Keywords: Algeria, primate evolution, toothcombed primates, activity pattern

(a). Included genera

AzibiusSudre, 1975 andAlgeripithecusGodinot & Mahboubi, 1992.

(b). Emended diagnosis

Azibiids (figures 1 and2) differ from all other primates in having high, mesio-distally aligned P_3–4 cusps, forming a blade-like structure; P_3–4 also present a degree of overlapping and a mesial crown elevation associated with an inclination of the lingual cingulid. On M_1–2, azibiid traits are the distally offset metaconid, the absence of hypoconulid, and the narrow sub-circular talonid basin, which is open lingually by a deep notch in front of the entoconid. The P^3–4 have a peak-shaped lateral profile resulting from the labially inclined protocone and the very high and vertical sharp edge aspect of the ectoloph. The bunodont M^1–2 have a large hypocone, a thick lingual cingulum, and lack a distinct metaconule.

(c). Remarks

Algeripithecus is smaller thanAzibius (table S2 in the electronic supplementary material). Based on the various available equations, deriving from the regressions of M₁ area against body mass of living primates (e.g.Conroy 1987;Bajpaiet al. 2008), the estimated body mass ofAlgeripithecus ranges from 65 to 85 g andAzibius from 115 to 160 g.Algeripithecus differs also fromAzibius by rather less bunodont teeth, a higher metaconid (or possibly protostylid) on P_3–4, a longer trigonid and shorter talonid on M₁, a smaller third lobe on M₃, the lack of both paraconule and parastyle on P⁴, and by a more reduced M³. Azibiids are only known from the late early or early middle Eocene (Mahboubi 1995;Mebrouk & Feist 1999;Adaciet al. 2007) of the Glib Zegdou Formation, Gour Lazib area, Algeria. However, another taxon, close toAlgeripithecus, could also be present in the contemporaneous site of Chambi, Tunisia (Seiffertet al. in press).

(a). The euprimate affinities of Azibiidae

Sudre (1975) describedAzibius as a possible ‘paromomyiform’ (=‘Plesiadapiformes’). Later,Gingerich (1976) suggestedAzibius is a euprimate (primates of modern aspect), and erected the Azibiinae, a new subfamily of Adapidae. He thereby rejected the assumption proposed bySzalay (1975) according to whichAzibius was a hyopsodontid-like condylarth. More recently,Holroyd & Simons (1991) have reinforced the adapid status ofAzibius, whileHartenbergeret al. (1997) have suggested a macroscelidid affinity. Finally, after the discovery ofDralestes, which was considered to be the sister taxon ofAzibius,Tabuceet al. (2004) suggested that azibiids are related to carpolestid plesiadapiforms, reviving Sudre's initial attribution. This hypothesis was criticized byGodinot (2006) andSilcox (2008), who favoured euprimate affinities for azibiids. The abundant new material reveals thatDralestes is invalid because its hypodigm contains specimens of bothAzibius andAlgeripithecus (table S1 in the electronic supplementary material). The supposed carpolestid affinities ofAzibius relied on the morphology of the P₄, which are enlarged in both taxa compared to the molars, exodaenodont (a lobe of enamel overhangs the labial side of the roots), and show apical cusps aligned anteroposteriorly in a blade-like structure. However, from a detailed comparison,Silcox (2008) suggested that this blade-like morphology is non-homologous betweenAzibius and carpolestids. We agree with her opinion because the P₃ of azibiids, previously unknown, are also enlarged, exodaenodont, high-crowned and have a similar shearing morphology as the P₄, while the P₃ of carpolestids is reduced and lacks the blade-like morphology. Most importantly, the new material reveals that the upper tooth originally thought to be the M² of ‘Dralestes’ (GZC-41, holotype) is in fact a P⁴ ofAzibius. This new dental allocation clearly precludes any carpolestid affinities for azibiids. The bona fide upper and lower molars ofAzibius show, as do those ofAlgeripithecus, a euprimate morphology.

