HUMERAL HOMOLOGY AND THE ORIGIN OF THE

TETRAPOD ELBOW: A REINTERPRETATION OF THE

ENIGMATIC SPECIMENS ANSP 21350 AND

GSM 104536

by PER E. AHLBERGSubdepartment of Evolution and Development, Department of Organismal Biology, Uppsala University, Norbyvagen 18A, 752 36 Uppsala, Sweden;

e-mail: per.ahlberg@ebc.uu.se

Typescript received 2 September 2010; accepted in revised form 28 February 2011

Abstract: Two putative tetrapod humeri of Devonian age,

ANSP 21350 from the late Famennian of Pennsylvania and

GSM 104536 from the late Frasnian of Scat Craig, Scotland,

are reinterpreted in the light of recent discoveries. The mor-

phology of ANSP 21350 can be more fully homologized with

those of elpistostegids and early tetrapods than previously

recognized. Unique features include distally displaced dorsal

muscle attachments and a ventrally rotated distal face of the

bone. This suggests that a weight-bearing ventrally directed

forearm was created, not by means of a flexed elbow as in

other tetrapods, but by distorting the humerus. The olecra-

non process on the ulna was probably poorly developed or

absent. Primitive characters that are absent in other tetrapods

add support to the contention that ANSP 21350 is the least

crownward of known tetrapod humeri. Contrary to previous

claims, Acanthostega has a characteristic tetrapod ulnar mor-

phology with an olecranon process; it does not resemble an

elpistostegid ulna and is not uniquely primitive for tetrapods.

This suggests that the flexed tetrapod elbow with ulnar

extensor muscles attached to the olecranon evolved simulta-

neously with the large rectangular entepicondyle typical for

early tetrapods, probably as part of a single functional com-

plex. GSM 104536 is definitely not a primitive tetrapod

humerus, nor a sarcopterygian branchial bone, but cannot be

positively identified at present.

Key words: tetrapod, elpistostegid, humerus, elbow, olecra-

non, Devonian.

T he first step towards terrestrial locomotion in the tet-

rapod stem group involved the transformation of the

pectoral fin into a weight-bearing appendage. The elpis-

tostegids Panderichthys and Tiktaalik both have enlarged

and incipiently limb-like pectoral fin skeletons but small

pelvic fins and are interpreted to have supported them-

selves tripodally on the pectoral fins and tail (Vorobyeva

and Kuznetsov 1992; Vorobyeva 2000; Boisvert 2005;

Daeschler et al. 2006; Shubin et al. 2006; Boisvert et al.

2008). A further change in the morphology and function

of the pectoral appendage occurred when the transforma-

tion of the pelvic fin into a large hind limb coupled to

the vertebral column via a sacrum allowed quadrupedal

walking to evolve, changing the biomechanical context in

which the pectoral appendage operated.

The transformation of the pectoral fin into a forelimb

affected every aspect of its morphology (Hall 2007 and

references therein; Diogo et al. 2009). Visually most

impressive were the loss of the fin web and the evolution

of an autopod (hand) with digits, separated from the

zeugopod (forearm) by a flexible wrist. However, equally

important changes occurred in the proximal parts of the

appendage: the elbow, humerus, shoulder and associated

musculature. The humerus carries a number of processes

and muscle attachment areas that can be homologized

between tetrapodomorph fishes, i.e. fish members of the

tetrapod stem group, and tetrapods (Andrews and Wes-

toll 1970; Rackoff 1980; Panchen and Smithson 1987;

Ahlberg 1989). Early research in this area focused largely

on establishing the detailed homologies between tetra-

podomorph fish and tetrapod humeri, using a limited

number of well-preserved exemplars such as the ‘osteolep-

iform’ fishes Eusthenopteron and Sterropterygion, and the

temnospondyl tetrapod Eryops (Andrews and Westoll

1970; Rackoff 1980). Insofar as the details of the morpho-

logical and functional transformation from fish to tetra-

pod were considered, the analyses were strongly

influenced by the, as we now know, very derived humeral

morphology of Eryops (Andrews and Westoll 1970; Rack-

off 1980). The only then known Devonian tetrapod

humerus, that of Ichthyostega, was interpreted by Jarvik

(1955, 1980) in a somewhat idiosyncratic manner – the

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

ª The Palaeontological Association doi: 10.1111/j.1475-4983.2011.01077.x 17

anterior margin was identified as the ectepicondyle

whereas the actual ectepicondyle was labelled ‘dorsal

ridge’ – and as a result was largely disregarded by other

workers (Andrews and Westoll 1970). This situation

began to change with the description in the 1980s and

1990s of earlier and more primitive tetrapod humeri such

as those of Proterogyrinus (Holmes 1984), Eoherpeton

(Smithson 1985), Greererpeton (Godfrey 1989), Acanthost-

ega (Coates and Clack 1990; Coates 1996), Tulerpeton

(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

Panderichthys (Vorobyeva 1992, 2000) further narrowed

the morphological gap and paved the way for the first

detailed, phylogenetically constrained examinations of

humeral shape change across the fish–tetrapod transition

(Coates 1996).

In 2004, Shubin and colleagues described a new Devo-

nian tetrapod humerus, ANSP 21350, from the Famen-

nian Catskill Formation of Pennsylvania. It has a number

of primitive characteristics, combined with autapomor-

phies that give the bone an unusual appearance and

imply a distinctive functional morphology (Shubin et al.

2004). Shubin et al. identified two sets of derived charac-

ters, one that first appears in elpistostegids (‘panderich-

thyids’ in Shubin et al.) and which they argued to

represent adaptations for trunk lifting and station holding

in water, and another that is exclusive to tetrapods

including ANSP 21350. The diversity of early tetrapod

humeral morphologies was highlighted and they drew

specific attention to the differences between ANSP 21350

and the humerus of Acanthostega, arguing that they repre-

sent ‘two extremes of humeral design in the earliest tetra-

pods’ (Shubin et al. 2004, p. 92).

New discoveries over the past few years relating to the

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-

ative context for ANSP 21350, allowing aspects of its

morphology – and humeral evolution across the fish–

tetrapod transition in general – to be reinterpreted

(Text-fig. 1). I argue here that ANSP 21350 is the phyloge-

netically least crownward of known tetrapod humeri (an

interpretation consonant with Shubin et al. (2004) and

implied but not explicitly stated in that paper); that its

distal morphology is strongly autapomorphic but can nev-

ertheless be homologized in detail with other tetrapods

and elpistostegids; that it represents an elbow architecture

different from all other known tetrapods; and that this

uniqueness reflects the evolution of weight-bearing adapta-

tions in a very primitive limb. I also reconsider another

puzzling specimen, GSM 104536, interpreted as a Devo-

nian tetrapod humerus by Ahlberg (1991, 1998, 2004) but

challenged by Shubin et al. (2004) and Coates et al. (2004).

