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Frontal Fusion: Collapse of Another Anthropoid Synapomorphy

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Frontal Fusion: Collapse of Another Anthropoid Synapomorphy THE ANATOMICAL RECORD 291:308–317 (2008) Frontal Fusion: Collapse of Another Anthropoid Synapomorphy 1,2,3 3 ALFRED L. ROSENBERGER AND ANTHONY S. PAGANO * 1Department of Anthropology and Archaeology, Brooklyn College, CUNY, Brooklyn, New York 2American Museum of Natural History, New York, New York 3Department of Anthropology, City University of New York Graduate Center, New York Consortium in Evolutionary Primatology (NYCEP), New York, New York ABSTRACT We test the hypothesis that the fused interfrontal suture of anthro- poids is a uniquely distinguishing feature and a derived characteristic indicative of their monophyletic origin. Our survey of nonanthropoid primates and several archontan families indicates frontal fusion is wide- spread. It is most variable (fused, open or partially fused) inter- and intra-specifically among strepsirhines. The frontal bone is more commonly fused in living lemuroids and indrioids than among lorisoids. It appears to be fused regularly among Eocene adapids. Among nonanthropoid haplorhines, the interfrontal is fused in Tarsius, even in neonates and invariably in adults, probably also in all fossil tarsiiforms preserving the frontal bone, and in the late Eocene protoanthropoid Rooneyia. The plesiadapiform pattern remains uncertain, but fusion is ubiquitous among living tree shrews, colugos and bats. Distributional evidence implies that interfrontal fusion was present in the last common ancestor (LCA) of haplorhine primates and possibly in the LCA of euprimates as well. Anthropoids, therefore, cannot be defined cladistically by interfrontal fusion, not out of concern for homoplasy but because it is probably a primitive feature inherited from other taxa related to anthropoids. Fusion of the large anthropoid frontal bone, which was extended anteriorly to roof the orbits and expanded laterally in connection with a wide forebrain in the LCA of anthropoids and protoanthropoids, may have been preadap- tive to the evolution of the postorbital septum. The zygomatico-frontal suture of the septum may provide an alternative mechanism for dissipat- ing the calvarial strains of mastication formerly taken up by an open interfrontal suture. Anat Rec, 291:308–317, 2008. Ó 2008 Wiley-Liss, Inc. Key words: interfrontal suture; frontal bone; skulls; postor- bital septum; anthropoids; primate phylogeny; tar- siers It is widely believed that closure of the interfrontal Grant sponsor: the EU; Grant sponsor: the Jerome Lejeune suture in primates, that is, the development of a fused Foundation. frontal bone (closure of the metopic suture of humans), *Correspondence to: Anthony S. Pagano, Department of An- is a shared derived homology unique to anthropoids. thropology, City University of New York Graduate Center, New This view appears regularly in detailed studies of York Consortium in Evolutionary Primatology (NYCEP), 65 anthropoid cranial morphology and origins (e.g., Rosen- Fifth Avenue, New York, NY 10016-4309. Fax: 718-951-3169. berger, 1985; Rosenberger and Shea, 2000; Miller E-mail: [email protected] et al., 2005), technical syntheses on primate evolution Received 10 July 2007; Accepted 30 August 2007 (e.g., Simons, 1972: Martin, 1990), more general summa- DOI 10.1002/ar.20647 ries of the order’s history and anatomy (e.g., Conroy, Published online 30 January 2008 in Wiley InterScience (www. 1990; Fleagle, 1999; Ankel-Simons, 2000), and recent interscience.wiley.com). Ó 2008 WILEY-LISS, INC. FRONTAL FUSION IN PRIMATES 309 assessments of Eocene fossils thought to pertain to this oversimplifies the facts behind the story, for one Anthropoidea (e.g., Gunnell et al., 2002; Takai and Shi- outstanding ‘‘prosimian,’’ Tarsius, was not prosimianlike gehara, 2004; Beard et al., 2005). However, there is rea- in pattern. Montagu’s assessment was uncharacteristi- son to think that frontal fusion may not be an anthro- cally muted concerning tarsiers. He stated that the poid synapomorphy at all. As with the mandibular sym- interfrontal was fused in all the individuals he exam- physis, which was long considered a shared derived ined, but he also hedged his conclusion by stressing that feature of anthropoids based on comparisons of living his sample size, seven individuals and only one juvenile, platyrrhines and catarrhines (e.g., Rosenberger, 1986) meant his observation were not conclusive. He further but now appears to be contravened by the report of an tempered his comments by noting that Remane (1923, open symphysis in some Fayum anthropoids (e.g., cited in Montagu, 1937) found the one infant Tarsius Simons, 1990), the fossil evidence—this time of nonan- that he examined to have had a patent suture. thropoids—suggests that a fused frontal bone evolved Other experienced anatomists of the era were quite cer- early in the history of primates, suggesting it may be a tain of the tarsier condition. Woolard (1925, p 1077), in his primitive retention in the anthropoid morphotype. classic anatomical study of the tarsier, simply said, ‘‘The In this report, we contribute new information pertinent frontal bone is single.’’ Hill (1955) agreed: ‘‘...the frontal is to this question by surveying the status of the interfrontal single in the adult, there being no interfrontal suture.’’ suture in a large sample of modern strepsirhines, tarsiers, Duckworth (1915) had previously made a finer point by fossil tarsiiforms and other early euprimates, as well as saying that, in Tarsius, the frontal fused earlier in life colugos, bats, and tree shrews. In several cases, our per- than in other nonanthropoids. Modern morphologists, sur- sonal observations correct ambiguities or errors that have prisingly, have rarely remarked on the status of the inter- appeared in the literature regarding the condition of the frontal in tarsiers. Its fused condition has not been dis- interfrontal suture in critical fossils. We caution, however, puted, nor has this character state been invoked as evi- in view of the variability we discovered among modern dence for the tarsier–anthropoid hypothesis—as one would lemuriforms and lorisiforms, and the diversity of Eocene imagine it should have been—during the preparsimony strepsirhine taxa, many of which are not known from decades when the support for this idea was based on skulls, that questions remain about the distribution and extensive trait-by-trait character analyses of the skull evolution of interfrontal closure in nonhaplorhine eupri- (e.g., Cartmill and Kay, 1978; Cartmill, 1980, 1994; Mac- mates. We also did not personally examine plesiadapiform Phee and Cartmill, 1986). Nor was this point promulgated fossils, another diverse group crucial to the matter. during the formative period when the Haplorhini hypothe- While the idea of frontal fusion as an anthropoid hall- sis was being wrought by Pocock (1918), who already mark can be traced to workers in the early 20th century, believed that the expanded postorbital bar of Tarsius was it is likely that a major study by Montagu (1937) helped a cranial homology shared with anthropoids and a strong cement the notion. In a comprehensive cross-sectional measure of their close relationship. survey of over 5,000 modern primate specimens, Ashley That the fused interfrontal has achieved almost iconic Montagu documented the near universality of early status as an anthropoid synapomorphy is evidenced by ontogenetic fusion of the interfrontal suture in anthro- rarity of any discussion of its evolution in a paleontologi- poids. Although Montagu’s survey was handicapped by cal context. Although those working on early higher pri- some notable taxonomic shortcomings in his appraisal of mate crania from the Fayum, or questionable Paleogene strepsirhines and callitrichines, for example, the large primate crania from the Far East, consistently point out sample sizes of platyrrhines and especially catarrhines, (or note when scoring characters) that the suture is and the range of specimens observed, from prenatals to fused in all of the anthropoid species for which the frontal infants to advanced adults, makes a convincing case is known (e.g., Simons, 1959, et seq.; Beard, 2002), few that all modern anthropoids do have a fused interfrontal have related this observation to nonanthropoid stocks suture. It should be noted for clarity that open interfron- implicated in anthropoid origins. One exception is the tal sutures, even in very young individuals, were found excellent character analysis of Ross (1994). Another excep- to be rare but not entirely inconsequential. Montagu tion is the review of Simons (1972). He drew attention to reported relatively high percentages of partially open several Eocene European tarsiiform fossils, including sutures in the sample of Pongo pygmaeus (21.8%, N 5 Necrolemur and some of its allies, where the frontals 87) and Macaca fascicularis (25%, N 5 16), and com- were known and proved to be merged, but he did not dis- pletely open sutures were recorded for Cercocebus chrys- cuss the possible systematic implications. Ross (1994) also ogaster (8.6%, N 5 35) and Cercopithecus aethiops noted that the interfrontal is fused in Necrolemur and (10.3%, N 5 29). Since then, however, some 70 years of wondered if that genus could be more closely related to additional observation made by numerous morphologists the hypothesized tarsier–anthropoid clade (see Ross and have not led to any questions about Montagu’s funda- Kay, 2004, for a review) he and his colleagues endorsed mental results regarding anthropoids. than the results of his parsimony analysis seemed to indi- In contrast,
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