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[Special Papers in Palaeontology, 86, 2011, pp. 17–29]

HUMERAL AND THE ORIGIN OF THE ELBOW: A REINTERPRETATION OF THE ENIGMATIC SPECIMENS ANSP 21350 AND GSM 104536 by PER E. AHLBERG Subdepartment of and Development, Department of Organismal , 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 age, crownward of known tetrapod humeri. Contrary to previous ANSP 21350 from the late 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 and is not uniquely primitive for . 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 was created, not by means of a flexed elbow as in , 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 in the tet- important changes occurred in the proximal parts of the rapod stem group involved the transformation of the : the elbow, humerus, and associated pectoral fin into a weight-bearing appendage. The elpis- musculature. The humerus carries a number of processes tostegids and both have enlarged and muscle attachment areas that can be homologized and incipiently -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 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 and Sterropterygion, and the the via a sacrum allowed quadrupedal temnospondyl tetrapod Eryops (Andrews and Westoll 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 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 () with digits, separated from the humerus, that of , 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 (Holmes 1984), 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 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 . 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 facet; scap-hum., scapulo-humeral muscle attachment; sup. ridge, supinator ridge; ul, ulnar facet. Interrupted purple shading in Tiktaalik and Acanthostega indicates uncertainty about the position and extent of the scapulo-humeral muscle attachment. AHLBERG: TETRAPOD HUMERI 19 20 SPECIAL PAPERS IN PALAEONTOLOGY, 86 ing) nor imbricated (indicating compression) anywhere on distally into the bone (another larger adjacent hole appears the bone. Furthermore, the articular surface of the humeral to be a puncture wound from a bite; Shubin et al. 2004). head is terminal, not shifted either dorsally or ventrally The distal margin of this featureless surface is a distinct (Shubin et al. 2004, fig. 1). It can thus safely be assumed raised edge with a - trajectory from the ectepicon- that features such as the positions of the various muscle dyle to the anterior edge of the bone. This edge also forms attachments and the ventral component of the orientation the dorsal margin of the aforementioned concave distal of the epipodial facets are natural, even though the bone is muscle attachment area. The concave surface is pierced by now almost certainly flatter than it was in . three small foramina (Shubin et al. 2004, fig. 1, ‘f, g, h’). ANSP 21350 has a number of unusual features (Text- Shubin et al. were not able to determine any detailed figs 1, 2): the confluent radial and ulnar facets are both homologies between this area and the corresponding ventrally positioned, the ectepicondyle projects further dis- regions of other humeri, beyond identifying a ‘broad shal- tally than in any other early tetrapod or elpistostegid, the low depression proximally for scapulohumeral muscle entepicondyle is smaller than in other early tetrapods but insertion’ and distally ‘an enlarged area for muscle inser- very robust and oriented transversely to the humeral shaft, tion above the radial condyle’ (Shubin et al. 2004, pp. 91– and there is a concave, distally facing muscle attachment 92, fig. 2, ‘8, 9’). In view of the fact that the processes on area above the radial facet (Shubin et al. 2004). On the ven- the anterior dorsal surface of the humerus have been tral face of the bone, the oblique transverse ridge is strongly homologized between tetrapodomorph fishes and tetra- developed and pierced by a row of foramina (Text-fig. 2B), pods (Andrews and Westoll 1970; Coates 1996) and more a primitive feature shared with elpistostegids and less recently between elpistostegids and tetrapods (Vorobyeva crownward tetrapodomorph fishes such as Eusthenopteron 2000; Boisvert 2009), this is an unsatisfactory state of (Andrews and Westoll 1970; Jarvik 1980), Sterropterygion affairs: the phylogenetic framework implies that it should (Rackoff 1980) and (Holland and Long 2009). be possible to interpret ANSP 21350 according to this Shubin et al. (2004) identified a pectoral process at the common pattern. anterior end of this ridge, but Callier et al. (2009) showed The key to reinterpreting ANSP 21350 is identifying the by comparison with Ichthyostega that the process is actually ridge that, in tetrapodomorph fishes and early tetrapods, located in the middle part of the ridge (Text-figs 1, 2B). runs anteriorly from the ectepicondyle towards the supina- This is the most primitive condition seen in any tetrapod, tor and deltoid processes. This ridge, hereafter termed the closely resembling the elpistostegid condition where no dis- ‘supinator ridge’ (see also Boisvert 2009), can be recog- tinct process is present but the highest part of the oblique nized inter alia in Eusthenopteron (Andrews and Westoll ridge occupies this same position (Callier et al. 2009). The 1970, text-fig. 10), Panderichthys (Vorobyeva 2000, fig. 2), emergence of a distinct pectoral process mirrors the break- Tiktaalik (Shubin et al. 2006, fig. 2), Ichthyostega (Jarvik up of the flexor muscle mass into dicrete muscles such as 1996, figs 44–45) and Acanthostega (Coates 1996, fig. 16; the pectoralis during the fish–tetrapod transition (Diogo Text-fig. 1, red). It is usually pierced by a short proximo- et al. 2009). distally oriented canal, the ectepicondylar foramen The dorsal surface of ANSP 21350 presents a bigger puz- (Andrews and Westoll 1970; Coates 1996; Boisvert 2009; zle. Anterior to the ectepicondyle the bone is almost fea- Callier et al. 2009), but in Panderichthys the canal is tureless, save for a small foramen of a canal that extends replaced by an open groove (contra Boisvert 2009). The supinator ridge forms the proximal boundary of a smooth and usually slightly concave area extending towards the AB radial facet (Text-fig. 1, pale green); the point where the ridge reaches the anterior margin of the bone (Text-fig. 1, orange) is marked by a distinct process coinciding with a dorsal inflection of the margin. In Acanthostega, there are two separate but almost confluent processes in this posi- tion, identified as supinator and deltoid processes by Coates (1996), but in the other taxa only a single process is evident. In ANSP 21350, the supinator ridge can be identified as the distally positioned ridge separating the featureless dorsal surface from the concave distal muscle attachment area (Text-fig. 1). As in the other taxa, it runs from the TEXT-FIG. 2. Photographs of cast of ANSP 21350 taken in ectepicondyle to the anterior margin of the bone, where it slanting light to emphasize muscle attachment areas. A, dorsal ends at a dorsally deflected process. It forms the proximal view. B, ventral view. Abbreviations as for Text-figure 1. boundary of a concave area extending to the radial facet. AHLBERG: TETRAPOD HUMERI 21