MATERIALS AND METHODS

In addition to the published description and figures of

ANSP 21350, the comparison has been based on a high-

fidelity cast of the specimen generously presented by E. B.

Daeschler. The humerus of Panderichthys has been studied

from the CT scan model of specimen GIT 343-1 prepared

by Boisvert et al. (2008), with additional data from Vo-

robyeva (2000). Other humeri are figured and discussed

on the basis of published information, although speci-

mens of Ichthyostega, Acanthostega and Tiktaalik have also

been examined first-hand. Virtual thin sections of a

humerus of Acanthostega, MGUH 29020, and the putative

Elginerpeton humerus GSM 104536, were produced at the

European Synchrotron Research Facility in Grenoble

using propagation phase contrast microtomography; this

work forms part of a collaboration with S. Sanchez, P.

Tafforeau and J. A. Clack.

Institutional abbreviations. ANSP, Academy of Natural Sciences,

Philadelphia. GIT, Institute of Geology at Tallinn University of

Technology. GSM, GSd, British Geological Survey. MGUH, Geo-

logical Museum, University of Copenhagen. PIN, Palaeontologi-

cal Institute, Academy of Sciences, Moscow.

COMPARATIVE MORPHOLOGY

As much of the discussion that follows centres on the unu-

sual proportions of ANSP 21350, it is important to note

from the beginning that the specimen appears to be dorso-

ventrally compressed but not otherwise distorted. It has

suffered extensive cracking, but the resulting cortical frag-

ments have been neither pulled apart (indicating stretch-

TEXT -F IG . 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 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.

18 S P E C I A L P A P E R S I N P A L A E O N T O L O G Y , 8 6

A H L B E R G : T E T R A P O D H U M E R I 19

ing) nor imbricated (indicating compression) anywhere on

the bone. Furthermore, the articular surface of the humeral

head is terminal, not shifted either dorsally or ventrally

(Shubin et al. 2004, fig. 1). It can thus safely be assumed

that features such as the positions of the various muscle

attachments and the ventral component of the orientation

of the epipodial facets are natural, even though the bone is

now almost certainly flatter than it was in life.

ANSP 21350 has a number of unusual features (Text-

figs 1, 2): the confluent radial and ulnar facets are both

ventrally positioned, the ectepicondyle projects further dis-

tally than in any other early tetrapod or elpistostegid, the

entepicondyle is smaller than in other early tetrapods but

very robust and oriented transversely to the humeral shaft,

and there is a concave, distally facing muscle attachment

area above the radial facet (Shubin et al. 2004). On the ven-

tral face of the bone, the oblique transverse ridge is strongly

developed and pierced by a row of foramina (Text-fig. 2B),

a primitive feature shared with elpistostegids and less

crownward tetrapodomorph fishes such as Eusthenopteron

(Andrews and Westoll 1970; Jarvik 1980), Sterropterygion

(Rackoff 1980) and Gogonasus (Holland and Long 2009).

Shubin et al. (2004) identified a pectoral process at the

anterior end of this ridge, but Callier et al. (2009) showed

by comparison with Ichthyostega that the process is actually

located in the middle part of the ridge (Text-figs 1, 2B).

This is the most primitive condition seen in any tetrapod,

closely resembling the elpistostegid condition where no dis-

tinct process is present but the highest part of the oblique

ridge occupies this same position (Callier et al. 2009). The

emergence of a distinct pectoral process mirrors the break-

up of the flexor muscle mass into dicrete muscles such as

the pectoralis during the fish–tetrapod transition (Diogo

et al. 2009).

The dorsal surface of ANSP 21350 presents a bigger puz-

zle. Anterior to the ectepicondyle the bone is almost fea-

tureless, save for a small foramen of a canal that extends

distally into the bone (another larger adjacent hole appears

to be a puncture wound from a bite; Shubin et al. 2004).

The distal margin of this featureless surface is a distinct

raised edge with a dog-leg trajectory from the ectepicon-

dyle to the anterior edge of the bone. This edge also forms

the dorsal margin of the aforementioned concave distal

muscle attachment area. The concave surface is pierced by

three small foramina (Shubin et al. 2004, fig. 1, ‘f, g, h’).

Shubin et al. were not able to determine any detailed

homologies between this area and the corresponding

regions of other humeri, beyond identifying a ‘broad shal-

low depression proximally for scapulohumeral muscle

insertion’ and distally ‘an enlarged area for muscle inser-

tion above the radial condyle’ (Shubin et al. 2004, pp. 91–

92, fig. 2, ‘8, 9’). In view of the fact that the processes on

the anterior dorsal surface of the humerus have been

homologized between tetrapodomorph fishes and tetra-

pods (Andrews and Westoll 1970; Coates 1996) and more

recently between elpistostegids and tetrapods (Vorobyeva

2000; Boisvert 2009), this is an unsatisfactory state of

affairs: the phylogenetic framework implies that it should

be possible to interpret ANSP 21350 according to this

common pattern.

The key to reinterpreting ANSP 21350 is identifying the

ridge that, in tetrapodomorph fishes and early tetrapods,

runs anteriorly from the ectepicondyle towards the supina-

tor and deltoid processes. This ridge, hereafter termed the

‘supinator ridge’ (see also Boisvert 2009), can be recog-

nized inter alia in Eusthenopteron (Andrews and Westoll

1970, text-fig. 10), Panderichthys (Vorobyeva 2000, fig. 2),

Tiktaalik (Shubin et al. 2006, fig. 2), Ichthyostega (Jarvik

1996, figs 44–45) and Acanthostega (Coates 1996, fig. 16;

Text-fig. 1, red). It is usually pierced by a short proximo-

distally oriented canal, the ectepicondylar foramen

(Andrews and Westoll 1970; Coates 1996; Boisvert 2009;

Callier et al. 2009), but in Panderichthys the canal is

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

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

ectepicondyle to the anterior margin of the bone, where it

ends at a dorsally deflected process. It forms the proximal

boundary of a concave area extending to the radial facet.

A B

TEXT -F IG . 2 . Photographs of cast of ANSP 21350 taken in

slanting light to emphasize muscle attachment areas. A, dorsal

view. B, ventral view. Abbreviations as for Text-figure 1.

