Zoological Journal of the Linnean Society, 2010, 159, 746–784. With 7 figures
Evidence of early evolution of Australidelphia
(Metatheria, Mammalia) in South America: phylogenetic
relationships of the metatherians from the Late
Palaeocene of Itaboraí (Brazil) based on teeth and
petrosal bones
SANDRINE LADEVÈZE* and CHRISTIAN DE MUIZON
Muséum National d’Histoire Naturelle, USM 0203, UMR 5143 CNRS, Paléobiodiversité et
paléoenvironnements, 8 rue Buffon, CP 38, F-75005 PARIS, Paris F-75005, France
Received 11 March 2008; accepted for publication 18 February 2009
New metatherian petrosal bones from the mid to Late Palaeocene of Itaboraí, belonging to three morphotypes (VI,
VII, and VII), are formally described and compared to fossil and extant taxa known by their auditory region. An
attempt at assigning petrosal types to tooth-based taxa from Itaboraí was made by combining parsimony and
morphometric methods. The first large scale phylogenetic analysis of the Itaboraían metatherians, involving
basicranial and dental characters in a larger number of taxa, is provided here and is at the basis of a systematic
revision of the metatherians from Itaboraí. The combination of morphometric and cladistic analyses helps in
understanding the affinities between the petrosals and the tooth-based taxa. The metatherians from Itaboraí were
taxonomically diverse, belonging to each of the most important radiations in marsupial evolutionary history
(Didelphimorphia, Paucituberculata, Eometatheria). The inclusion of Palaeocene taxa in the crown group Marsupialia and above all in the Eometatheria radiation points to an early emergence of these clades in South America
and corroborates the main molecular hypotheses.
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784.
doi: 10.1111/j.1096-3642.2009.00577.x
ADDITIONAL KEYWORDS: basicranium – early Tertiary – morphometry – phylogeny.
INTRODUCTION
The fossils from the mid to late Palaeocene Itaboraí
fissures of Brazil, along with the spectacularly complete specimens of the early Palaeocene Tiupampa
locality of Bolivia, represent the most important
sources of information for an understanding of the
beginning of metatherian mammal radiations in
South America (see de Paula Couto, 1952a, b, c, 1961,
1962; Marshall, 1987; de Muizon, 1992; de Muizon &
Brito, 1993; Marshall, de Muizon & SigogneauRussel, 1995; de Muizon, Cifelli & Céspedes Paz,
*Corresponding author. Present address: Royal Belgian
Institute of Natural Sciences, Department of Paleontology,
29 rue Vautier, B-1000 Bruxelles, Belgium.
E-mail: [email protected]
746
1997; de Muizon, Cifelli & Bergqvist, 1998; de Muizon
& Cifelli, 2001). In both localities, remains of metatherian auditory regions were discovered, in addition to numerous, abundantly described dental
remains (Marshall & de Muizon, 1995; Ladevèze,
2004, 2007b; Ladevèze & de Muizon, 2007).
The basicranial region, and in particular the petrosal bone, has proven to be of interest in therian
systematics (e.g. Carnivora, Hunt, 1974; primates,
MacPhee, Novacek & Storch, 1988; Marsupialia,
Sánchez-Villagra & Wible, 2002). The petrosal is the
most complex bone in the mammalian skull, resulting
from an endochondral ossification of the basicranium.
It contains a variety of soft tissue structures, such as
the organs of hearing and balance, components of the
central and peripheral nervous system, major cranial
arteries and veins, and muscles derived from the
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
mandibular and hyoid arches (Rougier & Wible,
2006). Most of these soft tissues leave impressions on
the petrosal bone, which can be interpreted and
reconstructed in fossil specimens. Although metatherian petrosal bones are uncommon in the fossil record,
some isolated petrosals, besides rare cases of complete skulls, were described from the Late Cretaceous
of North America (Clemens, 1966; Archibald, 1979;
Wible, 1990; Meng & Fox, 1995b) and the early to mid
Palaeocene of South America (Marshall & de Muizon,
1995; de Muizon et al., 1997; de Muizon, 1998;
Ladevèze, 2004, 2007b; Ladevèze & de Muizon, 2007),
and provided an important source of characters with
potentially relevant phylogenetic information as to
the early radiation of the South American metatherians. To date, the most comprehensive analyses of the
petrosal bone osteology of metatherian mammals are
those of Ladevèze (2004, 2007b), Ladevèze & de
Muizon (2007), Luo et al. (2003), Rougier & Wible
(2006), Rougier, Wible & Novacek (1998, 2004),
Sánchez-Villagra et al. (2007), Sánchez-Villagra &
Wible (2002), Wible (1990, 2003), Wible & Hopson
(1995).
Ladevèze (2004, 2007b) has described several isolated metatherian petrosal bones from Itaboraí,
which were referred to five different types (I to V).
They were not formally assigned to any metatherian
taxon, but Type II was identified as the sister group
of Pucadelphydae and Types I, III, IV, and V as
the stem taxa of the clade Australidelphia plus
Caenolestes.
Three new types of isolated metatherians petrosal
bones from the mid Palaeocene of Itaboraí (Brazil) are
herein described and compared to fossil and extant
metatherians known by their auditory region. They
represent the last undescribed metatherian petrosals
known so far from Itaboraí.
A first attempt to assign the isolated petrosal to
known taxa from Itaboraí was made by Ladevèze
(2007b), but her phylogenetic analysis did not incorporate any of the 19 genera of Itaboraían metatherians known by teeth remains. To date, no accurate
phylogenetic analysis of the Itaboraían metatherians
has ever been proposed. Marshall (1987), when revising the systematics of the metatherians from Itaboraí,
studied the distribution of 17 dental characters in 17
genera but his phylogenetic analysis is not relevant
as it did not consider enough characters to discriminate the genera.
The first phylogenetic analysis of the metatherians
from Itaboraí, based on petrosal, basicranial, and
dental characters, is here performed and includes the
eight petrosal types and the 19 known genera from
Itaboraí. An attempt at assigning the isolated petrosals to Itaboraían dental taxa is made on the basis of
a morphometric analysis based on dental and petrosal
747
remains. The results of the morphometric analysis
are compared to those of the phylogenetic analysis.
MATERIAL AND METHODS
A list of the institutional abbreviations used for
sample names is given in Supporting Information
Appendix S1.
MATERIAL
The metatherians from São José de Itaboraí
The São José de Itaboraí Basin, located in the County
of Itaboraí, Rio de Janeiro State, is formed in clayfilled fissures in a Precambrian limestone. The Itaboraían age is estimated as early Late Palaeocene;
about 57 to 59 Myr (Flynn & Swisher, 1995; Marshall,
Sempere & Butler, 1997). The numerous dental
remains allowed the identification of approximately
20 metatherian genera belonging to the Peradectidae,
Didelphidae,
Protodidelphidae,
Polydolopidae,
Hathlyacynidae, Borhyaenidae, Paucituberculata,
and Microbiotheriidae (Marshall, 1987; de Muizon &
Brito, 1993; Marshall et al., 1997; McKenna & Bell,
1997). However, we ignored the relationships of the
metatherian petrosals to the taxa based on dental
material, as they were not found in association.
The metatherian petrosals from Itaboraí described
herein are referred to three new types: Type VI
(MNRJ 6734-V), Type VII (MNRJ 6737-V, 6738-V,
6739-V), and Type VIII (MNRJ 6735-V, 6740-V).
Other previously described petrosals are: Type I
(MNRJ 6726-V, 6727-V) and Type II (MNRJ 6728-V,
6729-V) (Ladevèze, 2004); and Types III (MNRJ
6730-V, 6731-V), IV (MNRJ 6732-V), and V (MNRJ
6733-V, 6736-V) (Ladevèze, 2007b). A synthesized
table summarizes the anatomical characteristics of
each petrosal type from Itaboraí (Table 1).
The specimens of Itaboraían metatherians from
which were coded the dental characters for a cladistic
analysis and on which measurements of molars
(M2–3, second and third upper molars; m2–3, second
and third lower molars) were taken are listed in
Supporting Information Appendix S2.
Comparative material
The comparative extinct metatherians include wellpreserved skulls and isolated petrosals from the Early
Palaeocene of Tiupampa (Bolivia): Mayulestes ferox
(MHNC 1249), Andinodelphys cochabambensis
(MHNC 8264, 8308, 8370, 8371), and Pucadelphys
andinus (MHNC 8364, 8367, 8368, YPFB Pal 6105,
6110, 6470) (Marshall & de Muizon, 1995; de Muizon,
1998; Ladevèze & de Muizon, 2007).
As far as Recent marsupials are concerned, didelphids represent the sister group of all other taxa.
They retain several primitive osteological characters
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
Internal carotid
artery passes
through anterior pole
of promontorium
Present
Present
Present
Absent
Absent
Present
Present
Present
Petrosals
Type I
Type II
Type III
Type IV
Type V
Type VI
Type VII
Type VIII
Absent
Small process
Low, tiny tubercle
Small process
Absent
Well-developed,
anterolaterally
directed wing
Low, tiny tubercle
Absent
Rostral tympanic
process of petrosal
?
Expanded lamina
flooring the
post-promontorial
sinus
Expanded lamina
flooring the
post-promontorial
sinus
?
Small crest
Small crest
Small crest
Small crest
Caudal tympanic
process of petrosal
?
Small, ventrally
directed process
Large slanted process
Small, ventrally
directed process
Small, ventrally
directed process
Indistinct to absent
Small, ventrally
directed process
Small, ventrally
directed process
Mastoid process
Table 1. List of selected anatomical characteristics of each petrosal type (I to VIII)
Absent
Absent
Present
Present
?
Present
Absent
Present
Tympanic
crest
Present
Present
Present
Present
Absent
Present
Present
Present
Prootic canal
(tympanic
aperture)
Intermediate
Dorsal
Dorsal
Dorsal
Intermediate
Dorsal
Intermediate
Dorsal
Hiatus
Fallopii
?
?
Absent
Absent
Absent
Present
Absent
Absent
Diploetic
vessels
748
S. LADEVÈZE and C. DE MUIZON
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
and are defined by few derived characters (Rougier
et al., 1998, 2004; Wroe et al., 2000; Wible et al., 2001;
Horovitz & Sánchez-Villagra, 2003; Asher, Horovitz &
Sánchez-Villagra, 2004). They represent the most
appropriate taxon amongst extant metatherians to be
an anatomical model for studying fossil American
metatherians (Wible, 1990). This group was the main
basis for comparison to Recent taxa for the Itaboraí
petrosals. The other South American taxa caenolestids and microbiotheriids, and the less derived Australian taxa were chosen to help in the description of
the petrosals from Itaboraí.
A complete list of the studied specimens of fossil
and extant taxa is given in Supporting Information
Appendix S2.
METHODS
Several approaches could have been used to assign
the isolated petrosals herein described to taxa that
are previously known only from dentitions, such as
comparative anatomy, relative abundances, and size.
The petrosal types were identified as metatherians,
as they lack a stapedial artery sulcus on the promontorium and display an extrabullar pattern of the
internal carotid artery pathway. If we consider the
criterion of relative abundances, all the isolated petrosals should be attributed to Marmosopsis as it is, by
far, the most frequent taxon of the deposit (representing 20%, the other most abundant genera being Protodidelphis with 14% and Didelphopsis with 10% but
both are too large to be associated to any of the
petrosals; Ladevèze, 2007a). This criterion was thus
not accurate enough for our purpose. We therefore
chose to use both morphology (phylogeny) and size
(morphometry) criteria to assign the isolated petrosals to the taxa that are known from Itaboraí.
Cladistic method
Our dataset contained a total of 56 basicranial and 89
dental characters, examined in four outgroup and 40
ingroup taxa (fossil and extant metatherians, see
below, and the eight petrosal morphotypes and 17
dental-based genera from Itaboraí). A complete list of
the sampled characters is given in Appendix 1.
Two outgroup taxa were well-preserved fossils, the
auditory region of which is known. Vincelestes neuquenianus, from the Early Cretaceous of Argentina, is
a close relative of therians (MACN-N04, -N05, -N09
-N16; Rougier & Bonaparte, 1988; Rougier, Wible &
Hopson, 1992; Hopson & Rougier, 1993). Prokennalestes trofimovi, to which was assigned an isolated
petrosal, is a stem eutherian from the Early Cretaceous of Mongolia (PSS-MAE 136; Wible et al., 2001).
Two extant genera of Monotremata were included as
outgroup taxa: Ornithorhynchus anatinus (CG
749
ZMO-1962-2146, 1963-2145, 1985-1795, CG AC-7128,
1933-222) and Tachyglossus aculeatus (CG ZMO1962-2144, 1985-1796, CG AC-12452).
The ingroup was composed of extinct metatherians,
in which the auditory area is known. Deltatheridium
pretrituberculare (PSS-MAE 132; Rougier et al., 1998)
is from the Late Cretaceous of Ukhaa Tolgod, Gobi
Desert, Mongolia (Dashzeveg et al., 2005); Pediomys
‘Petrosal A’ (FMNH PM53907; Wible, 1990) is from
the early Palaeocene of the Bug Creek Anthills,
Montana (Lofgren, 1995; Kielan-Jaworowska, Cifelli
& Luo, 2004); Didelphodon vorax (UCMP 53896;
Clemens, 1966) is from the Late Cretaceous of Lance
Formation, Wyoming; Mayulestes ferox, Andinodelphys cochabambensis, and Pucadelphys andinus (all
three mentioned above) are from the Early Palaeocene of Tiupampa, Bolivia; and the petrosals Types I
and II (Ladevèze, 2004) plus Types III, IV, and V
(Ladevèze, 2007b) are from the middle Palaeocene of
Itaboraí, Brazil. The extant marsupials that were
included in the analysis were Didelphis, Marmosa,
Metachirus, Caenolestes, Dromiciops, Phascogale,
Dasycercus, Perameles, and Echymipera (see Supporting Information Appendix S2).