Furthermore, the three small foramina in the concave ABC area are probably in communication with the distally directed canal that opens on the middle of the featureless dorsal surface, because there is no other opening that appears well positioned to connect with them: this inferred branched canal running proximodistally under the ridge would correspond to the ectepicondylar fora- men (see also Boisvert 2009). The latissimus dorsi attachment is conserved between the elpistostegids Panderichthys and Tiktaalik, where it forms an area of oblique ridges (Vorobyeva 2000; Bois- vert 2009), and Acanthostega where it forms a single TEXT-FIG. 3. Schematic representation of the shape elongate process with the same position and orientation distortions ANSP 21350 has undergone compared to other early (Coates 1996; Text-fig. 1, pink). In Tulerpeton, a low tetrapod and elpistostegid humeri. A, dorsal. B, preaxial view. C, ridge with the same orientation extends between the ventral view. latissimus dorsi process and the deltoid process (Lebedev and Coates 1995). In ANSP 21350, the area proximal to This reinterpretation of ANSP 21350 implies a drastic the supinator ridge is in fact crossed by several proxi- but geometrically quite simple transformation compared mally-to-proximoposteriorly oriented faint ridges that to other early tetrapod and elpistostegid humeri. In effect probably represent this attachment (Text-fig. 1, pink; the proximal part of the dorsal surface of the humerus Text-fig. 2, lat. dorsi). In Ichthyostega, the latissimus dorsi has been stretched along the proximodistal axis, causing attachment is probably represented by a conspicuous the distal part of the dorsal surface to become compressed process on the proximal end of the ectepicondyle, ‘pro- and rotated ventrally along with the distal (i.e. articular) cess 1’ of Jarvik (1996). surface, which has been rotated into a ventral position On the anterior part of the proximal dorsal surface of (Text-fig. 3). The axis of rotation is oriented anteroposte- ANSP 21350, Shubin et al. (2004) identified a smooth riorly. This transformation explains not only the position concave surface as an insertion area for scapulohumeral of the supinator ridge and the existence of the concave muscles. However, just posterior to the concave area is a distal surface above the radial condyle, but also the ven- faintly convex but slightly recessed triangular region with tral orientation of the radial and ulnar condyles, the dis- a rugose surface texture that looks more convincingly like tally extended ectepicondyle, and the fact that the distal a scapulohumeral muscle attachment (Text-fig. 1, purple; margin of the entepicondyle runs posteroproximally from Text-fig. 2, scap-hum.). Interestingly, the smooth concave the ectepicondylar junction (rather than posteriorly or area can also be identified in Panderichthys, Tiktaalik posterodistally as in all the other taxa). Interestingly, the (pers. obs.), Ichthyostega, where it is very large and deep, junction between the oblique ventral ridge and the ante- and Acanthostega. The region immediately posterior to rior margin of the bone is also considerably more distal this hollow should, in each of these taxa, correspond to than in Ichthyostega (or than the anterior end of the ridge the rugose scapulohumeral muscle attachment of ANSP in Tiktaalik, Panderichthys and Eusthenopteron, where it 21350. In Ichthyostega, this position is occupied by a fails to contact the anterior margin of the bone), suggest- strongly developed, curving, rugose ridge that certainly ing that the anterior proximal part of the ventral surface looks like a muscle attachment. In Panderichthys, the has also been stretched along the proximodistal axis ridge is also present and again shows rugose texture (Text-figs 1, 3). (Boisvert 2009, fig. 2) although it is straighter and not quite as prominent. In Acanthostega, the same area is somewhat convex but shows no obvious attachment tex- FUNCTIONAL MORPHOLOGY AND ture, whereas the condition in Tiktaalik is undescribed. EVOLUTION Overall, the distribution of concave and convex surfaces on the proximal part of the dorsal surface of the humerus The transformation of the forearm and elbow appears to be conserved across the fish–tetrapod transi- tion, and there is some evidence that the posterior convex For a fuller understanding of ANSP 21350, it is necessary region is a scapulohumeral muscle attachment (Text- to consider the evolution of the elbow region across the fig. 1, purple). However, the condition in Tiktaalik and fish–tetrapod transition. The zeugopod or forearm of tet- Acanthostega must be regarded as uncertain. Compared to rapodomorph fishes such as Eusthenopteron, Gogonasus Ichthyostega and Panderichthys, the muscle attachment of and Rhizodopsis (Holland and Long 2009) is composed of ANSP 21350 is larger and more anteriorly positioned. a short, axially oriented ulna which articulates distally 22 SPECIAL PAPERS IN PALAEONTOLOGY, 86

