Forelimb myology of carnivorous marsupials (Marsupialia ...

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Warburton, N.M. and Marchal, C-R (2017) Forelimb myology of carnivorous marsupials (Marsupialia: Dasyuridae): Implications for the

ancestral body plan of the Australidelphia. The Anatomical Record, 300 (9). pp. 1589-1608.

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Forelimb myology of carnivorous marsupials (Marsupialia: Dasyuridae):

Implications for the ancestral body plan of the Australidelphia

Short title: Forelimb myology of carnivorous marsupials

Natalie M. Warburton1, 2 and Charlie-Rose Marchal 3

1School of Veterinary and Life Sciences, Murdoch University, 90 South Street, Murdoch,

Western Australia 6150

2Department of Earth and Planetary Sciences, Western Australian Museum, Kew Street,

Welshpool, Western Australia.

3L’Ecole Nationale Veterinaire de Toulouse, France

Corresponding author: Natalie Warburton email: [email protected]

This article has been accepted for publication and undergone full peer review but has not beenthrough the copyediting, typesetting, pagination and proofreading process which may lead todifferences between this version and the Version of Record. Please cite this article as an‘Accepted Article’, doi: 10.1002/ar.23612

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ABSTRACT

Carnivorous marsupials of the family Dasyuridae represent a more generalized

anatomical condition of both craniodental and postcranial features in comparison to other groups

of Australidelphian marsupials. Plesiomorphic characters include polyprotodont dentition,

didactylous (rather than syndactylous) pedal morphology, the retention of clavicles and epipubic

bones, and an unossified patelloid. In light of the anatomy of the postcranial skeleton, we

hypothesized that the muscular anatomy of the Dasyuridae would likely display a range of

plesiomorphic traits. We performed gross anatomical dissection on the forelimbs of four species

of dasyurid marsupials to produce anatomical descriptions and muscle origin and insertion maps

for Dasyurus geoffroii, D. hallucatus and Phascogale tapoatafa, together with comparative notes

for Antechinus flavipes. These new descriptions were then compared with those of other

marsupials from the published literature in order to establish the principal patterns in forelimb

muscular anatomy. In nearly all aspects of anatomy, we found that the arrangement of the

muscular origins and insertions, and the relative degree of separation between muscle bellies

among dasyurids, provide a natural starting point from which the anatomies of other

Australidelphian marsupial groups can be derived.

Keywords: Appendicular muscles, marsupial, evolution, Dasyuromorphia, Muscular anatomy

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The Anatomical Record


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INTRODUCTION

The dasyurid marsupials (Marsupialia: Dasyuridae) comprise the principal group of

carnivorous marsupials endemic to Australia and Papua New Guinea, ranging in size from the

tiny insectivorous ningauis (Ningaui spp.) that weigh as little as 3 grams, to the Tasmanian devil

(Sarcophilus harrisii), which weighs around 9 kg (Morton et al., 1989). Many of the smaller

species resemble placental insectivores such as shrews in their body plan, while the medium to

larger sized species exhibit convergence with carnivorans such as mustelids or small felids

(Table 1). Within Dasyuridae, four tribes are recognized; tribes Dasyurini (Dasycercus,

Dasykaluta, Dasyuroides, Dasyurus, Myoictis, Neophascogale, Parantechinus, Phascolosorex,

Pseudantechinus, Sarcophilus) and Phascogalini (Antechinus, Murexia, Phascogale) are grouped

into subfamily Dasyurinae and tribes Sminthopsini (Antechinomys, Ningaui, Smithopsis) and

Planigalini (Planigale) within the subfamily Sminthopsinae (Baverstock et al., 1982; Archer,

1984; Krajewski et al., 1997; Krajewski et al., 2000; Westerman et al., 2015). Dasyuridae is

grouped together with the Myrmecobiidae (the numbat Myrmecobius fasciatus) and the now

extinct clade Thylacinidae to comprise the order Dasyuromorphia (Fig. 1).

Within the monophyletic marsupial clade Australidelphia (Szalay, 1982; Aplin and

Archer, 1987; Marshall et al., 1990; Amrine-Madsen et al., 2003; Horovitz and Sanchez-

Villagra, 2003; Meredith et al., 2008), the Dasyuridae represent a more generalized anatomical

condition of both craniodental and postcranial features in comparison to other groups. Four pairs

of upper incisors and three pairs of lower incisors in the dental formula of dasyurids places them

on the plesiomorphic side of the polyprotodont-diprotodont dichotomy (Archer, 1976; Morton et

al., 1989). Among Australian marsupials, the polyprotodont incisor arrangement is shared with

Peramelemorphia (bandicoots and bilbies) and Notoryctemorphia (marsupial moles), and is

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distinct from the Diprotodontia (wombats, koalas, possums and kangaroos) that possess only one

procumbent pair of lower incisors. In the postcranial skeleton, dasyurids are characterised the

possession of four or five digits on the pes. In contrast, Peramelemorphia and Diprotodontia

(convergently) have a derived syndactylous condition of the pes in which the often diminutive

second and third digits are anatomically and developmentally bound together (Jones, 1949;

Szalay, 1982; Morton et al., 1989; Archer and Hand, 2006). Other plesiomorphic postcranial

traits in dasyurids include the retention of a clavicle in the pectoral girdle, which is reduced or

absent in peramelemorphians (Gordon and Hulbert, 1989; Warburton et al., 2014) and

Notoryctes (Stirling, 1891; Warburton, 2006), the presence of epipubic bones (reduced or lost in

Notoryctes (Stirling, 1891; Warburton, 2006) and Thylacinus (Dixon, 1989)), and the possession

of a cartilaginous patelloid, which is distinct to the ossified patella found in peramelemorphians

(Jones, 1968; Reese et al., 2001; Warburton et al., 2015) and Notoryctes (Stirling, 1891;

Warburton, 2006). On the basis of these skeletal plesiomorphies, we hypothesize that the

muscular anatomy of dasyurids is likely to represent a primitive arrangement among Australian

marsupials.

Detailed accounts of the muscular anatomy of dasyurids are limited to a small number of

nineteenth and early twentieth century publications (MacAlister, 1870; Macalister, 1872;

Cunningham, 1878b, 1878a, 1881, 1882; MacCormick, 1886a, 1886b; Carlsson, 1926; Jones,

1949), and a few early comparative studies of marsupial myology (Young, 1879; Elftman, 1929;

Shrivastava, 1962). Here we revisit the forelimb myology of dasyurid marsupials with new

descriptions of muscle anatomy in four dasyurid species, which synonymize previous

descriptions with current anatomical nomenclature and provide a platform for a comparison of

forelimb structure among dasyurids and among Australidelphian marsupials more broadly. The

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four species dissected represent a diversity of body sizes, locomotor traits, and habitats, and

together with those published in the literature provide a solid framework for understanding the

comparative muscular anatomy of the dasyurid forelimb.

MATERIALS and METHODS

This study provides descriptions and observations of the forelimb muscle anatomy of four

dasyurid marsupials: the Chuditch, or western quoll (Dasyurus geoffroii Gould, 1841; n=3),

northern quoll (Dasyurus hallucatus Gould, 1842; n=3), brush-tailed phascogale (Phascogale

tapoatafa Meyer, 1793; n=2) and mardo (Antechinus flavipes Waterhouse, 1838; n=1). Cadaver

specimens for dissection of the two Dasyurus species and one Phascogale were obtained from

Western Australian Department of Parks and Wildlife (DPaW), the second Phascogale and the

Antechinus specimens were collected as opportunistic finds of specimens – the Phascogale had

been found dead post breeding (male die-off) and the Antechinus found drowned in a water

vessel on a domestic property (DPaW licence SF 6788 with approval from the Murdoch

University Animals Ethics Committee 2012-2015). While Dasyurus spp. are known to have

some degree of sexual dimorphism in body size (Table 1), and sexual dimorphism has been

demonstrated to alter the relative development of muscles in some marsupials (Warburton et al.,

2013), we believe it is unlikely to have a significant effect of muscle origin and insertion sites.

Further, given our relatively small samples sizes dictated by the opportunistic collection of

specimens, we did not consider sexual dimorphism to be testable within this study.

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All specimens were frozen upon initial collection and were defrosted prior to preparation.

Specimens were skinned, eviscerated and embalmed in a 10% formalin 4% glycerol solution for

one week, before being stored in 70% ethanol. Dissections were made of the right and left

forelimbs. Muscles were dissected in major functional groups: extrinsic muscles of the pectoral

limb, intrinsic muscles of the shoulder and brachium, muscles of the antebrachium, and intrinsic

muscles of the manus, using standard dissection techniques and equipment. Following dissection,

the bones were cleaned with a degreasing agent and used as the basis for illustrations. The bones

have been retained for future work within the School of Veterinary and Life Sciences, Anatomy

Department at Murdoch University, Western Australia.

As highlighted in Diogo et al (2016), marsupials (typified by Didelphis in that study)

have a more plesiomorphic musculature in comparison to many eutherian mammals. This

plesiomorphic musculature in marsupials is more complex, having a greater number of muscles.

In her descriptive studies of musculature of marsupials, Warburton (Warburton, 2006; Harvey

and Warburton, 2010; Warburton et al., 2011; Warburton et al., 2012; Warburton et al., 2014;

Warburton et al., 2015) has attempted, where possible, to standardize the marsupial muscle

nomenclature with that of the Nomina Anatomica Veterinaria (Schaller, 2007). The greater

complexity of muscles in marsupials and the highly derived condition of cursorial domestic

eutherians, however, has made this a challenging task, and one that was often fraught with

confusion. Extensive work by Diogo and colleagues on the comparative anatomy, homologies

and evolution of the muscles of the head and neck, culminating in Diogo et al. (2012), provide a

direct comparison of the nomenclature used in comparative anatomy and zoology with that of the

Nomina Anatomica Veterinaria. In this current study, we follow the nomenclature presented in

Diogo et al. (2016), which is based on extensive review of the literature on muscle development

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and anatomy, as well as dissection, to facilitate a unified nomenclature. A small number of

differences observed between our specimens and Didelphis required the use of additional muscle

nomenclature, for which we followed Warburton et al. (2014; m. pectoralis abdominis ) and

Fisher et al. (2009; mm. opponens, m. palmaris brevis).

Comparisons were made with other marsupial groups by dissection of Brush-Tailed

Possums (Trichosurus vulpecula; n=3) collected as road-killed cadavers under the same licence

as above, and Western Grey Kangaroo (Macropus fuliginosus; n=3) purchased from licenced

abattoirs. These specimens were fixed and treated following the protocols set out above. These,

together with extensive review of the anatomical literature (Table 2) and by investigation of

skeletal material held in the Western Australian Museum, enabled comparisons between

marsupial groups.

