On the development of the shoulder girdle in Crocidura russula (Soricidae) and other placental mammals: evolutionary and functional aspects

J. Anat.

(2002)

201

, pp371–381

© Anatomical Society of Great Britain and Ireland 2002

Blackwell Science, Ltd

On the development of the shoulder girdle in

Crocidura russula

(Soricidae) and other placental mammals: evolutionary and functional aspects

Martin Großmann, Marcelo R. Sánchez-Villagra and Wolfgang Maier

Zoologisches Institut, Spezielle Zoologie, Universität Tübingen, Auf der Morgenstelle 28, D-72076 Tübingen, Germany

Abstract

The development of the shoulder girdle was studied in embryonic stages and a neonate of

Crocidura russula

using

histological sections and 3-D reconstructions. Neonatal stages of

Suncus etruscus

and

Mesocricetus auratus

, both

altricial placentals, were also studied. The earliest stage of

C. russula

, in which the scapula is still partially blastem-

atous, has already a supraspinous fossa. The dorsal portion of the scapular spine does not develop from the anterior

margin of the scapula. Its mode of development varies among the placentals studied to date. In some it is

completely appositional bone, in others it consists of bone formed mostly by endochondral ossification of a dorsal

cartilaginous process stemming from the acromium. During development the supraspinatus muscle increases in size

in proportion to the infraspinatus muscle and the humeral head increases in size in relation to the glenoid fossa.

Placentals have secondary cartilage in the sternal and acromial ends of the clavicle, a derived feature absent in

Marsupialia. Even the most altricial placentals have a more developed shoulder girdle at birth than any newborn

marsupial studied to date.

Key words

Crocidura

;

Mesocricetus

; ontogeny; phylogeny; Placentalia; scapula; shoulder girdle; Soricidae;

Suncus

.

Introduction

Correlated with the evolution of more parasagittal

limb posture and movements, therian (metatherian

and eutherian) mammals have a shoulder girdle

containing fewer and smaller elements compared to

that of other tetrapods (Broom, 1899; Romer, 1922, 1956;

Klima, 1973, 1985, 1987). One of the most diagnostic

therian features is the division of the lateral surface of

the scapula into two fossae separated by a scapular

spine, considered a novel compensatory and stabilizing

mechanism (Fischer, 2001). Ontogenetic studies have

played an important role in developing our under-

standing about the origin of the therian shoulder

girdle. These studies have served to establish homologies

and to understand the adaptations and constraints of

the developing therian (Klima, 1987; Sánchez-Villagra

& Maier, in press a). Most of the above-cited studies

have dealt with marsupials. The development of the

shoulder girdle in Placentalia has been studied only in

a handful of taxa (Klima, 1985;

Sus scrofa

: Hanson,

1919;

Homo sapiens

: Zawisch, 1954;

Tupaia belangeri

:

Eickhoff, 1990). Particular aspects of shoulder girdle

development were treated by Klima (1967) on bats and

by Howell (1937) on muscle development in therians.

Recently, Sánchez-Villagra & Maier (in press a, b)

proposed some modifications to the current model on

the origin of the therian scapula (Romer, 1956), after

studying the development of the shoulder girdle in some

marsupial taxa. Sánchez-Villagra & Maier (in press a)

also interpreted many of the features of perinatal

marsupials not as signs of recapitulation but rather as

adaptations to extra-uterine development. As a test to

these hypotheses, it is necessary to examine the placen-

tal condition. Of particular interest concerning adapta-

tions to an ‘early’ birth is the examination of altricial

placentals. A short gestation period and altriciality (as

Correspondence

Marcelo R. Sánchez-Villagra, Universität Tübingen, Spezielle Zoologie, Auf der Morgenstelle 28, D-72076 Tübingen, Germany. Tel. +44 7071 2974631; fax: +44 7071 295150; e-mail: [email protected]

Accepted for publication

2 September 2002

JOA_105.fm Page 371 Wednesday, October 16, 2002 11:40 AM

Development of the shoulder girdle in placental mammals, M. Großmann et al.