D

A

E

B

F

C

G

TEXT-FIG. 4. Ulnar morphology of tetrapodomorph fishes and tetrapods. A–C, ulnae of A, Eusthenopteron (modified from Andrews and Westoll 1970), B, Panderichthys (original, based on CT model figured in Boisvert et al. 2008), and C, Tiktaalik (modified from Shubin et al. 2006). Dorsal views on left, proximal views (with dorsal surface uppermost) in middle, ventral views on right. D–G, ulnae of D, Acanthostega (from Coates 1996), E, Ichthyostega (modified from Jarvik 1996), F, Tulerpeton (from Lebedev and Coates 1995) and G, Eryops (from Pawley and Warren 2006). Anterior views on left, proximal views (with anterior surface uppermost) in middle, posterior views on right. Not to scale. Dark grey indicates articular surfaces. In the proximal views, pale grey indicates non- articular surfaces sloping away towards the distal end of the bone; non-articular surfaces level with or proximal to the humeral articulation are shown white. In D–G, a star indicates the olecranon process. Abbreviations: ext. cr, extensor crest; h, humeral articulation; in, facet for intermedium; uln, facet for ulnare. with another similar-sized element (the ulnare), and a gin of the ulna (Text-fig. 4), serving as the insertion much longer anterodistally diverging . The fully point of a powerful extensor muscle, the triceps brachii, developed tetrapod forearm, seen in the crown-group and which extends proximally along the posterodorsal surface in derived stem-group members such as Pederpes (Clack of the humerus and onto the (Diogo et al. and Finney 2005), differs in several important respects: 2009). This contrasts with the condition in the living the radius and ulna are approximately equal in length, lie lobe-finned fishes and Neoceratodus (Braus parallel to each other, and both articulate distally with a 1901; Millot and Anthony 1958), where the corresponding collection of small wrist bones. These features allow the but much shorter and broader extensor muscles originate zeugopod to function as a mechanical ‘segment’ between on the mid-dorsal surface of the humerus and insert on the humerus and wrist, while retaining the pronatory and the mid-dorsal surface of the ulna. As these fishes have a supinatory ability present in this part of the fish fin. straight elbow resembling that in tetrapodomorph fishes, Another key difference is the angle of the elbow: in tetra- it is reasonable to infer that the latter had a similar mus- podomorph fishes, the long axes of the ulna and humerus culature. The existence of the olecranon process in tetra- are aligned, so that the elbow is straight in resting posi- pods allows the elbow to be flexed and extended tion, but in all crown-group tetrapods except some sec- vigorously by the antagonistic action of the triceps brachii ondarily aquatic forms (e.g. and ), the and the flexors inserting on the radius and ulna. The long axis of the ulna is deflected anteroventrally so that functional significance of this transformation of the elbow the resting elbow is flexed. becomes apparent when comparing the pectoral fin Coupled to this flexure is the emergence of an olecra- movements of Latimeria and Neoceratodus with the fore- non process on the proximal corner of the posterior mar- limb walking movements of a sprawling tetrapod such as AHLBERG: TETRAPOD HUMERI 23 a or . In the fishes, the amplitude of the lier et al. 2009) is crushed, meaning that the bone has elbow movements is modest and contributes to the flex- been flattened to a significant degree, whereas juvenile ing and twisting of the fin in response to present hydro- and adult Eusthenopteron humeri are undeformed. ANSP dynamic requirements; in the tetrapods, high-amplitude 21350 must also have undergone substantial flattening, flexion and extension of the elbow is an essential compo- judging by its fractured surface. The main shape differ- nent of the stride cycle and is reflected in the pattern of ence between tetrapodomorph fish humeri on the one muscular activity during walking (Sze´kely et al. 1969). hand and elpistostegid and tetrapod humeri on the other thus seems to be that the latter have angular cross-sec- tions with sharp anterior margins; this renders them more Transitional morphologies, 1: the elpistostegids susceptible to dorsoventral compression owing to sedi- ment , leading to an exaggerated impression of The earliest stage in the transformation of the elbow and flatness. However, the strap-shaped morphology of the zeugopod is shown by the elpistostegids Panderichthys and humeral head in elpistostegids and early tetrapods is a Tiktaalik (Shubin et al. 2006; Boisvert et al. 2008). Pande- genuine difference from the tetrapodomorph fish condi- richthys has a lengthened ulna and shortened ulnare com- tion where the head is pear-shaped or rounded (Andrews pared to less crownward tetrapodomorph fishes such as and Westoll 1970; Shubin et al. 2004). These shape Eusthenopteron, whereas in Tiktaalik (in other respects a changes point to a reduction in the rotatory movement at more tetrapod-like and probably more crownward the shoulder joint in favour of more constrained antero- than Panderichthys) the ulna and ulnare are of similar size. posterior and dorsoventral movements (Shubin et al. However, the presence of hyperextensible in the dis- 2004). tal part of the fin skeleton suggests that Tiktaalik was able In the distal part of the humerus, the main novelty in to prop itself up on its pectoral fins (Shubin et al. 2006). elpistostegids is the shape of the ectepicondyle, which Shoulder girdle morphology and general body shape sug- becomes proximodistally elongate (Vorobyeva 2000; Shu- gest that this ability was also present in Panderichthys (Vo- bin et al. 2004, 2006). This lengthening may be related to robyeva and Kuznetsov 1992; Shubin et al. 2004, 2006). changes in the ulnar extensor musculature, which was Nevertheless, the resting position of the elbow is essentially probably bounded anteriorly by the posterior flank of the straight in these , there is no olecranon process ectepicondyle. Possibly the origin of the muscles shifted (Text-fig. 4B, C) and the flexibility of the elbow seems to proximally, lengthening them and allowing more powerful have been limited (Shubin et al. 2006; Boisvert et al. 2008). elbow extension. Interestingly, there is no evidence of The pectoral fins project posterolaterally from the body. enlarged elbow flexor muscles. The elpistostegid humerus is morphologically interme- diate between those of tetrapodomorph fishes and early tetrapods (Vorobyeva 2000; Shubin et al. 2004, 2006; Transitional morphologies, 2: the earliest tetrapods Coates and Ruta 2007; Boisvert 2009). The fish humeri usually have cylindrical shafts (e.g. Andrews and Westoll The earliest and phylogenetically least crownward flexed 1970; Rackoff 1980; but see Holland and Long 2009), elbows known from the record are those of Ichthyo- whereas elpistostegid and early tetrapod humeri are often stega and Acanthostega (Jarvik 1955, 1980, 1996; Coates described as flattened (e.g. Shubin et al. 2004; Coates and and Clack 1990; Coates 1996). In Ichthyostega, the ulna Ruta 2007). However, this apparent flattening is at least articulates with the distal end of the humerus and carries in part a preservational artefact. In the humeral material a large bifid olecranon