The taxon/character states matrix (Appendix 2) was
analysed using heuristic parsimony searches implemented by PAUP* (Swofford, 2002). Polymorphic taxa
were coded with multiple character state entries. Ten
characters were considered as additive (see Appendix 1). Each heuristic parsimony search employed 100
replicates of random taxon addition with treebisection reconnection (TBR) branch swapping. This
matrix being complicated (i.e. lots of taxa, characters,
and unavailable data) and to avoid lengthy search
times on particular ‘islands’ of trees (Maddison, 1991),
we first extensively sampled the tree space using
1000 random sequence additions and keeping
ten trees per search (hsearch addseq = random
nchuck = 10 chuckscore = 1 nreps = 1000), and in the
next step we ran a search on the saved trees to find
all the shortest trees (hsearch start = current
nchuck = 0 chuckscore = 0). Moreover, we enforced a
topological constraint so that Metatheria was monophyletic.
The decay Bremer index (Bremer, 1988) for each
resolved node in the strict consensus of the equally
parsimonious trees was calculated with TreeRot v.3
(Sorenson & Franzosa, 2007) and PAUP* [command:
hsearch enforce converse constraints = node (number
of the node to converse) addseq = random timelimit = 30 limitperrep = yes nreps = 20].
Morphometric method
A morphometric analysis was conducted to try and
refer petrosals to taxa based on dental material. This
method, used by Ladevèze (2007b), compares the sizes
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
750
S. LADEVÈZE and C. DE MUIZON
of the isolated petrosals to tooth-based taxa. A preliminary analysis pointed out that M2-3 and m2-3 were the
least variable teeth, and were isometric amongst
extant metatherians. Moreover, the taxa from Itaboraí
are mostly represented by those teeth. Therefore, those
molar areas (M2-3 and m2-3) and promontorium areas
were calculated for Palaeocene metatherian mammals
from South America for which both dental and petrosal
remains are known: Pucadelphys andinus and
Andinodelphys cochabambensis. Additionally, measurements were taken from extant metatherians
(Didelphidae, Caenolestidae, and Dasyuridae).
Deltatheridium pretrituberculare was deleted from the
database because the petrosal specimen is that of a
juvenile individual and, therefore, cannot be associated with the adult teeth measurements.
Measurements were taken with a low-power stereo
microscope WILD TYP 308700 combined with a measurement machine WILD MMS 235 and are presented in Table 2. Most of the dental specimens from
Itaboraí were examined in Brazilian institutions
(DGM, MNRJ), as well as from casts of Itaboraí
metatherians from the MNHN collections.
The results of this morphometric analysis, detailed
further, revealed a correlation relationship (and equation) between the molar and promontorium areas that
allowed an estimation of the expected molar areas for
the taxa known exclusively by their petrosals.
DESCRIPTION OF THE TYPE VI PETROSAL
The paired petrosal bones contain the organs of
hearing and equilibrium. They provide attachment
for the muscles and ligaments of the middle-ear
ossicles, and contain grooves, canals, and foramina for
cranial blood vessels and nerves. For descriptive purposes, the petrosal is generally divided into two parts:
the pars cochlearis, enclosing the cochlear duct and
saccule of the inner ear, and the pars canalicularis,
housing the utricle and semicircular canals (e.g. Voit,
1909).
VENTRAL
SIDE
(FIG. 1A)
The two divisions of the petrosal are more easily
observable in ventral view: the pars cochlearis is
represented by the teardrop-shaped and inflated
promontorium and the flange projecting anteromedially from it; and the pars canalicularis by the portion
that is lateral and posterior to the promontorium. The
bulbous shape of the promontorium closely reflects
the enclosed cochlear duct, which coils in a ventrally
directed spiral. The cochlear canal is conspicuous in
the Type VII and VIII petrosals. Two openings lie in
the outer contour of the promontorium: posterolaterally, the fenestra vestibuli, which was in life closed by
the footplate of the stapes, and posteriorly, the
kidney-shaped fenestra cochleae, which was in life
closed by the secondary tympanic membrane. The
stapedial ratio of Segall (1970) (length/width of oval
window or footplate) is 1.525; this is somewhat elliptical, as in Type VIII (1.56 for MNRJ 6735-V and
1.407 for MNRJ 6740-V) and Type VII (1.5 for MNRJ
6737-V), although in the latter some individual variation is observed (1.235 for MNRJ 6738-V and 1.158
for MNRJ 6739-V).
The promontorium of Type VI exhibits a rostral
tympanic process that forms an anteriorly expanded
crest. The rostral tympanic process is anteromedial to
the fenestra cochleae. On the anterolateral apex of the
promontorium is a pronounced fossa that was likely to
provide attachment for the tensor tympani muscle,
which was inserted into the manubrium of the
malleus. Projecting anteromedially from the promontorium is a flat shelf of bone, the epitympanic wing
(sensu MacPhee, 1981) that contacts the basioccipital
in extant metatherians (Wible, 1990). Lateral to the
epitympanic wing and medial to the tensor tympani
fossa, Type VI presents a deep depression, which
indicates the path of the internal carotid artery
towards the entocarotid foramen. A similar condition is
observed in Types I, II, and III, whereas it is only
incipient in Types VII and VIII, and absent in Types IV
and V. This feature was observed by de Muizon et al.
(1997) in borhyaenids, and is also present in Pucadelphys, Andinodelphys, and Mayulestes from Tiupampa.
Type VI has an unidentified foramen on the posterior
end of the sulcus for the internal carotid artery.
Anterolateral to the fenestra vestibuli is a posteriorly directed aperture, the secondary facial
foramen, which transmitted the main, or hyomandibular, branch of the facial nerve into the middleear space (Wible, 1990; Wible & Hopson, 1993). A
deep sulcus for this branch of the facial nerve, the
sulcus facialis, lies posteriorly to the secondary
facial foramen and between the crista parotica and
the fenestra vestibuli.
The lateral aspect of the pars canalicularis is a
small shelf of bone that becomes narrower anteriorly
and can be interpreted as a vestigial lateral trough.
The lateral trough is a structure found in most nontherian mammals that reduces in size in therians and
floors the geniculate ganglion (Wible, 1990).
The area of the pars canalicularis posterolateral to
the promontorium and secondary facial foramen
shows a triangular depression, whose apex points
posteriorly. The deepest part of this depression is the
fossa incudis, which housed in life the crus breve of
the incus. The fossa incudis was probably bordered
posterolaterally by the squamosal, as in all extant
metatherians. Anterior to the fossa incudis is the
shallower and broader epitympanic recess, which was
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
751
Table 2. Measurements of second and third molars areas (in mm2) in a panel of extant and fossil metatherians
Species
Specimen
M2 area
m2 area
M3 area
m3 area
pr area
Didelphis aurita
CG
CG
CG
CG
32.60
31.25
31.37
31.42
20.01
18.51
20.04
20.94
33.70
32.99
34.22
34.22
23.14
20.23
23.03
23.73
45.99
42.00
53.25
54.51
Didelphis marsupialis
A9855 (right)
A9855 (left)
CG 1985-1805 (right)
CG 1985-1805 (left)
27.46
25.90
30.20
28.84
20.24
18.93
18.94
18.80
36.52
35.42
33.20
32.40
19.15
20.08
21.51
23.01
48.98
45.88
36.40
42.84
Didelphis albiventris
CG
CG
RH
RH
CG
CG
CG
CG
24.73
23.90
23.37
21.67
23.12
22.64
25.29
25.77
16.72
16.96
16.96
–
14.51
13.83
16.99
17.13
25.96
26.62
–
–
26.81
26.37
30.36
31.36
17.41
18.16
19.11
–
15.68
16.12
19.80
20.60
37.96
34.30
31.87
31.19
44.77
43.28
37.02
36.03
Marmosa murina
RH 82 (right)
RH 82 (left)
A3283 (right)
A3283 (left)
A3310 (right)
A3310 (left)
CG 2001-2239 (right)
CG 2001-2239 (left)
6.17
6.18
4.18
3.80
4.46
4.36
–
3.34
3.73
3.61
2.67
2.72
2.98
2.67
2.26
2.20
7.18
7.16
4.66
4.04
4.89
4.90
–
3.74
3.70
3.74
2.82
2.76
2.69
2.58
2.23
2.31
13.35
14.61
9.55
11.46
11.73
12.48
11.82
11.38
Metachirus nudicaudatus
RH
RH
CG
CG
CG
CG
16 (right)
16 (left)
ZMO 2175 (right)
ZMO 2175 (left)
1988-68 (right)
1988-68 (left)
15.18
14.85
9.48
9.09
11.02
10.53
9.55
9.85
5.99
5.88
7.03
6.93
19.56
19.19
11.84
11.29
13.69
12.34
11.31
11.12
6.63
6.23
7.26
7.32
21.20
25.40
26.88
26.97
22.79
21.96
Philander opossum
CG
CG
CG
CG
CG
CG
CG
CG
CG
CG
2001-1410
2001-1410
2001-1542
2001-1542
2001-1543
2001-1543
2001-1544
2001-1544
2001-1545
2001-1545
(right)
(left)
(right)
(left)
(right)
(left)
(right)
(left)
(right)
(left)
13.10
12.63
12.78
12.91
13.83
12.57
13.01
12.06
15.23
15.13
8.30
8.17
7.41
8.56
7.69
7.69
7.83
8.26
9.69
10.03
15.68
14.43
16.16
16.04
14.67
13.91
15.09
14.81
17.66
16.72
9.04
9.61
9.28
9.31
8.81
8.56
8.65
8.62
11.35
10.32
19.38
–
28.17
32.59
24.53
25.73
27.73
27.99
26.77
23.36
Caluromys philander
RH
RH
CG
CG
CG
CG
CG
CG
CG
CG
CG
CG
17 F (right)
17 F (left)
1880-1780 (right)
1880-1780 (left)
1986-140 (right)
1986-140 (left)
1986-142 (right)
1986-142 (left)
1986-143 (right)
1986-143 (left)
1986-144 (right)
1986-144 (left)
7.66
7.28
7.10
6.76
6.92
–
7.03
7.19
7.90
7.77
8.21
7.42
5.15
5.18
4.68
4.84
4.23
3.83
5.49
5.32
5.69
5.48
5.59
5.18
6.71
6.47
6.75
6.14
6.05
5.98
–
6.53
7.02
6.78
7.65
7.18
4.37
4.06
4.03
3.79
3.99
3.89
4.61
4.74
5.01
4.74
4.70
4.24
–
–
18.20
15.81
25.65
23.40
20.22
19.02
20.84
24.61
18.53
–
1984-058 (right)
1984-058 (left)
1949-70 (right)
1949-70 (left)
2000-217 (right)
2000-217 (left)
120 (right)
120 (left)
ZMO 1920-250 (right)
ZMO 1920-250 (left)
ZMO 1955-593 (right)
ZMO 1955-593 (left)
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
752
S. LADEVÈZE and C. DE MUIZON
Table 2. Continued
Species
Specimen
Caenolestes fuliginosus
RH
RH
CG
CG
CG
CG
CG
CG
Phascogale tapoatafa
M2 area
85 (right)
85 (left)
1981-607 (right)
1981-607 (left)
ZMO 1982-941
ZMO 1982-941
ZMO 1967-1338
ZMO 1967-1338
m2 area
M3 area
m3 area
pr area
3.57
3.46
3.74
3.72
3.38
3.28
3.37
3.39
2.57
2.47
2.77
2.55
2.49
2.43
2.12
2.19
2.77
2.76
3.06
3.06
2.62
2.76
2.46
2.45
2.14
2.22
2.32
2.31
2.18
1.99
1.77
1.78
11.74
11.68
7.67
–
10.44
10.52
9.30
8.91
CG 1897-1492 (right)
CG 1897-1492 (left)
4.00
4.19
2.51
2.27
4.54
4.47
2.52
2.47
14.03
13.22
Pucadelphys andinus
MHNC 8266 (right)
MHNC 8266 (left)
MHNC 8364 (left)
3.40
3.42
–
1.89
2.44
–
4.00
3.43
–
2.08
2.64
–
9.42
8.73
6.69
Andinodelphys cochabambensis
MHNC
MHNC
MHNC
MHNC
MHNC
MHNC
MHNC
MHNC
(right)
(left)
(right)
(left)
(right)
(left)
(right)
(left)
7.50
9.39
8.53
9.58
9.75
8.32
7.28
7.93
5.26
4.65
5.43
5.03
–
–
–
4.57
10.20
10.82
9.16
10.36
11.01
9.11
8.47
9.41
5.51
5.07
5.79
5.42
–
–
–
6.10
15.07
15.11
14.90
15.37
–
–
–
13.72
Mayulestes ferox
MHNC 1249 (right)
MHNC 1249 (left)
11.15
10.68
4.93
5.95
11.88
11.61
7.13
–
20.67
19.52
8264
8264
8308
8308
8372
8372
8370
8370
pr, promontorium; M2–3, second and third upper molars; m2–3, second and third lower molars.
in life dorsal to the tympanic membrane and housed
the mallear–incudal articulation (Van der Klaauw,
1931). The epitympanic recess is bounded laterally by
a prominent and triangular wall, which we define
here as the lateral wall of the epitympanic recess that
holds the tuberculum tympani (which might be the
homologue of the tegmen tympani of placentals; Kuhn
& Zeller, 1987), and anteromedially by a salient crest,
the ‘petrosal crest’ (sensu Archer, 1976; de Muizon,
1999). To avoid any confusion with the Latin term
‘crista petrosa’ that describes an endocranial structure, we suggest calling this structure the ‘tympanic
crest’. The tympanic crest makes a separation
amongst the anterior border of the epitympanic
recess, the posterior border of the ‘lateral trough’, and
the lateral border of the secondary facial foramen and
facial sulcus. A tympanic crest is found in most petrosals from Itaboraí (except in Types III, VII, and
VIII), Mayulestes and most borhyaenoids (except Prothylacinus and Borhyaena), Pucadelphys, Andinodelphys, and extant didelphids.