20 S P E C I A L P A P E R S I N P A L A E O N T O L O G Y , 8 6

Furthermore, the three small foramina in the concave

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

elongate process with the same position and orientation

(Coates 1996; Text-fig. 1, pink). In Tulerpeton, a low

ridge with the same orientation extends between the

latissimus dorsi process and the deltoid process (Lebedev

and Coates 1995). In ANSP 21350, the area proximal to

the supinator ridge is in fact crossed by several proxi-

mally-to-proximoposteriorly oriented faint ridges that

probably represent this attachment (Text-fig. 1, pink;

Text-fig. 2, lat. dorsi). In Ichthyostega, the latissimus dorsi

attachment is probably represented by a conspicuous

process on the proximal end of the ectepicondyle, ‘pro-

cess 1’ of Jarvik (1996).

On the anterior part of the proximal dorsal surface of

ANSP 21350, Shubin et al. (2004) identified a smooth

concave surface as an insertion area for scapulohumeral

muscles. However, just posterior to the concave area is a

faintly convex but slightly recessed triangular region with

a rugose surface texture that looks more convincingly like

a scapulohumeral muscle attachment (Text-fig. 1, purple;

Text-fig. 2, scap-hum.). Interestingly, the smooth concave

area can also be identified in Panderichthys, Tiktaalik

(pers. obs.), Ichthyostega, where it is very large and deep,

and Acanthostega. The region immediately posterior to

this hollow should, in each of these taxa, correspond to

the rugose scapulohumeral muscle attachment of ANSP

21350. In Ichthyostega, this position is occupied by a

strongly developed, curving, rugose ridge that certainly

looks like a muscle attachment. In Panderichthys, the

ridge is also present and again shows rugose texture

(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-

ture, whereas the condition in Tiktaalik is undescribed.

Overall, the distribution of concave and convex surfaces

on the proximal part of the dorsal surface of the humerus

appears to be conserved across the fish–tetrapod transi-

tion, and there is some evidence that the posterior convex

region is a scapulohumeral muscle attachment (Text-

fig. 1, purple). However, the condition in Tiktaalik and

Acanthostega must be regarded as uncertain. Compared to

Ichthyostega and Panderichthys, the muscle attachment of

ANSP 21350 is larger and more anteriorly positioned.

This reinterpretation of ANSP 21350 implies a drastic

but geometrically quite simple transformation compared

to other early tetrapod and elpistostegid humeri. In effect

the proximal part of the dorsal surface of the humerus

has been stretched along the proximodistal axis, causing

the distal part of the dorsal surface to become compressed

and rotated ventrally along with the distal (i.e. articular)

surface, which has been rotated into a ventral position

(Text-fig. 3). The axis of rotation is oriented anteroposte-

riorly. This transformation explains not only the position

of the supinator ridge and the existence of the concave

distal surface above the radial condyle, but also the ven-

tral orientation of the radial and ulnar condyles, the dis-

tally extended ectepicondyle, and the fact that the distal

margin of the entepicondyle runs posteroproximally from

the ectepicondylar junction (rather than posteriorly or

posterodistally as in all the other taxa). Interestingly, the

junction between the oblique ventral ridge and the ante-

rior margin of the bone is also considerably more distal

than in Ichthyostega (or than the anterior end of the ridge

in Tiktaalik, Panderichthys and Eusthenopteron, where it

fails to contact the anterior margin of the bone), suggest-

ing that the anterior proximal part of the ventral surface

has also been stretched along the proximodistal axis

(Text-figs 1, 3).

FUNCTIONAL MORPHOLOGY ANDEVOLUTION

The transformation of the forearm and elbow

For a fuller understanding of ANSP 21350, it is necessary

to consider the evolution of the elbow region across the

fish–tetrapod transition. The zeugopod or forearm of tet-

rapodomorph fishes such as Eusthenopteron, Gogonasus

and Rhizodopsis (Holland and Long 2009) is composed of

a short, axially oriented ulna which articulates distally

A B C

TEXT -F IG . 3 . Schematic representation of the shape

distortions ANSP 21350 has undergone compared to other early

tetrapod and elpistostegid humeri. A, dorsal. B, preaxial view. C,

ventral view.

A H L B E R G : T E T R A P O D H U M E R I 21

with another similar-sized element (the ulnare), and a

much longer anterodistally diverging radius. The fully

developed tetrapod forearm, seen in the crown-group and

in derived stem-group members such as Pederpes (Clack

and Finney 2005), differs in several important respects:

the radius and ulna are approximately equal in length, lie

parallel to each other, and both articulate distally with a

collection of small wrist bones. These features allow the

zeugopod to function as a mechanical ‘segment’ between

the humerus and wrist, while retaining the pronatory and

supinatory ability present in this part of the fish fin.

Another key difference is the angle of the elbow: in tetra-

podomorph fishes, the long axes of the ulna and humerus

are aligned, so that the elbow is straight in resting posi-

tion, but in all crown-group tetrapods except some sec-

ondarily aquatic forms (e.g. whales and ichthyosaurs), the

long axis of the ulna is deflected anteroventrally so that

the resting elbow is flexed.

Coupled to this flexure is the emergence of an olecra-

non process on the proximal corner of the posterior mar-

gin of the ulna (Text-fig. 4), serving as the insertion

point of a powerful extensor muscle, the triceps brachii,

which extends proximally along the posterodorsal surface

of the humerus and onto the shoulder girdle (Diogo et al.

2009). This contrasts with the condition in the living

lobe-finned fishes Latimeria and Neoceratodus (Braus

1901; Millot and Anthony 1958), where the corresponding

but much shorter and broader extensor muscles originate

on the mid-dorsal surface of the humerus and insert on

the mid-dorsal surface of the ulna. As these fishes have a

straight elbow resembling that in tetrapodomorph fishes,

it is reasonable to infer that the latter had a similar mus-

culature. The existence of the olecranon process in tetra-

pods allows the elbow joint to be flexed and extended

vigorously by the antagonistic action of the triceps brachii

and the flexors inserting on the radius and ulna. The

functional significance of this transformation of the elbow

becomes apparent when comparing the pectoral fin

movements of Latimeria and Neoceratodus with the fore-

limb walking movements of a sprawling tetrapod such as

A

D

E

F

G

B

C

TEXT -F IG . 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.

22 S P E C I A L P A P E R S I N P A L A E O N T O L O G Y , 8 6

a salamander or lizard. In the fishes, the amplitude of the

elbow movements is modest and contributes to the flex-

ing and twisting of the fin in response to present hydro-

dynamic requirements; in the tetrapods, high-amplitude

flexion and extension of the elbow is an essential compo-

nent of the stride cycle and is reflected in the pattern of

muscular activity during walking (Szekely et al. 1969).