process (Text-fig. 4E), while the of Panderichthys from Lode, Latvia, PIN 3547-19, which radius articulates anteroventrally on the humerus (Jarvik was figured by Vorobyeva (2000) and Boisvert (2009), is 1955, 1980, 1996; Callier et al. 2009). The radius and ulna extremely flat, whereas the humerus of GIT 343-1 (Bois- are of similar length, but the carpus and are vert et al. 2008; Boisvert 2009) is about three times dee- unknown. In Acanthostega, the radius and ulna both per with a diamond-shaped cross-section in its middle articulate distally with the humerus and the ulna is part (Text-fig. 1). The of GIT 343-1 is also narrower shorter than the radius (Coates and Clack 1990; Coates than those of Vorobyeva’s published specimens (Voroby- 1996). Coates (1996) stated that the ulna lacks an olecra- eva 1980; Vorobyeva and Schultze 1991) with vertical non process, a claim that has become established in the rather than splayed-out cheeks, suggesting that local literature (e.g. Janis and Farmer 1999; Carroll and taphonomic factors within the locality are responsible for Holmes 2007; Coates and Ruta 2007) as evidence of the different degrees of deformation. Tomographic studies primitive of this . In fact, a comparison with currently being carried out at the European Synchrotron other early tetrapod ulnae (Text-fig. 4D–G) shows that Radiation Facility show that the interior of the seemingly Acanthostega has a distinctively tetrapod ulnar morphol- well-preserved Acanthostega humerus MGUH 29020 (Cal- ogy and does possess an olecranon process. Unlike elpis- 24 SPECIAL PAPERS IN PALAEONTOLOGY, 86 tostegids and tetrapodomorph fishes (Text-fig. 4A–C), enlargement of the entepicondyle into a big subrectangu- where the proximal articular facet of the ulna is approxi- lar plate, which gives the early tetrapod humerus its mately circular and the sides of the bone all slope away characteristic L-shaped outline (Jarvik 1980, 1996; from this facet towards the slightly wider distal end, the Holmes 1984; Smithson 1985; Godfrey 1989; Coates and ulnae of the tetrapods are wider proximally than distally Clack 1990; Lebedev and Coates 1995; Lombard and and have a distinct posterior crest. This crest, the ‘exten- Bolt 1995; Coates 1996; Milner and Lindsay 1998). As sor crest’ of Pawley and Warren (2006), ends proximally the oblique ventral ridge runs along the proximal mar- in an olecranon process that is level with or elevated gin of the entepicondyle, this combined enlargement and above the proximal articular facet of the ulna (Text- shape change has the effect not only of greatly increas- fig. 4D–G). The very large and strongly elevated olecra- ing the available attachment area for ulnar flexors and non process of Ichthyostega is unique to that genus; other extensors, but also of increasing the distance between taxa, such as Tulerpeton and Eryops shown here, are more the ulnar facet and the oblique ridge. The long and nar- similar to Acanthostega. The poorly ossified state of the row ectepicondyle is also taller in the tetrapods than in process in MGUH 29019 (= MGUH f.n. 1227 of Coates elpistostegids (Shubin et al. 2004), creating space for a 1996), the only specimen of Acanthostega from which the thicker body of ulnar extensor musculature. These exten- ulna is known, may reflect the fact that this is a small sor muscles, inserting on the olecranon process, would and possibly immature individual (Callier et al. 2009). be homologues of the medial and lateral heads of the The early tetrapod humerus is modified in a number of triceps brachii of crown-group tetrapods (Diogo et al. respects relative to the elpistostegid humerus. The emer- 2009). The morphological novelties described here are gence of a distinct pectoral process, and the subsequent common not only to Ichthyostega and Acanthostega but anterior displacement of this process to form part of a persist in all more crownward stem-group and deltopectoral crest on the anterior margin of the bone, crown-group tetrapods (Lebedev and Coates 1995; must reflect changes in the flexor musculature running Coates 1996; Clack 2002; Carroll 2009); notwithstanding from the region to the humerus (Callier et al. the morphological and inferred functional diversity of 2009). As mentioned earlier, ANSP 21350 shows an early these humeri (Shubin et al. 2004), they must thus have stage of this transformation. Of greater interest in the shared certain functional characteristics that were not present context are those regions of the humerus that present in elpistostegids. serve as attachments for the flexor and extensor muscles Taken together, these changes in humeral morphology of the forearm. The area where the radial extensors origi- suggest that the origin of the flexed tetrapod elbow was nate (Text-fig. 1, red and pale green) differs little between associated initially with a greater change in ulnar than in elpistostegids, Ichthyostega and Acanthostega, except that radial movement patterns. The evolution of the olecranon adult individuals of Ichthyostega have a distinctive muscle process allowed the ulna to acquire the flexed resting scar near the margin of the radial facet (Callier et al. position and large proximally positioned extensor muscu- 2009) that is lacking in the others. On the ventral surface lature, coupled with high-amplitude flexion and extension of the bone, the oblique ventral ridge, which served as the movements, that characterizes sprawling locomotion in origin of radial flexors, is closer to the radial facet in tet- living tetrapods. This was followed slightly later by a rapods than in elpistostegids (much closer in Ichthyostega, proximal extension of the radial flexors. where the radius articulates ventrally). This presumably implies that the flexors inserted distally on the radius as they would otherwise have been very short. Crown-group The humeral morphology of ANSP 21350 tetrapods have a long radial flexor, either in the form of a humeroantebrachialis originating proximally on the We can now return to the peculiar morphology of ANSP humerus (in ) or a biceps brachii originating 21350. The ventrodistally facing radial and ulnar facets on the shoulder girdle (in ), that inserts proxi- imply that the forearm was oriented obliquely downwards mally on the radius (Diogo et al. 2009). However, in and that the limb had a weight-bearing function. An these animals, the oblique ventral ridge no longer exists, informative comparison can be made with Ichthyostega, and the pectoralis attachment has also moved far proxi- where the radial facet is oriented anteroventrally and the mally; this also applies to the humeri of early fossil elbow is permanently flexed (Jarvik 1980, 1996; Callier crown-group members (Coates 1996). It thus seems likely et al. 2009), suggesting a degree of functional similarity. that the radial flexors of early stem-group tetrapods were The fact that the distal part of ANSP 21350 nevertheless considerably shorter and ⁄ or more distally inserted on the differs from that of the Ichthyostega humerus in almost radius than those of the . every respect, and is far more divergent from the general The areas where the ulnar muscles originate are more condition in early tetrapods, is very interesting in this strongly modified. The most striking change is the context. AHLBERG: TETRAPOD HUMERI 25