372

opposed to precocity) is the most likely groundplan

condition of Placentalia (e.g. Portmann, 1965; Vogel,

1972; Sánchez-Villagra & Sultan, 2002).

In this paper the embryonic development of the

shoulder girdle until birth is studied in an altricial

Eulipotyphla, the soricid

Crocidura russula

, and the

results are compared with those in the literature and

with additional data on two other altricial placentals.

This study is mainly an examination of the mode of

development of the scapular spine and the supra-

spinous fossa and the condition at birth in altricial

placentals, with the main goal to examine issues about

the evolutionary origin of the therian scapula.

Materials and methods

Five stages of

Crocidura russula

were investigated, of

crown–rump length CRL (mm) = 8, 11, 12.5, 14 and

21, the largest one a neonate. The exact age of these

specimens is unknown, but based on data provided

by Vogel (1972) and the known CRL, rough estimates

can be made (Table 1). A neonate (CRL = 13 mm) of the

soricid

Suncus etruscus

, the smallest living mammal

(Starck, 1995), was also investigated. Both

C. russula

and

S. etruscus

have a gestation length of only

c

. 30 days (Vogel, 1972). They both show a shoulder

girdle anatomy not too different from the hypothesized

ancestral condition of Placentalia, having a clavicle and

lacking major specializations of the scapula (Starck, 1995).

In addition to the soricids, a neonate (CRL = 29 mm)

of a phylogenetically distant taxon was also studied:


, a member of the Muridae

(Rodentia) with a gestation length of 16 days, the

shortest among placentals. The study of this taxon

serves to expand the phylogenetic sample of altricial

placentals.

Almost all histological specimens were sectioned

in a more or less transverse plane; sections are between

10 and 20

µ

m. In most specimens the left side was

modelled. Mirror images of the model of

M. auratus

are presented since the right side was better preserved

in this specimen. Photographs of the specimens studied

before sectioning are reproduced in Fig. 1. All histolog-

ical material examined belongs to the collections of the

Zoological Institute of the University of Tübingen.

Three-dimensional models of the scapula and the

supraspinatus and infraspinatus muscles based on the

histological sections were made for all specimens

examined. The software programs Surfdriver v. 5.3

(Moody & Lozanoff, 1999) and Cinema 4D v. 5.3 (Losch

et al. 1999) were used and the method is described in

Sánchez-Villagra & Maier (in press a).

Results

Description of relevant events in the development of

the pectoral girdle in

Crocidura russula

Table 1 shows the absolute length of the scapula in all

the specimens studied.

Stage CRL = 8 mm (Figs 2A, 3A and 4A)

. The following

elements are already recognizable: scapula with acro-

mium, anlage of the scapular spine, glenoid fossa, clav-

icle and the supraspinatus and infraspinatus muscles.

The scapula is narrow and long in the dosoventral

plane. Only the position of the muscles indicates the

approximate location of the border between the

supraspinous and the infraspinous fossae (the latter

the larger of the two), since the spina anlage is not

complete yet. The supraspinous fossa is relatively small

and present only in the dorsal-most portion of the

scapula. The dorsal and ventral portions of the scapula

(including the glenoid area and acromium) are blast-

ematous, while only the middle portion consists of

young cartilage. The anlage of the coracoid process

cannot be separated from the glenoid fossa and forms

the cranial portion of the articular surface of the latter.

Table 1 Length of the scapula (distance glenoid fossa – dorsal scapular border) in the specimens studied. OT = days after conception. ZSH = Zoologische Sammlung, Zoologisches Institut; SZ = Schausammlung, Zoologisches Institut Universität Tübingen

Age CRL (mm)Length of the scapula (mm)

SoricidaeCrocidura russulaZSH Nr. 21 F ca. 19 OT 8 0.75ZSH Nr. 28 ca. 21 OT 11 1.4ZSH Nr. 39 ca. 22 OT 12.5 1.5ZSH ca. 23 OT 14 1.7ZSH Nr. 117 Neonate 21 2SZ 6647 Adult – 7.8Suncus etruscusZSH C Neonate 13 1.2

CricetidaeMesocricetus auratusZSH Neonate 29 3.9




373

Fig. 1 Photographs of specimens studied before sectioning. (A) Crocidura russula, (B) Mesocricetus auratus, (c) Suncus etruscus. Scale bar = 1 cm.