Transitional morphologies, 1: the elpistostegids

The earliest stage in the transformation of the elbow and

zeugopod is shown by the elpistostegids Panderichthys and

Tiktaalik (Shubin et al. 2006; Boisvert et al. 2008). Pande-

richthys has a lengthened ulna and shortened ulnare com-

pared to less crownward tetrapodomorph fishes such as

Eusthenopteron, whereas in Tiktaalik (in other respects a

more tetrapod-like and probably more crownward animal

than Panderichthys) the ulna and ulnare are of similar size.

However, the presence of hyperextensible joints in the dis-

tal part of the fin skeleton suggests that Tiktaalik was able

to prop itself up on its pectoral fins (Shubin et al. 2006).

Shoulder girdle morphology and general body shape sug-

gest that this ability was also present in Panderichthys (Vo-

robyeva and Kuznetsov 1992; Shubin et al. 2004, 2006).

Nevertheless, the resting position of the elbow is essentially

straight in these animals, there is no olecranon process

(Text-fig. 4B, C) and the flexibility of the elbow seems to

have been limited (Shubin et al. 2006; Boisvert et al. 2008).

The pectoral fins project posterolaterally from the body.

The elpistostegid humerus is morphologically interme-

diate between those of tetrapodomorph fishes and early

tetrapods (Vorobyeva 2000; Shubin et al. 2004, 2006;

Coates and Ruta 2007; Boisvert 2009). The fish humeri

usually have cylindrical shafts (e.g. Andrews and Westoll

1970; Rackoff 1980; but see Holland and Long 2009),

whereas elpistostegid and early tetrapod humeri are often

described as flattened (e.g. Shubin et al. 2004; Coates and

Ruta 2007). However, this apparent flattening is at least

in part a preservational artefact. In the humeral material

of Panderichthys from Lode, Latvia, PIN 3547-19, which

was figured by Vorobyeva (2000) and Boisvert (2009), is

extremely flat, whereas the humerus of GIT 343-1 (Bois-

vert et al. 2008; Boisvert 2009) is about three times dee-

per with a diamond-shaped cross-section in its middle

part (Text-fig. 1). The skull of GIT 343-1 is also narrower

than those of Vorobyeva’s published specimens (Voroby-

eva 1980; Vorobyeva and Schultze 1991) with vertical

rather than splayed-out cheeks, suggesting that local

taphonomic factors within the locality are responsible for

different degrees of deformation. Tomographic studies

currently being carried out at the European Synchrotron

Radiation Facility show that the interior of the seemingly

well-preserved Acanthostega humerus MGUH 29020 (Cal-

lier et al. 2009) is crushed, meaning that the bone has

been flattened to a significant degree, whereas juvenile

and adult Eusthenopteron humeri are undeformed. ANSP

21350 must also have undergone substantial flattening,

judging by its fractured surface. The main shape differ-

ence between tetrapodomorph fish humeri on the one

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

susceptible to dorsoventral compression owing to sedi-

ment pressure, leading to an exaggerated impression of

flatness. However, the strap-shaped morphology of the

humeral head in elpistostegids and early tetrapods is a

genuine difference from the tetrapodomorph fish condi-

tion where the head is pear-shaped or rounded (Andrews

and Westoll 1970; Shubin et al. 2004). These shape

changes point to a reduction in the rotatory movement at

the shoulder joint in favour of more constrained antero-

posterior and dorsoventral movements (Shubin et al.

2004).

In the distal part of the humerus, the main novelty in

elpistostegids is the shape of the ectepicondyle, which

becomes proximodistally elongate (Vorobyeva 2000; Shu-

bin et al. 2004, 2006). This lengthening may be related to

changes in the ulnar extensor musculature, which was

probably bounded anteriorly by the posterior flank of the

ectepicondyle. Possibly the origin of the muscles shifted

proximally, lengthening them and allowing more powerful

elbow extension. Interestingly, there is no evidence of

enlarged elbow flexor muscles.

Transitional morphologies, 2: the earliest tetrapods

The earliest and phylogenetically least crownward flexed

elbows known from the fossil record are those of Ichthyo-

stega and Acanthostega (Jarvik 1955, 1980, 1996; Coates

and Clack 1990; Coates 1996). In Ichthyostega, the ulna

articulates with the distal end of the humerus and carries

a large bifid olecranon process (Text-fig. 4E), while the

radius articulates anteroventrally on the humerus (Jarvik

1955, 1980, 1996; Callier et al. 2009). The radius and ulna

are of similar length, but the carpus and manus are

unknown. In Acanthostega, the radius and ulna both

articulate distally with the humerus and the ulna is

shorter than the radius (Coates and Clack 1990; Coates

1996). Coates (1996) stated that the ulna lacks an olecra-

non process, a claim that has become established in the

literature (e.g. Janis and Farmer 1999; Carroll and

Holmes 2007; Coates and Ruta 2007) as evidence of the

primitive nature of this taxon. In fact, a comparison with

other early tetrapod ulnae (Text-fig. 4D–G) shows that

Acanthostega has a distinctively tetrapod ulnar morphol-

ogy and does possess an olecranon process. Unlike elpis-

A H L B E R G : T E T R A P O D H U M E R I 23

tostegids and tetrapodomorph fishes (Text-fig. 4A–C),

where the proximal articular facet of the ulna is approxi-

mately circular and the sides of the bone all slope away

from this facet towards the slightly wider distal end, the

ulnae of the tetrapods are wider proximally than distally

and have a distinct posterior crest. This crest, the ‘exten-

sor crest’ of Pawley and Warren (2006), ends proximally

in an olecranon process that is level with or elevated

above the proximal articular facet of the ulna (Text-

fig. 4D–G). The very large and strongly elevated olecra-

non process of Ichthyostega is unique to that genus; other

taxa, such as Tulerpeton and Eryops shown here, are more

similar to Acanthostega. The poorly ossified state of the

process in MGUH 29019 (= MGUH f.n. 1227 of Coates

1996), the only specimen of Acanthostega from which the

ulna is known, may reflect the fact that this is a small

and possibly immature individual (Callier et al. 2009).

The early tetrapod humerus is modified in a number of

respects relative to the elpistostegid humerus. The emer-

gence of a distinct pectoral process, and the subsequent

anterior displacement of this process to form part of a

deltopectoral crest on the anterior margin of the bone,

must reflect changes in the flexor musculature running

from the coracoid region to the humerus (Callier et al.