All muscle descriptions relate to D. geoffroii, unless otherwise stated. For other species,

remarks are made only where differences were noted.

RESULTS

Extrinsic muscles of the pectoral limb

M. trapezius

Three portions of the m. trapezius were identified: pars capitis, pars cervicis, pars

thoracica. In D. geoffroii (Fig. 2) pars capitis and cervicalis arose as a continuous sheet of fleshy

fibers from the entire length of the nuchal crest, and from along the supraspinous ligament from

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the occiput to the spinous process of T5. The cranial portion (frequently mentioned as a division

of the m. brachiocephalicus in eutherian groups) was thick and passed over the lateral aspect of

neck to insert along the cranial aspect of the lateral half of the clavicle, adjacent to the origin of

the fleshy cleidomastoid muscle. The cervical portion inserted with fleshy fibers along the length

of the scapular spine (Fig. 3b). The most proximal part passed over the acromion to insert by a

small aponeurotic connection onto the distal extremity of the deltoid crest, superficial to the

acromial and clavicular portions of the deltoid. The pars thoracica arose by fleshy fibers along

the spinous processes of T5-T12 and inserted by an aponeurotic sheet along the proximal one

third of the scapular spine (Fig. 3c). In D. hallucatus the thoracic part originated from T7-T13. In

P. tapoatafa the insertion of the cervical portion onto the scapular spine was by fleshy fibers

proximally and aponeurotic distally (Fig. 3e,f). In A. flavipes, the origin of the pars thoracica

extended only to T10.

M. levator claviculae (m. atlantoscapularis anticus ; m. omotransversarius; m.

atlantoacromialis; m. omotrachelien ventralis)

In all species, m. levator claviculae arose as thin muscular sheet from the transverse

process of the atlas (C1) and inserted onto the distal two-fifths of scapula spine and cranial

aspect of the acromion (D. geoffroii Fig. 2 inset; Fig. 3c; P. tapoatafa Fig. 3f; 4).

M. atlantoscapularis posticus (m. atlantoscapularis; m. omotrachelien dorsalis; m. levator

scapulae posticus; m. rhomboideus profundus)

In D. hallucatus and P. tapoatafa a distinct sheet of fleshy fibers representing m.

atlantoscapularis posticus was found, originating from the wing of the atlas and inserting onto

the proximal part of the scapular spine (P. tapoatafa Fig. 3f, 4). This muscle was similarly

present in A. flavipes. In D. geoffroii the m. atlantoscapularis posticus was represented by an

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extremely thin layer of aponeurotic tissue overlying the m. supraspinatus near the vertebral

border of the scapula.

M. latissimus dorsi

In Dasyurus spp., m. latissimus dorsi arose as a broad but thin muscular sheet from the

dorsal spines and lumbar fascia between the T4 and the last rib (13) (D. geoffroii Fig. 2). The

muscle inserted via a strong tendon onto the rugose teres tubercle on the medial humeral shaft,

immediately distal to, and fused with, the insertion of the teres major (D. geoffroii Figs. 5, 6a). In

P. tapoatafa the origin was from the spinous processes of T4-T11, and the lumbar fascia to the

level of L4 (Fig. 4) and the insertion was slightly cranial to that of the teres major (Fig. 6e). In A.

flavipes the origin extended further caudally, from spinous processes T5-T11 and the lumbar

fascia to S1. In A. flavipes, the sheet became divisible into two portions near its humeral

insertion, as observed in Dasycercus (Jones, 1949).

M. rhomboideus

M. rhomboideus pars capitis and pars cervicis formed a thin sheet of long fleshy fibers

from the occiput and medial nuchal crest, and from along spinous process C2-C7, which inserted

onto the cranial angle of the scapula (D. geoffroii Fig. 2; Fig. 3a,c). Pars thoracis was a much

thicker muscle portion, comprised of short fibers passing from the proximal thoracic spinous

processes to the vertebral border of scapula. In D. geoffroii the origin was between T1 and T3.

In P. tapoatafa the origin was between T1 and T5 and the insertion more localized to the cranial

angle of the scapula (Fig. 3d,f). In A. flavipes the origin extended to T6.

M. serratus anterior (m. serratus ventralis)

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In Dasyurus spp., m. serratus anterior pars cervicis (‘levator scapulae’) arose from the

transverse processes of the cervical vertebrae C2-C7 (D. geoffroii Fig. 2) and had a narrow

fleshy insertion onto the deep surface of the cranial angle and vertebral border of scapula (facies

serrata) (D. geoffroii Fig. 3a). Pars thoracis arose by fleshy fibers from the lateral aspect of the

first eight ribs and inserted onto the superficial aspect of the caudal angle of scapula, opposite the

seventh rib. In P. tapoatafa the cervical portion was relatively feebly developed (Fig. 3d).

M. pectoralis major (m. pectoralis superficialis)

M. pectoralis major comprised a short m. pectoralis transversus, originating from the

manubrium and medial half of the clavicle, and longer m. pectoralis descendens arising from the

ventral midline of the second to the terminal sternebrae. The insertions of the transverse and

descending portions were contiguous along the length of the pectoral ridge of humerus (P.

tapoatafa Figs. 4, 6g,h; D. geoffroii Fig. 6d). This was the same for all species dissected.

M. pectoralis minor (m. pectoralis profundus)

The m. pectoralis minor arose by fleshy fibers from the ventral midline of the second to

sixth sternebrae, deep to the pectoralis major. It inserted onto the crest of the greater trochanter

(D. geofroii Fig. 6d). The pectoralis minor, being considerably smaller in both extent and

development, was completely hidden by the pectoralis major. This was similar for the species

dissected.

M. pectoralis abdominis (m. pectoralis quartus)

In Dasyurus spp. the “m. pectoralis abdominis” was a small strap muscle that arose from

the distal sternum, on the deep, caudal surface of the m. pectoralis major pars descendens, and

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inserted onto the distal half of the pectoral ridge deep to the pectoralis major. In P. tapoatafa, the

muscle was only a thin ribbon of fibers from caudal rib, which became inseparable from the

superficial pectoralis major at its insertion.

M. subclavius

M. subclavius arose by fleshy fibers from lateral edge of the manubrium, adjacent to the

articulation of the first rib, and passed deep to the clavicle to insert onto the cranial aspect of the

capsule of the acromioclavicular joint and fascia of the m. supraspinatus.

Shoulder

Mm. deltoideus

In D. geoffroii, mm. deltoideus consisted of three distinct muscles: deltoideus clavicularis

(m. cleidobrachialis), deltoideus acromialis and deltoideus scapularis (Fig. 2 inset; Fig. 3d,c) all

inserting to the deltoid crest of the humerus (D. geoffroii Fig. 6d; P. tapoatafa Fig. 6g,h). M.

deltoideus clavicularis arose from the lateral half of the clavicle and inserted onto the distal end

of the deltopectoral crest, immediately proximal to the insertion of the transverse portion of the

superficial pectoral and adjacent to the insertion of the cervical trapezius. M. deltoideus

acromialis arose from the acromion (D. geoffroii Fig. 3d) and inserted via aponeurotic fibers

along the length of the deltoid crest of humerus. M. deltoideus scapularis arose by fleshy fibers

from the broad hamate process of the acromion and along the distal two-thirds of the posterior

border of the scapular spine. The insertion of the scapular portion was immediately distal to that

of the acromial part. The arrangement of three distinct muscle bellies was the same throughout

all specimens dissected (P. tapoatafa Fig. 3f, 4). The scapular and clavicular portions appeared

to be much more strongly developed in D. hallucatus than in D. geoffroii.

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M. supraspinatus

M. supraspinatus arose by fleshy fibers from the supraspinous fossa and the cranial edge

of the scapular spine (D. geoffroii Fig. 2 inset; Fig. 3c; P. tapoatafa Fig. 3f, 4). It inserted cranio-

medially onto the greater tuberosity of the humerus by both fleshy and aponeurotic fibers in

Dasyurus spp., and the tendon was tightly adherent to the capsule of the shoulder joint (Fig. 6d).

In P. tapoatafa (Fig. 6g,h) the insertion was via a strong tendon; no fleshy fibers were as

observed.

M. infraspinatus

M. infraspinatus arose from the infraspinous fossa and the caudal aspect of the scapular

spine by fleshy and aponeurotic fibers (D. geoffroii Fig. 2 inset; Fig. 3c; P. tapoatafa Fig. 3f, 4).

A strong tendon inserted onto the lateral aspect of the greater tuberosity of humerus (D. geoffroii

Fig. 6b,c; P. tapoatafa Fig. 6g,h). This arrangement was consistent in all species dissected.

M. teres minor

M. teres minor was a small, distinct muscle that arose from the infraglenoid rugosity and

ridge along the distal one-fifth of the caudal border of the scapula (D. geoffroii Fig. 3b; P.

tapoatafa Fig. 3e) and inserted immediately below the base of the greater trochanter (D. geoffroii

Fig. 6d P. tapoatafa Fig. 6g). M. teres minor appeared to be relatively smaller in D. hallucatus

when compared to D. geoffroii.

M. teres major

M. teres major arose from the thickened caudal angle of the scapula (D. geoffroii Fig. 2;

Fig. 3a-c, 5; P. tapoatafa Fig. 3d-f, 4) and inserted onto the proximo-lateral aspect of humeral

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shaft. In Dasyurus spp. the insertion was fused with the inserting tendon of the m. latissimus

dorsi and the site of insertion was marked by a rugose teres tubercle on the humeral shaft (D.

geoffroii Fig. 6a). M. teres major appeared to be relatively larger in P. tapoatafa and A. flavipes.

Notably, in P. tapoatafa, m. teres major inserted over a larger area, and more distally than m.

latissimus dorsi, such that the muscle bellies overlapped somewhat at their humeral insertion

(Fig. 6e).

M. subscapularis

M. subscapularis was a multipennate muscle from the subscapular fossa, which covered

almost the entire medial surface of the scapula, as well as the supraspinatus fascia in the glenoid

notch (D. geoffroii Fig. 3a,b, 5; P. tapoatafa Fig. 3d,e). The insertion was by a thick tendon onto

the lesser humeral tuberosity (D. geoffroii Fig. 6a,d; P. tapoatafa Fig. 6e,f,h). This arrangement

was consistent in all species dissected.