Forming the medial wall of the fossa incudis is
the crista parotica, which supports a tiny protuberance, the tympanohyal (the ossified proximal
segment of Reichert’s cartilage). The crista parotica
extends to a U-shaped indentation, the stylomastoid
notch by which the facial nerve leaves the middleear. The stylomastoid notch is bounded laterally by
the tympanohyal, and medially by a large lamina,
the caudal tympanic process of the petrosal (sensu
MacPhee, 1981). The caudal tympanic process of the
petrosal extends medially from the stylomastoid
notch to the jugular foramen (posterior lacerate
foramen of Archer (1976), showing a slight decrease
in height. It lies laterally to the exoccipital, whose
sutural surface is visible on the medial face of the
pars canalicularis.
Between the caudal tympanic process and the
rear of the promontorium is a deep depression,
hidden in ventral view. The narrower medial part of
this depression is the postpromontorial tympanic
sinus (sensu Wible, 1990), partially covered by the
expansion of the caudal tympanic process; its
broader, slightly deeper, lateral part is the fossa for
the stapedius muscle.
On the posterolateral aspect of the pars canalicularis, a thin groove indicates the suture between the
petrosal and the squamosal. Medial to it, a large
surface faces the posterior side of the skull, the
mastoid exposure, which is located amongst the
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
753
Figure 1. Right petrosal of MNRJ 6734-V (Type VI) in ventral (A), dorsal (B), and lateral (C) views. Abbreviations: al,
anterior lamina; av, aqueductus vestibuli; cc, crus commune; cp, crista parotica; cr, crista petrosa; ctpp, caudal tympanic
process of petrosal; er, epitympanic recess; fai, foramen acousticum inferius; fas, foramen acousticum superius; fc, fenestra
cochleae; fi, fossa incudis; fn, facial nerve; fs, facial sulcus; fsa, fossa subarcuata; fss, foramen for the sigmoid sinus; fv,
fenestra vestibuli; gg, location of the subjacent geniculate ganglion; gpn, greater petrosal nerve; hF, hiatus Fallopii; iam,
internal auditory meatus; ica, internal carotid artery; ips, inferior petrosal sinus; lapc, lateral aperture of the prootic
canal; lhv, lateral head vein; lw, lateral wall of epitympanic recess (tuberculum tympani); me, mastoid exposure; mp,
mastoid tympanic process; pcv, prootic canal vein; pfc, prefacial commissure; pr, promontorium; ps, prootic sinus; psc,
posterior semicircular canal; psv?, probable prootic sinus vein; rtpp, rostral tympanic process of petrosal; sff, secondary
facial foramen; sica, sulcus for the internal carotid artery; sips, sulcus for the inferior petrosal sinus; smn, stylomastoid
notch; spev, sphenoparietal emissary vein; sps, sulcus for the prootic sinus; spsv?, sulcus for a probable vein connected
to the prootic sinus; ss, sigmoid sinus; sss, sulcus for the sigmoid sinus; th, tympanohyal; tt, tuberculum tympani; ttf,
tensor tympani fossa; ts, transverse sinus; tyc, tympanic crest; vf, vascular foramen; uf, unknown foramen; us, unknown
sulcus; V3?, probable medial border of the foramen ovale for the V3 nerve.
squamosal, supraoccipital, and
marsupials (Wible, 1990). The
petrosal (on the tympanic side
laris) develops a small slanted
exoccipital in extant
mastoid part of the
of the pars canalicuprocess, the mastoid
process (sensu Archer, 1976; Wible, 1990) that
projects ventrally from the posteromedial border of
the stylomastoid notch and extends posteriorly on the
mastoid.
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
754
S. LADEVÈZE and C. DE MUIZON
DORSAL
SIDE
(FIG. 1B)
The dorsal view is dominated by two large openings,
the fossa subarcuata posterodorsally and the internal acoustic meatus anteromedially. Posterodorsally,
the very large and deep fossa subarcuata accommodates the paraflocculus of the cerebellum and is
bounded by the three semicircular canals. The posterior semicircular canal forms the posterolateral
rim of the fossa subarcuata, and the crus commune
(conjunction of the anterior and posterior semicircular canals) forms its posteromedial rim. The fossa
subarcuata is anteriorly delimited by the crista
petrosa that forms a thin edge in Type VI. It
resembles the sharp crista petrosa of Types II, III,
IV, and V (Ladevèze, 2004, 2007b), whereas it differs
from the thick condition of the crista observed on
Type I (Ladevèze, 2004). The crista petrosa borders
posteromedially a large anterolaterally directed
bony wing, which we regard as a relict of the anterior lamina of nontherian mammals. Part of this
structure also includes the lateral flange. This interpretation follows Marshall & de Muizon (1995) and
Ladevèze & de Muizon (2007) who observed a relictual anterior lamina in Pucadelphys and Andinodelphys (for discussion, see below).
Posteromedial to the fossa subarcuata, behind the
crus commune and posterior semicircular canal, is the
narrow groove for the sigmoid sinus that extends
medially up to the aqueductus vestibuli. This sinus is
a branch of the transverse sinus (see below).
Anteromedial to the fossa subarcuata, the internal
acoustic meatus forms a large and deep depression
for the facial and vestibulocochlear nerves. The
internal acoustic meatus is subequal in size to the
fossa subarcuata and exhibits a broad transverse
septum. The lateral wall of the meatus is formed by
a thin but deep bar of bone, the prefacial commissure. The floor of the internal acoustic meatus has a
rough depression, the medial and lateral extremities
of which are larger than the centre. The larger and
medial aperture, the foramen acusticum inferius,
shows some tiny perforations that are interpreted as
evidence of the spiral cribriform tract or tractus spiralis foraminosus, which transmitted the fascicles of
the cochlear nerve, as in other therians (Meng &
Fox, 1995a, b). In the posterior part of the foramen
acusticum inferius is a large and shallow pit that
may be interpreted as the foramen singulare for the
passage of vestibular nerve bundles. The smaller
lateral aperture, the foramen acusticum superius,
hidden in dorsal view, has a small anterior opening
for the passage of the facial nerve and a posterior
pit, which is interpreted as the cribriform dorsal
vestibular area for the passage of the remaining
bundles of the vestibular nerve.
The aqueductus vestibuli for passage of the
endolymphatic duct is posteromedial to the fossa subarcuata and near the crus commune. The aqueductus
cochleae for passage of the perilymphatic duct is
posteromedial to the internal acoustic meatus but
hidden by a bony bar behind the foramen acusticum
inferius. The aqueductus cochleae opens into the
jugular foramen, which transmits cranial nerves (presumably the glossopharyngeal, vagus, and accessory
nerves as in didelphids; Wible, 2003) and occasionally
also a very small branch of the sigmoid sinus to the
internal jugular vein (Archer, 1976). In some metatherians (e.g. Monodelphis, Didelphis, Dasyurus,
Wible, 2003; Pucadelphys, Marshall & de Muizon,
1995), the jugular foramen has a separate foramen for
the inferior petrosal sinus anterior to it.
LATERAL
SIDE
(FIG. 1C)
The pars canalicularis is posterior to and includes the
sulcus for the prootic sinus and the lateral wall of the
epitympanic recess; the pars cochlearis is anterior
and ventral to these structures.
The groove for the prootic sinus is large but short,
and is visible on that side. It starts in the posterolateral angle of the ventral pars canalicularis, anterior
to the fossa subarcuata, and borders posterolaterally
the anterior lamina of the petrosal, before joining the
lateral aperture of the prootic canal.
The position of the hiatus Fallopii is better seen on
this side. The aperture for the greater petrosal nerve
is delimited ventrally and posteriorly by shelves of
bone arising from the lateral trough and crista
petrosa, respectively. The floor and roof of the cavum
supracochleare are of interest to delimitate the position of the hiatus Fallopii (Sánchez-Villagra & Wible,
2002). The cavum supracochleare is the space within
the petrosal that accommodates the geniculate ganglion of the facial nerve (Gaupp, 1908). As the floor of
the cavum supracochleare does not extend further
anteriorly than the roof, the hiatus Fallopii is considered as having a dorsal position.
ARTERIES
AND VEINS
The reconstitution of the cranial vascular and
nervous systems in fossil remains depends on the
preservation of the blood vessel impressions on
the bone (grooves, canals, foramina). The petrosals
studied here are well preserved (even if Types VII and
VIII are incomplete), and allow a reconstruction of the
blood vessels, mostly inferred from didelphid anatomy
(see Wible, 1990: 191, fig. 4; Wible & Hopson, 1995:
342, fig. 5; Wible, 2003: 163, fig. 8).
Transverse sinus distributaries
The major veins of the metatherian petrosal are distributaries of the transverse sinus. The transverse
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
sinus runs in the outer edge of the tentorium cerebelli
and divides into two branches. The anteroventral
branch exits from the skull via the postglenoid canal
(prootic sinus and sphenoparietal emissary vein), and
the posterodorsal branch via the foramen magnum
(Dom, Fisher & Martin, 1970).
The prootic sinus runs ventrally in a canal between
the squamosal and petrosal and leaves the skull as
the postglenoid vein via the postglenoid foramen in
the squamosal. According to Gelderen (1924), Wible
(1990), and Wible & Hopson (1995), the postglenoid
vein is composed of two elements: the ontogenetically
older prootic sinus and the sphenoparietal emissary
vein, the former giving rise to the latter at the lateral
aperture of the prootic canal. The prootic canal connects the groove for the prootic sinus on the lateral
surface with the sulcus facialis on the ventral surface.
The lateral aperture of the prootic canal is visible in
the ventral and lateral views of the described petrosals from Itaboraí, on the anteriormost part of the
sulcus for the prootic sinus, between the pars canalicularis and the squamosal. The tympanic opening of
the prootic canal is anterodorsal to the petrosal crest
and lateral to the secondary facial foramen. The
prootic canal of metatherians leads a vein from the
prootic sinus to the rudimentary lateral head vein,
which runs posteriorly to the geniculate ganglion of
the facial nerve and to the otic capsule and passes
through a groove lateral to the sulcus facialis. It
meets the inferior petrosal sinus at the jugular
foramen, where they both exit.
In extant adult marsupials, the development of the
sphenoparietal emissary vein causes a reduction of
the tympanic portion of the lateral head vein (Wible,
1990). The lateral head vein and the prootic canal are
retained in adult monotremes (Wible & Hopson,
1995), the eutherian Prokennalestes (Wible et al.,
2001), the metatherians Deltatheridium, Didelphodon, Pediomys (Rougier et al., 1998; Wible et al.,
2001), Pucadelphys, and Andinodelphys (Marshall &
de Muizon, 1995; Ladevèze & de Muizon, 2007), some
extant marsupials (didelphids, caenolestids, and some
dasyurids; Wible, 1990), and the petrosals from Itaboraí studied here (however, the occurrence of a complete canal for a prootic canal vein could not be
determined in the Type IV petrosal).
Type VI exhibits a groove just adjacent to the
prootic sinus, which probably contained a vein from
the prootic sinus, and enters the petrosal to join the
sigmoid sinus, via an intrapetrosal canal. This sulcus
is thus thought to be for the sigmoid sinus or for a
sigmoid sinus vein, as it can be observed in some
extant marsupials (i.e. Monodelphis, Wible, 2003;
Phascogale, S.L. pers. observ.). Such a groove was
observed on some petrosals of Pucadelphys andinus
(Marshall & de Muizon, 1995; Ladevèze & de Muizon,
755
2007) and the Type I and III petrosals (Ladevèze,
2004, 2007b).
The sigmoid sinus occupies a narrow sulcus, posteromedial to the fossa subarcuata, which ends near
the aqueductus vestibuli, and thus suggests that the
sigmoid sinus exits via the foramen magnum, as in
monotremes (Hochstetter, 1896; Wible, 1990), Prokennalestes (Wible et al., 2001), and all adult marsupials
(Dom et al., 1970; Archer, 1976; Wible, 1990; Wible
et al., 2001). In the petrosals studied here, the bifurcation of the transverse sinus is not visible on the
petrosal.
Inferior petrosal sinus and internal jugular vein
In Type VI, the inferior petrosal sinus runs in a large,
long, and deep groove on the anteromedial region of
the petrosal when seen in dorsal view. In recent
mammals, this sinus drains the blood from the cavernous sinus to the internal jugular vein, along the
petrosal–basioccipital suture (Rougier, Wible &
Hopson, 1996). The internal jugular vein exits from
the skull through either its own foramen, or the
jugular foramen (see Wible, 2003).