2009). As mentioned earlier, ANSP 21350 shows an early

stage of this transformation. Of greater interest in the

present context are those regions of the humerus that

serve as attachments for the flexor and extensor muscles

of the forearm. The area where the radial extensors origi-

nate (Text-fig. 1, red and pale green) differs little between

elpistostegids, Ichthyostega and Acanthostega, except that

adult individuals of Ichthyostega have a distinctive muscle

scar near the margin of the radial facet (Callier et al.

2009) that is lacking in the others. On the ventral surface

of the bone, the oblique ventral ridge, which served as the

origin of radial flexors, is closer to the radial facet in tet-

rapods than in elpistostegids (much closer in Ichthyostega,

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

tetrapods have a long radial flexor, either in the form of

a humeroantebrachialis originating proximally on the

humerus (in amphibians) or a biceps brachii originating

on the shoulder girdle (in amniotes), that inserts proxi-

mally on the radius (Diogo et al. 2009). However, in

these animals, the oblique ventral ridge no longer exists,

and the pectoralis attachment has also moved far proxi-

mally; this also applies to the humeri of early fossil

crown-group members (Coates 1996). It thus seems likely

that the radial flexors of early stem-group tetrapods were

considerably shorter and ⁄ or more distally inserted on the

radius than those of the crown group.

The areas where the ulnar muscles originate are more

strongly modified. The most striking change is the

enlargement of the entepicondyle into a big subrectangu-

lar plate, which gives the early tetrapod humerus its

characteristic L-shaped outline (Jarvik 1980, 1996;

Holmes 1984; Smithson 1985; Godfrey 1989; Coates and

Clack 1990; Lebedev and Coates 1995; Lombard and

Bolt 1995; Coates 1996; Milner and Lindsay 1998). As

the oblique ventral ridge runs along the proximal mar-

gin of the entepicondyle, this combined enlargement and

shape change has the effect not only of greatly increas-

ing the available attachment area for ulnar flexors and

extensors, but also of increasing the distance between

the ulnar facet and the oblique ridge. The long and nar-

row ectepicondyle is also taller in the tetrapods than in

elpistostegids (Shubin et al. 2004), creating space for a

thicker body of ulnar extensor musculature. These exten-

sor muscles, inserting on the olecranon process, would

be homologues of the medial and lateral heads of the

triceps brachii of crown-group tetrapods (Diogo et al.

2009). The morphological novelties described here are

common not only to Ichthyostega and Acanthostega but

persist in all more crownward stem-group and basal

crown-group tetrapods (Lebedev and Coates 1995;

Coates 1996; Clack 2002; Carroll 2009); notwithstanding

the morphological and inferred functional diversity of

these humeri (Shubin et al. 2004), they must thus have

shared certain functional characteristics that were not

present in elpistostegids.

Taken together, these changes in humeral morphology

suggest that the origin of the flexed tetrapod elbow was

associated initially with a greater change in ulnar than in

radial movement patterns. The evolution of the olecranon

process allowed the ulna to acquire the flexed resting

position and large proximally positioned extensor muscu-

lature, coupled with high-amplitude flexion and extension

movements, that characterizes sprawling locomotion in

living tetrapods. This was followed slightly later by a

proximal extension of the radial flexors.

The humeral morphology of ANSP 21350

We can now return to the peculiar morphology of ANSP

21350. The ventrodistally facing radial and ulnar facets

imply that the forearm was oriented obliquely downwards

and that the limb had a weight-bearing function. An

informative comparison can be made with Ichthyostega,

where the radial facet is oriented anteroventrally and the

elbow is permanently flexed (Jarvik 1980, 1996; Callier

et al. 2009), suggesting a degree of functional similarity.

The fact that the distal part of ANSP 21350 nevertheless

differs from that of the Ichthyostega humerus in almost

every respect, and is far more divergent from the general

condition in early tetrapods, is very interesting in this

context.

24 S P E C I A L P A P E R S I N P A L A E O N T O L O G Y , 8 6

The radial facet is oriented anterodistally both in elpis-

tostegids (especially Panderichthys) and in early tetrapods

such as Acanthostega (Text-fig. 1). The position of the

radial facet in Ichthyostega appears simply to be an exag-

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-

tle between Ichthyostega and these other taxa. The ulna of

Ichthyostega, articulating at an angle on a distal facet on

the humerus, is in many ways similar to that of later tet-

rapods such as Eryops (Pawley and Warren 2006) and dif-

fers from that of Acanthostega mostly in having a much

larger olecranon process (Text-fig. 4). The bent elbow of

Ichthyostega is thus an exaggerated version of the general-

ized early tetrapod condition, with a more steeply

inclined forearm, stronger olecranon process and anteri-

orly rotated foot compared to Acanthostega.

ANSP 21350 is constructed on a different principle: it

has acquired a ventrally directed forearm by deforming

the humerus rather than by flexing the elbow. The radial

and ulnar facets have been rotated to a ventral orientation

(Text-fig. 3), and both are almost flat. The actual elbow

of ANSP 21350 was probably ‘straight’, in the sense that

the proximal articular surfaces of both radius and ulna

were terminal so that the forearm extended orthogonally

from the facets on the humerus. If we assume that the

extensor surface of the radius proximally adjoined the

dorsal margin of the radial facet, as it does in the other

taxa under consideration here, it follows that this surface

faced distally and (to an uncertain degree, depending on

the exact shape of the specimen before postmortem flat-

tening) dorsally; in Ichthyostega, by contrast, it faces ante-

riorly (Jarvik 1996; Callier et al. 2009). More importantly,

the ulnar facet of ANSP 21350 does not show even the

beginnings of a cylindrical curvature. The movement pat-

tern of the ulna must thus have been different from that

in Ichthyostega and other tetrapods with flexed elbows

such as Eryops. Although the entepcondyle is positioned

more proximally and is more transversely oriented than

in elpistostegids, it remains small, and the ectepicondyle

is lower than in most other early tetrapods. This suggests

that the ulnar extensor musculature was weakly devel-

oped. It is evident that the ulna had a restricted range of

movement, particularly as regards extension, and it seems

quite likely that the olecranon process was poorly devel-

oped or absent.

In addition to these peculiar characteristics, ANSP

21350 displays a suite of primitive features that are absent

in Ichthyostega, Acanthostega and more crownward tetra-

pods: the small entepicondyle, weakly developed pectoral

process in the middle of the oblique ventral ridge, and

large foramina piercing the oblique ventral ridge all fall

into this category (Shubin et al. 2004; Callier et al. 2009).

This suggests that it is the least crownward of known tet-

rapods, and that its distinctive morphology represents an

early attempt at producing a weight-bearing forelimb in

an animal that had not yet evolved a fully developed

tetrapod elbow joint.

What is GSM 104536?