Brachium

M. coracobrachialis

M. coracobrachialis was a short, flat muscle belly that arose via a thin tendon from the

coracoid process of scapula, medial to m. biceps brachii (D. geoffroii Fig. 3a,c, 5; P. tapoatafa

Fig. 3d,f), and travelled superficial to the tendon of the m. subscapularis to insert onto the

proximal medial humeral neck, immediately proximal to the insertion of the m. teres major (D.

geoffroii Fig. 6a; P. tapoatafa Fig. 6e). In D. hallucatus it was not possible to separate the tendon

of origin of the coracobrachialis from the coracoid tendon of the biceps brachii.

M. biceps brachii

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M. biceps brachii comprised two incompletely separable fusiform portions. The gleno-

ulnar head arose from the supraglenoid tubercle of the scapula (D. geoffroii Fig. 2, 5; P.

tapoatafa Fig. 3f, 4), passed through the shallow bicipital groove, and inserted onto the proximal

cranial aspect of the ulna, immediately distal to the insertion of the m. brachialis. The coraco-

radial head arose from the coracoid process of the scapula (D. geoffroii Fig. 3a,c; P. tapoatafa

Fig. 3d,f). This tendon did not enter the bicipital groove, but rather descended along the cranial

facet of the lesser tuberosity. The fusiform belly gave rise to a short tendon that inserted onto the

bicipital tubercle of the radius (Fig. 7). In D. geoffroii it was relatively easy to separate the two

bellies, while in D. hallucatus the distal ends of the muscle bellies were incompletely separable

(D. hallucatus Fig. 8).

M. brachialis

M. brachialis originated from the proximolateral humeral shaft, descended obliquely

along the lateral aspect of the humerus, between the deltoid ridge and the lateral supracondylar

ridge (D. geoffroii Figs. 2, 6a-d; P. tapoatafa Figs. 4, 6e-h). A short bundle of fibers arose from

the cranio-distal humerus to become blended with the much longer preceding portion. The

insertion was mostly by fleshy fibers onto cranial aspect of the ulna, immediately distal to the

coronoid process, and proximal to the insertion of the ulnar insertion of the m. biceps brachii

(Fig. 7). In D. hallucatus, the bony origin was much more extensive, from along much of the

length of the lateral aspect of the humeral shaft (effectively making the two separate origins in D.

geoffroii continuous). In P. tapoatafa and A. flavipes, the distal origin of the m. brachialis

surrounded the patent supracondylar fossa.

M. triceps brachii

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M. triceps brachii caput longum arose along one-fourth of caudal border of the scapula

adjacent to the glenoid, deep to, and slightly longer than, the origin of the m. teres minor (D.

geoffroii Figs. 2, 3b, 5; P. tapoatafa Figs. 3d,e, 4). The m. triceps brachii caput laterale arose

from the lateral aspect of the humeral neck (D. geoffroii Fig. 6b,c; P. tapoatafa Fig. 6f). The m.

triceps brachii caput mediale took its origin from the medial aspect of the humeral neck and

proximal two-thirds of humeral shaft (D. geoffroii Fig. 6a,b; P. tapoatafa Fig. 6e,f,h). The medial

and lateral heads were closely situated at their proximal origin and incompletely separable

throughout. The three muscular bellies converge to insert onto the olecranon process of the ulna

(D. geoffroii Fig. 7; P. tapoatafa Fig. 7).

M. dorsoepitrochlearis (m. tensor fascia antebrachii)

M. dorsoepitrochlearis arose by fleshy fibers from caudal margin of the m. latissimus

dorsi, close to its insertion on the humerus and passed over the superficial, medial aspect of the

m. triceps brachii. The insertion was by aponeurotic fibers into the medial fascia of the elbow

and olecranon (D. geoffroii Fig. 5). This muscle was relatively larger and thicker in D. geoffroii

than in D. hallucatus.

M. epitrochleoanconeus (m. anconeus internus; m. triceps brachii caput mediale

accessorium)

M. epitrochleoanconeus was a small fleshy muscle mass, passing from the distolateral

humerus, above the medial epicondyle (D. geoffroii Fig. 6b; P. tapoatafa Fig. 6f), to insert onto

the olecranon.

M. anconeus lateralis (m. anconeus externus; m. anconeus)

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M. anconeus lateralis arose from fascia over the lateral epicondyle and posterior aspect of

the humerus, surrounding the olecranon fossa (D. geoffroii Fig. 6b; P. tapoatafa Fig. 6f), and

inserted onto the lateral aspect of the olecranon. The muscle was much larger than the m.

epitrochleoanconeus. This arrangement was consistent in all of the species dissected.

Antebrachium – ventral division

M. pronator teres

M. pronator teres arose by fleshy and aponeurotic fibers from the cranial aspect of the

medial epicondyle of the humerus, proximal to the flexor carpi radialis and deep to the humeral

head of the flexor digitorum profundus (D. geoffroii Fig. 6a; P. tapoatafa Fig. 6e; D. hallucatus

Fig. 8). It inserted by fleshy fibers onto the proximal half of the craniomedial aspect of the radius

(D. geoffroii Fig. 7b). This arrangement was consistent in all of the species dissected.

M. flexor carpi radialis

M. flexor carpi radialis originated from the medial epicondyle, completely under cover of

humeral portion of the m. flexor digitorum profundus (D. geoffroii Fig. 6a; P. tapoatafa Fig. 6e;

D. hallucatus Fig. 8). The thin muscle belly was incompletely separable into two portions. Two

tendons arose in the distal half of the antebrachium. The dorsal portion gave a thin tendon to the

carpal fascia surrounding the proximoradial (scapholunate) bone of the carpus, and the ventral

belly gave a strong tendon that inserted onto the base of the second and third metacarpals (D.

geoffroii Fig. 9). In P. tapoatafa the insertion was only traced to metacarpal II.

M. flexor carpi ulnaris

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M. flexor carpi ulnaris had a broad, flat muscle belly that arose from the caudal aspect of

medial epicondyle and medial aspect of olecranon (D. geoffroii Fig. 6a,b P. tapoatafa Figs. 5, 6e;

D. hallucatus Fig. 8). The belly passed along the medial aspect of ulna to insert via a thick

tendon along the distal third of the antebrachium onto the pisiform bone (accessory carpal) and

via an extension of the tendon to the base of metacarpal V (D. geoffroii Fig. 9). In D. hallucatus

and P. tapoatafa, this insertion could be traced to the pisiform bone only.

M. palmaris longus

M. palmaris longus arose from the medial epicondyle of the humerus, between m. flexor

digitorum profundus and m. flexor carpi ulnaris (D. geoffroii Fig. 6a; P. tapoatafa Fig. 6e; D.

hallucatus Fig. 8). The long, thin belly passed along the ventral edge of the deep flexor to insert

into the deep fascia of ventral carpus over the flexor tendons to digits II-V (P. tapoatafa Fig. 5).

This arrangement was consistent in all the species dissected.

M. flexor digitorum superficialis (m. flexor sublimis, m. flexor perforatus)

M. flexor digitorum superficialis was a tiny slip of muscle from the distal superficial

aponeurosis of the m. flexor digitorum profundus (P. tapoatafa Fig. 5). The small tendons passed

through a superficial groove on deep flexor tendon and across the palm to insert onto the base of

the proximal phalanx of digits II-V (D. geoffroii Fig. 9). M. flexor digitorum superficialis

appeared relatively larger in A. flavipes than in the other species dissected.

M. flexor digitorum profundus (historically considered to include m. flexor longus pollicis, though see Diogo et al. 2016)

M. flexor digitorum profundus was a massive muscle and divisible into three thick

bellies: caput humerale, pars radiale and caput ulnare. The large, superficial belly arose from the

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medial flexor crest of the humerus proximal to the epicondyle (D. geoffroii Fig. 6a; P. tapoatafa

Figa. 5, 6e). The origin was so broad as to cover all of the muscles that arose from the medial

epicondyle. The ulnar belly, from the olecranon, was a more elongate muscle mass (D.

hallucatus Fig. 8). A short, deep belly arose in the distal half of the antebrachium from the

medial aspect of the radial shaft. The large tendons from each portion merged in the distal

antebrachium to pass through the carpal canal under the flexor retinaculum. In the palm, five

thick tendons were traced to the distal phalanx of each digit (D. geoffroii Fig. 9).

M. pronator quadratus

The fleshy fibers of the m. pronator quadratus passed between the medial aspects of distal

half of the radius and ulna, in the interosseous space (D. geoffroii Fig. 7b; P. tapoatafa Fig. 7d).

This arrangement was consistent in all of the species dissected.

Antebrachium – dorsal division

M. brachioradialis (M. supinator longus)

M. brachioradialis was relatively small muscle that arose from the most proximal tip of

the lateral supracondylar ridge, in close connection with the m. extensor carpi radialis (D.

geoffroii Figs. 2, 6c-d; P. tapoatafa Figs. 4, 6g,h). The thin muscle gave rise to a tiny tendon,

which passed on the medial aspect of the m. extensor carpi radialis, and deep to the tendon of the

m. abductor pollicis longus, to insert onto the radial aspect of the proximoradial carpal bone (D.

geoffroii Fig. 9). This arrangement was also present in the other species.

M. extensor carpi radialis

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M. extensor carpi radialis arose as a large single muscle belly from the lateral

supracondylar ridge (D. geoffroii Figs. 2, 6d; P. tapoatafa Fig. 4, 5, 6g,h) and inserted via an

obvious tendon onto the base of metacarpals II and III (D. geoffroii Fig. 9).

M. extensor digitorum communis

M. extensor digitorum communis consisted of many small bellies which arose from the

lateral humeral epicondyle via tendinous fibers, and also from the proximal radius via fleshy

fibers (D. geoffroii Figs. 2, 6c,d, 7; P. tapoatafa Figs. 4, 6g, 7). The tendons passed together deep

to the dorsal annular ligament of wrist before giving paired (lateral and medial) insertions to the

proximal phalanx of digits II-V (D. geoffroii Fig. 9).

M. extensor digiti minimi (m. extensor digitorum lateralis)

M. extensor digiti minimi arose from the lateral epicondyle of humerus adjacent to the

common digital extensor (D. geoffroii Figs. 2, 6c,d; P. tapoatafa Fig. 4, g). The muscle belly

gave rise to short tendon, which divided to insert onto the dorsal aspect proximal phalanx of

digits four and five (D. geoffroii Fig. 9; D. hallucatus Fig. 10).