The radial facet is oriented anterodistally both in elpis- rapods, and that its distinctive morphology represents an tostegids (especially Panderichthys) and in early tetrapods early attempt at producing a weight-bearing forelimb in such as Acanthostega (Text-fig. 1). The position of the an animal that had not yet evolved a fully developed radial facet in Ichthyostega appears simply to be an exag- tetrapod elbow joint. gerated, anteroventrally rotated version of this condition, a conclusion supported by the fact that the muscle attach- ment areas on the humerus for radial extensors differ lit- What is GSM 104536? tle between Ichthyostega and these other taxa. The ulna of Ichthyostega, articulating at an angle on a distal facet on The earliest reasonably extensive body of tetrapod skeletal the humerus, is in many ways similar to that of later tet- material comes from the late Frasnian locality of Scat (or rapods such as Eryops (Pawley and Warren 2006) and dif- Scaat) Craig in Scotland (Ahlberg 1991, 1995, 1998; Ahl- fers from that of Acanthostega mostly in having a much berg et al. 2005). It consists mostly of lower material, larger olecranon process (Text-fig. 4). The bent elbow of larger and smaller fragments from different individuals Ichthyostega is thus an exaggerated version of the general- that collectively document almost the whole ramus, but ized early tetrapod condition, with a more steeply there are also three incomplete premaxillae, some other inclined forearm, stronger olecranon process and anteri- fragmentary cranial elements, and a number of postcra- orly rotated foot compared to Acanthostega. nial bones. A binomen Elginerpeton pancheni was created ANSP 21350 is constructed on a different principle: it by Ahlberg (1995) for the lower and upper jaw material; has acquired a ventrally directed forearm by deforming some or all of the postcranial bones may also belong to the humerus rather than by flexing the elbow. The radial this genus but the attribution is of course less certain. and ulnar facets have been rotated to a ventral orientation The material is relevant here because it includes a puta- (Text-fig. 3), and both are almost flat. The actual elbow tive humerus, GSM 104536 (Text-fig. 5), which has been of ANSP 21350 was probably ‘straight’, in the sense that the subject of intensive debate (Ahlberg 1998, 2004; the proximal articular surfaces of both radius and ulna Coates et al. 2004; Shubin et al. 2004). The other postcra- were terminal so that the forearm extended orthogonally nial specimens, which include fragments of broadly Ich- from the facets on the humerus. If we assume that the thyostega-like pectoral and pelvic girdles along with an extensor surface of the radius proximally adjoined the incomplete and , are relatively uncontroversial dorsal margin of the radial facet, as it does in the other (Ahlberg 1998; Coates and Ruta 2007). taxa under consideration here, it follows that this surface As interpreted by Ahlberg (1991, 1998), GSM 104536 faced distally and (to an uncertain degree, depending on is a tetrapod humerus characterized by a small head, the exact shape of the specimen before postmortem flat- very short proximal shaft, large entepicondyle, no supi- tening) dorsally; in Ichthyostega, by contrast, it faces ante- nator foramen, ventrally positioned radial facet and no riorly (Jarvik 1996; Callier et al. 2009). More importantly, oblique ventral ridge (Text-fig. 5A–F). In the light of the ulnar facet of ANSP 21350 does not show even the more recent discoveries (Callier et al. 2009), we can also beginnings of a cylindrical curvature. The movement pat- note that the bone, under this interpretation, has a del- tern of the ulna must thus have been different from that topectoral crest rather than separate deltoid and pectoral in Ichthyostega and other tetrapods with flexed elbows processes as in Ichthyostega and ANSP 21350. It should such as Eryops. Although the entepcondyle is positioned immediately be apparent that this does not resemble the more proximally and is more transversely oriented than transitional and primitive tetrapod morphologies in elpistostegids, it remains small, and the ectepicondyle described earlier: primitive characters for the tetrapod is lower than in most other early tetrapods. This suggests humerus include a large humeral head, moderately long that the ulnar extensor musculature was weakly devel- proximal shaft, strongly developed oblique ventral ridge, oped. It is evident that the ulna had a restricted range of and discrete deltoid and pectoral processes separated by movement, particularly as regards extension, and it seems a prepectoral space (Shubin et al. 2004; Callier et al. quite likely that the olecranon process was poorly devel- 2009). If GSM 104536 is a humerus at all, it derives oped or absent. from a relatively crownward tetrapod, at least at the level In addition to these peculiar characteristics, ANSP of Tulerpeton or whatcheeriids (which is where the obli- 21350 displays a suite of primitive features that are absent que ventral ridge and ectepicondylar foramen disappear), in Ichthyostega, Acanthostega and more crownward tetra- which is also highly autapomorphic. pods: the small entepicondyle, weakly developed pectoral Alternatively, GSM 104536 may be a quite different process in the middle of the oblique ventral ridge, and bone. Interpretation is made more difficult by the fact large foramina piercing the oblique ventral ridge all fall that it, like many bones from Scat Craig, shows a combi- into this category (Shubin et al. 2004; Callier et al. 2009). nation of pristine and severely abraded surfaces. The This suggests that it is the least crownward of known tet- putative location of the ulnar articulation is abraded, 26 SPECIAL PAPERS IN PALAEONTOLOGY, 86 while the area where the entepicondylar foramen would known to occur at Scat Craig. They did not however have been located is broken. Coates et al. (2004) made a attempt to identify the bone. An investigation by propa- comparison with a porolepiform branchial element, gation phase contrast microtomography currently being mostly to illustrate the difficulties of interpreting isolated carried out at the European Synchrotron Radiation Facil- bones, but with an added note that porolepiforms are ity in Grenoble has revealed that the Scat Craig bones