374

Fig. 2 Photomicrographs of coronal sections through portions of the scapular region in Crocidura russula (ZSH). (A) CRL = 8 mm, (B) CRL = 11 mm, (C) CRL = 12.5 mm, (D,E,G) CRL = 14 mm, (F) CRL = 21 mm; (E) is detail of (G). Scale bar = 0.1 mm. Abbreviations: a acromion, cl clavicle, clc clavicle/secondary cartilage, g glenoid fossa, h humerus, ism Infraspinatus muscle, s scapula, sbm Subscapularis muscle, ss scapular spine, ssm Supraspinatus muscle.




375

Fig. 3 Photomicrographs through portions of the scapular region in (A) Crocidura russula (CRL = 8 mm), (B) Suncus etruscus (neonate) and (C,D) Mesocricetus auratus (neonate). Scale bar = 0.1 mm. Abbreviations: a acromion, cl clavicle, g glenoid fossa, h humerus, ism Infraspinatus muscle, s scapula, sbm Subscapularis muscle, ss scapular spine, ssm Supraspinatus muscle.




376

Fig. 4 Three-dimensional models of the left scapula in an ontogenetic series of Crocidura russula, lateral view. (A) CRL = 8 mm, (B) CRL = 11 mm, (C) CRL = 12.5 mm, (D) CRL = 14 mm, (E) CRL = 21 mm. Figure A3 shows a posterior view; asterisk points to the separation of the cartilaginous anlage of the scapular spine from the scapula itself. As development progresses, this area will be filled with appositional ossification. Scale bars: A = 0.1 mm, B,C,D,E = 0.5 mm. Abbreviations: a acromion, ism Infraspinatus muscle, ma metacromium, s scapula, sbm Subscapularis muscle, ss scapular spine, ssm Supraspinatus muscle.




377

In the acromium there is a small process, the anlage of

the metacromium. A blastematous dorsal process of

the acromium represents the anlage of the scapular

spine, which at this stage does not reach the surface of

the scapula itself. The middle portion of the clavicle is

bone and at its sternal and scapular ends it is blastem-

atous. The infraspinatus muscle joins the supraspinatus

muscle between the acromium and fossa glenoidea,

both muscles inserting in the anlage of the major

tubercle of the humerus. Most of the supraspinatus

muscle is situated cranial to the scapula; only a small

portion of it rests on the lateral side of the scapula, on

the supraspinous fossa. The head of the humerus is

relatively small in relation to the glenoid fossa and

has a round shape. The whole of the humeral head is

blastematous.

Stage CRL = 11 mm (Figs 2B, 4B and 5A)

. The scapula is

relatively narrower than in the earlier stage examined.

The supraspinous fossa has grown relatively more

dorsally and cranially and extends up to the middle of

the entire length of the scapula. The dorsal portion

of the infraspinous fossa forms a triangular surface

extending up to the glenoid fossa; dorsally it is shorter

than the supraspinous fossa. Starting in this stage the

boundary between the two fossae is clearly demarc-

ated by the scapular spine anlage. The dorsal portion

of the scapula consists of young cartilage. On the

cranial border of the middle portion there are already

the first signs of ossification. The spine anlage consists

dorsally of young cartilage; between the spine and the

scapular blade itself there is no direct connection. The

acromium is formed of young cartilage and consists of

a cranially directed process (acromium

sensu stricto

)

and the ventrocaudally directed metacromium. The

glenoid fossa consists of young cartilage; its cranial end

is formed by the coracoid process. The clavicle is S-

shaped, and its sternal end is formed by secondary

cartilage, which is found at the very lateral end as well.

The infraspinatus muscle is, relative to the scapula,

larger than it was in the earliest stage examined and

rests on a dorso-caudal portion of the infraspinous

fossa. The supraspinatus muscle has clearly grown and

Fig. 5

Three-dimensional models of the ventral portion of the left scapula and the humeral head in two embryonic and a neonate specimen of

Crocidura russula

. (A) CRL = 11 mm, (B) CRL = 14 mm, (C) CRL = 21 mm. All figures show a lateral view. Scale bars = A,B = 0.1 mm, C = 0.5 mm. Abbreviations: g glenoid fossa, h humerus, ma metacromium.