M. extensor digitorum profundus (m. extensor secundi internodii pollicis + m. ext. indicis, medii digiti et quarti of McCormick)

M. extensor digitorum profundus arose as a single, thin belly from the olecranon (D.

geoffroii Fig. 7a). The muscle passed on the deep aspect of the lateral extensor and gave rise to

two tendons. The first tendon inserted onto fascia of the proximal phalanx of digit I; the second

tendon split into three, which ran to digits II, III and IV (D. geoffroii Fig. 9; D. hallucatus Fig.

10). In P. tapoatafa the origin was much longer, from along the proximal third of the ulna (Fig.

7c).

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M. extensor carpi ulnaris (m. ulnaris lateralis)

M. extensor carpi ulnaris arose by fleshy fibers from the lateral humeral epicondyle (D.

geoffroii Fig. 6c,d; P. tapoatafa Fig. 6g). The insertion was to the lateral carpal bone (hamate),

the adjoining intercarpal ligaments, the capsule of the lateral carpometacarpal joint and the base

of metacarpal V (D. geoffroii Figs. 2,9). In P. tapoatafa (Fig. 4) the insertion was restricted to

the carpal bones.

M. supinator (supinator brevis)

M. supinator was a very small muscle from the lateral humeral epicondyle, originating

deep to m. extensor carpi radialis (D. geoffroii Fig. 6c,d; P. tapoatafa Fig. 6g). The fleshy fibers

passed obliquely to insert onto the proximal one-quarter of the cranial aspect of the radius (D.

geoffroii Fig. 7a,b; P. tapoatafa Fig. 7c,d).

M. abductor pollicis longus (M. abductor digiti I longus; M. extensor ossis metacarpi

pollicis, M. extensor carpi obliquus)

M. abductor pollicis longus arose along the entire length of the cranial border of radius,

interosseus membrane and ulnar shaft, deep to m. extensor carpi radialis and the common digital

extensor (D. geoffroii Figs. 2, 7a; P. tapoatafa Fig. 4, 7c; D. hallucatus Fig. 10). The thick,

flattened tendon of m. abductor pollicis longus emerged from between the two muscles, and

followed an oblique course to insert onto the base of metacarpal I (D. geoffroii Fig. 9). The

oblique tendon of m. abductor pollicis longus passed superficial to the tendons of m. extensor

carpi radialis (D. hallucatus Fig. 10).

Manus

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The following descriptions of the intrinsic muscles of the hand pertain to D. geoffroii and

D. hallucatus; the origins and insertions could not be traced with confidence in the smaller P.

tapoatafa and A. flavipes.

Mm. lumbricales

Four lumbricales arose from between the clefts of the thick mesial tendon of the deep

digital flexor and inserted onto the extensor expansions of the deep aponeurosis of the digits (II-

V).

Mm. contrahentes (mm. adductores digitorum breves) (D. hallucatus Fig. 11)

The short adductor of the thumb, m. adductor digiti I (pollicis) arose from the flexor

retinaculum and deep palmar fascia. The muscle belly passed obliquely to insert onto the fascia

over the metacarpophalangeal joint and base of the proximal phalanx of the first digit. The

contrahentes of digits II (adductor indicis) and IV (adductor annularis) arose from the palmar

carpal ligament (superficial to the flexor breves) and inserted to the lateral base of proximal

phalanx II and medial aspect of the base of proximal phalanx IV respectively. The contrahens of

digit V (m. adductor digiti minimi) arose from the ulnar side of the flexor retinaculum. The

muscle lay in an oblique orientation and we traced the insertion only as far as the fascia over the

head of the fifth metacarpal and the fifth metacarpophalangeal joint.

Mm. flexores breves profundi

The short digital flexors were represented by ten small muscular bellies, arranged in

pairs, which arose from the fascia over the carpo-metacarpal joints, and passed to each of the five

digits (D. hallucatus Fig. 11). The paired lateral and medial muscles for each of the five digits

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inserted by fleshy fibers onto their respective side of base of the proximal phalanx and

surrounding fascia. The most radial of the flexores breves, often referred to as m. flexor pollicis

brevis, arose from the tough fascia over the trapezoid, at the base of the second metacarpal and

inserted onto the radial aspect of the base of proximal phalanx of digit I. The most ulnar of the

flexores breves, the short flexor of the digit V, arose from the tough fascia at base of metacarpal

III and inserted onto the base of the proximal phalanx of digit V, immediately distal to the

insertion of m. flexor carpi ulnaris.

M. abductor digiti I (pollicis) brevis

The short abductor of the pollex was a small muscle, which arose from the radial distal

carpal bone (trapezium) and inserted onto the fascia on the radial side of the

metacarpophalangeal joint of digit I (D. geoffroii Fig. 9; D. hallucatus Fig. 11).

M. opponens pollicis

The m. opponens pollicis was a tiny fusiform muscle belly that originated from the radial

aspect of the thenar eminence, passing from the trapezoid to insert onto the fascia surrounding

the radial aspect of the proximal interphalangeal joint of the first digit (D. hallucatus Fig. 11).

M. abductor digiti minimi

The abductor of the fifth digit arose as fleshy fibers from the fascia between the pisiform

bone and hamate and inserted directly onto the fascia of the metacarpophalangeal joint of digit V

(D. hallucatus Fig. 11).

M. palmaris brevis

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The m. palmaris brevis was a fleshy muscle originating from the hypothenar eminence

over the pisiform bone. It inserted by a short tendon onto the ulnar side proximal phalanx of the

fifth digit (D. hallucatus Fig. 11).

M. intermetacarpales

Four intermetacarpales were observed, lying between adjacent metacarpals (D. hallucatus

Fig. 10). They had a bipennate arrangement, arising from the adjacent sides of the proximal ends

of the metacarpal bones. The m. intermetacarpales of the first and second intermetacarpal space

inserted to radial side of the proximal phalanges of the second and third digit respectively, in the

region of the insertion of the flexores breves and adjacent dorsal extensor fascia. The third and

fourth intermetacarpales similarly arise from the adjacent bases of the metacarpals and inserted

onto the ulnar aspect of the respective digits.

Discussion

Variation within Dasyuridae

The dissections and review of the literature performed in this study revealed a highly

conservative pattern of muscular anatomy within the Dasyuridae. The muscular anatomy of the

two species of Dasyurus dissected here corresponded very closely with that of D. viverrinus

described by MacCormick (1886a). The anatomical variation between species, with respect to

the origins and insertions of muscles within the forelimb was very slight, particularly in light of

intraspecific variation observed here and also discussed in the literature (MacAlister, 1870;

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Macalister, 1872; Fisher et al., 2009). The principle source of variation between species was the

relative surface area of the fleshy muscle origins; the general pattern being that muscle origins

covered a relatively larger area in species of smaller body size. For instance, the origin of the m.

brachialis in P. tapoatafa covered a relatively larger area on the lateral aspect of the humerus

than the same muscle in D. hallucatus, which in turn had relatively greater areas of origin than in

D. geoffroii. This pattern was even more pronounced when A. flavipes was considered, and

especially so for the origin and strengthened insertion of m. latissimus dorsi (also in Dasycercus;

Jones, 1949) and the extended thoracic origin of m. rhomboideus. Conversely, S. harrisii

reportedly has relatively small area of origin of m. trapezius pars thoracica and insertion of m.

trapezius pars capitis to the lateral one-quarter to one-third (rather than half) of the clavicle

(MacAlister, 1870; Macalister, 1872). The larger muscle attachments in P. tapoatafa and A.

flavipes in comparison to Dasyurus spp. likely reflect differences in limb posture with

corresponding differences in size and behaviour. Biewener (1989) demonstrated that while small

mammals run with more flexed limbs and crouched postures that favour manoeuvrability and

accelerative capability, larger mammals utilize more upright postures in which the limbs are

more closed aligned with ground forces in order to reduce bone stresses and muscle force

requirements. Antechinus flavipes, as the smallest animal within our sample, indeed displays a

more crouched posture with highly flexed limbs, which would require relatively greater muscle

force to move, and thus larger muscles relative to its body size.

The relatively larger attachments of muscles including the medial head of the m. triceps

brachii, m. brachialis, m. flexor digitorum profundus and m. abductor longus pollicis in P.

tapoatafa (in comparison to Dasyurus spp.) may also be correlated with adaptation for arboreal

behaviours in this species. As well as having a relatively more flexed limb posture, which in

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arboreal animals brings the centre of gravity closer to the supporting surface (tree trunk or

branch) and improves stability in the complex three-dimensional arboreal habitus (Cartmill,

1985), P. tapoatafa also has a more sprawling, abducted limb posture during climbing. The

relatively large size of the m. teres major, an adductor as well as extensor of the shoulder, also

represents an adaption for improved grasping during vertical climbing as has been reported in

other climbing mammals (Taylor, 1974; Warburton et al., 2011).

The myological descriptions of Sarcophilus harrisii (MacAlister, 1870; Macalister, 1872)

suggest a number of subtle differences relating to the extent of muscle attachments in this species

including the m. latissimus dorsi, the insertion of the m. teres major (though this was variable

between species in our observations), extension of the m. subclavius to dorsal aspect of scapula,

indistinct m. teres minor, incomplete separation of the acromial and clavicular heads of the

deltoid, and larger lateral head of the m. triceps brachii. Without quantitative data on muscle size

and architecture, functional comparisons are difficult and will await future studies.

Primitive retentions in Dasyuridae and the patterns of myology in Australidelphian marsupials

The anatomy of the m. trapezius has been identified as one of the key differences

between marsupials and placental mammals, and in particular the relationship between the

trapezius and the deltoid muscle group (Shrivastava, 1962). The trapezius of dasyurids forms a

broad, continuous sheet of muscle from along the nuchal crest and the mid-dorsal line of the

cervical and thoracic regions that wraps around the lateral aspect of the neck to have a substantial

insertion along the clavicle, the length of the scapular spine and the deltoid crest of the humerus.