A B

C D

E F

G

H AHLBERG: TETRAPOD HUMERI 27 have well-preserved histology. The femur, GSd 4240, of caution as it is a much smaller animal with a maxi- shows a thin cortex and extensive spongiosa similar to mum length of about 50 cm. Elpistostegids reached at the humeral histology of Acanthostega, but GSM 104536 least 1.5 m in length. Clarias moves over land by support- is extremely heavily ossified with a very thick cortex and ing itself alternately on left and right pectoral fin spines, thick-walled spongiosa (Text-fig. 5G–H). It is certainly twisting the body into a series of C-curves so that the tail not a branchial bone, because these are lightly ossified flips forward on the side where the pectoral fin is in con- with a thin cortex in sarcopterygian fishes (Jarvik 1972, tact with the ground. The head yaws strongly from side fig. 22, 1980, fig. 76), but it is harder to make a positive to side, and this yawing motion contributes most of the identification. If it is a limb bone, its histology most clo- stride length; the fins themselves are held rigid (Johnels sely resembles a relatively derived tetrapod (S. Sanchez, 1957). This type of locomotion does not require a flexible pers. comm. 2010; PEA, pers. obs), but it is also possible elbow. In a sprawling tetrapod walk, on the other hand, that it is a dermal element. Three-dimensional modelling yaw is much less important and may be altogether absent. of the histology should settle this question. Suffice it to This creates a requirement for the to be able to say that GSM 104536 remains an enigma, but that an achieve a reasonable stride length, which in turn requires identification as a primitive tetrapod humerus can now elbow flexion and extension. Trackway evidence indicates be discounted. It is either a quite derived (as well as auta- that the sprawling walk had evolved by the early Middle pomorphic) humerus or something else entirely. Devonian (Niedzwiedzki et al. 2010). A downward-sloping forearm and a flexible elbow with an olecranon process relate to different mechanical DISCUSSION AND CONCLUSIONS requirements during locomotion: the former is needed for lifting the body off the ground, whereas the latter ANSP 21350 was described by Shubin et al. (2004) as a enables forearm extension and flexion during the stride somewhat peculiar humerus, combining primitive and cycle. This distinction is important for the interpretation derived features and representing one extreme of a spec- of ANSP 21350. Although it is impossible to know the trum of early tetrapod humeral morphologies. The reinter- exact movement range of the forearm, it seems clear that pretation begun by Callier et al. (2009) and completed ulnar extension in particular was relatively limited. This here reveals that it is both more primitive and more auta- suggests a forelimb stride cycle rather different from that pomorphic than the original authors recognized. While its in other early tetrapods, possibly with a shorter stride. At overall architecture conforms more fully to the pattern the same time, the forelimb was evidently specialized for shared by elpistostegids and other early tetrapods than has weight-bearing. The overall impression is of an extremely previously been appreciated, the weakly developed and primitive tetrapod, perhaps with a relatively yaw-depen- centrally positioned pectoral process and the small entep- dent mode of walking, that was nevertheless fairly terres- icondyle indicate that it is the least crownward of known trial. It is remarkable that such an animal should be tetrapod humeri. Its distal end is modified in a unique found in the late Famennian, some 30 myr after the - manner that appears to reflect the need to create a weight- liest tetrapod footprints (Niedzwiedzki et al. 2010) and at bearing forearm in a limb without a fully developed olecra- a time when the tetrapod crown group may already have non process. This combination of characters makes it pos- been in existence (San Mauro et al. 2005). This further sible to draw some tentative inferences about the underscores the emerging picture of poor stratophyloge- transition from elpistosegid fin to tetrapod forelimb, and netic fit and large gaps in the fossil record of the earliest the position of ANSP 21350 in relation to this process. tetrapods (Callier et al. 2009; Friedman and Brazeau The ‘walking catfish’, Clarias batrachus, is often seen as 2011). While GSM 104536 remains an intractable puzzle, a reasonable interpretative model for elpistostegid terres- the discoveries of the last few years reveal ANSP 21350 trial locomotion (Vorobyeva and Kuznetsov 1992; Bois- to be even more informative about tetrapod origins than vert 2005), although it should be treated with a measure we thought.