The earliest reasonably extensive body of tetrapod skeletal

material comes from the late Frasnian locality of Scat (or

Scaat) Craig in Scotland (Ahlberg 1991, 1995, 1998; Ahl-

berg et al. 2005). It consists mostly of lower jaw material,

larger and smaller fragments from different individuals

that collectively document almost the whole ramus, but

there are also three incomplete premaxillae, some other

fragmentary cranial elements, and a number of postcra-

nial bones. A binomen Elginerpeton pancheni was created

by Ahlberg (1995) for the lower and upper jaw material;

some or all of the postcranial bones may also belong to

this genus but the attribution is of course less certain.

The material is relevant here because it includes a puta-

tive humerus, GSM 104536 (Text-fig. 5), which has been

the subject of intensive debate (Ahlberg 1998, 2004;

Coates et al. 2004; Shubin et al. 2004). The other postcra-

nial specimens, which include fragments of broadly Ich-

thyostega-like pectoral and pelvic girdles along with an

incomplete femur and tibia, are relatively uncontroversial

(Ahlberg 1998; Coates and Ruta 2007).

As interpreted by Ahlberg (1991, 1998), GSM 104536

is a tetrapod humerus characterized by a small head,

very short proximal shaft, large entepicondyle, no supi-

nator foramen, ventrally positioned radial facet and no

oblique ventral ridge (Text-fig. 5A–F). In the light of

more recent discoveries (Callier et al. 2009), we can also

note that the bone, under this interpretation, has a del-

topectoral crest rather than separate deltoid and pectoral

processes as in Ichthyostega and ANSP 21350. It should

immediately be apparent that this does not resemble the

transitional and primitive tetrapod morphologies

described earlier: primitive characters for the tetrapod

humerus include a large humeral head, moderately long

proximal shaft, strongly developed oblique ventral ridge,

and discrete deltoid and pectoral processes separated by

a prepectoral space (Shubin et al. 2004; Callier et al.

2009). If GSM 104536 is a humerus at all, it derives

from a relatively crownward tetrapod, at least at the level

of Tulerpeton or whatcheeriids (which is where the obli-

que ventral ridge and ectepicondylar foramen disappear),

which is also highly autapomorphic.

Alternatively, GSM 104536 may be a quite different

bone. Interpretation is made more difficult by the fact

that it, like many bones from Scat Craig, shows a combi-

nation of pristine and severely abraded surfaces. The

putative location of the ulnar articulation is abraded,

A H L B E R G : T E T R A P O D H U M E R I 25

while the area where the entepicondylar foramen would

have been located is broken. Coates et al. (2004) made a

comparison with a porolepiform branchial element,

mostly to illustrate the difficulties of interpreting isolated

bones, but with an added note that porolepiforms are

known to occur at Scat Craig. They did not however

attempt to identify the bone. An investigation by propa-

gation phase contrast microtomography currently being

carried out at the European Synchrotron Radiation Facil-

ity in Grenoble has revealed that the Scat Craig bones

A B

C D

E

G

F

H

26 S P E C I A L P A P E R S I N P A L A E O N T O L O G Y , 8 6

have well-preserved histology. The femur, GSd 4240,

shows a thin cortex and extensive spongiosa similar to

the humeral histology of Acanthostega, but GSM 104536

is extremely heavily ossified with a very thick cortex and

thick-walled spongiosa (Text-fig. 5G–H). It is certainly

not a branchial bone, because these are lightly ossified

with a thin cortex in sarcopterygian fishes (Jarvik 1972,

fig. 22, 1980, fig. 76), but it is harder to make a positive

identification. If it is a limb bone, its histology most clo-

sely resembles a relatively derived tetrapod (S. Sanchez,

pers. comm. 2010; PEA, pers. obs), but it is also possible

that it is a dermal element. Three-dimensional modelling

of the histology should settle this question. Suffice it to

say that GSM 104536 remains an enigma, but that an

identification as a primitive tetrapod humerus can now

be discounted. It is either a quite derived (as well as auta-

pomorphic) humerus or something else entirely.

DISCUSSION AND CONCLUSIONS

ANSP 21350 was described by Shubin et al. (2004) as a

somewhat peculiar humerus, combining primitive and

derived features and representing one extreme of a spec-

trum of early tetrapod humeral morphologies. The reinter-

pretation begun by Callier et al. (2009) and completed

here reveals that it is both more primitive and more auta-

pomorphic than the original authors recognized. While its

overall architecture conforms more fully to the pattern

shared by elpistostegids and other early tetrapods than has

previously been appreciated, the weakly developed and

centrally positioned pectoral process and the small entep-

icondyle indicate that it is the least crownward of known

tetrapod humeri. Its distal end is modified in a unique

manner that appears to reflect the need to create a weight-

bearing forearm in a limb without a fully developed olecra-

non process. This combination of characters makes it pos-

sible to draw some tentative inferences about the

transition from elpistosegid fin to tetrapod forelimb, and

the position of ANSP 21350 in relation to this process.

The ‘walking catfish’, Clarias batrachus, is often seen as

a reasonable interpretative model for elpistostegid terres-

trial locomotion (Vorobyeva and Kuznetsov 1992; Bois-

vert 2005), although it should be treated with a measure

of caution as it is a much smaller animal with a maxi-

mum length of about 50 cm. Elpistostegids reached at

least 1.5 m in length. Clarias moves over land by support-

ing itself alternately on left and right pectoral fin spines,

twisting the body into a series of C-curves so that the tail

flips forward on the side where the pectoral fin is in con-

tact with the ground. The head yaws strongly from side

to side, and this yawing motion contributes most of the

stride length; the fins themselves are held rigid (Johnels

1957). This type of locomotion does not require a flexible

elbow. In a sprawling tetrapod walk, on the other hand,

yaw is much less important and may be altogether absent.

This creates a requirement for the forelimbs to be able to

achieve a reasonable stride length, which in turn requires

elbow flexion and extension. Trackway evidence indicates

that the sprawling walk had evolved by the early Middle

Devonian (Niedzwiedzki et al. 2010).