This arrangement appears likely to represent the plesiomorphic condition among

Australidelphian marsupials. The broad continuous origin from the nuchal crest/occipital region,

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cervical and thoracic spine is consistent with that of other marsupial groups including didelphids

(Jenkins and Weijs, 1979), peramelids (Parsons, 1903; Filan, 1990; Warburton et al., 2014), and

diprotodonts (Young, 1882; Sonntag, 1922; Boardman, 1941; Barbour, 1963). The marsupial

moles (Notoryctes spp.) are unusual in the distinct separation of the spinotrapezius, but retains

the continuous origin of the cranial and cervical portions (Warburton, 2006). Among marsupials

generally, the cranial portion of the trapezius passing around the neck is thick and fleshy in

comparison to the much thinner thoracic portion, and has a robust insertion to the clavicle. There

is some degree of fusion of these anterior fibers of the trapezius with the clavicular deltoid in

Phascolarctos, Pseudocheirus, Phalanger (Sonntag, 1922), and more substantially in Notoryctes

(Warburton, 2006) and Phascolomys (Sonntag, 1922). In dasyuromorphians, however, while the

insertion of the trapezius was very closely arranged with the insertion of the deltoids, blending of

fibers was not apparent. In the aclaviculate peramelids, the very thick anterior trapezius

continues to the distal deltoid crest forming a strong cephalohumeral muscle (Warburton et al.,

2014). This highly derived condition presents a similar arrangement to that observed in placental

mammals where the clavicle is reduced or absent, particularly among the Carnivora (Wood,

1870; Davison, 1944; Miller, 2012).

The m. omotransversarius of veterinary nomenclature, derived from the levator scapulae

(Arlamowska-Palider and Zablocki, 1972; Diogo et al., 2016), presents a nomenclatorial

difficulty. The plesiomorphic condition for both marsupials and eutherian mammals is the

presence of two distinct muscles, atlantoscapularis anticus (considered more appropriately

named levator claviculae by Diogo et al. 2016) and atlantoscapularis posticus. Thus the

veterinary m. omotransversarius of domestic species represents only the atlantoscapularis

anticus, in the derived condition in which the atlantoscapularis posticus is absent. The presence

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of both these muscles in all dasyurids considered here, consistent with previous findings in

Dasyurus (MacCormick, 1886a; "acromio-trachelien") and Phascogale (Cunningham, 1882),

reflects the plesiomorphic condition for dasyuromorphians; note that for S. harrisii, while only

the ventral portion was observed in MacAlister (1870; "omo-atlantic"), both portions were

identified in (Macalister, 1872; "trachelo-acromiales muscles"). Both muscles are present in

Didelphis (Coues, 1871; Jenkins and Weijs, 1979; atlanto-acromialis and atlanto-scapularis) and

Caluromys (Argot, 2001; omotransversarius and levator scapulae dorsalis), as well as many

eutherian mammals and thus the presence of two muscles has been interpreted as the

plesiomorphic arrangement in all mammals (Arlamowska-Palider and Zablocki, 1972; Diogo and

Abdala, 2010; Diogo et al., 2016). In Diprotodontian marsupials (Sonntag, 1922; Boardman,

1941; "omo-cleido-transversarius"; Harvey and Warburton, 2010; for dorsal portion see "serratus

ventrals cervicis: atlantoscapularis"; Warburton et al., 2011), the two muscles often have a

broadly continuous insertion along the length of the scapular spine. In Phascolomys and

Phascolarctos there appears to be a greater separation between the two muscles, with the levator

claviculae apparently reduced and incorporated into the m. serratus ventralis as “levator anguli

scapulae” (Sonntag, 1922) or not reported at all (Macalister, 1865, 1870; Young, 1882).

Marsupial taxa in which the atlantoscapularis posticus has become reduced or absent tend to be

those with a more strongly adducted forelimb posture and emphasis on limb movements in the

parasagittal plane for terrestrial locomotion and/or digging (Chaeropus (Parsons, 1903), Isoodon

(Filan, 1990; Warburton et al., 2014), Notoryctes (Warburton, 2006), and thus the absence of this

muscle should be considered the derived condition amongst marsupials. A similar conclusion has

been made for eutherian mammals (Arlamowska-Palider and Zablocki, 1972). The presence of

the two muscles (atlantoscapularis anterior and posterior, or omotransversarius and rhomboideus

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profundus) is a common condition for Mephitidae and Mustelidae, lineages with an extremely

diverse range of locomotory habits (Ercoli et al., 2015), contrary to some other carnivorans

(ursids; Davis, 1964; canids; Miller, 2012) . Together, the m. omotransversarius and m.

rhomboideus profundus are efficient to advance and rotate the scapula in the parasagittal plane,

and to laterally flex the neck. Canis, however, a more specialised cursor, possess only the m.

levator claviculae (m. omotransversarius) (Miller, 2012) and thus the absence or reduction of the

atlantoscapularis posticus (m. rhomboideus profundus) muscle may be linked to a reduction of

these muscles functions in animals which tend to have a more restricted suite of limb

movements. Support for this hypothesis is the apparent absence of the atlantoscapularis posticus

in Thylacinus (Cunningham, 1882 reported in MacCormick 1886a) and in cursorial placental

mammals more generally (Chauveau, 1891; Miller, 2012).

The nomenclature of the pectoral muscles in marsupials has historically been very

variable (Boardman, 1941; Horiguchi, 1981; Warburton, 2006; Diogo et al., 2009; Harvey and

Warburton, 2010; Warburton et al., 2011; Warburton et al., 2014). As far as can be ascertained

from this study, it would appear that the following generalisations might be made regarding the

plesiomorphic condition of this group. Firstly, the m. pectoralis major (superficialis) is by far the

largest component of the pectoral group arising from the length of the sternum, and having an

elongate insertion along the length of pectoral ridge of the humerus. The division between a

cranial pars transversus and caudal pars descendens can usually be made, and the pars

transversus from the manubrium often has some fibers of clavicular origin. Secondly, the m.

pectoralis minor (profundus) is generally relatively small in comparison to the major, almost

always being completely hidden by the more superficial muscle and thus is very different to the

condition in Canis (Miller, 2012) and eutherian mammals more generally. Finally, the abdominal

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portion of the pectorales “m. pectoralis abdominis (quartus)” of Australidelphian marsupials

appears to be a derivative of the superficial pectoralis major, rather than the pectoralis minor. We

found a very close association between the origin superficial and abdominal portions; only in P.

tapoatafa was the origin of the m. pectoralis abdominis positioned caudal to the margin of the m.

pectoralis descendens. The insertion of m. pectoralis abdominis is variable amongst marsupials,

though we found it underlay the proximal part of the insertion of the superficial pectoral in most

cases and suggest this may be the plesiomorphic condition for Australidelphian taxa. Where the

insertion is more closely opposed that of the m. pectoralis profundus, as in some

peramelemorphians (Warburton et al., 2014), we hypothesize that this reflects a derived

condition which corresponds to a greater emphasis on movements of limb retraction in a

parasagittal plane. Diogo et al. (2016) found the abdominal portion to be part of the pectoralis

minor in Didelphis, but notes that the derivation of the abdominal pectoral is likely to be

variable.

The intrinsic muscles of the forelimb in dasyurids provides a useful reference for

interpreting the anatomies of other Australiadelphian marsupials. The coracobrachialis was

found to be generally single (contra Cunningham, 1882; double in Phascogale) as is typical of

marsupials (Diogo et al., 2016), with the reported exceptions of two bellies in Phascolarctos

(Young, 1882) and Phalangista (Cunningham, 1882), and possible absence in in Chaeropus

(Parsons, 1903) and Notorytes (Warburton, 2006). As summarised in (Warburton et al., 2014),

two heads of the biceps are generally found, and correspond to the long and short heads of

eutherian mammals (Diogo et al., 2016). There is, however, often some degree of fusion either

proximally, as in Phascolarctos (Young, 1882), Vombatus and Phalanger (Sonntag, 1922), and

Trichosurus (Barbour, 1963), or distally, as in D. hallucatus (this study) among marsupials. The

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retention of only a single coraco-radial head of m. biceps brachii in Chaeropus (Parsons, 1903)

and Notorytes (Warburton, 2006) clearly represents a derived condition. The m. flexor carpi

radialis is generally small with insertions to metacarpals II and III, while m. flexor carpi ulnaris

is relatively much larger with the typical insertion to the pisiform occasionally extending to

metacarpal V (MacAlister, 1870; Macalister, 1872; Young, 1882; Hopwood, 1974). We found

both m. flexor digitorum superficialis and distinct m. palmaris longus to be present in dasyurids,

as it is in Didelphis (Coues, 1871) and Australian marsupials generally (Barbour, 1963;

Warburton et al., 2014); both of these muscles are typically very small and have a strong

connection to the relatively massive and complex m. flexor digitorum profundus. Diogo and

Abdala (2010) and Diogo et al., (2016), following the detailed descriptions of the flexor tendons

of the didelphid manus in Abdala et al. (2006) provide detailed commentary on the variable

nature of the palmaris longus, which in Didelphis and some eutherian mammals is represented by

two muscle bellies, and may in fact be derived variably from either the flexor digitorum

superficialis, flexor carpi ulnaris and/or occasionally from the flexor carpi radialis. The “gain” of

a second head (palmaris longus internus) was considered a derived trait in Didelphis (Diogo et

al., 2016; p.1250), with which we agree given that only one palmaris longus appears typical of

dasyurids and most Austalidelphian marsupials. The intrinsic muscles of the manus, derived

from the ventral division of the forelimb, appear in dasyurids to reflect the general arrangement

described in detail in Lewis (1989).

Nine muscles were found to be present in the extensor division of the forearm of the

dasyurids studied: m. brachioradialis, m. supinator, m. extensor carpi radialis, m. extensor carpi

ulnaris, m. extensor digitorum communis, m. extensor digitorum profundus (“indicis”), m.

extensor digiti minimi, m. abductor pollicis longus, together with the m. anconeus lateralis which

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is a derivative of this group (Lewis, 1989). This appears to reflect the typical arrangement of this

group within Australidelphian marsupials. Both m. brachioradialis (supinator longus) and m.

supinator (brevis) are present in dasyurids, as they are in Didelphis (Diogo et al., 2016),

reflecting the plesiomorphic condition among mammals generally. M. brachioradialis has been

lost in Peramelemorphia (Parsons, 1903; Warburton et al., 2014) and Notoryctes (Warburton,

2006). M extensor digitorum communis in dasyurids was found to have insertions to the four

ulnar digits, as is typical of most marsupials (Coues, 1871; Barbour, 1963; note this was

mistakenly reported in Warburton et al., 2014 to go to all five digits), and considered the

plesiomorphic condition by Lewis (1989). Derived conditions have been noted in Phascolarctos

(Young, 1882; Sonntag, 1922), Chaeropus (Parsons, 1903) and Notoryctes (Wilson, 1894;

Warburton, 2006) in which the number of insertions has been reduced. Barbour (1964)

considered the m. extensor digitorum profundus to represent the combined m. extensor pollicis

longus and m. extensor indicis within marsupials, but notes significant variation between species;

many authors have described these as separate muscles. Lewis (1989) describes a “proprius”

division of the deep extensor mass with insertions to the first, second and third digits to be

general pattern. Given that we traced insertions to at least four digits in our specimens, as did

Macalister (1872) and Jones (1949) for Sarcophilus and Dasycercus respectively, we suggest

that the general condition of this muscle group likely involved insertion to at least the four radial

digits (pollicis, indicis, medius and annularis) in dasyurids. Barbour (1963) noted that in many

marsupials including Dasycercus (Jones, 1949), the insertion of m. extensor digiti minimi

extends to both the fourth and fifth digits, as did MacCormick (1886a) for D. viverrinus and

Cunningham (1882) for Phascogale, Cuscus and Thylacinus. Lewis (1989) and Diogo et al.

