Anthropoid versus strepsirhine status of the African Eocene primates Algeripithecus and Azibius: craniodental evidence

Abstract

Recent fossil discoveries have demonstrated that Africa and Asia were epicentres for the origin and/or early diversification of the major living primate lineages, including both anthropoids (monkeys, apes and humans) and crown strepsirhine primates (lemurs, lorises and galagos). Competing hypotheses favouring either an African or Asian origin for anthropoids rank among the most hotly contested issues in paleoprimatology. The Afrocentric model for anthropoid origins rests heavily on the >45 Myr old fossil Algeripithecus minutus from Algeria, which is widely acknowledged to be one of the oldest known anthropoids. However, the phylogenetic position of Algeripithecus with respect to other primates has been tenuous because of the highly fragmentary fossils that have documented this primate until now. Recently recovered and more nearly complete fossils of Algeripithecus and contemporaneous relatives reveal that they are not anthropoids. New data support the idea that Algeripithecus and its sister genus Azibius are the earliest offshoots of an Afro-Arabian strepsirhine clade that embraces extant toothcombed primates and their fossil relatives. Azibius exhibits anatomical evidence for nocturnality. Algeripithecus has a long, thin and forwardly inclined lower canine alveolus, a feature that is entirely compatible with the long and procumbent lower canine included in the toothcomb of crown strepsirhines. These results strengthen an ancient African origin for crown strepsirhines and, in turn, strongly challenge the role of Africa as the ancestral homeland for anthropoids.

Figure 1.

Algeripithecus minutus. (a) Composite of isolated P² (HGL50/297, reversed), P³ (HGL50/298, reversed), P⁴ (HGL50/299, reversed), M¹ (GZC7), M² (GZC1) and M³ (HGL50-321) in occlusal views. (b) M² (GZC1). (c) P⁴ (HGL50/299) in mesial and distal views, respectively. (d–f) Mandible with P₃–M₃ and alveoli for C–P₂ (denoted by red and yellow arrows, respectively) (HGL50/397) (d) in occlusal, (e) mesial and (f) labial views. (g) P_3–4 (HGL50/397) in lingual view. Scale bar, 1 mm.

Figure 2.

Azibius trerki. (a,b) Maxilla with P^3–4 (HGL51/46) in labial (a) and disto-lingual (b) views. (c) Composite of maxilla with M^1–2 (HGL50/396, reversed), P^3–4 and M³ with alveoli for C–P² (denoted by red and yellow circles, respectively) (HGL51/46) in occlusal view. (d) P³ (HGL51/46) and (e) P⁴ (GZC41) in distal view. (f) M₁ (HGL50/248, reversed) in occlusal view. (g,h) Mandible with P₃–M₃ (HGL50/256) in occlusal (g) and labial (h) views. Abbreviations: hard palate, hp; infra-orbital canals, ioc; infra-orbital foramens, iof; jugo-maxillary suture, jms; lacrimal canal, lc; orbital floor, of. Scale bar, 1 mm.

Figure 3.

Variability in the configuration of the lacrimal and infraorbital canal in extant and extinct primates (virtual three-dimensional surfaces derived from µCT image data; see text 3 and table S3 in the electronic supplementary material). (a) Adapis sp., (b) Microcebus murinus, (c) Microchoerus erinaceus, (d) Tarsius syrichta, (e) Cebus apella and (f) Aotus trivirgatus. Note how these canals tend to be perpendicular in anthropoids and Tarsius, but form a narrower angle in Azibius trerki (figure 2), crown and stem strepsirrhines and Microchoerus, an extinct omomyiform primate. Scale bar, 5 mm.

Figure 4.

Phylogenetic position of the azibiids Algeripithecus and Azibius (in bold) within the Strepsirhini clade (denoted by the asterisk). This topology results from an analysis, including 83 primate taxa and 341 dental, cranial and postcranial characters, having generated 369 equally most parsimonious trees of 2851 steps each (consistency index, CI = 0.1887; retention index, RI = 0.5335) (see text 2 and figure S2 in the electronic supplementary material). Abbreviations: Azibiidae, A.; Adapidae, Ad.; Djebelemurinae, D.; Sivaladapidae, S.