TEXT-FIG. 5. A–F, specimen GSM 104536 from Scat Craig in A, dorsal, B, ventral, C, distal, D, proximal, E, preaxial and F, postaxial views (orientations following humeral interpretation of Ahlberg 1998). G, section image from propagation phase contrast synchrotron scan of same specimen, resolution 7.46 lm, with inset close-up image of the histology: the cortex is very thick and grades into a spongy core with robust trabeculae. H, section image from propagation phase contrast synchrotron scan of a probable femur from Scat Craig, GSd 4240 (see Ahlberg 1998, fig. 18), resolution 20 lm, with inset close-up image of the histology: this specimen shows a characteristic endoskeletal histology with a well-defined and relatively thin cortex sharply demarkated from a spongiosa of thin-walled trabeculae. Abbreviations (inverted commas indicate labelling following Ahlberg 1998): co, cortical bone; ‘dpc’, deltopectoral crest; ‘ect’, ectepicondyle; ‘ent’, entepicondyle; ‘he’, humeral head; ‘ra’, radial facet; sp, spongy endochondral bone. Vertical hatching denotes broken bone. 28 SPECIAL PAPERS IN PALAEONTOLOGY, 86

Acknowledgements. It gives me great pleasure to dedicate this —— MARK-KURIK, E. and AHLBERG, P. E. 2008. The paper to Angela Milner, as a tribute both to her professional pectoral fin of Panderichthys and the origin of digits. Nature, achievements and to our long friendship. Our acquaintance began 456, 636–638. in earnest, as I recall, over a Chinese dinner with her and Andrew BRAUS, H. 1901. Die Muskeln und Nerven der Ceratodus- in Belfast during the 1986 SVPCA meeting; 8 years later, she flosse: ein Beitrag zur vergleichenden Morphologie der freien became my boss when I started work in the Palaeontology Depart- Gliedmaase bei niederen Fischen und sur Archipterygiumthe- ment of the Natural History Museum. For the next 10 years, orie. Denkschriften der Medecinisch Naturwissenschaftlichen Angela kept a beady eye on my work. She was an outstanding Gesellschaft zu Jena, 4, 137–300. manager, unfailingly supportive and interested, who contributed CALLIER, V., CLACK, J. A. and AHLBERG, P. E. 2009. enormously to my enjoyment of the years at the NHM. Since my Contrasting developmental trajectories in the earliest known move to Sweden, we seem to have come full circle and are back to tetrapod forelimbs. Science, 324, 364–367. meeting over conference dinners, but it is always a pleasure to CARROLL, R. L. 2009. The rise of amphibians: 365 million catch up again and I nurture a small hope of eventually repaying years of evolution. The John Hopkins University Press, Balti- all the drinks I owe her. Thanks for everything, Angela! more, 392 pp. I am indebted to for presenting me with a —— and HOLMES, R. B. 2007. Evolution of the Appendicular high-quality cast of ANSP 21350 that has formed a cornerstone Skeleton of Amphibians. 185–224. In HALL, B. K. (ed.). of this work. Neil Shubin kindly gave permission to examine the into limbs: evolution, development and transformation. Univer- humeri of Tiktaalik, including undescribed material. I thank The sity of Chicago Press, Chicago, 344 pp. British Geological Survey for loaning specimens GSM 104536 CLACK, J. A. 2002. Gaining ground: the origin and early evolu- and GSd 4240. The synchrotron scans of GSM 104536, GSd 4240 tion of tetrapods. Indiana University Press, Bloomington, IN, and MGUH 29020 were performed by Paul Tafforeau of the USA, 369 pp. European Synchrotron Radiation Facility (ESRF) in Grenoble, —— and FINNEY, S. M. 2005. Pederpes finneyae, an articu- France; virtual thin sections were prepared from the scan data by lated tetrapod from the of Western Scotland. Sophie Sanchez, as part of ESRF project EC 351 and with addi- Journal of Systematic Palaeontology, 2, 311–346. tional funding from ERC Advanced Investigator Grant 233111. COATES, M. I. 1996. The Devonian tetrapod Acanthostega gunnari Jarvik: postcranial anatomy, basal tetrapod interrela- Editor. Andrew Milner tionships and patterns of skeletal evolution. Transactions of the Royal Society of Edinburgh: Sciences, 87, 363–421. —— and CLACK, J. A. 1990. Polydactyly in the earliest known REFERENCES tetrapod limbs. Nature, 347, 66–69. —— and RUTA, M. 2007. Skeletal changes in the transition AHLBERG, P. E. 1989. Paired fin skeletons and relationships of from fins to limbs. 15–38. In HALL, B. K. (ed.). Fins into the fossil group (: ). limbs: evolution, development and transformation. University of Zoological Journal of the Linnean Society, 96, 119–166. Chicago Press, Chicago, 344 pp. —— 1991. Tetrapod or near-tetrapod from the Upper —— SHUBIN, N. H. and DAESCHLER, E. B. 2004. Devonian of Scotland. Nature, 354, 298–301. Response to comment on ‘The early evolution of the tetrapod —— 1995. Elginerpeton pancheni and the earliest tetrapod . humerus’. Science, 305, 1715d. Nature, 373, 420–425. DAESCHLER, E. B., SHUBIN, N. H. and JENKINS, F. A. ——1998. Postcranial stem tetrapod remains from the Devonian Jr 2006. A Devonian tetrapod-like fish and the evolution of of Scat Craig, Morayshire, Scotland. Zoological Journal of the the tetrapod . Nature, 440, 757–763. Linnean Society, 122, 99–141. DIOGO, R., ABDALA, V., AZIZ, M. A., LONERGAN, N. —— 2004. Comment on ‘The Early Evolution of the Tetrapod and WOOD, B. A. 2009. From fish to modern – Humerus’. Science, 305, 1715d. , homologies and the evolution of the —— FRIEDMAN, M. and BLOM, H. 2005. New light on the pectoral and forelimb musculature. Journal of Anatomy, 214, earliest known tetrapod jaw. Journal of , 694–716. 25, 720–724. FRIEDMAN, M. and BRAZEAU, M. D. 2011. Sequences, ANDREWS, S. M. and WESTOLL, T. S. 1970. The postcra- stratigraphy and scenarios: what can we say about the fossil nial skeleton of Eusthenopteron foordi Whiteaves. Transactions record of the earliest tetrapods? Proceedings of the Royal Society of the Royal Society of Edinburgh, 68, 207–329. B, 278, 432–439. BOISVERT, C. A. 2005. The pelvic fin and girdle of Pande- GODFREY, S. J. 1989. The postcranial skeletal anatomy of the richthys and the origin of tetrapod locomotion. Nature, 438, tetrapod Greererpeton burkemorani. Philosophi- 1145–1147. cal Transactions of the Royal Society B, 323, 75–133. —— 2009. The humerus of Panderichthys in three dimensions HALL, B. K. (ed.) 2007. Fins into limbs: evolution, development, and its significance in the context of the fish-tetrapod and transformation. University of Chicago Press, Chicago, 344 transition. 297–305. In AHLBERG, P. E., BLOM, H. and pp. BOISVERT, C. A. (eds). Forty years of early : HOLLAND, T. and LONG, L. A. 2009. On the phyloge- papers from the 11th International Symposium on early and netic position of Gogonasus andrewsae Long 1985, within lower vertebrates. Acta Zoologica, 90 (Suppl. s1), 384 pp. the Tetrapodomorpha. 285–296. In AHLBERG, P. E., AHLBERG: TETRAPOD HUMERI 29