A downward-sloping forearm and a flexible elbow with

an olecranon process relate to different mechanical

requirements during locomotion: the former is needed

for lifting the body off the ground, whereas the latter

enables forearm extension and flexion during the stride

cycle. This distinction is important for the interpretation

of ANSP 21350. Although it is impossible to know the

exact movement range of the forearm, it seems clear that

ulnar extension in particular was relatively limited. This

suggests a forelimb stride cycle rather different from that

in other early tetrapods, possibly with a shorter stride. At

the same time, the forelimb was evidently specialized for

weight-bearing. The overall impression is of an extremely

primitive tetrapod, perhaps with a relatively yaw-depen-

dent mode of walking, that was nevertheless fairly terres-

trial. It is remarkable that such an animal should be

found in the late Famennian, some 30 myr after the ear-

liest tetrapod footprints (Niedzwiedzki et al. 2010) and at

a time when the tetrapod crown group may already have

been in existence (San Mauro et al. 2005). This further

underscores the emerging picture of poor stratophyloge-

netic fit and large gaps in the fossil record of the earliest

tetrapods (Callier et al. 2009; Friedman and Brazeau

2011). While GSM 104536 remains an intractable puzzle,

the discoveries of the last few years reveal ANSP 21350

to be even more informative about tetrapod origins than

we thought.

TEXT -F IG . 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.

A H L B E R G : T E T R A P O D H U M E R I 27

Acknowledgements. It gives me great pleasure to dedicate this

paper to Angela Milner, as a tribute both to her professional

achievements and to our long friendship. Our acquaintance began

in earnest, as I recall, over a Chinese dinner with her and Andrew

in Belfast during the 1986 SVPCA meeting; 8 years later, she

became my boss when I started work in the Palaeontology Depart-

ment of the Natural History Museum. For the next 10 years,

Angela kept a beady eye on my work. She was an outstanding

manager, unfailingly supportive and interested, who contributed

enormously to my enjoyment of the years at the NHM. Since my

move to Sweden, we seem to have come full circle and are back to

meeting over conference dinners, but it is always a pleasure to

catch up again and I nurture a small hope of eventually repaying

all the drinks I owe her. Thanks for everything, Angela!

I am indebted to Ted Daeschler for presenting me with a

high-quality cast of ANSP 21350 that has formed a cornerstone

of this work. Neil Shubin kindly gave permission to examine the

humeri of Tiktaalik, including undescribed material. I thank The

British Geological Survey for loaning specimens GSM 104536

and GSd 4240. The synchrotron scans of GSM 104536, GSd 4240

and MGUH 29020 were performed by Paul Tafforeau of the

European Synchrotron Radiation Facility (ESRF) in Grenoble,

France; virtual thin sections were prepared from the scan data by

Sophie Sanchez, as part of ESRF project EC 351 and with addi-

tional funding from ERC Advanced Investigator Grant 233111.

Editor. Andrew Milner

REFERENCES

A H L B E R G, P. E. 1989. Paired fin skeletons and relationships of

the fossil group Porolepiformes (Osteichthyes: Sarcopterygii).

Zoological Journal of the Linnean Society, 96, 119–166.

—— 1991. Tetrapod or near-tetrapod fossils from the Upper

Devonian of Scotland. Nature, 354, 298–301.

—— 1995. Elginerpeton pancheni and the earliest tetrapod clade.

Nature, 373, 420–425.

—— 1998. Postcranial stem tetrapod remains from the Devonian

of Scat Craig, Morayshire, Scotland. Zoological Journal of the

Linnean Society, 122, 99–141.

—— 2004. Comment on ‘The Early Evolution of the Tetrapod

Humerus’. Science, 305, 1715d.

—— F R I E D M A N , M. and B L O M , H. 2005. New light on the

earliest known tetrapod jaw. Journal of Vertebrate Paleontology,

25, 720–724.

A N D R E W S , S. M. and W E S TO L L , T. S. 1970. The postcra-

nial skeleton of Eusthenopteron foordi Whiteaves. Transactions

of the Royal Society of Edinburgh, 68, 207–329.

B OI S V E R T , C. A. 2005. The pelvic fin and girdle of Pande-

richthys and the origin of tetrapod locomotion. Nature, 438,

1145–1147.

—— 2009. The humerus of Panderichthys in three dimensions

and its significance in the context of the fish-tetrapod

transition. 297–305. In A H L BE R G , P. E., B L OM , H. and

BO I S V E R T , C. A. (eds). Forty years of early vertebrates:

papers from the 11th International Symposium on early and

lower vertebrates. Acta Zoologica, 90 (Suppl. s1), 384 pp.

—— M A R K - KU R I K , E. and A H L B E R G , P. E. 2008. The

pectoral fin of Panderichthys and the origin of digits. Nature,

456, 636–638.

B R A US , H. 1901. Die Muskeln und Nerven der Ceratodus-

flosse: ein Beitrag zur vergleichenden Morphologie der freien

Gliedmaase bei niederen Fischen und sur Archipterygiumthe-

orie. Denkschriften der Medecinisch Naturwissenschaftlichen

Gesellschaft zu Jena, 4, 137–300.

C A L L I E R , V., CL A C K , J. A. and A HL B E R G , P. E. 2009.

Contrasting developmental trajectories in the earliest known

tetrapod forelimbs. Science, 324, 364–367.

C A R R OL L , R. L. 2009. The rise of amphibians: 365 million

years of evolution. The John Hopkins University Press, Balti-

more, 392 pp.

—— and HO L M E S , R. B. 2007. Evolution of the Appendicular

Skeleton of Amphibians. 185–224. In H A L L , B. K. (ed.). Fins

into limbs: evolution, development and transformation. Univer-

sity of Chicago Press, Chicago, 344 pp.

C L A CK , J. A. 2002. Gaining ground: the origin and early evolu-

tion of tetrapods. Indiana University Press, Bloomington, IN,

USA, 369 pp.

—— and F I N N E Y , S. M. 2005. Pederpes finneyae, an articu-

lated tetrapod from the Tournaisian of Western Scotland.

Journal of Systematic Palaeontology, 2, 311–346.

C OA T E S , M. I. 1996. The Devonian tetrapod Acanthostega

gunnari Jarvik: postcranial anatomy, basal tetrapod interrela-

tionships and patterns of skeletal evolution. Transactions of the

Royal Society of Edinburgh: Earth Sciences, 87, 363–421.

—— and C L A CK , J. A. 1990. Polydactyly in the earliest known

tetrapod limbs. Nature, 347, 66–69.

—— and R UT A , M. 2007. Skeletal changes in the transition

from fins to limbs. 15–38. In H A L L , B. K. (ed.). Fins into

limbs: evolution, development and transformation. University of

Chicago Press, Chicago, 344 pp.

—— S H UB I N , N. H. and D A E S C HL E R , E. B. 2004.

Response to comment on ‘The early evolution of the tetrapod

humerus’. Science, 305, 1715d.

D A E S C HL E R , E. B., S H UB I N , N. H. and J E N KI N S , F. A.

Jr 2006. A Devonian tetrapod-like fish and the evolution of

the tetrapod body plan. Nature, 440, 757–763.

