Skeletal and dental morphology supports diphyletic origin of baboons and mandrills

Abstract

Numerous biomolecular studies from the past 20 years have indicated that the large African monkeys Papio, Theropithecus, and Mandrillus have a diphyletic relationship with different species groups of mangabeys. According to the results of these studies, mandrills and drills (Mandrillus) are most closely related to the torquatus-galeritus group of mangabeys placed in the genus Cercocebus, whereas baboons (Papio) and geladas (Theropithecus) are most closely related to the albigena-aterrimus mangabeys, now commonly placed in the genus Lophocebus. However, there has been very little morphological evidence linking mandrills on the one hand and baboons and geladas on the other with different groups of mangabeys. In a study of mangabey locomotion and skeletal anatomy, we have identified features of the postcranial skeleton and the dentition that support the molecular phylogeny and clearly link mandrills with Cercocebus and Papio with Lophocebus. Moreover, the features linking Cercocebus and Mandrillus accord with ecological studies of these species indicating that these two genera are a cryptic clade characterized by unique adaptations for gleaning insects, hard nuts, and seeds from the forest f loor.Mangabeys are a group of large African monkeys characterized by moderately projecting snouts, large incisors, hollow cheek bones, long limbs, and long tails (1-3). They are found throughout much of sub-Saharan Africa from Senegal on the west to Kenya and Tanzania on the east (4). Traditionally placed in a single genus Cercocebus (5-6), these monkeys are commonly divided into two species groups-the terrestrial species galeritus, torquatus, atys, and agilis in one group, and the arboreal species albigena and aterrimus in another group. The three largest African monkeys, mandrills, baboons, and geladas have long been considered a single radiation of closely related species, commonly placed in three separate genera Mandrillus, Papio, and Theropithecus. In 1976, immunological studies by Cronin and Sarich (7) and demonstrated that the two species groups of mangabeys were polyphyletic with respect to other papionins. The albigena group was more closely related to baboons and geladas, whereas the torquatus-galeritus group was more closely related to mandrills and macaques. Groves (2) reported numerous cranial differences between the two species groups and urged separation of the albigena group into a separate genus, Lophocebus. Most recently Nakatsukasa (9-11) has documented skeletal differences between the two genera of mangabeys that distinguish the more terrestrial (12-15) Cercocebus from the more arboreal (16-19) Lophocebus. Subsequent molecular studies, especially by Disotell (20, 21) and colleagues (22,23) have confirmed the polyphyly of the mangabeys and clarified that the central African mandrills and drills (Mandrillus) are the sister taxon of Cercocebus whereas Lophocebus, Papio, and Theropithecus form a separate, unresolved clade.

The relative correspondence of cranial and genetic distances in papionin taxa and the impact of allometric adjustments

“…In particular, one subset of mangabeys (now called Lophocebus) was suggested to be more closely related to baboons (Papio), and the other (Cercocebus) to drills and mandrills (Mandrillus). Dental and postcranial similarities among the Cercocebus/Mandrillus and Lophocebus/Papio pairs were uncovered shortly thereafter, further supporting the idea of paraphyly in this clade (Fleagle and McGraw, 1999;2002;McGraw and Fleagle, 2006;Gilbert, 2007).…”

“…Numerous studies have described allometric patterning in papionin cranial morphology (Fleagle and McGraw, 1999;2002;Frost et al, 2003;Gilbert, 2007;Gilbert et al, 2009), the result of which can obscure the phylogenetic signal in the skull of this tribe (Gilbert and Rossie, 2007;Gilbert et al, 2009;Gilbert, 2011). While considerable discussion has centered around how to adjust for unwanted allometric cranial characteristics to reveal underlying phylogenetic and taxonomic information (Frost et al, 2003;Gilbert and Rossie, 2007;Gilbert et al, 2009;Gilbert, 2011), no consensus exists as to the most effective method of allometric adjustment, particularly in the case of 3D geometric morphometric data.…”

“…Previous studies of cranial morphology in the papionin taxa have suggested relatively high levels of craniomorphic homoplasy in this tribe (Fleagle and McGraw, 1999;Lockwood and Fleagle, 1999;McGraw and Fleagle, 2006;Gilbert, 2007;Gilbert et al, 2009). Phylogenetic studies based on traditional morphometric variables resulted in three primary groups of papionins initially being recognized: mangabeys, baboons, and geladas (Thorington and Groves, 1970;Jolly, 1972;Szalay and Delson, 1979;Strasser and Delson, 1987).…”

“…Previous studies have revealed notable sex differences in the patterns of cranial morphology between male and female papionin primates (Fleagle and McGraw, 1999;2002;Frost et al, 2003;McGraw and Fleagle, 2006;Gilbert, 2007;Gilbert et al, 2009). Thus, in order to determine whether the degree of correspondence between cranial matrices and the genetic distance matrix varied between the sexes, we also conducted separate sex analyses.…”

“…Many papionin species are characterized by extreme sexual dimorphism, and considerable size differences exist among sexes and taxa (Jolly, 1972;Groves, 1978;Fleagle and McGraw, 1999). As such, some aspects of their cranial morphology appear homoplastic, until the influence of sexual dimorphism and body size allometry are thoroughly accounted for (Singleton, 2002;Frost et al, 2003;Gilbert and Rossie, 2007;Gilbert, 2008;Gilbert et al, 2009;Gilbert, 2011).…”