(b). Testing the anthropoid status ofAlgeripithecus andAzibius

Algeripithecus was successively considered as a propliopithecid, a proteopithecid or a parapithecoid anthropoid (Godinot & Mahboubi 1992;Godinot 1994; Seiffertet al.2005a,in press). Its upper molars strongly resemble those ofBiretia, a primitive parapithecoid from the late middle Eocene of Algeria and the early late Eocene of Egypt (de Boniset al. 1988;Seiffertet al. 2005a). Common traits include a similar degree of bunodonty, the same occlusal outline, the robustness and the postero-lingual position of the hypocone, and the important development of the lingual cingulum (figure 1a). Upper molars ofBiretia differ in having an uninterrupted lingual cingulum and enlarged conules. Further differences that are evident on premolars and molars clearly distinguish parapithecoids from azibiids: P² ofBiretia is three-rooted, P⁴ is less molariform due to the absence of the metacone, the roots of P_3–4 are oblique in orientation, their crown is low, their metaconid is offset lingually and the entoconid is present on P₄; the paraconid occurs on M₁, the metaconid is transverse to the protoconid on M_2–3, the cristid obliqua reaches the trigonid wall at a more labial point, the hypoconulid is enlarged and central on the postcristid of M_1–2, and M₃ is reduced. Azibiids also lack some dental features of later parapithecoids (Abuqatrania,Apidium andParapithecus;Seiffertet al. in press) such as the bulbous conules on upper molars and the absence of lower molar protocristids. Other basal anthropoid families such as proteopithecids and eosimiids are also distinct from azibiids, and all dental resemblances represent only primitive retentions or convergences (see text 2 in the electronic supplementary material). Azibiids also differ from most omomyiforms by their large hypocone and the loss of the paraconid. Some superficial similarities on lower premolars with microchoerines and anaptomorphines are the anterior elevation of the thick basal cingulid and the pronounced overlapping of P_3–4 (Godinot 2006). However, the buccolingually enlarged and molariform P₄ of omomyiforms are clearly distinct from the mesiolingually elongated and blade-like P₄ of azibiids.

In addition to this purely dental evidence, the newly recovered fossils ofAlgeripithecus andAzibius include dentary and maxilla, which are decisive in reconstructing the affinities of azibiids. The maxilla ofAzibius lacks P¹ and shows above P^2–3 a very anterior position of the infraorbital foramina (IOF) (figure 2a–c). In occlusal view, the lateral maxillary broadening starts at the level of the P². By comparisons with extant and extinct primates, these characters indicate thatAzibius possesses a short rostrum. The pronounced curve and the thickening of the mandible under P₄ inAlgeripithecus are also indicative of a short jaw (figure 1d). Besides,Azibius presents a reduced suborbital depth of the maxilla above P⁴. This feature is also observed in the omomyidNecrolemur, in the platyrrhineAotus, as well as in most small and medium-sized modern strepsirhines (e.g.Loris,Galago,Microcebus).Tarsius andBiretia megalopsis show an extreme compression of the suborbital region in having a complete orbitopalatal fusion and an exposure of the lingual roots of molars in the orbit floor (Seiffertet al. 2005a). The reduced suborbital depth of the maxilla and the orbitopalatal fusion are observed in primates having large orbits and a nocturnal activity pattern. Comparative scans performed using conventional and synchrotron microtomography (see text 3 in the electronic supplementary material) of the maxilla through the lingual P⁴ root of some of these primates (see figure S1 in the electronic supplementary material) show thatAzibius is comparable toAotus and intermediate in condition betweenTarsius andLoris, thereby suggesting very large orbits inAzibius probably associated with a nocturnal activity pattern. The cumulative area (0.74 mm²) of the two IOFs inAzibius is greater than it is inTarsius, most small anthropoids and living strepsirhines of equivalent weight (e.g.Galago senegalensis,Loris tardigradus;Muchlinsky 2008;Rossieet al. 2006). Several omomyiforms (e.g.Shoshonius,Necrolemur) have a large IOF, likeAzibius. In mammals, the IOF transmits the infraorbital nerve and a small artery to the maxillary region; a large IOF is correlated with an increase in vibrissa number, which is characteristic of nocturnal species (Muchlinsky 2008). The large IOF inAzibius thus indicates a fine sensory acuity of the face, and strengthens the hypothesis of a nocturnal activity pattern. Comparative three-dimensional microtomographic reconstructions show that the course of the lacrimal canals inAzibius is oblique rostroventrally (figure 2a–b) as in all living strepsirhines, adapiforms (e.g.Adapis) and omomyiforms (e.g.Microchoerus;figure 3). In contrast,Tarsius and all anthropoids (Rossieet al. 2006), including taxa with long snouts such asTheropithecus, show a lacrimal canal that is vertical and oriented perpendicular to the infraorbital canal (figure 3). The maxilla ofAzibius, although partially preserved, thus reveals distinctive cranial traits that allow us to exclude anthropoid affinities for azibiids.

Consequently, the first unquestionable occurrence of anthropoids in Afro–Arabia is the parapithecoidBiretia from the late middle to early late Eocene of Algeria (Bir El Ater) and Egypt (Birket Qarun Locality 2) (de Boniset al. 1988;Seiffertet al. 2005a). This result, along with the recent discovery of a putative early Eocene eosimiid in India (Bajpaiet al. 2008; see alsoRoseet al. 2009) and the well-supported basal position of this primate family within the anthropoids (Kayet al. 1997;Jaeger & Marivaux 2005;Bajpaiet al. 2008), seems to support a South Asian origin for anthropoids (Beard2004,2006) and a subsequent dispersal into Africa during the middle Eocene. Such a mammalian dispersal event between Africa and South Asia has also been proposed for several groups including anthracotheriid artiodactyls, and anomaluroid and hystricognathous rodents (Tabuce & Marivaux 2005;Gheerbrant & Rage 2006).

