. Little can be seen of the crowns of the molars in either plate A (Fig. 5) or plate B. However, we have succeeded in extracting three molars using micro-CT and graphic reconstruction (Fig. 6). PPT PowerPoint slide

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larger image TIFF original image Download: Figure 6. Micro-CT reconstructions of molar teeth of Darwinius masillae, new genus and species. Tooth crowns shown here were extracted digitally to show the entire crown for teeth that are only partially exposed in Plate A (see Fig. 5). (A–B)— right M1, in buccal and occlusal view. (C–D)— right M 1 , in buccal and occlusal view. (E–F)— right M 2 , in buccal and occlusal view. Note the absence of a mesostyle on M1, and the presence of a hypocone on the broad lingual cingulum of this tooth. Note too the absence of a distinct paraconid and hypoconulid on M 1–2 , and the very broad talonid on M 2 . Molars of Darwinius masillae are distinct in morphology and intermediate in size between those of contemporary species of Periconodon and Europolemur. https://doi.org/10.1371/journal.pone.0005723.g006 The crown of M1 is subrectangular in occlusal outline, with a prominent protocone, paracone, and metacone well spaced on the crown. There is a well-developed hypocone developed on a broad lingual cingulum, but a pericone, if present, was weakly developed (Fig. 6A–B). This tooth has the classic simplicity of cercamoniine upper molars. Roots are relatively well developed, which is consistent with its early eruption. Measurements are listed in Table 2. The crown of M 1 is relatively long and narrow (Fig. 6C–D). There is no distinct paraconid, but a looping paracristid encloses a basined trigonid. The protoconid and metaconid are well developed on the trigonid, followed by a distinct hypoconid and entoconid on the talonid. There is no hypoconulid, but a well developed metastylid distally from the metaconid. The talonid of M 1 is distinctly broader than the trigonid, but less broad than the talonid on M 2 . The cristid oblique or prehypocristid runs mesiolingually toward the notch in the postprotocristid but then turns abruptly to join the protoconid. There is a narrow cingulid bordering the lingual side of the tooth. Measurements are listed in Table 2. The crown of M 2 is shorter than that of M 1 , with a broader trigonid and a much broader talonid (Fig. 6E–F). The trigonid is short anteroposteriorly. It lacks a paraconid, and again has a looping paracristid enclosing a shallowly basined trigonid. The protoconid and metaconid are well developed on the trigonid, and again they are followed by a distinct hypoconid and entoconid on the talonid. There is neither a hypoconulid nor a metastylid. The lingual cingulid is more pronounced than that on M 1 . As on M 1 , there is a distinct cristid oblique that ends near the base of the protoconid. Measurements are listed in Table 2 and Appendix S1.

Vertebral column. (Figs. 1–2, 7, S3, and measurements in Appendix S1). The vertebral column is complete, although laterally compressed and, in part, crushed. Altogether it comprises 7 cervical, 11 thoracic, 7 lumbar, 3 sacral, and 31 caudal vertebrae. The whole vertebral column, from the proximal end of the atlas to the end of the last caudal vertebra, measures ca. 53 cm (Table 2). Together with a basal length of the skull of about 5 cm, this results in a total skeleton length of ca. 58 cm, whereas the head and body length is ca. 24 cm without the tail. PPT PowerPoint slide

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larger image TIFF original image Download: Figure 7. Length profile for caudal vertebrae of Darwinius masillae, new genus and species, compared to those of other primates. Measurements of Darwinius were taken from plate A (Fig. 1). Darwinius, Europolemur, and Notharctus are Eocene adapoids; Ateles and Callithrix are extant Ceboidea; and Avahi and Eulemur are extant Lemuroidea. Measurements of comparative specimens are from [23], [38], with new measurements added for Avahi. Note that the profile for Darwinius is flatter (rises less high and declines less rapidly) than that for any of the comparative specimens. https://doi.org/10.1371/journal.pone.0005723.g007 The atlas is broken and incomplete. It is attached to the planum nuchale of the cranium. The left wing of the atlas is crushed, whereas the right wing is seen in dorsal view, with a well-developed foramen vertebrale laterale. The lateral surface of the axis is visible in plate A, however the prominent processus spinalis is crushed. C3–C5 are visible in lateral view. Their processus spinales are only partially exposed, whereas their processus transversi are clearly visible. Caudally in the cervical series, the processus transversi become more and more expanded. C6 is crushed, whereas the right scapula covers C7. By including the first and second thoracic vertebrae, which are hidden below the right scapula, 11 thoracic vertebrae are present although their exact number is difficult to determine and therefore somewhat ambiguous. Whereas T3–T5 are laterally exposed, T6–T8 have rotated around their long axis so that they are seen in dorsal aspect, while T9–T11 are visible laterally. There is no diaphragmatic vertebra, because even the processus spinalis of T11 is slightly but clearly dipping caudally. The ribs are not well preserved. Most of their cartilaginous parts exist only as natural casts. The right humerus mostly covers the sternum. Caudal to the thoracics are 7 lumbar vertebrae. They are comparatively massive and display cranially oriented transverse processes, which become more and more expanded caudally. No spinal processes are evident on L1–L3, but L4 carries a rather small process slightly dipping caudally. The spinal process of the lumbar vertebrae becomes somewhat larger caudally and dips more in this direction. The os sacrum comprises 3 vertebrae, S1–S3, the most proximal one of which is damaged. Altogether, there are 31 caudal vertebrae but the last one ends fragmented at a fault. So there may have been one or two more. The 3 most proximal are comparatively short and display strong transverse processes that become weaker more distally in the series. The last transverse process is developed on Ca4, which is already considerably longer and shows only a small processus transversus at its caudal end. All following vertebrae have no processus transversi. In D. masillae the dorsal vertebral column shown on plate A is gently curved (that of plate B is fake) and the tail is only slightly curved. The length profile of the proximal half of caudal vertebrae is close to that of living Callithrix jacchus, while more distally D. masillae has much longer vertebrae. Altogether, the tail is much longer than that referred to Europolemur koenigswaldi (Fig. 7). In D. masillae, the length profile of Ca8–Ca20 differs from that of the living Avahi laniger, even more so from Eulemur mongoz, and considerably from Ateles geoffroyi. Clearly, Darwinius did not have a prehensile tail. The tail was presumably used primarily for balance, and possibly for steering while leaping. Its soft body contours are incomplete. Therefore, it is impossible to decide whether it was bushy or not.