378

has relatively larger cranial and dorsal extensions. Since

the supraspinous fossa is present only in the dorsal-

most portion of the scapula, most of the supraspinatus

muscle lies simply cranial to the scapular spine without

any medial skeletal support. The humeral head consists

of young cartilage and has a slightly oval shape; the

major tubercle is clearly recognizable.

Stage CRL = 12.5 mm (Figs 2C and 4C)

. The scapula has

now a dorso-ventrally elongated shape. The supra-

spinous fossa extends up to the middle portion of the

scapula. It is now more cranially expanded in its ventral

portion in comparison with the previous stage. The

infraspinous fossa has expanded dorsally, reaching

almost the level of the supraspinous fossa. The dorsal

portion of the scapula consists of young cartilage; some

portions of the cranial border are blastematous while

others have started ossification. More or less in the

middle portion of the scapula there is periosteal ossifica-

tion and early marrow (Streeter, 1951). In its ventral

portion the scapula consists again of cartilage. The

concave surface of the glenoid fossa is now deeper

and consists of young cartilage. Cranially the fossa is

formed by the anlage of the coracoid process. Both

the metacromium and the acromium

sensu stricto

consist also of young cartilage. The clavicle is not

preserved in this stage, an artefact of the histological

preparation. Most of the supraspinatus muscle still lies

lateral to the scapula. The infraspinatus muscle covers

most of the infraspinous fossa, except for a free small

dorso-caudal area. The humeral head, which is cartilag-

inous, is slightly oval and has increased in relative size

to the glenoid fossa in comparison to the previous

stage.

Stage CRL = 14 mm (Figs 2D,E,G, 4D and 5B)

. Scapular

form and proportions are very similar to those of the

previous stage, the only significant difference being

the more caudal orientation of the metacromium.

Histologically, all elements of the shoulder girdle

are similar in this and the previous stage.

Stage CRL = 21 mm, neonate (Figs 2F, 4E and 5C)

. The

scapula is much wider in comparison with younger

stages. The supraspinous fossa has expanded cranially,

while the infraspinous fossa has expanded caudally and

dorsally. The infraspinous fossa is dorsally longer than

the supraspinous fossa; in this the neonate has attained

the adult condition. The anlage of the coracoid process

still forms the cranial portion of the glenoid cavity; the

latter is orientated caudoventrally. In this stage the first

sign of ossification in the caudal border of the scapula

is recorded. The dorsal-most portion of the spine is

mostly cartilaginous, while more medially it is ossi-

fied as is now much of the main body of the scapula.

The area limiting the dorsal portion of the spine

from the acromial portion consists of blastem. The

supraspinatus and infraspinatus muscles have

expanded following the growth of the supraspinous

and infraspinous fossae, respectively. The proximal

portion of the humeral head is cartilaginous; medial to

this are hypertrophic cells.

The pectoral girdle in neonatal

Suncus etruscus

and


Suncus etruscus CRL = 13 mm, neonate (Figs 3B and

6A,B).

The coracoid process is part of the glenoid cavity

as is the case in

Crocidura russula

. Both the acromial

and the sternal ends of the clavicle consist of secondary

cartilage. The structures studied are in a similar histo-

logical condition as those of the neonate

Crocidura

russula

.

Mesocricetus auratus CRL = 29 mm, neonate (Figs 3C,D

and 6C,D)

. The supraspinous fossa has a large surface

of attachment for the supraspinous fossa. The anlage

of the scapular spine does not show any cartilage

and can be best described as appositional ossification

(‘Zuwachsknochen’ in the German language). The

clavicle has a major S-shaped bony portion and distal

and proximal ends consisting of secondary cartilage.

The supraspinatus muscle covers the whole of the supra-

spinous fossa. Ventrally, it lies on the cranial side of the

anlage of the scapular spine and runs between the

acromium and the glenoid fossa to the major tubercle

of the humerus. The infraspinatus muscle reaches the

dorsal-most extension of the infraspinous fossa.