NERVES
Facial nerve and greater petrosal nerve
The general metatherian pattern, which can be
inferred to petrosal Type VI, is the following. The
facial nerve leaves the cranial cavity via the internal
acoustic meatus, runs beneath the prefacial commissure, and enters into the cavum supracochleare by the
primary facial foramen (Wible, 1990; Wible & Hopson,
1993). The cavum supracochleare, which encloses the
geniculate ganglion of the facial nerve (Gaupp, 1908),
is ventrally closed by an osseous floor, the ‘lateral
trough’.
The main branch or hyomandibular ramus of the
facial nerve leaves the posterior aspect of the geniculate ganglion and enters the middle-ear space via the
secondary facial foramen. This posteroventral branch
of the facial nerve runs in the sulcus facialis and exits
the skull by the stylomastoid notch.
The greater petrosal nerve or palatine ramus of the
facial nerve leaves the anterior part of the geniculate
ganglion and is transmitted from the hiatus Fallopii
to the posterior opening of the pterygoid canal. The
hiatus Fallopii is the anterolateral opening situated
just at the anterior tip of termination of the anterior
lamina of the petrosal Type VI. This opening has a
dorsal position, as defined by Sánchez-Villagra &
Wible (2002). A tiny sulcus originates from the sulcus
for the greater petrosal nerve, just medial to the
notch located on the lateral edge of the hiatus Fallopii. This sulcus apparently passes within the notch
to emerge on the ventral side. Such a sulcus was
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
756
S. LADEVÈZE and C. DE MUIZON
observed on the Type III specimen MNRJ 6731-V and
the Type V specimen MNRJ 6733-V. Moreover, a
small foramen anterolateral to the hiatus Fallopii
was observed on the Type VI petrosal, and may be the
origin of this sulcus. On the ventral side, this tiny
sulcus reaches a small foramen, located just anterior
to the secondary facial foramen, and from which
another tiny sulcus emerges and runs anteriorly and
lateral to the promontorium. These foramina and
sulci are probably related to the facial nerve
branches, but as this conformation has previously
never been observed in any metatherian or other
mammal, its interpretation as a secondary branching
of the greater petrosal nerve is uncertain.
Trigeminal nerve (mandibular branch)
The cavum epiptericum is the space anterolateral to
the petrosal, at the level of the sphenoparietal fenestra in the chondrocranium (Wible, 1990: 189, fig. 3),
and it houses the trigeminal ganglion and other
nerves and vascular structures (Gaupp, 1902, 1905;
Kuhn & Zeller, 1987). A fossa that probably housed a
part of the trigeminal ganglion is visible on the small
anterior lamina. This feature indicates that the
cavum epiptericum was probably floored by the petrosal and alisphenoid as it occurs in some metatherians (Wible et al., 2001).
The presence of a prominent notch on the anterolateral part of the ‘lateral trough’ probably denotes
the passage of the mandibular branch of the trigeminal nerve (V3), and is likely to indicate that the
foramen ovale was bounded by the petrosal and
alisphenoid.
DESCRIPTION OF THE TYPE VII
PETROSALS
The petrosals assigned to Type VII differ from that
belonging to Type VI in size (23% smaller), and in
some features described below. All three petrosals
have a broken pars canalicularis; nonetheless, the
pars canalicularis is less damaged in MNRJ 6737-V
and most of its features can be observed.
VENTRAL
SIDE
(FIG. 2A)
A deep sulcus for the internal carotid artery was
identified at the anteromedial apex of the promontorium and differs from that observed in Type VI in that
it is not bordered by sharp shelves of bone. Lateral to
this sulcus is a very tiny fossa, which is likely to
accommodate the tensor tympani muscle.
The vestigial ‘lateral trough’ is more markedly
developed than in Type VI and includes a deep
depression, anterolateral to the secondary facial
foramen and facial sulcus, and anteromedial to a
sharp, anterolaterally directed crest that borders the
epitympanic recess.
The lateral wall of the epitympanic recess is
broken, and there is no evidence of a tympanic crest.
On the crista parotica is a prominent and rounded
tympanohyal, and medially to it, a large caudal tympanic process that shows the same development as in
Type VI, except that it does not decrease medially.
Moreover, the caudal tympanic process of petrosal is
ventrally bent.
The anteriormost aspect of the mastoid tympanic
process is preserved and similar to that observed in
Type VI, suggesting the presence of a small, anteriorly slanted mastoid process.
DORSAL
SIDE
(FIG. 2B)
The internal acoustic meatus exhibits an enormous
and bulged transverse septum and is walled laterally
by a very thin, sharp, and elevated prefacial commissure. The internal acoustic meatus is separated from
the fossa subarcuata by a sharp and blade-like edge.
The fossa subarcuata is highly damaged and probably formed a large and deep depression.
A large and bulbous ovoid structure bulges on both
sides of the crista petrosa and is visible on the anterolateral edge of the fossa subarcuata and on the
posteromedial side of the anterior lamina. This structure is interpreted as containing the anterior
ampulla, adjoined dorsomedially by the lateral
ampulla.
The anterior lamina is reduced in width compared
to that observed in Type VI, and exhibits a small
depression for the temporal part of the brain and
posteriormost part of the trigeminal ganglion.
The sulcus for the inferior petrosal sinus is narrow
and shallow.
DESCRIPTION OF THE TYPE VIII
PETROSALS
COMPARISON
WITH THE OTHER MORPHOTYPES
The overall shape of the petrosals assigned to Type
VIII is actually similar to that of the Type VII petrosals (Fig. 3), notably as regards the inflation of the
dorsal structure. The internal acoustic meatus exhibits a broad and bulbous transverse septum, with a
sharp prefacial commissure. The separation between
the internal acoustic meatus and the fossa subarcuata
is a sharp edge of bone. The fossa subarcuata is
broken, but seems large and deep.
The Type VIII differs from the Type VI and Type
VII petrosals in some important features. Dorsally,
the hiatus Fallopii has an intermediate position. Ven-
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
757
Figure 2. Right petrosal of MNRJ 6737-V (Type VII) in ventral (A) and dorsal (B) views. Abbreviations: aa, anterior
ampulla; ac, aqueductus cochleae; al, anterior lamina; cp, crista parotica; cr, crista petrosa; ctpp, caudal tympanic process
of petrosal; er, epitympanic recess; fai, foramen acousticum inferius; fas, foramen acousticum superius; fc, fenestra
cochleae; fi, fossa incudis; fn, facial nerve; fs, facial sulcus; fsa, fossa subarcuata; fv, fenestra vestibuli; gg, location of the
subjacent geniculate ganglion; gpn, greater petrosal nerve; hF, hiatus Fallopii; iam, internal auditory meatus; ica, internal
carotid artery; ips, inferior petrosal sinus; la, lateral ampulla; lapc, lateral aperture of the prootic canal; lhv, lateral head
vein; lw, lateral wall of epitympanic recess (tuberculum tympani); me, mastoid exposure; mp, mastoid tympanic process;
pcv, prootic canal vein; pfc, prefacial commissure; pr, promontorium; ps, prootic sinus; rtpp, rostral tympanic process of
petrosal; sff, secondary facial foramen; sica, sulcus for the internal carotid artery; sips, sulcus for the inferior petrosal
sinus; smn, stylomastoid notch; spev, sphenoparietal emissary vein; sps, sulcus for the prootic sinus; th, tympanohyal; vf,
vascular foramen; V3?, probable medial border of the foramen ovale for the V3 nerve.
trally, the promontorium does not develop any
process; neither does it exhibit depressions on its
anterior aspect for the tensor tympani muscle nor the
internal carotid artery. The pars canalicularis is
damaged in its main part; nevertheless, there is no
evidence of a tympanic crest (as in the Type VII
petrosals), the crista parotica is broken, and the preserved part of the caudal tympanic process may
suggest a large expansion of this process, as is the
case in the Type VII petrosals.
OSSEOUS
INNER EAR
Figure 3A2 shows the restoration of the osseous labyrinth that is a cavity within the petrosal, and which
in life contained the perilymph in which the membranous labyrinth was suspended. This restoration was
made possible because of damage to the specimen
MNRJ 6735-V, revealing its internal morphology.
The osseous labyrinth consists of three parts: the
cochlea, which contained the cochlear duct; the
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
758
S. LADEVÈZE and C. DE MUIZON
Figure 3. Right petrosal of MNRJ 6735-V (Type VIII) in ventral (A) and dorsal (B) views, with a reconstruction of the
inner ear (A2). Abbreviations: aa, anterior ampulla; al, anterior lamina; asc, anterior semicircular canal; av, aqueductus
vestibuli; cc, crus commune; cocd, cochlear duct; cp, crista parotica; cr, crista petrosa; ctpp, caudal tympanic process of
petrosal; er, epitympanic recess; fai, foramen acousticum inferius; fas, foramen acousticum superius; fc, fenestra cochleae;
fi, fossa incudis; fn, facial nerve; fs, facial sulcus; fsa, fossa subarcuata; fv, fenestra vestibuli; gg, location of the subjacent
geniculate ganglion; gpn, greater petrosal nerve; hF, hiatus Fallopii; iam, internal auditory meatus; ips, inferior petrosal
sinus; la, lateral ampulla; lapc, lateral aperture of the prootic canal; lhv, lateral head vein; lsc, lateral semicircular canal;
lw, lateral wall of epitympanic recess (tuberculum tympani); pa, posterior ampulla; pcv, prootic canal vein; pfc, prefacial
commissure; pr, promontorium; ps, prootic sinus; psc, posterior semicircular canal; sff, secondary facial foramen; sips,
sulcus for the inferior petrosal sinus; smn, stylomastoid notch; spev, sphenoparietal emissary vein; sps, sulcus for the
prootic sinus; tt, tuberculum tympani.
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
vestibule, which contained the utricle and saccule;
and the semicircular canals, which contained the
semicircular ducts.
The most prominent feature of the osseous labyrinth is the cochlea, which occupies most of the available space in the pars cochlearis. The connection
between the cochlea and vestibule is at the posteromedial aspect of the pars cochlearis. We were able to
estimate the number of cochlear turns as more than
two, which is fewer than in didelphids (near 2.5
Fernández & Schmidt, 1963; Sánchez-Villagra &
Schmelzle, 2007) but greatly more than other extinct
metatherians (1.6 for Herpetotherium, SánchezVillagra et al., 2007; 1.5 for the basal metatherians of
the Late Cretaceous of Montana reported by Meng &
Fox, 1995a).
Anteromedial to its origin, the cochlea is joined by
the short, narrow cochlear canaliculus, which transmitted the cochlear aqueduct of the perilymphatic
duct. Beyond the cochlear canaliculus, the cochlea
coils in a clockwise direction, spiralling ventrally and
ending anterior to the fenestra vestibuli.
The vestibule communicates with the cochlea anteriorly and the semicircular canals posteriorly. It consists of an irregular, oval central space and three
distal swellings, or ampullae, on the semicircular
canals, at their junction with the vestibule. The anterior and lateral ampullae lie dorsolateral and ventrolateral to the vestibule, respectively.
The posterior ampulla is ventromedial, and the crus
commune, formed by the union of the non-ampullated
ends of the anterior and posterior semicircular canals,
is dorsomedial. The lateral semicircular canal lies in
a nearly horizontal plane in the floor of the subarcuate fossa. The posterior semicircular canal is in a
nearly vertical plane in the medial wall of the subarcuata fossa; it joins the anterior canal in the crus
commune dorsally and the posterior canal ventrally.
The anterior ampulla is the only direct evidence for
the anterior semicircular canal, which in life formed
the rim for the orifice into the subarcuate fossa. The
vestibular aqueduct for the endolymphatic duct has
its endocranial aperture on the crus commune.
RESULTS AND DISCUSSION
PARSIMONY
ANALYSIS OF THE PHYLOGENETIC
RELATIONSHIPS OF THE
ITABORAÍAN METATHERIANS
METATHERIA
AND TYPE PETROSALS AMONGST
The analysis under PAUP* resulted in 9680 equiparsimonious trees of 563 steps [consistency index
(CI) = 0.343, retention index (RI) = 0.562], the strict
consensus and majority rule consensus trees of which
are given in Figure 4 [length (L) = 621, CI = 0.340,
RI = 0.514]. The relationships mostly agree with
759
current views of mammal phylogeny (Rougier et al.,
1998; Wible et al., 2001; Horovitz & Sánchez-Villagra,
2003; Luo et al., 2003; Ladevèze & de Muizon, 2007).
The metatherian dichotomy argued by Szalay (1982a)
is not recovered here as Australidelphia is monophyletic whereas ‘Ameridelphia’ is paraphyletic. The
present hypothesis of the evolutionary history of Metatheria shows the early divergence of ‘borhyaenoids’
(Patene and Mayulestes), followed by the Type VIII
petrosal, and a clade composed of the boreometatherians (represented by Didelphodon and Pediomys),
and the Itaboraían metatherians Bobbschaefferia and
Eobrasilia. Notometatheria (i.e. South American
and Australasian metatherians) thus appears polyphyletic here.