(2016) highlight the insertion to both digits four and five to be the plesiomorphic arrangement

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(“extensor digiti quarti et quinti”). The insertion of the lateral extensor in Chaeropus to digit IV

only (Parsons, 1903), and the complete absence of this muscle in Notoryctes (Wilson, 1894;

Warburton, 2006), reflect the highly modified manus in these species.

Derived features of Dasyuridae

In only one instance do we consider the general muscular anatomy of dasyurids to present

a derived state among Australidelphian marsupials. The m. extensor carpi radialis, is described as

being “double” Didelphis; Diogo et al. 2016) and Trichosurus (Barbour, 1963) with separate

long and short heads to the second and third metacarpals respectively. Barbour (1963), later

confirmed by Lewis (1989), regarded the presence of two fairly distinct extensor carpi radialis

muscles as being the plesiomorphic condition among marsupials. Thus the arrangement here for

dasyurids in which a single (combined) belly with insertions to both the second and third

metacarpals is clearly derived from the former pattern. Further modification of this has been

found in D. viverrinus (MacCormick, 1886a), Chaeropus (Parsons, 1903) and Notoryctes

(Wilson, 1894; Warburton, 2006), in which only a single insertion is retained.

Shrivistava (1962) suggested that a tripartite arrangement of the m. deltoideus, in which

cleido-, acromion- and spino-deltoids are clearly separable from one another is plesiomorphic to

an arrangement in which there is some degree of fusion between the various parts, as in

Phascolomys and Phascolarctos (Sonntag, 1922) and large Macropus spp. (Boardman, 1941;

Hopwood, 1974). In contrast, Diogo et al. (2016), on the basis of dissections and literature

review of Didelphis and many eutherian mammals, consider a single deltoideus acromialis and

clavicularis (rather than these being two separate muscles) to be plesiomorphic for all mammals.

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If the latter is true, then the differentiated arrangement in dasyuromorphians must be considered

derived, though we reserve judgement on this point.

CONCLUSIONS

It is interesting that there are very few points of difference between Didelphis (Diogo et

al. 2016) and dasyurid marsupials: the abdominal pectoral muscle appears to be part of the

pectoralis major in dasyurids, as opposed to the pectoralis minor in Didelphis; the absence of a

cleidoacromialis in dasyurids; separate cleido- and acromial deltoids in dasyurids; single

palmaris longus and single extensor carpi radialis in dasyurids. Diogo et al. (2016) demonstrated

that Didelphis has undergone relatively fewer changes in muscular anatomy from the last

common ancestor of marsupial and eutherian mammals, than many eutherian groups including

rodents and primates. The relatively few differences between dasyurids and Didelphis, suggest

that the dasyurids have similarly undergone relatively few changes in forelimb muscular

anatomy from the last common ancestor of the two therian mammal clades. Indeed, in some

aspects, such as the single palmaris longus, the tripartite arrangement of the deltoid and the

presence of m. opponens pollicis and m. palmaris brevis, dasyurids appear to retain more

plesiomorphic traits than Didelphis. As hypothesized in the introduction, the musculature of

dasyurid marsupials does indeed appear to correlate with their relatively generalized body forms

and skeletal morphology among Australidelphian marsupials, and thus the anatomy described

herein provides a useful framework for understanding the evolutionary changes that have

occurred in other Australidelphian marsupials.

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Marsupials are characterized by giving birth to young that are in an altricial state relative

to their eutherian counterparts. There are different grades of development among marsupials

neonates, and the dasyurid quolls, or “native cats”, (Dasyurus spp.) are among the most highly

altricial at birth (Hill and Hill, 1955). While embryonic in appearance and form, marsupial

neonates also have a range of heterochronic changes, particularly of the craniofacial region and

forelimb, that enable them to make their way to their mothers’ pouch and to suckle (Smith, 2006;

Keyte and Smith, 2010). It is interesting to note, then, that despite their highly embryonic state at

birth, the anatomy of the forelimb muscles in dasyurids appears to develop in line with that of

other marsupials, and that there appears to be no ongoing effects on the arrangement of the

muscles resulting from any heterochronic patterning during development.

ACKNOWLEDGEMENTS

The authors would like to sincerely thank D. Nottle, Z. Wong and J. Hong of the

Murdoch University Veterinary Anatomy Department for their assistance in the laboratory. We

thank the editor and reviewers, especially R. Diogo and M. Ercoli, for the time they gave in

preparing detailed comments and suggestions for the improvement of the manuscript.

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LITERATURE CITED

Abdala V, Moro S, Flores DA. 2006. The flexor tendons in the didelphid manus. Mastozool Neotrop 13:193-204.

Amrine-Madsen HA, Scally M, Westerman M, Stanhope MJ, Krajewski C, Springer MS. 2003. Nuclear gene sequences provide evidence for the monophyly of australidelphian marsupials. Mol Phylogenet Evol 28:186-196.

Aplin K, Archer M. 1987. Recent advances in marsupial systematics with a new syncretic classification. In: Archer M, editor. Possums and Opossums: Studies in Evolution. Sydney: Surrey Beatty & Sons & Roy Zool Soc NSW. p xv–lxxii.

Archer M. 1976. The dasyurid dentition and its relationships to that of didelphis, thylacinids, borhyaenids (Marsupicarnivora) and peramelids (Peramelina: Marsupialia). Aust J Zool Supp 39:1-34.

Archer M. 1984. The Australian marsupial radiation. In: Clayton MAG, editor. Vertebrate Zoogeography and Evolution in Australasia. Perth: Hesperian Press. p 633-808.

Archer M, Hand SJ. 2006. The Australian marsupial radiation. In: Merrick JR, Archer M, Hickey GM, Lee MSY, editors. Evolution and biogeography of Australiasian vertebrates. Oatlands, NSW: Australia Auscipub. p 575-646.

Argot C. 2001. Functional-adaptive anatomy of the forelimb in the Didelphidae, and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus. J Morphol 247:51-79.

Arlamowska-Palider A, Zablocki J. 1972. Musculus omotransversarius in the light of comparative anatomy. Acta Theriol (Warsz) 17:381-398.

Barbour RA. 1963. The musculature and limb plexus of Trichosurus vulpecula. Aust J Zool 11:488-610.

Baverstock PR, Archer M, Adams M, Richardson BJ. 1982. Genetic relationships among 32 species of Australian dasyurid marsupials. In: Archer M, editor. Carnivorous marsupials. Chipping Norton, NSW: Surrey Beatty & Sons. p 641-650.

Biewener AA. 1989. Scaling body support in mammals: limb posture and muscle mechanics. Science 245:45-48.

Boardman W. 1941. On the anatomy and functional adaptation of the thorax and pectoral girdle in the wallaroo (Macropus robustus). J Linn Soc NSW 66:349-387.

Carlsson A. 1914. Uber Dendrolagus dorianus. Zoologische Jahrbuecher Abteilung fuer Systematic Oekol Geograph der Tiere 36:547-617.

Carlsson A. 1926. Über den Bau des Dasyuroides byrnei und seine Beziehungen zu den übrigen Dasyuridae. Acta Zool 7:249-275.

Cartmill M. 1985. Climbing. In: Hildebrand M, Bramble DM, Liem KF, Wake DB, editors. Functional Vertebrate Morphology. Cambridge: Belknap Press. p 73–88.

Chauveau A. 1891. The comparative anatomy of the domesticated animals. 2nd English ed. New York: D. Appleton.

Cheng C. 1955. The development of the shoulder region of the opossum, Didelphis virginiana, with special reference to musculature. J Morphol 97:415-471.

Coues E. 1871. The osteology and myology of Didelphis virginiana. Mem Bost Soc Nat Hist 2:41-149.

Crowther MS. 2008. Yellow-footed antechinus, Antechinus flavipes (Waterhouse, 1838). In: Van Dyck S, Strahan R, editors. The Mammals of Australia. Sydney: Reed Holland. p 86-88.

Page 35 of 54




36

Cunningham DJ. 1878a. The Intrinsic Muscles of the Hand of the Thylacine (Thylacinus cynocephalus), Cuscus (Phalangista maculata), and Phascogale (Phascogale calura). J Anat Physiol 12:434-444.

Cunningham DJ. 1878b. The Nerves of the Fore-Limb of the Thylacine (Thylacinus cynocephalus or harrisii) and Cuscus (Phalangista maculata). J Anat Physiol 12:427–433.

Cunningham DJ. 1881. The nerves of the hind-limb of the thylacine (Thylacinus harrisii or cynocephalus) and cuscus (Phalangista maculata). J Anat 15:265–277.

Cunningham DJ. 1882. Report on Some Points in the Anatomy of the thylacine (Thylacinus cynocephalus), cuscus (Phalangista maculata), and phascogale (Phascogale calura), collected during the Voyage of H. M. S. Challenger in the years 1873-1876; with an account of the Comparative Anatomy of the Intrinsic Muscles and Nerves of the Mammalian Pes. Voy H M S Challenger, Zool V, pt. XVI.

Davis DD. 1964. The giant panda: a morphological study of evolutionary mechanisms. Field Zool Mem 3:1-339.

Davison A. 1944. Mammalian anatomy with special reference to the cat. Revised by Stromstein FA, editor. Sixth Edition. Philadelphia: The Blakiston Company.

Diogo R, Abdala V. 2010. Muscles of vertebrates - comparative anatomy, evolution, homologies and development. Oxford: Taylor and Francis.

Diogo R, Abdala V, Aziz MA, Lonergan N, Wood BA. 2009. From fish to modern humans; comparative anatomy, homologies and evolution of the pectoral and forelimb musculature. J Anat 214:694-716.

Diogo R, Bello-Hellegouarch G, Kohlsdorf T, Esteve-Altava B, Molnar JL. 2016. Comparative Myology and Evolution of Marsupials and Other Vertebrates, With Notes on Complexity, Bauplan, and “Scala Naturae”. Anat Rec 299:1224-1255.