Discussion

Development of the scapula and other elements of the

shoulder girdle

Supraspinous and infraspinous fossae

. A supraspinous

fossa, although restricted to the dorsal portion of

the scapula, is present already in the earliest stage

examined. The ventral portion of this fossa appears




379

later in development. In

Tupaia belangeri

(Eickhoff,

1990) and in

Sus scrofa

(Hanson, 1919; cf. plate 1, figs 1

and 2) as in

Crocidura russula

and all marsupials

examined to date (Sánchez-Villagra & Maier in press a),

a supraspinous fossa is already present in early stages

in which the scapula is still cartilaginous.

In all placentals and marsupials examined to date, includ-

ing

Crocidura russula

, the infraspinous fossa is present

along the whole of the scapula already in the earliest

stage examined. In the adult

C. russula

the infraspinous

fossa is more dorsally expanded than the supraspinous

one (Fig. 7A), a condition found already in the neonate.

Scapular spine

. The ossification mode of the scapular

spine is apparently different among the taxa examined.

In

Crocidura russula

most of the spine (continuous with

the acromium) has a cartilaginous precursor and ossi-

fies endochondrally. The connection with the scapula

itself occurs through appositional bone. Based on what

was observed in just one stage (neonate) of

Suncus

etruscus

, this mode apparently characterizes this

species as well. In contrast, in


the

whole of the dorsal spine is probably the result of

appositional ossification of an intermuscular septum,

since in the neonate of this species there are no signs

Fig. 6 Three-dimensional models of the left scapula in neonatal specimens of (A) Suncus etruscus and (B) Mesocricetus auratus. All figures show a lateral view. Scale bars = A 0.5 mm, B 1 mm. Abbreviations: a acromion, g glenoid fossa, ims intermuscular septum, isf infraspinous fossa, ism Infraspinatus muscle, ma metacromium, pcs coracoid process, s scapula, ss scapular spine, ssf supraspinous fossa, ssm Supraspinatus muscle.

Fig. 7 Photographs of the left scapula in (A) lateral and (B) medial views in a macerated skeleton of an adult Crocidura russula (SZ 6647); (C) shows a lateral view of the ventral portion. Scale bars = 1 mm. Abbreviations: a acromion, g glenoid fossa, isf infraspinous fossa, ma metacromium, pcs coracoid process, ssf supraspinous fossa.




380

of cartilage in the anlage of the spine, formed by

connective tissue. Eickhoff (1990) described the devel-

opment of the dorsal portion of the scapular spine in

Tupaia belangeri

as an example of Zuwachsknochen or

appositional bone.

Metacromiom

. The metacromiom is present already in

the earliest stages of

Crocidura russula

examined. The

metacromiom is present in many placental groups and

provides enlarged attachment for the deltoid muscle

(Fig. 7; Giebel, 1874).

Glenoid fossa and coracoid process

. In all stages of

Crocidura russula

and in the neonate

Suncus etruscus

examined, the coracoid process is continuous with the

scapula itself, forming part of the glenoid cavity. The

anlage of the coracoid process participates in the formation

of the articular cavity, as is also the case in perinatal

marsupials (Klima, 1987; Sánchez-Villagra & Maier in press a).

In none of the stages examined of

Crocidura russula

did we find a connection of the scapula with the sternum

through the metacoracoid, as is the case in adults

monotremes and in perinatal stages of most marsupials

examined to date (Broom, 1899; Klima, 1987; Sánchez-

Villagra & Maier in press a). This supports the hypothesis

that the marsupial perinatal condition does not repres-

ent a case of recapitulation, but rather part of a suite

of characters related to adaptations to an early

extra-uterine life (Sánchez-Villagra & Maier in press a).