The clade including the Pucadelphydae and Type II
and the one composed of the Itaboraían metatherians
Guggenheimia and Mirandatherium form here the
stem groups to the clade Marsupialia (i.e. the common
ancestor of all extant marsupials plus all of its
descendants). The clade formed by the Didelphidae
(extant didelphids plus Itaboraidelphys and Marmosopsis) and Protodidelphidae (Didelphopsis, Procaroloameghinia, and Protodidelphis) is the sister
group of a large clade composed of what is recognized
here as the clade Australidelphia (i.e. Peramelia, Paucituberculata, Microbiotheria, Dasyuromorphia) and
a series of stem australidelphian taxa (Types I, III, IV,
VI, VII, Derorhynchus, Carolopaulacoutoia, and
Gaylordia).
The grade ‘Didelphimorphia’ is here identified and
contains the generalized metatherians with a
didelphid-like dentition, which form a paraphyletic
assemblage stem to the Australidelphia lineage (i.e.
pucadelphyds, protodidelphids, didelphids, Types I,
III, IV, VI, VII, Derorhynchus, Carolopaulacoutoia,
and Gaylordia).
Paucituberculata (Caenolestes, Epidolops, and Type
V) is here the sister group of Peramelia, instead of
Australidelphia (i.e. Australasian marsupials plus
Dromiciops) as highlighted by the most recent
molecular and morphological studies (SánchezVillagra, 2001a, b; Sánchez-Villagra & Wible, 2002;
Amrine-Madsen et al., 2003; Horovitz & SánchezVillagra, 2003; Asher et al., 2004; Cardillo et al., 2004;
Beck, 2008). The exclusion of Peramelia from the
Australasian radiation is in agreement with certain
phylogenetic views (Kirsch, Lapointe & Springer,
1997; Wroe, 1999; Wroe et al., 2000; Sánchez-Villagra,
2001b). As a consequence, Australidelphia is here
more inclusive as it includes the paucituberculate
Caenolestes. The clade composed of all Australasian
marsupials plus Dromiciops but with Peramelia
outside is recognized as the Eometatheria clade as
defined by Kirsch et al. (1997). The Itaboraían
metatherians Zeusdelphys, Minusculodelphis, and
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
760
S. LADEVÈZE and C. DE MUIZON
Figure 4. Strict consensus tree (A) [length (L) = 621, consistency index (CI) = 0.340, retention index (RI) = 0.514] and
majority rule consensus tree (B) of the 9680 parsimonious trees (L = 563, CI = 0.343, RI = 0.562) resulting from the first
analysis.
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
Monodelphopsis share close relationships with Dromiciops and dasyurids. The nesting of Dromiciops
within Australidelphia or Eometatheria is well supported by many biochemical, molecular, and morphological studies (Szalay, 1982a, b, 1994; Kirsch, Reig &
Springer, 1991; Luckett, 1994; Kirsch et al., 1997;
Springer et al., 1998; Phillips et al., 2001; AmrineMadsen et al., 2003; Horovitz & Sánchez-Villagra,
2003; Luo et al., 2003; Nilsson et al., 2003), although
some analyses did not recover this group (e.g. Palma
& Spotorno, 1999). The position of Dromiciops
amongst Australidelphia is still disputed: either sister
group to all Australasian marsupials (AmrineMadsen et al., 2003; Phillips et al., 2006; Beck,
2008);or nested within the Australasian radiation
(Asher et al., 2004; Cardillo et al., 2004; Nilsson et al.,
2004).The present phylogeny supports a close relationship of dasyurids and Dromiciops.
The main metatherian groups now being recovered,
we focus our discussion on the phylogenetic positions
of the Itaboraían types and dental-based metatherians. The complete list of character state distributions
amongst each node is given in Supporting Information Appendix S3.
Node A – Metatheria
The basicranial synapomorphies supporting the clade
Metatheria have already been discussed by Ladevèze
(2007b). The dental synapomorphies supporting this
clade are: the presence of four molars (601>0), a
marked posterior increase of the molars (620>2,
becomes moderate in node C, marked in node E,
absent in node S, and moderate in peramelians and
dasyurids), a first upper premolar with diastema
(690>1, no diastema in Eometatheria) and procumbent
(700>1, not procumbent in node S), a strongly developed postmetacrista with a large metastylar area on
upper molars (780>1), a moderately to well-developed
preparacrista (941>0, becomes short, rounded, and virtually absent in node D, short and blade-like in node
F, short, rounded, and virtually absent in nodes N and
T, well developed in dasyurids), the presence of a
staggered lower incisor (1090>1, absent in node S,
present in peramelians and node X),a metaconid at
the extreme lingual margin of the tooth (1360>1), and
bladed and sharp paracristids and protocristids
(1440>1, rounded in pucadelphyds, node N, extant
didelphids, and peramelians).
Node G – Type II included within the
Pucadelphydae
This relationship was pointed out in previous analyses (Ladevèze, 2004, 2007b) and is supported in the
present analysis by two unambiguous synapomorphies: the presence of a deep groove for the internal
carotid artery excavated on the anterior pole of prom-
761
ontorium (100>1) and the presence of a tympanic sinus
in the lateral trough of the petrosal (150>1).
Pucadelphys and Andinodelphys share four unambiguous synapomorphies, all derived from the ear
region. One synapomorphy is strict: the fenestra
cochleae is surrounded by a broad shelf of bone and
thus separated from the aqueductus cochleae (160>1).
The presence of an anterior lamina in Andinodelphys and Pucadelphys (62>1) has been questioned by
Wible et al. (2001) and Rougier & Wible (2006)
because it is not part of the sidewall of the braincase.
However, the anterior lamina of Pucadelphys and
Andinodelphys receives on its cerebral side at least
part of the trigeminal ganglion (and probably part of
the temporal lobe of the cerebrum) as in the nontherian mammaliaforms (see Kermack, Mussett &
Rigney, 1981; Wible, 1990; Hopson & Rougier, 1993;
Wible & Hopson, 1993). Furthermore, the anterior
lamina of the nontherian mammaliaforms is perforated by the foramen ovale. In Pucadelphys and Andinodelphys the foramen ovale is formed posteriorly by
the anterior lamina of the petrosal and anteriorly by
the alisphenoid. This condition is the consequence of
the reduction of the anterior lamina and posterior
extension of the alisphenoid in therians. Another consequence of this is the inclusion of the foramen rotundum (V2) in the therian alisphenoid. It is noteworthy
that in Morganucodon the foramen rotundum and
foramen ovale open in the anterior lamina; in Vincelestes the foramen rotundum opens between the
alisphenoid and the anterior lamina and the foramen
ovale opens totally in the anterior lamina, therefore
indicating a reduction of the anterior lamina. The
next stage is the condition of metatherians, where the
foramen rotundum opens in the alisphenoid and the
foramen ovale between the alisphenoid and the anterior lamina. The most derived condition is that of
eutherians, where the anterior lamina has totally
disappeared (except in Prokennalestes) and where
both the foramen rotundum and the foramen ovale
are completely enclosed in the alisphenoid. In nontherian mammaliaforms the foramen ovale opens laterally in the anterior lamina, which is distinctly
lateral. In Pucadelphys and Andinodelphys the
foramen ovale opens ventrally and the relictual anterior lamina is therefore partially ventral. Furthermore, because of the posterior extension of the
alisphenoid in metatherians (relative to the nontherian mammaliaforms), a contact is established laterally between this bone and the squamosal. The
reduced anterior lamina of early metatherians is
therefore excluded from the lateral wall of the braincase, but still contributes to the internal wall of the
braincase.
The anterior lamina is a structure of the lateral
wall of the braincase that is present in nontherian
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
762
S. LADEVÈZE and C. DE MUIZON
mammaliaforms and disappears in most therians
(Wible, 1990; Rougier et al., 1992; Hopson & Rougier,
1993; Wible & Hopson, 1993). However, Wible et al.
(2001: 9) described an isolated petrosal (referred to
Prokennalestes), in which they identified a small anterior lamina (partly broken) on the basis of the single
piece of evidence that they ‘believe it was exposed on
the sidewall of the braincase’. Whether or not this
structure was external on the braincase, we agree
that it represents a relictual anterior lamina. Therefore, the condition of Prokennalestes and that of early
South American metatherians demonstrate that an
anterior lamina was still present at early stages of
therian evolution.
Three dental synapomorphies are considered as
unambiguous as the alternative optimization shows
an appearance in node G although Type II is not
known from teeth. Pucadelphyds are thus defined by:
a tall and sharply recurved hypoconulid on the last
molar (1250>1), paracristids and protocristids subequal
in length (1431>0, convergent with node M, node T)
and rounded (1441>0, convergent with Protodidelphis
and Procaroloameghinia, extant didelphids, and
peramelians).
Node I – Guggenheimia and Mirandatherium sister
group of Marsupialia
The sister-group relationship of the clade
Guggenheimia + Mirandatherium and Marsupialia is
supported by two unambiguous synapomorphies: the
stylar cusp E on the upper molars is absent or poorly
developed (861>0, absent or poorly developed in extant
didelphids and peramelians), and the last lower molar
is smaller than the penultimate molar or lost (1450>1,
subequal in size in node O, peramelians, and
dasyurids).
Marshall (1987) first considered Mirandatherium to
be a Microbiotheriidae [then followed by Kirsch et al.
(1997) and McKenna & Bell (1997)] but he later
removed it to Didelphinae (Marshall, Case & Woodburne, 1990). Guggenheimia was thought to be a
protodidelphid polydolopimorphian, together with
Bobschaefferia, Zeusdelphys, and Protodidelphis
(Marshall et al., 1990; Kirsch et al., 1997; McKenna &
Bell, 1997) or a protodidelphid didelphimorphian
together with Protodidelphis and Carolocoutoia
(Goin, Oliveira & Candela, 1998). Here we suggest a
sister-group relationship of the clade Mirandatherium
plus Guggenheimia to Marsupialia.
Node K – Marsupialia
The clade Marsupialia is here supported by two unambiguous synapomorphies: the first lower premolar is
orientated in line with the jaw axis (1140>1), and the
anterior cingulid on the lower molars forms a welldeveloped sulcus (1350>1, absent in Eometatheria).
Various characters from the ear region can be considered as unambiguous synapomorphies for Marsupialia, as the alternative optimization suggests an
appearance at the node I although Guggenheimia and
Mirandatherium are only known by teeth (Supporting
Information Appendix S3). These basicranial characters defining the clade Marsupialia have already been
discussed by Ladevèze (2007b).
Node L – Protodidelphidae and Didelphidae
The grouping of the Didelphidae (i.e. extant opossums
plus Marmosopsis and Itaboraidelphys) and Protodidelphidae (Didelphopsis, Procaroloameghinia, Protodidelphis) is supported by two unambiguous
synapomorphies: the M2 is shorter than the M3
(750>1), and the M1–3 have a precingulum (1060>1,
absent in didelphids).
The closest relatives to extant opossums are Itaboraidelphys and Marmosopsis; they share with them a
p2 and p3 subequal in size (1150>1, but p2 becomes
larger than p3 in didelphids; convergent with node X),
a large and labially salient hypoconid (1302>1, convergent with node T, Eometatheria, large but not salient
labially in dasyurids), and a last lower molar subequal in size to the penultimate molar (1451>0, convergent with peramelians and dasyurids).
The grouping of Didelphopsis, Procaroloameghinia,
and Protodidelphis is supported by the presence of
low and robust molars (610>2), anteroposteriorly compressed trigonid on m1–3 (1171>2, convergent with
node E), and paracristids and protocristids subequal
in length (1431>0, convergent with pucadelphyds and
node T).
Node S – Australidelphia and stem relatives
The Itaboraían metatherian Types I, III, IV, VI, VII,
Carolopaulacoutoia, Derorhynchus, and Gaylordia
form a paraphyletic stem group of the clade composed
of Caenolestes, Epidolops, Type V, Peramelia, and
Australidelphia (in 95% of the trees). These overlapping branches diverging from the Didelphidae +
Protodidelphidae clade can be regarded as ‘didelphimorphian’ divergence branches leading to an Australasian radiation.
This clade is supported by 11 unambiguous synapomorphies. These taxa exhibit a large and deep fossa
subarcuata that creates a bulbous and rounded
ventral part of the mastoid (40>1, reversal in Perameles and Echymipera). The presence of a foramen on
the sigmoid sinus and/or prootic sinus that apparently connects both vessels (350>1) is found in Types I,
V, VI, Caenolestes, and Phascogale, whereas it is
unknown in the other taxa comprising this clade,
except for Perameles where it is lost, and it is present
in a specimen of Pucadelphys (YPFB Pal 6470, Marshall & de Muizon, 1995). A vascular groove adjacent
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
to the prootic sinus sulcus, suggesting the presence of
a prootic sinus vein or connection (360>1), is present in
Types I, III, and VI, and Phascogale (but unknown for
Dasycercus and Dromiciops), and is also found in
pucadelphyds. Both the post-temporal sulcus and
notch are absent on the petrosal bone (370>1, 380>1) and
are found, besides this clade, in pucadelphyds.
Dental characters also support this clade: the
molars do not markedly increase posteriorly (621>0,
but moderate posterior increase in peramelians and
dasyurids), the first upper premolar is not procumbent (701>0), the last upper molar is smaller than the
penultimate upper molar (760>1), the metacone on the
last upper molar is present but not distinct from the
metastylar corner of the tooth (920>1), the entoconid
and metaconid are close (1290>1, entoconid at an
extreme posterior position in node T, entoconid and
metaconid close in peramelians, but distant in node
Y), and the paraconid is greatly reduced relative to
the protoconid in m1 (1381>2, paraconid and protoconid subequal in size in node T, paraconid lower than
protoconid in peramelians and dasyurids).