D I O GO , R., A BD A L A , V., A Z I Z , M. A., L O N E R GA N , N.

and W O OD , B. A. 2009. From fish to modern humans –

comparative anatomy, homologies and the evolution of the

pectoral and forelimb musculature. Journal of Anatomy, 214,

694–716.

F R I E D M A N , M. and B R A Z E A U, M. D. 2011. Sequences,

stratigraphy and scenarios: what can we say about the fossil

record of the earliest tetrapods? Proceedings of the Royal Society

B, 278, 432–439.

G O DF R E Y , S. J. 1989. The postcranial skeletal anatomy of the

Carboniferous tetrapod Greererpeton burkemorani. Philosophi-

cal Transactions of the Royal Society B, 323, 75–133.

H A L L , B. K. (ed.) 2007. Fins into limbs: evolution, development,

and transformation. University of Chicago Press, Chicago, 344

pp.

H OL L A N D , T. and L ON G , L. A. 2009. On the phyloge-

netic position of Gogonasus andrewsae Long 1985, within

the Tetrapodomorpha. 285–296. In A H L BE R G , P. E.,

28 S P E C I A L P A P E R S I N P A L A E O N T O L O G Y , 8 6

B L OM , H. and B OI S V E R T , C. A. (eds). Forty years of

early vertebrates: papers from the 11th International Sympo-

sium on early and lower vertebrates. Acta Zoologica, 90 (Sup-

pl. s1), 384 pp.

H O L M E S , R. B. 1984. The Carboniferous amphibian Protero-

gyrinus scheelei Romer, and the early evolution of tetrapods.

Philosophical Transactions of the Royal Society B, 306, 431–

527.

J A N I S , C. M. and F A R M E R , C. 1999. Proposed habitats of

early tetrapods: gills, kidneys and the water-land transition.

Zoological Journal of the Linnean Society, 126, 117–126.

J A R V I K , E. 1955. The oldest tetrapods and their forerunners.

Scientific Monthly, 80, 141–154.

—— 1972. Middle and Upper Devonian Porolepiformes from

East Greenland with special reference to Glyptolepis groenlan-

dica n. sp. Meddelelser om Grønland, 187, 1–307.

—— 1980. Basic structure and evolution of vertebrates, Vol. 1.

Academic Press, London, 575 pp.

—— 1996. The Devonian tetrapod Ichthyostega. Fossils and

Strata, 40, 1–206.

J OH N E L S , A. G. 1957. The mode of terrestrial locomotion in

Clarias. Oikos, 8, 122–129.

L E B E D E V , O. A. and C O A T E S , M. I. 1995. The post-

cranial skeleton of the Devonian tetrapod Tulerpeton curtum

Lebedev. Zoological Journal of the Linnean Society, 114, 307–

348.

L O M B A R D, R. E. and BO L T , J. R. 1995. A new primitive tet-

rapod, Whatcheeria deltae, from the Lower Carboniferous of

Iowa. Palaeontology, 38, 471–494.

M I L L O T, J. and A N T H ON Y , J. 1958. Anatomie de Latimeria

chalumnae. Tome I. Squelette, muscles et formations du soutien.

Editions du CNRS, Paris, 122 pp.

M I L N E R , A. C. and L I N DS A Y , W. 1998. Postcranial remains

of Baphetes and their bearing on the relationships of the

Baphetidae (= Loxommatidae). Zoological Journal of the Lin-

nean Society, 122, 211–235.

N I E DZ W I E DZ K I , G., S ZR E K , P., N A R K I E W I C Z, K.,

N A R K I E W I CZ , M. and A H L B E R G , P. E. 2010. Tetrapod

trackways from the early Middle Devonian period of Poland.

Nature, 463, 43–48.

P A N C HE N , A. L. and S M I T HS O N , T. R. 1987. Character

diagnosis, fossils, and the origin of tetrapods. Biological

Reviews, 62, 341–438.

P A W L E Y , K. and W A R R E N , A. 2006. The appendicular skel-

eton of Eryops megacephalus Cope 1877 (Temnospondyli:

Eryopoidea) from the Lower Permian of North America. Jour-

nal of Paleontology, 80, 561–580.

R A C KO F F , J. S. 1980. The origin of the tetrapod limb and the

ancestry of tetrapods. 255–292. In PA N C H E N , A. L. (ed.).

The terrestrial environment and the origin of land vertebrates.

Academic Press, New York, 633 pp.

S A N M A UR O , D., V E N C E S , M., A L C OB E N DA S , M.,

Z A R DO Y A , R. and M E Y E R , A. 2005. Initial diversification

of living amphibians predated the breakup of Pangaea. The

American Naturalist, 165, 590–599.

S H U BI N , N. H., DA E S CH L E R , E. B. and C O A T E S , M. I.

2004. The early evolution of the tetrapod humerus. Science,

304, 90–93.

—— —— and J E N K I N S , F. A. Jr 2006. The pectoral fin of

Tiktaalik roseae and the origin of the tetrapod limb. Nature,

440, 764–771.

S M I T H S O N , T. R. 1985. The morphology and relationships of

the Carboniferous amphibian Eoherpeton watsoni Panchen.

Zoological Journal of the Linnean Society, 85, 317–410.

S Z E K E L Y , G., C ZE H , G. and V O R OS , G. 1969. The activity

pattern of limb muscles in freely moving normal and deaffe-

rented newts. Experimental Brain Research, 9, 53–62.

V O R O BY E V A , E. I. 1980. Observations on two rhipidistian

fishes from the Upper Devonian of Lode, Latvia. Zoological

Journal of the Linnean Society, 70, 191–201.

—— 1992. The problem of the terrestrial vertebrate origin. Nauka,

Moscow, 344 pp [in Russian].

—— 2000. Morphology of the humerus in the rhipidistian

Crossopterygii and the origin of tetrapods. Paleontological

Journal, 34, 632–641.

—— and KU Z N E T S OV , A. 1992. The locomotor apparatus

of Panderichthys rhombolepis (Gross); a supplement to the

problem of fish-tetrapod transition. 131–140. In M A R K-

KU R I K , E. (ed.). Fossil fishes as living animals. Academy of

Sciences of Estonia, Tallin, 299 pp.

—— and S CH U L TZ E , H.-P. 1991. Description and systemat-

ics of panderichthyid fishes with comments on their relation-

ship to tetrapods. 68–109. In S CH UL T Z E , H.-P. and

T R UE B , L. (eds). Origins of the higher groups of tetrapods:

controversy and consensus. Cornell University Press, Ithaca,

NY, USA, 576 pp.

A H L B E R G : T E T R A P O D H U M E R I 29