However, this paleobiogeographical issue for the early evolution of anthropoids is complicated by (i) the morphological gap between African parapithecoids and Asian eosimiids and (ii) the poorly documented omomyiformAltiatlasius from the late Paleocene of Morocco (Sigéet al. 1990), which was recently reconsidered either as a stem primate (Tabuceet al. 2004;Marivaux 2006;Silcox 2008) or a possible eosimiid-like anthropoid (Beard2004,2006;Seiffertet al. 2005a;Marivaux 2006;Bajpaiet al. 2008; our phylogenetic results, see figure S2 in the electronic supplementary material). As such,Altiatlasius could be the earliest anthropoid, a record that equivocally supports an African origin of anthropoids during the late Paleocene, or their early dispersal into Africa from Asia, at least during the Paleocene (Beard 2006). This would extend the root of the Anthropoidea clade back to the Paleocene. In the absence of any undisputedAltiatlasius descendant in Africa during the early to middle Eocene (with the exception of two half-teeth, putatively related toAltiatlasius, from the Lutetian of Morocco (Tabuceet al. 2005), a Paleocene African origin of anthropoids would imply a big gap of about 20 Myr in the anthropoid fossil record in Africa, pre-dating the first appearance of the earliest parapithecoids. The existence of such a long ghost lineage seems speculative given the debate surrounding the phylogenetic affinities ofAltiatlasius. Indeed, the extremely fragmentary nature ofAltiatlasius cautions against over-interpreting its affinities, especially in light of the example ofAlgeripithecus.

(c). Higher-level affinities of the Azibiidae

Phylogenetic analyses of primates based on craniodental and postcranial characters show that azibiids are nested within the Strepsirhini clade, settingAlgeripithecus clearly apart from the Anthropoidea clade. The analysis reveals two major groups within Strepsirhini (figure 4): (i) the paraphyletic adapiforms mainly known from the Eocene of Europe, North America and Asia (Godinot 1998;Marivauxet al. 2006); and (ii) an Eocene–Oligocene Afro–Arabian clade that gave rise to living crown strepsirhines (lemurs, lorises, galagos) (Seiffertet al.2003,2005b;Godinot 2006). Within this Afro–Arabian clade, azibiids are successive sister taxa of djebelemurines (Djebelemur,Hartenberger & Marandat 1992; ‘Anchomomys’milleri,Simons 1997b) and a group that embracesPlesiopithecus (Simons 1992;Simons & Rasmussen 1994a) and crown strepsirhines, including their late Eocene–Oligocene fossil representatives from the Fayum, that is,Wadilemur,Saharagalago andKaranisia (Seiffertet al.2003,2005b;figure 4), and possiblyOmanodon andShizarodon from the Oligocene of Oman (Gheerbrantet al. 1993;Godinot 2006). Also, noteworthy is the putative lemuriformBugtilemur from the Asian Oligocene, which is now regarded as a peculiar adapiform without direct affinities with crown strepsirhines (Marivauxet al. 2006). Within the paraphyletic adapiforms, the European cercamoniineAnchomomys appears to be the sister taxa of the Afro–Arabian strepsirhine clade.Anchomomys does not present, however, the derived characters of the Paleogene Afro–Arabian taxa, notably the overlapping and the anterior coronal elevation of lower premolars. The tree topology could be explained by some convergences on molars betweenAnchomomys species and ‘Anchomomys’milleri, hence the initial name given to this Fayum primate (see alsoSeiffertet al. 2005b). Considering the middle Eocene age of the oldestAnchomomys and the much earlier age of both azibiids andDjebelemur, it is difficult to conceive that a European ‘anchomomyine’ lineage, having developed a hypocone, gave rise to the Afro–Arabian strepsirhine clade.

