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Patterns of Astragalar Fibular Facet Orientation in Extant and Fossil Primates and Their Evolutionary Implications

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Patterns of Astragalar Fibular Facet Orientation in Extant and Fossil Primates and Their Evolutionary Implications AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 151:420–447 (2013) Patterns of Astragalar Fibular Facet Orientation in Extant and Fossil Primates and Their Evolutionary Implications Doug M. Boyer1* and Erik R. Seiffert2 1Department of Evolutionary Anthropology, Duke University, Durham, NC 27708 2Department of Anatomical Sciences, Stony Brook University, Health Sciences Center T-8, Stony Brook, NY 11794-8081 KEY WORDS astragalus; talus; fibula; haplorhine; strepsirrhine; ancestral states; Cantius; Teilhardina ABSTRACT A laterally sloping fibular facet of the catarrhines relative to non-callitrichine platyrrhines). astragalus (5talus) has been proposed as one of few Euprimate outgroups exhibit a mosaic of character osteological synapomorphies of strepsirrhine primates, states with Cynocephalus having a more obtuse strepsir- but the feature has never been comprehensively quanti- rhine-like facet and sampled treeshrews and plesiadapi- fied. We describe a method for calculating fibular facet forms having more acute haplorhine-like facets. orientation on digital models of astragali as the angle Surprisingly, the earliest species of the adapiform Can- between the planes of the fibular facet and the lateral tius have steep haplorhine-like facets as well. We used a tibial facet. We calculated this value in a sample that Bayesian approach to reconstruct the evolution of fibular includes all major extant primate clades, a diversity of facet orientation as a continuous character across a Paleogene primates, and nonprimate euarchontans (n 5 supertree of living and extinct primates. Mean estimates 304). Results show that previous characterization of a for crown Primatomorpha (97.9), Primates (99.5), Hap- divide between extant haplorhines and strepsirrhines is lorhini (98.7), and Strepsirrhini (108.2) support the hy- accurate, with little overlap even when individual data pothesis that the strepsirrhine condition is derived, points are considered. Fibular facet orientation is while lower values for crown Anthropoidea (92.8) and conserved in extant strepsirrhines despite major differ- Catarrhini (88.9) are derived in the opposite direction. ences in locomotion and body size, while extant Am J Phys Anthropol 151:420–447, 2013. VC 2013 Wiley anthropoids are more variable (e.g., low values for Periodicals, Inc. Beard et al. (1988), Gebo (1988, 1993, 2011), Gebo Darwinius masillae has exposed ambiguity in the identi- et al. (1991, 2000, 2001), Dagosto (1993), Dagosto and fication and phylogenetic interpretation of fibular facet Gebo (1994), Dagosto et al. (2008), Williams et al. (2009, orientation. Darwinius was described as having a 2010), Boyer et al. (2010), Maiolino et al. (2012), and straight-sided haplorhine-like facet (Franzen et al., many others have assessed trait variation among prima- 2009), but other researchers debated the accuracy of this tes with the goal of determining potential synapomor- assessment because the astragalar trochlea is not visible phies of a monophyletic Strepsirrhini (i.e., the extant in the flattened specimen, and the fibular facet is largely primate clade that includes the “toothcombed” lemuri- obscured by the articulating fibular malleolus (Seiffert form and lorisiform primates). The slope of the fibular et al., 2009; Williams et al., 2009; Boyer et al., 2010). facet of the astragalus has received considerable atten- Therefore, even this linchpin feature has been muddied tion because astragali are relatively common in the early by differences in perspective in the absence of quantifi- primate fossil record, and the feature is ostensibly both cation. This calls into question the reliability of previous easy to evaluate and consistently distinguishes strepsir- subjective assessments of this trait and reveals the need rhines from haplorhines (Beard et al., 1988; Gebo, 1988, 1993, 2011; Gebo et al., 2001). Fibular facet orientation has been particularly important for debates surrounding Grant sponsor: NSF; Grant number: BCS 1317525 (formerly BCS the phylogenetic position of the earliest crown primates, 1125507) and BCS 1231288 (to D.B. and E.S.); Grant sponsor: adapiforms and omomyiforms. Adapiforms have consis- American Association of Physical Anthropologists Professional De- tently been described as having laterally sloping fibular velopment Grant (in 2009 to D.B.); Grant sponsor: NSF DDIG; Grant number: SBE-1028505 (to S.C.). facets like those of extant strepsirrhines, while omomyi- forms have been described as having more acute haplor- *Correspondence to: Doug M. Boyer, Department of Evolutionary hine-like fibular facets (e.g., Gebo, 1988, 2011; Gebo