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HUMERAL HOMOLOGY and the ORIGIN of the TETRAPOD ELBOW: a REINTERPRETATION of the ENIGMATIC SPECIMENS ANSP 21350 and GSM 104536 by PER E

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HUMERAL HOMOLOGY and the ORIGIN of the TETRAPOD ELBOW: a REINTERPRETATION of the ENIGMATIC SPECIMENS ANSP 21350 and GSM 104536 by PER E [Special Papers in Palaeontology, 86, 2011, pp. 17–29] HUMERAL HOMOLOGY AND THE ORIGIN OF THE TETRAPOD ELBOW: A REINTERPRETATION OF THE ENIGMATIC SPECIMENS ANSP 21350 AND GSM 104536 by PER E. AHLBERG Subdepartment of Evolution and Development, Department of Organismal Biology, Uppsala University, Norbyva¨gen 18A, 752 36 Uppsala, Sweden; e-mail: [email protected] Typescript received 2 September 2010; accepted in revised form 28 February 2011 Abstract: Two putative tetrapod humeri of Devonian age, crownward of known tetrapod humeri. Contrary to previous ANSP 21350 from the late Famennian of Pennsylvania and claims, Acanthostega has a characteristic tetrapod ulnar mor- GSM 104536 from the late Frasnian of Scat Craig, Scotland, phology with an olecranon process; it does not resemble an are reinterpreted in the light of recent discoveries. The mor- elpistostegid ulna and is not uniquely primitive for tetrapods. phology of ANSP 21350 can be more fully homologized with This suggests that the flexed tetrapod elbow with ulnar those of elpistostegids and early tetrapods than previously extensor muscles attached to the olecranon evolved simulta- recognized. Unique features include distally displaced dorsal neously with the large rectangular entepicondyle typical for muscle attachments and a ventrally rotated distal face of the early tetrapods, probably as part of a single functional com- bone. This suggests that a weight-bearing ventrally directed plex. GSM 104536 is definitely not a primitive tetrapod forearm was created, not by means of a flexed elbow as in humerus, nor a sarcopterygian branchial bone, but cannot be other tetrapods, but by distorting the humerus. The olecra- positively identified at present. non process on the ulna was probably poorly developed or absent. Primitive characters that are absent in other tetrapods Key words: tetrapod, elpistostegid, humerus, elbow, olecra- add support to the contention that ANSP 21350 is the least non, Devonian. T he first step towards terrestrial locomotion in the tet- important changes occurred in the proximal parts of the rapod stem group involved the transformation of the appendage: the elbow, humerus, shoulder and associated pectoral fin into a weight-bearing appendage. The elpis- musculature. The humerus carries a number of processes tostegids Panderichthys and Tiktaalik both have enlarged and muscle attachment areas that can be homologized and incipiently limb-like pectoral fin skeletons but small between tetrapodomorph fishes, i.e. fish members of the pelvic fins and are interpreted to have supported them- tetrapod stem group, and tetrapods (Andrews and Wes- selves tripodally on the pectoral fins and tail (Vorobyeva toll 1970; Rackoff 1980; Panchen and Smithson 1987; and Kuznetsov 1992; Vorobyeva 2000; Boisvert 2005; Ahlberg 1989). Early research in this area focused largely Daeschler et al. 2006; Shubin et al. 2006; Boisvert et al. on establishing the detailed homologies between tetra- 2008). A further change in the morphology and function podomorph fish and tetrapod humeri, using a limited of the pectoral appendage occurred when the transforma- number of well-preserved exemplars such as the ‘osteolep- tion of the pelvic fin into a large hind limb coupled to iform’ fishes Eusthenopteron and Sterropterygion, and the the vertebral column via a sacrum allowed quadrupedal temnospondyl tetrapod Eryops (Andrews and Westoll walking to evolve, changing the biomechanical context in 1970; Rackoff 1980). Insofar as the details of the morpho- which the pectoral appendage operated. logical and functional transformation from fish to tetra- The transformation of the pectoral fin into a forelimb pod were considered, the analyses were strongly affected every aspect of its morphology (Hall 2007 and influenced by the, as we now know, very derived humeral references therein; Diogo et al. 2009). Visually most morphology of Eryops (Andrews and Westoll 1970; Rack- impressive were the loss of the fin web and the evolution off 1980). The only then known Devonian tetrapod of an autopod (hand) with digits, separated from the humerus, that of Ichthyostega, was interpreted by Jarvik zeugopod (forearm) by a flexible wrist. However, equally (1955, 1980) in a somewhat idiosyncratic manner – the ª The Palaeontological Association doi: 10.1111/j.1475-4983.2011.01077.x 17 18 SPECIAL PAPERS IN PALAEONTOLOGY, 86 anterior margin was identified as the ectepicondyle distal morphology is strongly autapomorphic but can nev- whereas the actual ectepicondyle was labelled ‘dorsal ertheless be homologized in detail with other tetrapods ridge’ – and as a result was