Node T – Type V, Epidolops, Caenolestes,
and Peramelia
The exclusion of peramelians from the clade comprising Dromiciops and Australasian marsupials has
already been suggested by Kirsch et al. (1997) in their
Eometatheria hypothesis. The grouping of peramelians with a clade formed by Caenolestes, Epidolops,
and Type V and identified here as Paucituberculata,
is supported by 13 synapomorphies, most of which are
dental ones. The upper molars are rectangular or
semisquare in occlusal view (740>1), there is no distinct ectoflexus on the upper molars (790>1, convergent
with nodes M and X), the stylar cusp C is absent on
the penultimate upper molar (831>0, convergent with
nodes N and V), the preparacrista is short, rounded,
and virtually absent (941>2, convergent node N) and is
oblique relative to the long axis of the tooth (950>1),
the upper molars have a hypocone (980>1), the m4
talonid has two cusps (1190>1, convergent with Eometatheria), the entoconid is bladed and forms a prominent wall lingual to the talonid basin (1280>1,
convergent with node X), the hypoconid is large and
labially salient (1302>1, convergent with node O and
Eometatheria), there is no labial postcingulid on the
lower molars (1331>0, convergent with node M, didelphids, node V), and the paraconid is subequal in size
to the protoconid in m1 (1382>0, paraconid lower than
protoconid in peramelians). Two basicranial synapomorphies support this clade: an indistinct to absent
mastoid process of the petrosal (242>3, convergent with
Eometatheria), and the absence of a vascular groove
adjacent to the prootic sinus sulcus on the mastoid
(361>0).
763
In 60% of the trees, peramelians are the sister
group of the clade (Type V (Epidolops, Caenolestes)).
The close relationship of the caenolestid Caenolestes
and the polydolopid Epidolops has already been suggested by different authors. Marshall et al. (1990)
grouped together the Polydolopoidea, Caenolestoidea,
and Argyrolagoidea, whereas Kirsch et al. (1997) and
McKenna & Bell (1997) placed the Polydolopoidea
within the Paucituberculata. Therefore, Paucituberculata is here defined as containing caenolestoids
(Caenolestes), polydolopoids (Epidolops), and Type V.
Node V – Eometatheria
Zeusdelphys was alternatively considered as a caenolestoid (Marshall et al., 1990) or polydolopoid
(Kirsch et al., 1997), but it is known by so scarce
remains and is so derived that its affinities to other
marsupials are difficult to highlight even though Goin
et al. (1998) suggested several similarities with Protodidelphidae. Our result is interesting in the fact
that it re-evaluates the phylogenetic status of this
taxon and highlights a sister-group relationship of
Zeusdelphys with the Eometatheria as defined by
Kirsch et al. (1997). This grouping is supported by
three unambiguous synapomorphies: the stylar cusp
B is larger than the paracone (823>2, convergent with
pucadelphyds and extant didelphids), the stylar cusp
C is absent on the penultimate upper molar (831>0,
convergent with nodes N and T), and the upper
molars have no conules (972>0, convergent with node N
and extant didelphids).
Node W – Dromiciops, Minusculodelphis,
Monodelphopsis, and dasyurids
The grouping of Dromiciops and Australasian marsupials excluding peramelians represents the clade
Eometatheria as defined by Kirsch et al. (1997). This
clade is here defined by two unambiguous synapomorphies: the stylar cusp A is very small to indistinct
(810>2, convergent with didelphids and node T), and
the protocone is tall, approaching paracone and/or
metacone height (1020>1, convergent with didelphids
and node M).
Eleven basicranial synapomorphies, most of which
are strict, are here considered as unambiguous for this
clade, as the alternative optimization is in support of
the clade V although Zeusdelphys is only known by
dental remains. The crista petrosa forms a thin lamina
that covers the anterolateral part of the fossa subarcuata (50>1), the anterior lamina of petrosal is absent
and thus shows no depression (70>1, convergent with
didelphids and peramelians), the rostral tympanic
process of the petrosal forms an anterolaterally
directed wing that extends for the whole length of the
promontorium and sometimes contacts the ectotympanic (180>2, convergent with peramelians), the
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
764
S. LADEVÈZE and C. DE MUIZON
petrosal exhibits a hypotympanic sinus (190>1), a stylomastoid foramen encloses the facial foramen (210>1),
the mastoid process is indistinct to absent (242>3,
convergent with node T), a petrosal plate is present
(270>1), the petrosal contribution to the lateral wall of
the epitympanic recess forms a thin lamina (311>2,
convergent with peramelians), the prootic canal is
absent and the lateral head vein has disappeared
(320>1, convergent with peramelians), the alisphenoid
tympanic process extends posteriorly to reach the
posterior limit of the alisphenoid hypotympanic sinus
in ventral view (430>1), and the tubal foramen is
present and just posterior and ventral to the foramen
ovale (470>1).
The sister-group relationship of Minusculodelphis
and Monodelphopsis plus dasyurids is supported by
two unambiguous synapomorphies: p2 and p3 subequal in size (1150>1, convergent with node O), and
oblique protocristid (1371>0, convergent node N). This
close relationship of Minusculodelphis with Australasian marsupials is amazing because this taxon has
usually been regarded as a derorhynchine didelphid
(Marshall et al., 1990; Kirsch et al., 1997; McKenna &
Bell, 1997). It is worth noting that some of the characters highlighting a close relationship of Minusculodelphis and Monodelphopsis plus dasyurids are
actually convergences with either didelphimorphs
(790>1), Marmosopsis and didelphids (1280>1), Itaboraidelphys, Marmosopsis plus didelphids (1150>1), or protodidelphids (, 1321>0, 1371>0).
Monodelphopsis is the sister taxon of dasyurids.
They share the following unambiguous synapomorphy: the anterior point of termination of the cristid
obliqua in m3 is beneath the carnassial notch (1232>0,
convergent with peramelians).
Monodelphopsis has alternatively been regarded as
a Microbiotheriidae (Marshall et al., 1990), Pediomyidae (McKenna & Bell, 1997), or derorhynchine didelphid (Kirsch et al., 1997). Our present hypothesis
suggests a relationship of Monodelphopsis with
Microbiotheriidae inside Eometatheria, but it would
be worth testing the phylogenetic affinities of this
taxon by including other microbiotheres (Microbiotherium) and Australasian marsupials.
MORPHOMETRIC
ANALYSIS AND SYSTEMATIC
IDENTIFICATION OF THE
ITABORAÍAN
TYPE PETROSALS
The promontorium and M2–3/m2–3 areas were
plotted on four graphs to investigate the correlation
between the promontorium and molars for these taxa
(Fig. 5). The exponent of the allometric equation is
close to 1, and reveals that the molars and petrosal
sizes are practically isometric. The r-values of the
curve for these data when they were plotted were
superior to 0.85, suggesting a strong relationship
between the promontorium and molar areas for these
taxa. The first equation of the curve is y = 0.174x1.3287
where x = promontorium area and y = M2 area.
The second equation is y = 0.1107x1.327 where x =
promontorium area and y = m2 area. The third equation is y = 0.1282x1.4474 where x = promontorium
area and y = M3 area. The fourth equation is
y = 0.0804x1.4426 where x = promontorium area and
y = m3 area. These equations were used to estimate
the M2–3/m2–3 areas for the isolated petrosal specimens from Itaboraí (Table 3).
The estimated molar areas of the Type VIII petrosals fall within the range of Minusculodelphis
minimus, Type III, V, and VII within the range of
Marmosopsis juradoi and Gaylordia doelloi, and Type
I and VI within the range of Gaylordia macrocynodonta and Mirandatherium alipoi. Therefore, in
three cases, several Itaboraí petrosal types can be
regarded as possible candidates for a single dental
taxon. This does not mean that we refer several types
of petrosal to the same genus, which would be in
contradiction with the morphological differences
existing amongst the petrosal types. Those size-based
relationships are discussed below and compared to
the present phylogenetic hypothesis (Fig. 6).
The bivariate morphometric analysis pointed out
different size groupings that do not always correlate
with the phylogenetic groupings.
• Type VIII is comparable in size the eometatherian
Minusculodelphis minimus, whereas the parsimony analysis places it as a stem metatherian.
• Types III and VII are comparable in size with the
didelphimorph Marmosopsis juradoi. Types I and
VI are both comparable with the ‘didelphimorph’
Gaylordia macrocynodonta and the stem Marsupialia Mirandatherium alipoi. The Type IV petrosal
size may be correlated to the molar size of the
‘didelphimorph’ Carolopaulacoutoia itaboraiensis.
The parsimony analysis highlighted a stem-group
relationship of Types I, III, IV, VI, and VII to the
clade composed of paucituberculates and Australasian marsupials, which therefore can be regarded
as paraphyletic offshoots of ‘Didelphimorphia’
leading to a paucituberculate and Australasian
radiation. As a consequence, Types III and VI can
be considered as ‘didelphimorphs’ and should be
attributed to Marmosopsis alipoi, even if the latter
is closer to didelphids. Types I and VI are assigned
to Gaylordia macrocynodonta, and Type IV to
Carolopaulacoutoia itaboraiensis.
• Type V is comparable in size with the didelphimorph
Marmosopsis juradoi. However, the cladistic
analysis highlighted the sharing of apomorphic
characters between Type V and the Paucitubercu-
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
765
Figure 5. Molar area vs. promontorium area for extant and fossil metatherians with associated petrosal and teeth
remains. A, M2 area vs. promontorium area; B, m2 area vs. promontorium area; C, M3 area vs. promontorium area; D,
m3 area vs. promontorium area. Open square, Didelphis marsupialis, closed square; Didelphis aurita; grey square,
Didelphis albiventris; open circle, Marmosa murina; closed circle, Philander opossum; grey circle, Metachirus nudicaudatus; cross, Caluromys philander; closed lozenge; Caenolestes fuliginosus; grey lozenge, Phacogale tapoatafa; open
triangle, Pucadelphys andinus; closed triangle, Andinodelphys cochabambensis; grey triangle, Mayulestes ferox; line,
Deltatheridium pretrituberculare. M2–3, second and third upper molars; m2–3, second and third lower molars.
lata. Type V should thus be assigned to a paucituberculate marsupial, although Epidolops has larger
dimensions.
• Type II is comparable in size with the boreometatherian Bobschaefferia fluminensis and the protodidelphid Procaroloameghinia pricei. This is not
congruent with the phylogenetic hypothesis presented here, which assumes a close relationship of
Type II and Pucadelphydae.
CONCLUSIONS
The simultaneous analysis of living and fossil taxa
is a powerful phylogenetic approach as it results in
the most strongly corroborated global hypothesis of
relationships (Nixon & Carpenter, 1996; Kearney &
Clark, 2003). In spite of their incompleteness, which
results in abundant missing data, fossils provide
valuable information that can be used to test phylogenetic hypotheses. The inclusion of fossil taxa has
drastically improved our understanding of the evolutionary history of therians, and especially metatherians (Rougier et al., 1998; Wible et al., 2001;
Luo, Kielan-Jaworowska & Cifelli, 2002; Luo et al.,
2003). The metatherian fossil record suggests a
divergence of metatherians and eutherians in Asia
no later than 125 Mya in the Early Cretaceous (Luo
et al., 2003). The recent discovery of abundant
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
766
S. LADEVÈZE and C. DE MUIZON
Table 3. Promontorium areas and estimated molar areas of the Itaboraían type petrosals (A) and molar area of the
Itaboraían taxa known by dental remains (B)
(A)
Morphotype
Specimen
L pr
W pr
ventr
pr area
Estimated
M2 area
Estimated
m2 area
Estimated
M3 area
Estimated
m3 area
Type I
MNRJ 6726-V
MNRJ 6727-V
3.81
3.58
3.12
3.16
11.89
11.31
4.67
4.37
2.96
2.77
4.61
4.29
2.86
2.66
Type II
MNRJ 6728-V
MNRJ 6729-V
4.73
4.19
4.38
5.23
20.72
21.91
9.76
10.52
6.18
6.66
10.31
11.18
6.37
6.91
Type III
MNRJ 6730-V
MNRJ 6731-V
2.74
2.79
2.76
2.85
7.56
7.95
2.56
2.74
1.62
1.73
2.40
2.58
1.49
1.60
Type IV
MNRJ 6732-V
3.02
2.80
8.46
2.97
1.88
2.82
1.75
Type V
MNRJ 6733-V
MNRJ 6736-V
3.03
2.51
2.57
2.48
7.79
6.22
2.66
1.98
1.69
1.25
2.50
1.81
1.55
1.12
Type VI
MNRJ 6734-V
3.51
3.31
11.62
4.53
2.87
4.46
2.77
Type VII
MNRJ 6737-V
MNRJ 6738-V
MNRJ 6739-V
2.62
2.42
2.27
2.05
1.92
1.90
5.37
4.65
4.31
1.62
1.34
1.21
1.03
0.85
0.77
1.46
1.18
1.06
0.91
0.74
0.66
Type VIII
MNRJ 6735-V
MNRJ 6740-V
1.84
2.49
1.66
2.10
3.05
5.23
0.77
1.57
0.49
0.99
0.65
1.41
0.40
0.87
(B)
Minusculodephis minimus
Marmosopsis juradoi
Gaylordia doeloi
Carolopaulacoutoia itaboraiensis
Derorhynchus singularis
Monodelphopsis travassosi
Gaylordia macrocynodonta
Mirandatherium alipoi
Gugenhemia brasiliensis
Epidolops ameghinoi
Bobbschaefferia fluminensis
Procaroloameghinia pricei
Itaboraidelphys camposi
Didelphopsis cabrerai
Patene simpsoni
Protodidelphis vanzolinii
Protodidelphis mastodontoidea
Carolocoutoia ferigoloi
Zeusdelphys complicatus
M2 area range
m2 area range
M3 area range
m3 area range
Morphotypes
2.10/2.62
0.40/0.49
1.04/1.30
1.34/1.56
2.38
0.48
1.04/1.63
1.40/1.66
Type
Type
Type
Type
Type
3.06/3.80
3.91/4.20
4.79
4.04
5.04
7.09/7.52
2.08/2.48
1.87/2.66
2.16/2.60
2.49/3.20
3.08/5.27
5.47/6.39
6.19/8.30
17.23/17.85
23.85/26.79
24.68/27.54
24.99/26.16
26.31/31.35
7.31
7.54/9.80
8.58/13.08
10.02/19.64
16.00/17.68
19.98/23.28
2.95/4.00
3.8
5.04
4.60/4.74
18/18.39
19.21/35.44
34.09
32.36
2.09/2.44
2.04/2.66
2.16/2.38
2.69/3.47
3.08/4.48
5.45/6.72
3.15/6.26
6.9
6.48
7.50/10.03
11.96/14.04
16.7/30.11
15.64/19.78
21/25.01
VIII
VII
V
III
IV
Type VI
Type I
Type II
48.96
63.08
The estimated molar area ranges of the type petrosals are assigned to the calculated molar area ranges of the Itaboraían
taxa. M2–3, second and third upper molars; m2–3, second and third lower molars.
