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Darwinius Masillae Is a Haplorhine D Reply to Williams Et Al

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Darwinius Masillae Is a Haplorhine D Reply to Williams Et Al Journal of Human Evolution 59 (2010) 574e579 Contents lists available at ScienceDirect Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol News and Views Darwinius masillae is a Haplorhine d Reply to Williams et al. (2010) Philip D. Gingerich a,*, Jens L. Franzen b,c, Jörg Habersetzer b, Jørn H. Hurum d, B. Holly Smith e a Museum of Paleontology and Department of Geological Sciences, University of Michigan, Ann Arbor, Michigan 48109, USA b Senckenberg Forschungsinstitut und Naturmuseum, Senckenberganlage 25, D-60325 Frankfurt, Germany c Naturhistorisches Museum, Augustinergasse 2, CH-4001 Basel, Switzerland d Naturhistorisk Museum, Universitetet i Oslo, Postboks 1172, Blindern, N-0318 Oslo, Norway e Museum of Anthropology, University of Michigan, Ann Arbor, Michigan 48109, USA article info Fossils are important for primate phylogeny because the origin of each of the major groups involves an evolutionary transition Article history: deep in geological time. Fossils calibrate these transitions and often Received 11 December 2009 support established relationships to living animals, but fossils may Accepted 21 May 2010 also change our understanding. Darwinius is an example of such Keywords: change. Primate phylogeny Williams et al. (2010: 567) describe Darwinius as a Anthropoid origins “crushed skeleton” and question our interpretation of Darwinius as Eocene primates a haplorhine primate (Franzen et al., 2009). Inference in our earlier Haplorhini study was based on the relative likelihood of membership in Strepsirrhini or Haplorhini, considered as alternative hypotheses. Here we apply the cladistic methods advocated by Williams et al. (2010), which, with a proper understanding of ‘total evidence,’ reaffirm our earlier interpretation that Darwinius is a haplorhine important for understanding the transition to Anthropoidea. Introduction A forty-seven-million-year-old primate Darwinius masillae from Preservation at Messel the middle Eocene of Messel in Germany is worthy of attention because it is one of the most complete fossil primates found to date Messel is a UNESCO World Heritage Site famous for extraordi- fl (Franzen et al., 2009). Darwinius is exceptional because it demon- nary preservation of a diverse ora of fossil plants and a diverse fi strates association of the skull, vertebral column, rib cage, arm, fauna of insects, sh, reptiles, birds, and mammals (Schaal and hand, leg, foot, body outline, and gastrointestinal contents of one Ziegler, 1992; Koenigswald et al., 1998; Franzen, 2007; Gruber fl individual primate in death position on a single plate of shale. and Micklich, 2007). All, like Darwinius, are more or less at as Completeness constrains speculation about bones that have not preserved. Seiffert et al. (2009), Williams et al. (2010), and others ’ fl been found, and association constrains conjecture about bones that infer from Darwinius atness that the skeleton must be crushed. belong together. Together these enable us to learn things about Thus it is important to consider how Messel fossils are preserved. Eocene primates that cannot be learned from fragmentary remains. Messel fossils represent Eocene organisms that died and settled Most primate fossils are isolated teeth, jaw fragments, or indi- to the bottom of an anoxic volcanic lake. All are preserved on vidual bones. Fragmentary fossils are important for documenting bedding planes in oil shale. Fossil mammals at Messel appear to be the distribution and diversity of primates through time, but most two-dimensional because they are often whole skeletons, which provide limited information relevant for higher-level phylogeny. collapse in thickness when tissues connecting the bones decom- Consequently, higher-level relationships of primates are based pose. Bulbous braincases are normally compressed, as are the largely on neontological comparisons of living lemurs, lorises, diaphyses of long bones, especially when they overlie each other. tarsiers, ceboids, cercopithecoids, and hominoids, for which we Compact bones of most skeletons retain their three-dimensional know soft-tissue anatomy, behavior, and complete skeletons. shape. Crown clades are defined by living taxa, and molecular approaches The two-dimensional nature of Messel fossils is exaggerated to phylogeny are necessarily focused on living animals. when they are collected because the fossils are found by separating oil shale along bedding planes. Presence of a fossil makes a bedding plane weaker, and thus separation often preferentially splits * Corresponding author. a fossil. This divides the fossil, leaving part and counterpart on E-mail address: [email protected] (P.D. Gingerich). separate