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Ontogeny and Homoplasy in the Papionin Monkey Face

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Ontogeny and Homoplasy in the Papionin Monkey Face EVOLUTION & DEVELOPMENT 3:5, 322–331 (2001) Ontogeny and homoplasy in the papionin monkey face Mark Collarda* and Paul O’Higginsb aDepartment of Anthropology and AHRB Centre for the Evolutionary Analysis of Cultural Behaviour, University College London, Gower Street, London WC1E 6BT, UK bDepartment of Anatomy and Developmental Biology, University College London, London WC1E 6BT, UK *Author for correspondence (email: [email protected]) SUMMARY Recent molecular research has provided a con- whether the facial homoplasies exhibited by the adult papion- sistent estimate of phylogeny for the living papionin monkeys ins are to some degree present early in the post-natal period (Cercocebus, Lophocebus, Macaca, Mandrillus, Papio, and or whether they develop only later in ontogeny. The results of Theropithecus). This phylogeny differs from morphological our analyses go some way to resolving the debate over which phylogenies regarding the relationships of the mangabeys papionin genera display homoplasic facial similarities. They (Cercocebus and Lophocebus) and baboons (Mandrillus, Pa- strongly suggest that the homoplasic facial similarities are ex- pio, and Theropithecus). Under the likely assumption that the hibited by Mandrillus and Papio and not by Cercocebus and molecular estimate is correct, the incongruence between the Lophocebus, which share the putative primitive state with molecular and morphological data sets indicates that the latter Macaca. Our results also indicate that Mandrillus and Papio include numerous homoplasies. Knowledge of how these ho- achieve their homoplasic similarities in facial form not through moplasies emerge through development is important for un- simple extension of the ancestral allometric trajectory but derstanding the morphological evolution of the living papionins, through a combination of an extension of allometry into larger and also for reconstructing the phylogenetic relationships and size ranges and a change in direction of allometry away from adaptations of their fossil relatives. Accordingly, we have used the ancestral trajectory. Thus, the face of Mandrillus is not geometric morphometric techniques and the molecular phy- simply a hypermorphic version of the face of its sister taxon, logeny to investigate the ontogeny of a key area of morpho- Cercocebus, and the face of Papio is not merely a scaled-up logical homoplasy in papionins, the face. Two analyses were version of the face of its sister taxon, Lophocebus. Lastly, our carried out. The first compared allometric vectors of Cercoce- results show that facial homoplasy is not restricted to adult pa- bus, Lophocebus, Macaca, Mandrillus, and Papio to determine pionins; it is also manifest in infant and juvenile papionins. which of the facial resemblances among the genera are ho- This suggests that the homoplasic facial similarities between moplasic and which are plesiomorphic. The second analysis Mandrillus and Papio are unlikely to be a result of sexual se- focused on early post-natal facial form in order to establish lection. INTRODUCTION sub-Saharan Africa, from Kenya in the east, to Equatorial Guinea in the west, and to Angola in the south. Baboons are The tribe Papionini comprises the macaques, mangabeys, the largest Old World monkeys (12–50 kg). They are charac- and baboons. Paraphrasing Fleagle (1999), macaques are terized by long, robust limbs, elongated faces, pronounced medium- to large-sized monkeys (3–10 kg) with robust supraorbital tori, long molars, broad incisors, and, in males, limbs, moderately long faces, high-crowned but low-cusped daggerlike canines. Most taxonomists now divide baboons molar teeth, and long third molars. There are some 19 extant into three genera: Papio, the savannah baboon; Mandrillus, species of macaque, all of which are assigned to the genus the forest baboon; and Theropithecus, the gelada baboon. Macaca. Macaques are found throughout much of temperate Papio is widely distributed throughout the woodlands and and tropical Asia, as well as in parts of North Africa and on grasslands of sub-Saharan Africa, whereas Mandrillus is re- Gibraltar, to which they were introduced. Macaques occupy stricted to the forests of western Africa and Theropithecus is a broad range of habitats, from lowland secondary forests to limited to the grasslands of the Ethiopian highlands. upland hilly environments. Mangabeys are large (6–10 kg), Molecular and morphological analyses of papionin phy- stout-limbed monkeys that have elongated molars, very large logeny have reached different conclusions regarding the af- incisors, prognathic faces, and deeply excavated suborbital finities of the mangabeys (Cercocebus and Lophocebus) and fossae. There