Anthropology, Duke University, Durham, NC 27708, USA. E-mail: et al., 2012). The adapiform-strepsirrhine condition has [email protected] been interpreted as apomorphic relative to that of the primate common ancestor and supporting the placement Received 7 January 2013; accepted 28 March 2013 of adapiforms as stem members of Strepsirrhini (Beard et al., 1988; Gebo, 1988, 2011; Gebo et al., 2012). DOI: 10.1002/ajpa.22283 As obvious as this feature would appear to be, debate Published online in Wiley Online Library surrounding the middle Eocene Messel adapiform (wileyonlinelibrary.com). Ó 2013 WILEY PERIODICALS, INC. FIBULAR FACET ORIENTATION IN PRIMATES 421 for a more objective, quantitative approach to its evalua- modalities. Most specimens were scanned using one of tion. Boyer et al. (2010) measured this angle on a small four instruments: at SBU, two different ScancoMedical sample of digital models, and Rose et al. (2011) used the brand machines were used (VivaCT 75, mCT 40); at the same method to estimate the angle in earliest Eocene AMNH Microscopy and Imaging Facility, a Phoenix Teilhardina brandti. This first attempt at quantification brand v=tome=x s240 was used; and for specimens of Na- of fibular facet orientation is, however, difficult to repli- salis, Gorilla, Pan, and Pongo a GE eXplore Locus SP cate because of sensitivity to landmark choice. machine was used at the Ohio University mCT Facility. Here we describe a new method for assessing fibular A small subset of specimens was created with a Cyber- facet orientation and demonstrate that it has high ware 3D scanner. These include the Homo sample (from repeatability (less than 2% error on average). Use of 3D the New York medical collection housed in the AMNH digital models from high-resolution lCT scans allowed us Department of Anthropology), the Hoolock hoolock sam- to obtain data from the largest and smallest primates— ple, and AMNH 106581 and AMNH 106584 of the Sym- ranging in size from approximately 70 g to 200,000 g— phalangus sample. Specimens were mounted in foam or with the same measurement control and allowed us to packed in cotton to prevent movement while scanning. calculate rather than measure fibular facet orientation, Most specimens were scanned at a resolution of 39 lmor further reducing the potential for bias and interobserver less. The highest resolutions used were on the order of error. We present fibular facet orientation for 304 3–5 lm for the very smallest fossil specimens. The scan- euarchontans, of which 291 are euprimates (probable ning resolution was usually high enough to result in an crown primates=“primates of modern aspect”), and recon- initial polygonal mesh surface with between 1 million struct the evolutionary history of the trait within a and 5 million faces (i.e., the surface resulting from crea- Bayesian framework. tion of a “label field” representing the boundary between the bone and air in the image stack of raw CT data MATERIALS AND METHODS using the software Avizo 6-7, followed by application of Materials the “Surf-Gen” function with “no smoothing”). All speci- mens were subsequently downsampled using the Our sample of euarchontan astragali numbers 304 “simplify” function in Avizo 6-7 to between 300,000 and individuals, including 125 anthropoids (110 extant, 15 500,000 faces. See Appendix for the original scan resolu- fossil), 6 extant tarsiids, 86 extant strepsirrhines, 51 fos- tion of each specimen based on a microCT dataset. sil adapiforms, 23 omomyiforms, 4 fossil plesiadapiforms, 3 extant dermopterans, and 6 extant scandentians Measurements (Tables 1 and 2; Fig. 1; Appendix). Three measurements were taken on the astragalus (Fig. 2): trochlear width and ectal facet area were used Institutional abbreviations to represent overall size. Fibular facet angle was calcu- AMNH, American Museum of Natural History, New lated as the minimum angle formed between the plane York, NY; CGM, Egyptian Geological Museum, Cairo, of the dorsal aspect of the fibular facet and the plane Egypt; DPC, Duke Lemur Center Division of Fossil Pri- formed by the medial and lateral edges of the lateral tib- mates, Durham, NC; CM, Carnegie Museum of Natural ial facet. Specifically, we used linear regression to model History, Pittsburgh, PA; GU, H.N.B. Garhwal University, the plane of each facet, as represented by coordinates Srinagar, Uttarakhand, India; HTB, Cleveland Museum extracted from a 3D model of the astragalus, followed by of Natural History, Hamann-Todd non-human primate trigonometry to find the angle between the planes. osteological collection, Cleveland, OH; IRSNB, Institut Selecting anatomy for computing fibular facet Royal des Sciences Naturelles de Belgique, Brussels, Bel- orientation gium; IVPP, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, Each 3D model was opened in Avizo 7.0 (Fig. 2). Using China; MCZ, Museum of Comparative Zoology, Harvard the surface
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