largely disregarded by other and elpistostegids; that it represents an elbow architecture workers (Andrews and Westoll 1970). This situation different from all other known tetrapods; and that this began to change with the description in the 1980s and uniqueness reflects the evolution of weight-bearing adapta- 1990s of earlier and more primitive tetrapod humeri such tions in a very primitive limb. I also reconsider another as those of Proterogyrinus (Holmes 1984), Eoherpeton puzzling specimen, GSM 104536, interpreted as a Devo- (Smithson 1985), Greererpeton (Godfrey 1989), Acanthost- nian tetrapod humerus by Ahlberg (1991, 1998, 2004) but ega (Coates and Clack 1990; Coates 1996), Tulerpeton challenged by Shubin et al. (2004) and Coates et al. (2004). (Lebedev and Coates 1995), Whatcheeria (Lombard and Bolt 1995) and Baphetes (Milner and Lindsay 1998). The discovery of a tetrapod-like humerus in the elpistostegid MATERIALS AND METHODS Panderichthys (Vorobyeva 1992, 2000) further narrowed the morphological gap and paved the way for the first In addition to the published description and figures of detailed, phylogenetically constrained examinations of ANSP 21350, the comparison has been based on a high- humeral shape change across the fish–tetrapod transition fidelity cast of the specimen generously presented by E. B. (Coates 1996). Daeschler. The humerus of Panderichthys has been studied In 2004, Shubin and colleagues described a new Devo- from the CT scan model of specimen GIT 343-1 prepared nian tetrapod humerus, ANSP 21350, from the Famen- by Boisvert et al. (2008), with additional data from Vo- nian Catskill Formation of Pennsylvania. It has a number robyeva (2000). Other humeri are figured and discussed of primitive characteristics, combined with autapomor- on the basis of published information, although speci- phies that give the bone an unusual appearance and mens of Ichthyostega, Acanthostega and Tiktaalik have also imply a distinctive functional morphology (Shubin et al. been examined first-hand. Virtual thin sections of a 2004). Shubin et al. identified two sets of derived charac- humerus of Acanthostega, MGUH 29020, and the putative ters, one that first appears in elpistostegids (‘panderich- Elginerpeton humerus GSM 104536, were produced at the thyids’ in Shubin et al.) and which they argued to European Synchrotron Research Facility in Grenoble represent adaptations for trunk lifting and station holding using propagation phase contrast microtomography; this in water, and another that is exclusive to tetrapods work forms part of a collaboration with S. Sanchez, P. including ANSP 21350. The diversity of early tetrapod Tafforeau and J. A. Clack. humeral morphologies was highlighted and they drew specific attention to the differences between ANSP 21350 Institutional abbreviations. ANSP, Academy of Natural Sciences, and the humerus of Acanthostega, arguing that they repre- Philadelphia. GIT, Institute of Geology at Tallinn University of sent ‘two extremes of humeral design in the earliest tetra- Technology. GSM, GSd, British Geological Survey. MGUH, Geo- pods’ (Shubin et al. 2004, p. 92). logical Museum, University of Copenhagen. PIN, Palaeontologi- New discoveries over the past few years relating to the cal Institute, Academy of Sciences, Moscow. humeri of Tiktaalik (Shubin et al. 2006), Panderichthys (Boisvert et al. 2008; Boisvert 2009), Ichthyostega and Acanthostega (Callier et al. 2009) provide a richer compar- COMPARATIVE MORPHOLOGY ative context for ANSP 21350, allowing aspects of its As much of the discussion that follows centres on the unu- morphology – and humeral evolution across the fish– sual proportions of ANSP 21350, it is important to note tetrapod transition in general – to be reinterpreted from the beginning that the specimen appears to be dorso- (Text-fig. 1). I argue here that ANSP 21350 is the phyloge- ventrally compressed but not otherwise distorted. It has netically least crownward of known tetrapod humeri (an suffered extensive cracking, but the resulting cortical frag- interpretation consonant with Shubin et al. (2004) and ments have been neither pulled apart (indicating stretch- implied but not explicitly stated in that paper); that its TEXT-FIG. 1. Comparative morphology of elpistostegid and Devonian tetrapod humeri. Not to scale. Panderichthys reconstructed from scan of GIT 343-1 with additional information from Vorobyeva (2000) and Boisvert (2009). Tiktaalik modified from Shubin et al. (2006). ANSP 21350 modified from Shubin et al. (2004) and Callier et al. (2009). Ichthyostega and Acanthostega modified from Callier et al. (2009). Phylogeny based on generally accepted topologies (e.g. Daeschler et al. 2006) and evidence presented here. Abbreviations: ant. margin, anterior margin; dpc, deltopectoral crest; ect, ectepicondyle; ent, entepicondyle; lat. dorsi, latissimus dorsi attachment; pect. process, pectoral process; prepect, prepectoral space; ra, radial
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