metatherians from the Late Cretaceous of North
America and Palaeocene of South America has clarified
the origin and relationships of extant metatherians. In
particular, the increased number of cranial remains
(petrosal bones, but also complete skulls) of fossil
metatherian has helped to improve morphological
knowledge and has proved to be relevant in parsimony
analyses because basicranial characters support many
mammalian clades (e.g. Rougier et al.,1998; Luo et al.,
2002; Horovitz & Sánchez-Villagra, 2003).
The present study is the first extensive analysis of
dental and basicranial character state distribution
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
767
Figure 6. Comparisons of the morphometric and phylogenetic assessments as regards the possible assignment of petrosal
types to dental-based taxa from Itaboraí. Scale bars = 2 mm.
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
768
S. LADEVÈZE and C. DE MUIZON
amongst all Itaboraían taxa (both dental genera and
petrosal morphotypes), and allows the systematic
revision of the Itaboraían metatherians and consequently an arguable attribution of the morphotypes to
dental remains from Itaboraí. It is noteworthy that it
has not been possible to associate the metatherian
postcranial bones from Itaboraí with any of the Itaboraían dental taxa (except for some specimens referred
to the didelphid Gaylordia) (Szalay & Sargis, 2001).
The isolated metatherian petrosal bones from the
Palaeocene of Itaboraí were assigned to eight morphotypes, therefore suggesting that they may belong to
different taxa. Type VIII is a stem Metatheria. Type II
is close to Pucadelphydae, Types III and VI are compatible with the didelphid Marmosopsis juradoi, Types
I and VII with the ‘didelphimorph’ Gaylordia macrocynodonta, and Type IV with the ‘didelphimorph’ Carolopaulacoutoia itaboraiensis. Type V, which is closely
related to Caenolestes and Epidolops, should thus be
regarded as a Paucituberculata.
The phylogenetic analysis of Metatheria performed
in this paper suggests new relationships amongst
Itaboraían metatherians within Metatheria, and consequently an interesting palaeobiogeographical scenario. It is noteworthy however that these results
must be regarded with circumspection because of the
important homoplasy displayed by some dental
characters.
The close relationship of Bobbschaefferia and
Eobrasilia with the North American Pediomys and
Didelphodon is unusual but interesting as it underlines new possible affinities between metatherians
from the two Americas. To date, the only metatherians that permitted a link to be made between both
subcontinents were the peradectids, typical North
American taxa found in the early Palaeocene of Tiupampa (Marshall & de Muizon, 1988),and Polydolopimorphia (Case, Goin & Woodburne, 2005).
The ‘Didelphimorphia’ is a paraphyletic grouping
and therefore regarded as a grade. It includes the
Pucadelphydae,
Guggenheimia + Mirandatherium,
the Didelphidae + Protodelphidae and their paraphyletic offshoots, stem to the Australidelphia lineage.
The inclusion of Type II from Itaboraí within the
early Palaeocene Tiupampan Pucadelphydae provides
evidence of close affinities between the two faunas.
Moreover, the metatherians from Itaboraí (20 taxa)
and from Tiupampa (15 taxa, of which three are still
undescribed) are taxonomically very diverse and
related to various fossil and Recent groups, even
including representatives of some of the most
crowned marsupial orders.
The close relationship of extant opossums and
Marmosopsis and Itaboraidelphys was previously
suggested by Marshall et al. (1990) who placed them
within the tribe Didelphini, as well as McKenna &
Bell (1997) and Kirsch et al. (1997) who grouped
them within the subfamily Didelphinae. As a consequence, the oldest known fossil record of Didelphidae is from the mid-Palaeocene of Itaboraí. This
corroborates the molecular divergence date estimates, which suggest that didelphids diverged from
the rest of crown marsupials during the Late Cretaceous (Nilsson et al., 2004; Beck, 2008), and therefore there is no gap in the fossil record of opossums,
contrary to Sánchez-Villagra et al. (2007) and Horovitz et al. (2008).
The sister group of the Didelphidae is the Protodidelphidae, here composed of Didelphopsis, Procaroloameghinia, and Protodidelphis. The close
relationship of Procaroloameghinia and Protodidelphis has already been suggested by Marshall et al.
(1990). In their concept of Caroloameghiniidae,
McKenna & Bell (1997) and Kirsch et al. (1997)
grouped together Robertbutleria (now considered
as synonymous with Protodidelphis) and Procaroloameghinia. Here we refer this grouping to Protodidelphidae, which is sister group to Didelphidae,
rather than to Caroloameghiniidae, which was
included by Kirsch et al. (1997) and McKenna & Bell
(1997) in the order Paucituberculata. This concept of
protodidelphid didelphimorphians differs from that of
Goin et al. (1998), who excluded Procaroloameghinia
from this family but included in it Protodidelphis and
their new genera Carolocoutoia. It is noteworthy
however that the latter is represented by one upper
molar only and is indeed very similar to the more
bunodont species of Protodidelphis, P. mastodontoides
(= Robertbutleria mastodontoidea).
The Polydolopimorphia as defined by Goin et al.
(2006) are here polyphyletic because Procarolomaeghinia is included within Protodidelphidae and Epidolops is the sister group of Caenolestes. In our
phylogenetic hypothesis, the Polydolopimorphia (represented by Epidolops) are included within the Paucituberculata (with the caenolestid Caenolestes and
Type V).
The Australidelphia as defined here include
paucituberculate marsupials, which are the sister
group of the Australasian Peramelia. In turn,
Paucituberculata + Peramelia are the sister group of
the clade Eometatheria (sensu Kirsch et al., 1997,
= microbiotheres plus all the Australasian marsupials
except peramelians). As they include Itaboraían taxa,
Eometatheria probably split from the other marsupials during the Late Cretaceous. Monodelphopsis (considered as a microbiothere by Marshall et al., 1990) is
close to Dromiciops, representing with Minusculodelphis and Dromiciops a stem paraphyletic assemblage
to dasyurids.
The occurrence of crown marsupial taxa in the
Palaeocene of South America points to an early emer-
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
769
Figure 7. Timing of the earliest evolution of metatherians according to the hypotheses highlighted in the most
parsimonious trees (Fig. 4). Data sources: minimal age of Sinodelphys (Swisher et al., 1999), age for the North American
metatherians (Clemens, 1966), dating of the Mongolian taxon Deltatheridium (Dashzeveg et al., 2005), dating of the South
American metatherians (de Muizon, 1994; Flynn & Swisher, 1995; Marshall et al., 1997); molecular estimate of divergence
of marsupial ordinal clades (Nilsson et al., 2004; Beck, 2008; Meredith et al., 2008). Thick and grey strokes represent fossil
species. Geological stages: Ab, Albian; Bm, Barremian; C, Coniacian; Ca, Campanian; Ce, Cenomanian; Eo, Eocene; H,
Hauterivian; Ma, Maastrichtian; Pa, Palaeocene; S, Santonian; T, Turonian; V, Valanginian.
gence of Marsupialia in that continent and corroborates the molecular hypothesis stating that most
extant marsupial orders were separate lineages by
60–70 Mya (Kirsch et al., 1997; Springer, 1997;
Springer, Kirsch & Case, 1997) or even earlier,
80.6 Mya (Beck, 2008; Fig. 7).
Paucituberculata had a long Cenozoic history as
their oldest fossil remains, Type V and Epidolops, are
mid to late Palaeocene in age. Carolopaulacoutoia
and Procaroloameghinia were previously considered
as paucituberculates, but in the present phylogenetic
analysis they are ‘didelphimorph’ offshoots stem
grouped to a paucituberculate and Australasian clade.
The inclusion of Zeusdelphys, Minusculodelphis,
and Monodelphopsis within the Australasian clade
Eometatheria sheds new light on the early history of
the group as it identifies the oldest eometatherian
taxa known in South America. Some other fossil
forms, considered as possible microbiotheres, have
also been included within Australidelphia. This is the
case of the Palaeocene Itaboraían Mirandatherium,
which was firstly described as a microbiothere (Marshall, 1987), although later removed to Didelphinae
(Marshall et al., 1990). The still-earlier Tiupampan
Khasia (Marshall & de Muizon, 1988) and Eocene
remains from Antarctica (Seymour Island, Goin &
Carlini, 1995; Woodburne & Case, 1996) are referred
to Microbiotheria, on the basis of dental remains.
Khasia being the oldest known taxon referred to as
Australidelphia, it has been used for molecular calibration although its position in Australidelphia is
considered doubtful (Szalay, 1994; Beck, 2008). Here
we confirm that the ancient split of Australidelphia
and Eometatheria from other marsupials is as old as
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
770
S. LADEVÈZE and C. DE MUIZON
the late Cretaceous (Fig. 7), as estimated by Beck
(2008). Australasian orders are estimated to have
diverged by the age of the early Eocene Tingamarra
fauna (54.6 Mya; Beck, 2008). However, the presence
of Australasian taxa in the mid Palaeocene of South
America as demonstrated here, suggests that South
America was a centre of origin for these groups,
instead of Australasia or eastern Gondwana, and that
the splitting of the Australasian orders occurred in
that subcontinent well before the final separation of
Australasia and Antarctica.
ACKNOWLEDGEMENTS
For permitting access to materials and help, we thank
J. Bonaparte and A. Kramatz (MACN, Buenos Aires),
G. W. Rougier (University of Louisville, Kentucky), L.
Bergqvist (UFRJ, DNPM, Rio de Janeiro), A. Kellner
and D. Enriques (MNRJ, Rio de Janeiro), and F. Goin
(Museo de La Plata). We are grateful to P. Janvier
(MNHN, USM203-UMR5143, Paris), Zhe-Xi Luo
(Carnegie Museum, Pittsburgh), R. Debruyne
(Ancient DNA Center, McMaster University, Hamilton, ON), and D. Germain (UMR7179, UPMC-Paris
VI) for their fruitful discussions and critical comments. We appreciate the careful and useful revisions
to the manuscript provided by J. R. Wible (Carnegie
Museum, Pittsburgh), G. W. Rougier (University of
Louisville, Kentucky), and an anonymous reviewer
who greatly improved the manuscript. We thank
A. Benz, J. Cuisin, and F. Renoult (MNHN,
UMR8570, Paris), who gave access to extant marsupial collections under their care, and D. Serrette and
P. Loubry (MNHN, USM203-UMR5143, Paris) for the
photographs. This work was supported by a MENRT
Grant (ED 227-2237) from the French Ministry of
Research and fellowships from the MNHN and the
Société des Amis du Muséum, Paris.
REFERENCES
Amrine-Madsen H, Scally M, Westerman M, Stanhope
MJ, Krajewski C, Springer MS. 2003. Nuclear gene
sequences provide evidence for the monophyly of australidelphian marsupials. Molecular Phylogenetics and Evolution 28: 186–196.
Archer M. 1976. The basicranial region of marsupicarnivores
(Marsupialia), interrelationships of carnivorous mammals,
and affinities of the insectivorous marsupial peramelids.
Zoological Journal of the Linnean Society 59: 217–322.
Archibald JD. 1979. Oldest known eutherian stapes and a
marsupial petrosal bone from the Late Cretaceous of North
America. Nature 281: 669–670.
Asher RJ. 1999. A morphological basis for assessing the
phylogeny of the ‘Tenrecoidea’ (Mammalia, Lipotyphla). Cladistics 15: 231–252.
Asher RJ, Horovitz I, Sánchez-Villagra MR. 2004. First
combined cladistic analysis of marsupial mammal interrelationships. Molecular Phylogenetics and Evolution 33: 240–
250.
Beck RMD. 2008. A dated phylogeny of marsupials using a
molecular supermatrix and multiple fossil constraints.
Journal of Mammalogy 89: 175–189.
Bremer K. 1988. The limits of amino acid sequence data in
angiosperm phylogenetic reconstruction. Evolution 42: 795–
803.