Within this group, the djebelemurines and crown strepsirhines have more derived lower molars than the azibiids by the development of a mesial fovea built by the connection of the long curved paracristid with the premetacristid. Except on the M₃ ofAzibius, where this mesial fovea occurs, azibiids show instead a short premetacristid on M_2–3 (generally absent on M₁), which is usually isolated from the paracristid. Lower molars ofOmanodon andPlesiopithecus also display this incomplete mesial fovea. Furthermore, azibiids along withDjebelemur,Plesiopithecus andWadilemur differ fromKaranisia,Saharagalago and ‘Anchomomys’milleri by the absence of the posterolingually protruding entoconid lobe on lower molars; inAzibius the entoconid is moderately expanded posteriorly on the M₁. On upper molars, azibiids are more primitive than crown strepsirhines by the association of a larger paraconule, a symmetrical crown without waisting of the distal border, and by the absence of the connection between the mesiolingually directed hypometaconulecrista and the postprotocrista (except on some M¹ ofAlgeripithecus).Azibius andPlesiopithecus differ in numerous premolar and molar traits but they share bunodont molars and, more importantly, a cranium with a short rostrum and very large orbits indicative of a nocturnal activity pattern. As many adapiforms are diurnal according to their rather small orbit sizes, they appear much more distant from crown strepsirhines than azibiids. This is critical regarding the ancestry of crown strepsirhines as this group was indeed considered as emerging from a nocturnal lineage (e.g.Godinot 2006). However, recent results based on opsin genes have shown that ancestral strepsirhines were diurnal or cathemeral, and that nocturnality has evolved several times within crown strepsirhines and haplorhines as well (Tanet al. 2005;Ankel-Simons & Rasmussen 2008). Despite the apparent lability of nocturnality, it is worth pointing out that some stem strepsirhines, such asAzibius, have already achieved this trait early in the Tertiary.

(d). The early diversity of ‘pre-toothcombed’ primates in Africa

The lower toothrow of crown strepsirhines is characterized by an unusual incisor–canine toothcomb, in which the incisiform canine is reduced and strongly procumbent (Rosenberger & Strasser 1985).Wadilemur andKaranisia provide the earliest fossil evidence for such a lower dental structure (Seiffertet al.2003,2005b). Djebelemurines are considered to be stem strepsirhines because they do not develop the toothcomb, their canine being only moderately reduced. The anterior dentition of azibiids is unknown, but the alveoli in front of P₃ in the mandible ofAlgeripithecus show that the canine alveolus is long, thin and forwardly inclined, suggesting that this tooth would be incisiform and procumbent (figure 1d–f). Such a canine may indicate that azibiids were toothcombed primates. The broadening of the maxilla at the level of the large canine inAzibius is also characteristic of the dental arcade morphology of some extant strepsirhines. However, as azibiids seem to diverge cladistically before djebelemurines (figure 4), a group without the toothcomb, this implies either the absence of a ‘true’ toothcomb in azibiids or its secondary loss in djebelemurines, a hypothesis that appears unlikely. Even if further evidence is required to ascertain the presence of a ‘true’ toothcomb in azibiids, it appears thatAlgeripithecus is unique among early Paleogene African primates documented to date in having a long and procumbent lower canine. This morphology seems compatible with the incisor–canine functional unit that pre-dates the toothcomb of crown strepsirhines. The toothcomb of crown strepsirhines is coupled with a P₂, which is often caniniform and commonly higher and/or larger than the other premolars. These derived traits, observed in Miocene and Recent strepsirhines (Fleagle 1999), are achieved as early as the late Eocene inWadilemur (Seiffertet al. 2005b). The tall and sub-caniniform P₂, along with the loss of P₁ and the reduced and procumbent canine, were proposed as synapomorphies of crown strepsirhines (Rasmussen & Nekaris 1998). Therefore, even ifAlgeripithecus possesses the two latter traits, its reduced P₂ seems to preclude direct relationships between azibiids and crown strepsirhines. However, this character is not as definite asKaranisia (a crown strepsirhine or even a stem lorisiform based on molar characters) and seems also to present a reduced P₂, thereby suggesting that the toothcomb could pre-date the specialization of the P₂ within Paleogene Afro–Arabian strepsirhines.

Thus, the question of whether azibiids are stem or crown strepsirhines is unresolved based on the known morphology of their front dentition. However, the phylogenetic analysis assessed on the global morphological evidence suggests that azibiids are the earliest offshoot of stem strepsirhines to the exclusion of adapiforms. Azibiids are furthermore characterized by numerous autapomorphic features such as a pronounced bunodonty of molars, a large hypocone, a loss of paraconid and high-crowned posterior premolars forming a blade-like structure. AsPlesiopithecus does by its very large procumbent lower canine, azibiids exemplify, therefore, an aberrant group of stem strepsirhines, reinforcing the diversity, unsuspected for a long time, of Afro–Arabian Paleogene strepsirhines. The apparent high degree of specialization of the azibiid family, associated with its late early or early middle Eocene age reveals the antiquity of this Afro–Arabian clade. As a result, we cannot exclude the possibility that this clade is rooted in a primitive, yet unknown, African lineage older than the earliest Eocene. This working hypothesis is tantalizing, especially in view of the age ofAltiatlasius, testifying to the presence of primates as early as the late Paleocene in Africa. The divergence time of crown strepsirhines, estimated by recent molecular analysis as between 67 and 84 Ma (Horvathet al. 2008), and the possibility thatAlgeripithecus displays a true toothcomb are two interesting arguments in favour of the great antiquity of ‘pre-toothcombed’ primates in Africa.

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