are four species of mangabey, two of which are baboons (Mandrillus, Papio, and Theropithecus). The con- assigned to the genus Cercocebus and two to the genus Lo- sensus molecular phylogeny (Fig. 1) suggests that the mang- phocebus. Mangabeys are found in many of the forests of abeys of the genus Cercocebus are most closely related to the © BLACKWELL SCIENCE, INC. 322 Collard and O’Higgins Ontogeny and homoplasy 323 forest baboons of the genus Mandrillus, whereas the mang- Secondly, because osseous characters can be highly influ- abeys of the genus Lophocebus are most closely related to enced by external stimuli, such as the forces generated by ha- the savannah baboons of the genus Papio and the gelada ba- bitual activities (Murray 1934; Currey 1968, 1984; Lieber- boons of the genus Theropithecus (Disotell 1994, 1996, man 1995, 1997, 1999, 2000; Lieberman et al. 1996), they 2000; Disotell et al. 1992; van der Kuyl et al. 1994; Harris can be expected to provide misleading information about and Disotell 1998; Harris 2000). In contrast, the majority of phylogeny more frequently than genetic characters, which morphological phylogenies have supported a sister-group re- are less subject to such stimuli. Thirdly, the methods of mo- lationship between Papio and Mandrillus and a sister-group lecular phylogenetics have been successfully tested on taxa relationship between Cercocebus and Lophocebus (Jolly of known phylogeny, whereas comparable tests of morpho- 1966, 1967, 1970; Delson 1975, 1993; Szalay and Delson logical phylogenetic methods have proved unsuccessful 1979; Strasser and Delson 1987; Delson and Dean 1993). (Fitch and Atchley 1987; Atchley and Fitch 1991; Hillis et One recent morphology-based phylogenetic analysis of the al. 1992). It may be argued that because these tests are based papionins supported a sister-group relationship between on subspecific taxa (e.g., inbred strains of mice), they are of Cercocebus and Mandrillus (Groves 2000), but another, little significance regarding the relationships among the pa- more comprehensive, analysis published in the same year pionin genera. However, we contend that since subspecific found strong support for phylogenetic relationships that are phylogenies can be expected to be more difficult to recon- incompatible with the consensus molecular phylogeny (Fig. struct than genus-level phylogenies, the tests actually pro- 2) (Collard and Wood 2000). vide strong reason to favor the molecular phylogeny for the It has been argued recently that there are several reasons papionins over any of the phylogenies based on their mor- for considering the molecular estimate of papionin phylog- phological characteristics. Lastly, the consensus molecular eny to be more accurate than the morphological one (Collard cladogram for the extant papionins is supported by several and Wood 2000, 2001). Firstly, in phylogenetics, morphol- sets of independent data (Disotell 1994, 1996, 2000; Disotell ogy can never be more than a proxy for genetic data as phy- et al. 1992; van der Kuyl et al. 1994; Harris and Disotell logenetic relationships are essentially genetic relationships. 1998; Harris 2000). These data sets differ regarding the rela- Fig. 1. Consensus molecular phylogeny for Papionini (Disotell 1994, 1996, 2000; Disotell et al. 1992; van der Kuyl et al. 1994; Fig. 2. Collard and Wood’s (2000) morphology-based phylogeny Harris and Disotell 1998; Harris 2000). for the papionin monkeys. 324 EVOLUTION & DEVELOPMENT Vol. 3, No. 5, September–October 2001 tionships among Lophocebus, Papio, and Theropithecus, but literature. Disotell (1994) and Harris (2000) have suggested they agree that Lophocebus, Papio, and Theropithecus form that the long faces of Mandrillus, Papio, and Theropithecus one clade within Papionini and that Cercocebus and Man- are independently derived from a common ancestor that ex- drillus form a second. Agreement among multiple indepen- hibited a similar facial form to Cercocebus and Lophocebus, dent data sets is the strongest support possible for a phyloge- whereas Groves (1978) and Kingdon (1997) have argued netic hypothesis. that the common ancestor of Cercocebus, Lophocebus, Man- If the consensus molecular phylogeny is accepted as ac- drillus, Papio, and Theropithecus was long-faced like Man- curate (cf. Fleagle and McGraw 1999; Collard and Wood drillus, Papio, and Theropithecus and that Cercocebus and 2000, 2001), then the disagreement between the phylogenies Lophocebus have independently reevolved shorter faces. derived from the molecular and morphological data sets in- It has been argued frequently that ontogenetic data can be dicates that the latter contain a large number of homopla- used to distinguish homologies from homoplasies (e.g., Nel- sies—similarities resulting from mechanisms other than de- son 1978; Reidl 1978; Patterson 1982; Roth
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