Diogo R, Pastor F, De Paz F, Potau JM, BelloSHellegouarch G, Ferrero EM, Fisher RE. 2012. The head and neck muscles of the serval and tiger: homologies, evolution, and proposal of a mammalian and a veterinary muscle ontology. Anat Rec 295:2157-2178.

Dixon JM. 1989. Thylacinidae. In: Walton WD, Richardson BJ, editors. Fauna of Australia. 1B Mammalia. Canberra: Australian Government Publishing Service. p 549-559.

Elftman HO. 1929. Functional adaptations of the pelvis in marsupials. Bull Am Mus Nat Hist 58:189-232.

Ercoli MD, Alvarez A, Stafanini MI, Busker F, Morales MM. 2015. Muscular anatomy of the forelimbs of the lesser grison (Galictis cuja), and a functional and phylogenetic overview of mustelidae and other Caniformia. J Mamm Evol 22:57-91.

Filan SL. 1990. Myology of the head and neck of the bandicoot (Marsupialia; Peramelemorphia). Aust J Zool 38:617-634.

Fisher RE, Adrian B, Barton M, Holmgren J, Tang SY. 2009. The phylogeny of the red panda (Ailurus fulgens): evidence from the forelimb. J Anat 215:611-635.

Gordon G, Hulbert AJ. 1989. Peramelidae. In: Walton DW, Richardson BJ, editors. Fauna of Australia. 1B Mammalia. Canberra: Australian Government Publishing Service. p 603-624.

Harvey KJ, Warburton NM. 2010. Forelimb musculature of kangaroos with particular emphasis on the tammar wallaby Macropus eugenii (Desmarest, 1817). Aust Mammal 32:1-9.

Page 36 of 54




37

Hill JP, Hill WC. 1955. The growthSstages of the pouchSyoung of the native cat (Dasyurus viverrinus) together with observations on the anatomy of the newSborn young. Trans Zool Soc Lond 28:349-352.

Hopwood PR. 1974. The intrinsic musculature of the pectoral limb of the Eastern Grey Kangaroo (Macropus major (Shaw) Macropus giganteus (Zimm)). J Anat 118:445-468.

Horiguchi M. 1981. A comparative anatomical study of the pectoral muscle group in the brindled bandicoot (Isoodon macrourus Gould 1842) an Australian marsupial. Acta Anat Nippon 56:375-399.

Horovitz I, Sanchez-Villagra MR. 2003. A morphological analysis of marsupial mammal higher-level phylogenetic relationships. Cladistics 19:181-212.

Jenkins FA, Weijs WA. 1979. The functional anatomy of the shoulder in the Virginia opossum (Didelphis virginiana). J Zool 188:379-410.

Jones FW. 1949. The study of a generalised marsupial (Dasycercus cristicauda Krefft). Trans Zool Soc 26:409-501.

Jones FW. 1968. The Mammals of South Australia. Adelaide: Government Printer. Jones M. 1995. Tasmanian devil, Sarcophilus harrisii. In: Strahan R, editor. The Mammals of

Australia. NSW, Australia: Reed Books Australia. p 82-84. Keyte AL, Smith KK. 2010. Developmental origins of precocial forelimbs in marsupial neonates.

Development 137:4283-4294. Krajewski C, Blacket M, Buckley L, Westerman M. 1997. A Multigene Assessment of

Phylogenetic Relationships within the Dasyurid Marsupial Subfamily Sminthopsinae. Mol Phylogenet Evol 8:236-248.

Krajewski C, Wroe S, Westerman M. 2000. Molecular evidence for the pattern and timing of cladogenesis in dasyurid marsupials. Zool J Linn Soc 130:375-404.

Lewis OJ. 1989. Functional morphology of the evolving hand and foot. Oxford: Clarendon Press. Macalister A. 1872. XIX. The muscular anatomy of the koala (Phascolarctos cinereus). Ann

Mag Nat Hist 10:127-135. MacAlister A. 1870. XVI. On the myology of the Wombat (Phascolomys wombata) and the

Tasmanian devil (Sarcophilus ursinus). Ann Mag Nat Hist 5:153-173. Macalister A. 1872. Further observations on the myology of Sarcophilus ursinus. Ann Mag Nat

Hist 10:17-20. MacCormick A. 1886a. The myology of the limbs of Dasyurus viverrinus. A. Myology of the

forelimb. J Anat Physiol 21:103-137. MacCormick A. 1886b. The myology of the limbs of Dasyurus viverrinus. B. Myology of the

hindlimb. J Anat Physiol 21:199-226. Marshall LG, Case JA, Woodburne MO. 1990. Phylogenetic relationships of the families of

marsupials. Current Mammal 2:433-505. Masters P. 2008. Crest-tailed mulgara, Dasycercus cristicauda (Kreft, 1867). In: Van Dyck S,

Strahan R, editors. The Mammals of Australia. Sydney: Reed Holland. p 49-50. Meredith RW, Westerman M, Case JA, Springer MS. 2008. A Phylogeny and Timescale for

Marsupial Evolution Based on Sequences for Five Nuclear Genes. J Mamm Evol 15:1-36.

Miller ME. 2012. Miller's anatomy of the dog. Howard E. Evans, George C. Christensen, editors. 2nd ed. Philadelphia: Saunders.

Page 37 of 54




38

Morton SR, Dickman CR, Fletcher TP. 1989. Dasyuridae. In: Walton DW, Richardson BJ, editors. Fauna of Australia. 1B Mammalia. Canberra: Australian Government Publishing Service. p 560-582.

Oakwood M. 2008. Northern quoll, Dasyurus hallucatus (Gould, 1842). In: Van Dyck S, Strahan R, editors. The Mammals of Australia. Sydney: Reed Holland. p 57-59.

Parsons FG. 1896. On the anatomy of Petrogale xanthopus, compared with that of other kangaroos. Proc Zool Soc Lond 64:683-714.

Parsons FG. 1903. Anatomy of the pig-footed bandicoot (Chaeropus castanotis). J Linn Soc Lond 29:64-80.

Reese S, Pfuderer U, Bragulla H, Loeffler K, Budras K. 2001. Topography, structure and function of the patella and the patelloid in marsupials. Anat Histol Embryol 30:289-294.

Rounsevell DE, Mooney N. 1995. Thylacine, Thylacinus cynocephalus. In: Strahan R, editor. The Mammals of Australia. NSW, Australia: Reed Books. p 164-165.

Serena M, Soderquist T. 2008. Western quoll, Dasyurus geoffroii (Gould, 1841). In: Van Dyck S, Strahan R, editors. The Mammals of Australia. Sydney: Reed Holland. p 54-56.

Schaller O. 2007 Illustrated Veterinary Anatomical Nomenclature. Stuttgart: Enke Verlag. Shrivastava RK. 1962. The deltoid musculature of the Marsupialia. Am Midl Nat 67:305-320. Smith KK. 2006. Craniofacial development in marsupial mammals: developmental origins of

evolutionary change. Dev Dyn 235:1181-1193. Soderquist T, Rhind S. 2008. Brush-tailed Phascogale, Phascogale tapoatafa (Meyer, 1793). In:

Van Dyck S, Strahan R, editors. The Mammals of Australia. Sydney: Reed Holland. p 105-107.

Sonntag CF. 1922. On the myology and classification of wombat, koala and phalanger. Proc Zool Soc Lond 92:863-869.

Stirling EC. 1891. Description of a new genus and species of Marsupialia, Notoryctes typhlops. Trans Roy Soc S Aust 14:154-187.

Szalay FS. 1982. A new appraisal of marsupial phylogeny and classification. In: Archer M, editor. Carnivorous Marsupials. Sydney: Roy Zool Soc NSW. p 612-640.

Taylor ME. 1974. The functional anatomy of the forelimb of some African Viverridae (Carnivora). J Morphol 143:307-336.

Warburton NM. 2006. Functional morphology of marsupial moles (Marsupialia: Notoryctidae). Verhandlungen des Naturwissenschaftlichen Vereins Hamburg 42:39-149.

Warburton NM. 2014. Relicts, Reproduction and Reintroductions - A century of marsupial research in Western Australia. J Roy Soc W Aust 97:65-85.

Warburton NM, Bateman PW, Fleming PA. 2013. Sexual selection on forelimb muscles of western grey kangaroos (Skippy was clearly a female). Biol J Linn Soc 109:923-931.

Warburton NM, Gregoire L, Jacques S, Flandrin C. 2014. Adaptations for digging in the forelimb muscle anatomy of the southern brown bandicoot (Isoodon obesulus) and bilby (Macrotis lagotis). Aust J Zool 61:402-419.

Warburton NM, Harvey KJ, Prideaux GJ, O'Shea JE. 2011. Functional morphology of the forelimb of living and extinct tree-kangaroos (Marsupialia: Macropodidae). J Morphol 272:1230-1244.

Warburton NM, Malric A, Yakovleff M, Leonard V, Cailleau C. 2015. Hind limb myology of the southern brown bandicoot Isoodon obesulus and greater bilby Macrotis lagotis (Marsupialia: Peramelemorphia). Aust J Zool 63:147-162.

Page 38 of 54




39

Warburton NM, Yakovleff M, Malric A. 2012. Anatomical adaptations of the hind limb musculature of tree-kangaroos for arboreal locomotion (Marsupialia: Macropodinae). Aust J Zool 60:246-258.

Westerman M, Krajewski C, Kear BP, Meehan L, Meredith RW, Emerling CA, Springer MS. 2015. Phylogenetic relationships of dasyuromorphian marsupials revisited. Zool J Linn Soc 176:686-701

Wilson JT. 1894. On the myology of Notoryctes typhlops with comparative notes. Trans Roy Soc S Aust 18:3-74.

Wood JT. 1870. On a group of varieties of the muscles of the human neck, shoulder, and chest, with their transitional forms and homologies in the Mammalia. Phil Trans Roy Soc Lond 160:83-116.

Young AH. 1879. The intrinsic muscles of the marsupial hand. J Anat Physiol 14:149-167. Young AH. 1882. The muscular anatomy of the koala. J Anat 16:217-242.

FIGURE CAPTIONS

Figure 1. Simplified phylogenetic tree of the Dasyuromorphia (modified from Westerman et al.

2015; branch lengths are not indicative).

Figure 2. Superficial lateral view of the right forelimb muscles in Dasyurus geoffroii; inset:

shoulder region with trapezius removed.