BLOM, H. and BOISVERT, C. A. (eds). Forty years of PAWLEY, K. and WARREN, A. 2006. The appendicular skel- early vertebrates: papers from the 11th International Sympo- eton of Eryops megacephalus Cope 1877 (: sium on early and lower vertebrates. Acta Zoologica, 90 (Sup- Eryopoidea) from the Lower of North America. Jour- pl. s1), 384 pp. nal of Paleontology, 80, 561–580. HOLMES, R. B. 1984. The Carboniferous Protero- RACKOFF, J. S. 1980. The origin of the tetrapod limb and the gyrinus scheelei Romer, and the early evolution of tetrapods. ancestry of tetrapods. 255–292. In PANCHEN, A. L. (ed.). Philosophical Transactions of the Royal Society B, 306, 431– The terrestrial environment and the origin of land vertebrates. 527. Academic Press, New York, 633 pp. JANIS, C. M. and FARMER, C. 1999. Proposed of SAN MAURO, D., VENCES, M., ALCOBENDAS, M., early tetrapods: , kidneys and the water-land transition. ZARDOYA, R. and MEYER, A. 2005. Initial diversification Zoological Journal of the Linnean Society, 126, 117–126. of living amphibians predated the breakup of . The JARVIK, E. 1955. The oldest tetrapods and their forerunners. American Naturalist, 165, 590–599. Scientific Monthly, 80, 141–154. SHUBIN, N. H., DAESCHLER, E. B. and COATES, M. I. —— 1972. Middle and Upper Devonian Porolepiformes from 2004. The early evolution of the tetrapod humerus. Science, East Greenland with special reference to Glyptolepis groenlan- 304, 90–93. dica n. sp. Meddelelser om Grønland, 187, 1–307. —— —— and JENKINS, F. A. Jr 2006. The pectoral fin of —— 1980. Basic structure and evolution of vertebrates, Vol. 1. Tiktaalik roseae and the origin of the tetrapod limb. Nature, Academic Press, London, 575 pp. 440, 764–771. —— 1996. The Devonian tetrapod Ichthyostega. Fossils and SMITHSON, T. R. 1985. The morphology and relationships of Strata, 40, 1–206. the Carboniferous amphibian Eoherpeton watsoni Panchen. JOHNELS, A. G. 1957. The mode of terrestrial locomotion in Zoological Journal of the Linnean Society, 85, 317–410. Clarias. Oikos, 8, 122–129. SZE´ KELY, G., CZE´ H, G. and VO¨ RO¨ S, G. 1969. The activity LEBEDEV, O. A. and COATES, M. I. 1995. The post- pattern of limb muscles in freely moving normal and deaffe- cranial skeleton of the Devonian tetrapod Tulerpeton curtum rented newts. Experimental Brain Research, 9, 53–62. Lebedev. Zoological Journal of the Linnean Society, 114, 307– VOROBYEVA, E. I. 1980. Observations on two rhipidistian 348. fishes from the Upper Devonian of Lode, Latvia. Zoological LOMBARD, R. E. and BOLT, J. R. 1995. A new primitive tet- Journal of the Linnean Society, 70, 191–201. rapod, Whatcheeria deltae, from the Lower Carboniferous of —— 1992. The problem of the terrestrial vertebrate origin. Nauka, Iowa. Palaeontology, 38, 471–494. Moscow, 344 pp [in Russian]. MILLOT, J. and ANTHONY, J. 1958. Anatomie de Latimeria —— 2000. Morphology of the humerus in the rhipidistian chalumnae. Tome I. Squelette, muscles et formations du soutien. Crossopterygii and the origin of tetrapods. Paleontological E´ ditions du CNRS, Paris, 122 pp. Journal, 34, 632–641. MILNER, A. C. and LINDSAY, W. 1998. Postcranial remains —— and KUZNETSOV, A. 1992. The locomotor apparatus of Baphetes and their bearing on the relationships of the of Panderichthys rhombolepis (Gross); a supplement to the Baphetidae (= Loxommatidae). Zoological Journal of the Lin- problem of fish-tetrapod transition. 131–140. In MARK- nean Society, 122, 211–235. KURIK, E. (ed.). Fossil fishes as living animals. Academy of NIEDZWIEDZKI, G., SZREK, P., NARKIEWICZ, K., Sciences of Estonia, Tallin, 299 pp. NARKIEWICZ, M. and AHLBERG, P. E. 2010. Tetrapod —— and SCHULTZE, H.-P. 1991. Description and systemat- trackways from the early Middle Devonian period of Poland. ics of panderichthyid fishes with comments on their relation- Nature, 463, 43–48. ship to tetrapods. 68–109. In SCHULTZE, H.-P. and PANCHEN, A. L. and SMITHSON, T. R. 1987. Character TRUEB, L. (eds). Origins of the higher groups of tetrapods: diagnosis, fossils, and the origin of tetrapods. Biological controversy and consensus. Cornell University Press, Ithaca, Reviews, 62, 341–438. NY, USA, 576 pp.