Clavicle

. The clavicle is the first element among those

examined and in fact is the first post-cranial element to

ossify in therians (Sánchez-Villagra, 2002). All three

investigated taxa possess cartilaginous areas at both

the sternal and the scapular ends of the clavicle, inter-

preted here as secondary cartilage. Cartilaginous

portions of the clavicle are also documented for other

placental taxa, including

Homo

(Zawisch, 1953; Koch,

1960; Andersen, 1963),

Macaca mulatta

(Hall, 2001)

and

Mus

(Hall & Tran, 1989; Huang et al. 1997). In

marsupials, the clavicle is completely dermal, with no signs

of cartilage in either the sternal or the scapular ends

(Broom, 1899; Sánchez-Villagra & Maier in press a). In

monotremes the clavicle is completely dermal, so it can

be concluded that the presence of secondary cartilage

as part of the clavicle in Placentalia is a derived feature.

Supraspinatus and infraspinatus muscles

. During onto-

geny, the supraspinatus muscle increases in size relative

to the scapula and the infraspinatus muscle. In

Mono-

delphis domestica

the opposite is true (Sánchez-Villagra

& Maier in press a).

Humeral head and glenoid fossa

. The relative size of

the humeral head in relation to the glenoid fossa changes

during development in

Crocidura russula

in a similar

fashion to what was reported for

Monodelphis domestica

(Sánchez-Villagra & Maier in press a). Early in ontogeny

the humeral head is relatively small. By the time of birth

the size relations are already similar to that of adults.

Condition at birth

. The altricial placental taxa

examined have at birth a more developed shoulder girdle

than any marsupial examined to date. The scapulacora-

coid of marsupials at birth shows no signs of ossifica-

tion and the metacoracoid still represents a large

portion of the former. Concerning the taxa included in

this study, the shoulder girdle of the neonates of the

two soricids and the rodent


are in

a similar stage of histological differentiation. Vogel

(1972) reported that ossification of the skull and the

limbs is more advanced in the soricids in comparison to


.

Origin of the therian scapula and development of

the scapular spine

Based on their study of didelphids and a few other

marsupial taxa, Sánchez-Villagra & Maier (in press a, b)

hypothesized that the scapular spine and not the

supraspinous fossa is an evolutionary novelty of Theria.

This hypothesis, supported by a cursory examination

of the fossil record of mammaliaformes (Rowe, 1988;

Luo et al. 2001; Sánchez-Villagra & Maier, in press b),

contradicts the standard conception that the therian

scapular spine is entirely homologous to the anterior

margin of the ancestral mammalian scapula (Romer,

1956; Jenkins & Weijs, 1979).

A fundamental observation of Sánchez-Villagra &

Maier (in press a, b) to base their new hypothesis

was that in none of the marsupial species studied to

date does the dorsal portion of the scapular spine

develop through the anterior margin of the scapula.

This is also true for

Crocidura russula

. Even in the

earliest stage of

C. russula

examined, the supraspinous

fossa is already present and there is an anlage of the

scapular spine, even though the scapula is still partially

blastematous. This is also the case in

Tupaia belangeri




381

(Eickhoff, 1990) and in diverse marsupial taxa

(Sánchez-Villagra & Maier, in press a). The fact that all

these phylogenetically distant taxa share this feature

of development supports the hypothesis that it charac-

terized the last common ancestor of Theria.

The difference in the mode of development of the

scapular spine (appositional ossification) in comparison

with the rest of the scapula (endochondral ossification)

was also considered by Sánchez-Villagra & Maier (in

press a, b) in their discussion of the origin of the therian

scapula. As described above, the mode of ossification

of the scapular spine is variable among placentals, with

a more or less important component of appositional

bone. There are other examples among mammals of

variability in the mode of development of a homolo-

gous structure across taxa. For example, Klima (1967)

described five different modes of ossification in the

sternum of bats, although the adult structure is homo-

logous across bat taxa.

Acknowledgments

We thank T. T. Fussnegger and M. Meinert for the prep-

aration of histological materials, P. Vogel (Lausanne)

for kindly providing some of the material on which this

study is based and K. K. Smith and an anonymous

reviewer for helpful suggestions. This research was

partially supported by the German National Science

Foundation (DFG Grant SA-883/4 to MRSV).

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Documents

On the development of the shoulder girdle in Crocidura russula (Soricidae) and other placental mammals: evolutionary and functional aspects