Figure 3. Muscle attachments on the right scapula of Dasyurus geoffroii (A, B, C) and

Phascogale tapoatafa (D, E, F). (A,D) medial view, (B,E) caudal view and (C,F) lateral view

(D,G). Atl, m. atlantoscapularis posticus; BiB, m. biceps brachii; Cor, m. coracobrachialis; DeA,

m. deltoideus acromialis; DeS m. deltoideus scapularis; Inf, m. infraspinatus; LCl, m. levator

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claviculae; OmH, m. omohyoideus; Rho, m. rhomboideus; SAn, m. serratus anterior; Sub, m.

subscapularis; Sup, m. supraspinatus; TMj, m. teres major; TMn, m. teres minor; TrC, m.

trapezius pars cervicalis; TrT, m. trapezius pars thoracis; TLn, m. triceps caput longum.

Figure 4. Lateral view of the right forelimb muscles in Phascogale tapoatafa, with m. trapezius

and mm. rhomboideus removed.

Figure 5. Superficial medial view of the right forelimb muscles in Dasyurus geoffroii.

Figure 6. Muscle attachments on the right humerus of Dasyurus geoffroii (A-D) and Phascogale

tapoatafa (E-H). (A,E) medial view, (B,F) caudal view and (C,G) lateral view, (D, H) cranial

view. ALt, m. anconeus lateralis; Bra, m. brachialis; BRd, m. brachioradialis; Cor, m.

coracobracialis; Del, m. deltoideus; ECR, m. extensor carpi radialis; ECU, m. extensor carpi

ulnaris; EDC, m. extensor digitorum communis; EDM, m. extensor digiti minimi; Epi, m.

epitrochleoanconeus; FCR, m. flexor carpi radialis; FCU, m. flexor carpi ulnaris; FDP, m. flexor

digitorum profundus; Inf, m. infraspinatus; LtD, m. latissimus dorsi; PaL, m. palmaris longus;

PeM, m. pectoralis major; Pmn, m. pectoralis minor; PrT, m. pronator teres; Spr, m. supinator;

Sub, m. subscapularis; Sup, m. supraspinatus; TLt, m. triceps caput lateral; TMd, m. triceps

caput medial; TMj, m. teres major; TMn, m. teres minor.

Figure 7. Muscle attachments on the right radius, ulna and carpus of Dasyurus geoffroii (A,B)

and Phascogale tapoatafa (C, D). (A,C) lateral view and (B, D) medial view. ALt, m. anconeus

lateralis; APL, M. abductor pollicis longus; BiB, m. biceps brachii; Bra, m. brachialis; EDC, m.

extensor digitorum communis; EDP, m. extensor digitorum profundus; Epi, m.

epitrochleoanconeus; FDP, m. flexor digitorum profundus; PrQ, m. pronator quadratus; PrT, m.

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41

pronator teres; Spr, m. supinator; TMd, m. triceps caput medial, TLn, m. triceps caput longum;

TLt, m. triceps caput lateral.

Figure 8. Medial view of the intrinsic forelimb muscles in Dasyurus hallucatus (right), humeral

head m. flexor digitorum profundus reflected.

Figure 9. Muscle attachments of the right manus of Dasyurus geoffroii, A dorsal view, B palmar

view.

Figure 10. Deep lateral view of the extensor muscles in the right forearm of Dasyurus hallucatus.

Figure 11. Deep intrinsic muscles of the right manus of Dasyurus hallucatus.

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Figure 1. Simplified phylogenetic tree of the Dasyuromorphia (modified from Westerman et al. 2015; branch lengths are not indicative).

33x20mm (600 x 600 DPI)

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Figure 2. Superficial lateral view of the right forelimb muscles in Dasyurus geoffroii; inset: shoulder region with trapezius removed.

39x28mm (600 x 600 DPI)

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Figure 3. Muscle attachments on the right scapula of Dasyurus geoffroii (A, B, C) and Phascogale tapoatafa (D, E, F). (A,D) medial view, (B,E) caudal view and (C,F) lateral view (not to scale). Atl, m. atlantoscapularis posticus; BiB, m. biceps brachii; Cor, m. coracobrachialis; DeA, m. deltoideus acromialis; DeS m. deltoideus

scapularis; Inf, m. infraspinatus; LCl, m. levator claviculae; OmH, m. omohyoideus; Rho, m. rhomboideus; SAn, m. serratus anterior; Sub, m. subscapularis; Sup, m. supraspinatus; TMj, m. teres major; TMn, m. teres minor; TrC, m. trapezius pars cervicalis; TrT, m. trapezius pars thoracis; TLn, m. triceps caput

longum.

46x40mm (600 x 600 DPI)

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Figure 4. Lateral view of the right forelimb muscles in Phascogale tapoatafa, with m. trapezius and mm. rhomboideus removed.

36x24mm (600 x 600 DPI)

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Figure 5. Superficial medial view of the right forelimb muscles in Dasyurus geoffroii.

32x19mm (600 x 600 DPI)

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Figure 6. Muscle attachments on the right humerus of Dasyurus geoffroii (A-D) and Phascogale tapoatafa (E-H). (A,E) medial view, (B,F) caudal view and (C,G) lateral view, (D, H) cranial view. ALt, m. anconeus

lateralis; Bra, m. brachialis; BRd, m. brachioradialis; Cor, m. coracobracialis; Del, m. deltoideus; ECR, m.

extensor carpi radialis; ECU, m. extensor carpi ulnaris; EDC, m. extensor digitorum communis; EDM, m. extensor digiti minimi; Epi, m. epitrochleoanconeus; FCR, m. flexor carpi radialis; FCU, m. flexor carpi

ulnaris; FDP, m. flexor digitorum profundus; Inf, m. infraspinatus; LtD, m. latissimus dorsi; PaL, m. palmaris longus; PeM, m. pectoralis major; Pmn, m. pectoralis minor; PrT, m. pronator teres; Spr, m. supinator; Sub, m. subscapularis; Sup, m. supraspinatus; TLt, m. triceps caput lateral; TMd, m. triceps caput medial;

TMj, m. teres major; TMn, m. teres minor.

52x74mm (600 x 600 DPI)

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Figure 7. Muscle attachments on the right radius, ulna and carpus of Dasyurus geoffroii (A,B) and Phascogale tapoatafa (C, D). (A,C) lateral view and (B, D) medial view. ALt, m. anconeus lateralis; APL, M. abductor pollicis longus; BiB, m. biceps brachii; Bra, m. brachialis; EDC, m. extensor digitorum communis;

EDP, m. extensor digitorum profundus; Epi, m. epitrochleoanconeus; FDP, m. flexor digitorum profundus; PrQ, m. pronator quadratus; PrT, m. pronator teres; Spr, m. supinator; TMd, m. triceps caput medial, TLn,

m. triceps caput longum; TLt, m. triceps caput lateral.

32x19mm (600 x 600 DPI)

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Figure 8. Medial view of the intrinsic forelimb muscles in Dasyurus hallucatus (right), humeral head m. flexor digitorum profundus reflected.

39x28mm (600 x 600 DPI)

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Figure 9. Muscle attachments of the right manus of Dasyurus geoffroii, A dorsal view, B palmar view.

27x14mm (600 x 600 DPI)

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Figure 10. Deep lateral view of the extensor muscles in the right forearm of Dasyurus hallucatus.

52x80mm (600 x 600 DPI)

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Figure 11. Deep intrinsic muscles of the right manus of Dasyurus hallucatus.

52x52mm (600 x 600 DPI)

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Table 1 - Biological characteristics of dasyuromorphian species investigated in this study (modified from (Warburton, 2014).

Species Body mass Ecology References

Antechinus flavipes

Yellow-footed antechinus,

mardo

26-79 g males;

21-52 g females

Primarily terrestrial; insectivorous; inhabits varied

habitats from forests to swamps and dry mulga

country.

(Crowther, 2008)

Dasycercus cristicauda

Crest-tailed mulgara,

ampurta

110-185 g males;

65-120 g females

Terrestrial; diet of arthropods and small

vertebrates; constructs burrows in desert sand

dunes with sparse cover.

(Masters, 2008)

Dasyurus geoffroii

Western quoll, chuditch

1310 g males (mean);

890 g females (mean)

Arboreal and terrestrial; mixed carnivorous diet,

mostly small to medium sized vertebrates;

sclerophyll forest, dry woodland or shrubland of

the south-west Australia.

(Serena and Soderquist,

2008)

Dasyurus hallucatus

Northern quoll

340-1120 g males; 240-

690 g females

Arboreal and terrestrial; diet mostly small

vertebrates; most commonly inhabits rocky

escarpments; also found in woodlands.

(Oakwood, 2008)

Phascogale tapoatafa

Brush-tailed phascogale,

common wambenger

175-311 g males;

106-212 g females

Arboreal specialist; primarily arthropod diet; open

forest with sparse groundcover.

(Soderquist and Rhind,

2008)

Sarcophilus harrisii

Tasmanian devil

9 kg males (mean);

7 kg females (mean)

Terrestrial; hypercarnivore, efficient scavenger;

inhabits varied habitats across Tasmania (formerly

Australian mainland)

(Jones, 1995)

Thylacinus cynocephalus

Tasmanian tiger

15-35 kg (species

mean)

Cursorial apex predator; varied habitats, most

abundant in open forest and woodland. Extinct.

(Rounsevell and Mooney,

1995)

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5051525354555657585960


Table 2 – Sources of Data for the Order Marsupialia (taxonomy after (Aplin and Archer, 1987))

Didelphimorphia Dasyuromorphia Diprotodontia Peramelemorphia Notoryctemorphia

Caluromys Dasycercus Dendrolagus Chaeropus Notoryctes

(Argot, 2001) (Jones, 1949) (Carlsson, 1914) (Parsons, 1903) (Wilson, 1894)

(Warburton et al., 2011) (Warburton, 2006)

Didelphis Dasyurus Echymypera

(Coues, 1871) (MacCormick, 1886a) Macropus (Filan, 1990)

(Jenkins and Weijs, 1979) (Boardman, 1941)

(Cheng, 1955) Sarcophilus (Hopwood, 1974) Isoodon

(MacAlister, 1870) (Harvey and Warburton, 2010) (Filan, 1990)

(Macalister, 1872) (Horiguchi, 1981)

Petrogale (Warburton et al., 2014)

Thylacinus (Parsons, 1896)

(Cunningham, 1878b) Macrotis

(Cunningham, 1878a) Phalanger (Filan, 1990)

(Sonntag, 1922) (Warburton et al., 2014)

Phascolactos

(Macalister, 1872)

(Young, 1882)

(Sonntag, 1922)

Phascolomys

(MacAlister, 1870)

(Sonntag, 1922)

Trichosurus

(Barbour, 1963)

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