slabs of oil shale, each containing a half-skeleton. In the 0047-2484/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2010.07.013 P.D. Gingerich et al. / Journal of Human Evolution 59 (2010) 574e579 575 process, individual bones are also split into part and counterpart on a list of 30 characteristics cited by authors as distinguishing these the two slabs. Specimens are then preserved by pouring a layer of groups. Most came from the classic monographs on Strepsirrhini epoxy resin over the split surface of each slab (polyester resin, used and Haplorhini by Hill (1953, 1955) and from the widely-used in former times, was banned in 1992). When cured, the resulting current primate textbook by Fleagle (1999). The purpose of this plates are turned and the remaining oil shale is removed from each. compilation was a statistical consideration of relative likelihood at As a result, one plate preserves the top lateral surface of a skeleton, a high taxonomic level. Thus it was important that the character- and a second plate preserves the bottom lateral surface of the same istics tabulated be (1) representative of the range of characteristics skeleton. In favorable circumstances an entire specimen is distinguishing high-level taxa, and (2) developmentally, function- preserved. Skeletons are sometimes incomplete because parts were ally, and evolutionarily as independent of each other as possible. lost due to predation or scavenging before a carcass settled to the Strepsirrhini and Haplorhini were originally recognized by char- bottom of the Messel lake, and bone is sometimes lost when part acteristics of soft anatomy that cannot be studied in fossils and counterpart are split during the collecting process. (Geoffroy Saint-Hilaire, 1812; Hubrecht, 1897; Pocock, 1918), but Williams et al. (2010) state that the ankle of Darwinius is too ancillary characteristics like a toothcomb in Strepsirrhini or spat- crushed to be certain of talofibular morphology, but there is no ulate incisors in Haplorhini can be recognized in fossils. crushing and little deformation of these robust bones visible on the We coded Table 3 of Franzen et al. (2009) as follows: strepsir- surface (Fig. 1). The fibular facet on the talus is partially covered by rhine characteristics were arbitrarily coded ‘0,’ and haplorhine the distal end of the fibula, but the talus is sufficiently well exposed characteristics were coded ‘1’ or sometimes ‘1’ and ‘2’ for two-step to show the slope of the lateral surface. The talus does not appear to characters. We added tree shrews or Tupaioidea, represented by be broken, let alone crushed. Tupaia, as an outgroup. Phylogenetic analysis using parsimony Two disadvantages of Messel preservation and of the process of (PAUP; Swofford, 2001) yielded two equally most-parsimonious preparation of Messel fossils are that bones of a skeleton cannot be cladograms of 37 steps. These have a high consistency index (0.84) removed and handled individually, and the joint surfaces of bones and high retention index (0.90). The two trees differ only in the often remain obscured by articulation. However, computerized monophyly or paraphyly of Strepsirrhini, and the cladogram with tomography (CT) now makes it possible, in favorable circum- Strepsirrhini monophyletic is shown in Figure 2, scaled as a phylo- stances, to remove virtual copies of individual bones to expose their gram to represent relative change (character coding and a full log of joint surfaces. There is a cost, because CT scanning is expensive and the analysis are provided in the Supplementary Online Material interpretation of images is both labor intensive and time- [SOM] that appears with the online version of this paper). consuming, which explains why our study of Darwinius is ongoing. Strepsirrhini, comprising Lemuroidea and Lorisoidea, is mono- Initial studies of Darwinius were focused on the skull and dentition phyletic at node 9 in Figure 2, and Haplorhini, comprising Tarsioi- (Franzen, 2000; Franzen et al., 2009) and on the digestive tract dea, Ceboidea, Cercopithecoidea, and Hominoidea, is monophyletic (Franzen and Wilde, 2003). Detailed CT studies of the hands and at node 13 in Figure 2. Most characteristics distinguishing Strep- feet of Darwinius and contemporary Messel primates are in sirrhini and Haplorhini are on the long stem connecting nodes 14 progress. and 13, but many are also on the long stem connecting nodes 13 and 12. Tarsioidea branches at node 13, reflecting its intermediate Cladistic analysis status in the spectrum of anatomical and morphological changes separating Strepsirrhini and Haplorhini. The strepsirrhine-haplorhine dichotomy can be considered from Changes in some characteristics such as postorbital closure are a phylogenetic point of view, and the characteristics distinguishing ambiguous, with partial closure
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