Cardillo M, Bininda-Emonds ORP, Boakes E, Purvis A.
2004. A species-level phylogenetic supertree of marsupials.
Journal of Zoology (London) 264: 11–31.
Case JA, Goin FJ, Woodburne MO. 2005. ‘South American’
marsupials from the Late Cretaceous of North America and
the origin of marsupial cohorts. Journal of Mammalian
Evolution 12: 461–494.
Cifelli RL. 1993. Early Cretaceous mammal from North
America and the evolution of marsupial dental characters.
Proceedings of the National Academy of Sciences of the
United States of America 90: 9413–9416.
Clemens WA. 1966. Fossil mammals of the Type Lance
Formation Wyoming. Part II. Marsupialia. University of
California Publications in Geological Sciences 62: 1–122.
Dashzeveg D, Dingus L, Loope DB, Swisher CC III,
Dulam T, Sweeney MR. 2005. New stratigraphic subdivision, depositional environment, and age estimate for the
upper Cretaceous Djadokhta Formation, Southern Ulan
Nur Basin, Mongolia. American Museum Novitates 3498:
1–31.
Dom R, Fisher BL, Martin GF. 1970. The venous system of
the head and neck of the opossum (Didelphis virginiana).
Journal of Morphology 132: 487–496.
Fernández C, Schmidt RS. 1963. The opossum ear and
evolution of the coiled cochlea. Journal of Comparative
Neurology 121: 151–159.
Flynn JJ, Swisher CC III. 1995. Cenozoic South American
land mammal ages: correlation to global geochronologies. In:
Berggren WA, Kent DV, Aubry M-P, Hardenbol J, eds.
Geochronology, time scales and global stratigraphic correlation. Tulsa, OK: Society of Economic Paleontologists and
Mineralogists, 317–334.
Gaudin TJ, Wible JR, Hopson JA, Turnbull WD. 1996.
Reexamination of the morphological evidence for the cohort
Epitheria (Mammalia, Eutheria). Journal of Mammalian
Evolution 3: 31–79.
Gaupp E. 1902. Über die Ala temporalis des Saügetierschädels und die Regio orbitalis einiger anderer Wirbeltierschädels. Anatomische Hefte 19: 155–230.
Gaupp E. 1905. Neue Deutungen auf dem Gebiete der
Lehre vom Säugetierschädel. Anatomischer Anzeiger 27:
273–310.
Gaupp E. 1908. Zur Entwicklungsgeschichte und vergleichenden Morphologie des Schädels von Echidna aculeata
var. typica. Semon’s Zoologische Forschungsreisen in Australien. Denkschriften der medicinischnaturwissenscaftliche
Gesellschaft zu Jena 6: 539–788.
Gelderen C. 1924. Die Morphologie der Sinus durae matris.
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
Zweiter Teil. Die vergleichende Ontogenie der neurokraniellen Venen der Vögel und Säugetiere. Zeitschrift für
Anatomie und Entwickelungsgeschichte 74: 432–508.
Godthelp H, Wroe S, Archer M. 1999. A new marsupial
from the Early Eocene Tingamarra local fauna of Murgon,
Southeastern Queensland: a prototypical Australian marsupial. Journal of Mammalian Evolution 6: 289–313.
Goin FJ, Carlini AA. 1995. An early Tertiary microbiotheriid marsupial from Antartica. Journal of Vertebrate
Paleontology 15: 205–207.
Goin FJ, Oliveira EV, Candela AM. 1998. Carolocoutoia
ferigoloi nov. gen. and sp. (Protodidelphidae), a new Paleocene ‘opossum-like’ marsupial from Brazil. Palaeovertebrata 27: 145–154.
Goin FJ, Pascual R, Tejedor MF, Gelfo JN, Woodburne
MO, Case JA, Reguero MA, Bond M, López GM, Cione
AL, Udrizar Sauthier D, Balarino L, Scasso RA,
Medina FA, Ubaldón MC. 2006. The earliest Tertiary
therian mammal from South America. Journal of Vertebrate
Paleontology 26: 505–510.
Hochstetter F. 1896. Beitraïge zur Anatomie und Entwickelungsgeschichte des Blutgefaïsssystems der Monotremen.
Semon’s Zoologische Forschungsreisen in Australien 5: 189–
243.
Hopson JA, Rougier GW. 1993. Braincase structure in the
oldest known skull of therian mammal: implications for
mammalian systematics and cranial evolution. American
Journal of Science 293: 268–299.
Horovitz I, Ladevèze S, Argot C, Hooker JJ, Macrini TE,
Martin T, Kurz C, de Muizon C, Sánchez-Villagra MR.
2008. The anatomy of Herpetotherium fugax Cope 1873,
a metatherian from the Oligocene of North America.
Palaeontographica Abt. A 284: 109–141.
Horovitz I, Sánchez-Villagra MR. 2003. A morphological
analysis of marsupial mammal higher-level phylogenetic
relationships. Cladistics 19: 181–212.
Hunt RM. 1974. The auditory bulla in Carnivora: an anatomical basis for reappraisal of carnivore evolution. Journal
of Morphology 143: 21–76.
Kearney M, Clark JM. 2003. Problems due to missing data
in phylogenetic analyses including fossils: a critical review.
Journal of Vertebrate Paleontology 23: 263–274.
Kermack KA, Mussett F, Rigney HW. 1981. The skull of
Morganucodon. Zoological Journal of the Linnean Society
71: 1–158.
Kielan-Jaworowska Z, Cifelli RL, Luo Z-X. 2004.
Mammals from the age of dinosaurs: origins, evolution, and
structure. New York, NY: Columbia University Press.
Kirsch JAW, Lapointe F-J, Springer MS. 1997. DNAhybridisation studies of marsupials and their implications
for metatherian classification. Australian Journal of
Zoology 45: 211–280.
Kirsch JAW, Reig OA, Springer MS. 1991. DNA hybridization evidence for the Australian affinity of the American
marsupial Dromiciops australis. Proceedings of the National
Academy of Sciences of the United States of America 88:
10465–10469.
Kuhn H-J, Zeller U. 1987. The cavum epiptericum in
771
monotremes and therian mammals. In: Kuhn H-J, Zeller U,
eds. Morphogenesis of the mammalian skull. Hamburg:
Verlag Paul Varey, 51–70.
Ladevèze S. 2004. Metatherian petrosals from the Late Paleocene of Itaboraí (Brazil), and their phylogenetic implications. Journal of Vertebrate Paleontology 24: 202–213.
Ladevèze S. 2007a. Isolated mammalian fossil remains of
petrosals and teeth: what to do with? Morphometric and
phylogenetic analyses of metatherian petrosal bones from
the Paleocene of South America. 8th International Congress
of Vertebrate Morphology. Journal of Morphology 268:
1097.
Ladevèze S. 2007b. Petrosal bones of metatherian mammals
from the Late Paleocene of Itaboraí (Brazil), and a cladistic
analysis of petrosal features in metatherians. Zoological
Journal of the Linnean Society 150: 85–115.
Ladevèze S, de Muizon C. 2007. The auditory region of
early Paleocene Pucadelphydae (Mammalia, Metatheria)
from Tiupampa, Bolivia, with phylogenetic implications.
Palaeontology 50: 1123–1154.
Lofgren DL. 1995. The Bug Creek problem and the
Cretaceous-Tertiary transition at McGuire Creek, Montana.
University of California Publications in Geological Sciences
140: 1–185.
Luckett WP. 1994. Suprafamilial relationships within Marsupialia: resolution and discordance from multidisciplinary
data. Journal of Mammalian Evolution 2: 255–283.
Luo Z-X, Ji Q, Wible JR, Yuan C-X. 2003. An early Cretaceous tribosphenic mammal and metatherian evolution.
Science 302: 1934–1940.
Luo Z-X, Kielan-Jaworowska Z, Cifelli RL. 2002. In quest
for a phylogeny of Mesozoic mammals. Acta Palaeontologica
Polonica 47: 1–78.
McKenna MC, Bell SK. 1997. Classification of mammals
above the species level. New York, NY: Columbia University
Press.
MacPhee RDE. 1981. Auditory regions of primates and eutherian insectivores: morphology, ontogeny, and character
analysis. Contributions to Primatology 18: 1–282.
MacPhee RDE, Novacek MJ, Storch G. 1988. Basicranial
morphology of early Tertiary Erinaceomorphs and the origin
of primates. American Museum Novitates 2921: 1–42.
Maddison DR. 1991. The discovery and importance of multiple islands of most-parsimonious trees. Systematic Zoology
40: 315–328.
Marshall LG. 1987. Systematics of Itaboraían (Middle Paleocene) age opossum-like marsupials from the limestone
quarry at São José de Itaboraí, Brazil. In: Archer M, ed.
Possums and opossums: studies in evolution. Sydney: Surrey
Beatty & Sons and the Royal Zoological Society of New
South Wales, 91–160.
Marshall LG, Case JA, Woodburne MO. 1990. Phylogenetic relationships of the families of marsupials. In: Genoways HH, ed. Current mammalogy. New York, NY: Plenum
Press, 433–505.
Marshall LG, Kielan-Jaworowska Z. 1992. Relationships
of the dog-like marsupials, deltatheroidans, and early tribosphenic mammals. Lethaia 25: 361–374.
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
772
S. LADEVÈZE and C. DE MUIZON
Marshall LG, de Muizon C. 1988. The dawn of the Age of
Mammals in South America. National Geographic Research
4: 23–55.
Marshall LG, de Muizon C. 1995. Part II. The skull. In: de
Muizon C, ed. Pucadelphys andinus (Marsupialia, Mammalia) from the early Paleocene of Bolivia. Paris: Mémoires du
Muséum national d’Histoire naturelle, 21–90.
Marshall LG, de Muizon C, Sigogneau-Russel D. 1995.
Pucadelphys andinus (Marsupialia, Mammalia) from the
early Paleocene of Bolivia. Paris: Mémoires du Muséum
national d’Histoire naturelle.
Marshall LG, Sempere T, Butler RF. 1997. Chronostratigraphy of the mammal-bearing Paleocene of South America.
Journal of South American Earth Sciences 10: 49–70.
Meng J, Fox RC. 1995a. Osseous inner ear structures and
hearing in early marsupials and placentals. Zoological
Journal of the Linnean Society 115: 47–71.
Meng J, Fox RC. 1995b. Therian petrosals from the Oldman
and Milk River Formations (Late Cretaceous), Alberta.
Journal of Vertebrate Paleontology 15: 122–130.
Meredith RW, Westerman M, Case J, Springer MS. 2008.
Phylogeny and timescale for marsupial evolution based on
sequences for five nuclear genes. Journal of Mammalian
Evolution 15: 1–36.
de Muizon C. 1992. La fauna de mamíferos de Tiupampa
(Paleoceno inferior, Formación Santa Lucía), Bolivia. In:
Suárez-Soruco R, ed. Fósiles y Fácies de Bolivia, Vol. I,
Vertebrados. Santa Cruz: Revista Técnica, Yacimientos
Petrolíferos Fiscales Bolivianos, 575–624.
de Muizon C. 1994. Marsupial skeletons from the Early
Paleocene of Tiupampa (Bolivia) diagnostic features of fossil
marsupials. Journal of Vertebrate Paleontology 14 (Suppl.
3): 39A.
de Muizon C. 1998. Mayulestes ferox, a boryaenoid (Metatheria, Mammalia) from the early Palaeocene of Bolivia. Phylogenetic and palaeobiologic implications. Geodiversitas 20:
19–142.
de Muizon C. 1999. Marsupial skulls from the Deseadan
(Late Oligocene) of Bolivia and phylogenetic analysis of the
Borhyaenoidea (Marsupialia, Mammalia). Geobios 32: 483–
509.
de Muizon C, Brito IM. 1993. Le bassin calcaire de São José
de Itaboraí (Rio de Janeiro, Brésil): ses relations fauniques
avec le site de Tiupampa (Cochabamba, Bolivie). Annales de
Paléontologie 79: 233–268.
de Muizon C, Cifelli RL. 2001. A new basal ‘Didelphoid’
(Marsupialia, Mammalia) from the Early Paleocene of Tiupampa (Bolivia). Journal of Vertebrate Paleontology 21:
87–97.
de Muizon C, Cifelli RL, Bergqvist LP. 1998. Eutherian
tarsals from the early Paleocene of Bolivia. Journal of
Vertebrate Paleontology 18: 655–663.
de Muizon C, Cifelli RL, Céspedes Paz R. 1997. The origin
of the dog-like borhyaenoid marsupials of South America.
Nature 389: 486–489.
Nilsson MA, Arnason U, Spencer PBS, Janke A. 2004.
Marsupial relationships and a timeline for marsupial radiation in South Gondwana. Gene 340: 189–196.
Nilsson MA, Gullberg A, Spotorno AE, Arnason U, Janke
A. 2003. Radiation of extant marsupials after the K/T
boundary: evidence from complete mitochondrial genome.
Journal of Molecular Evolution 57: 3–12.
Nixon KC, Carpenter JM. 1996. On simultaneous analysis.
Cladistics 12: 221–241.
Palma RE, Spotorno AE. 1999. Molecular systematics of
marsupials based on the rRNA 12S mitochondrial gene: the
phylogeny of didelphimorphia and of the living fossil microbiotheriid Dromiciops gliroides Thomas. Molecular Phylogenetics and Evolution 13: 525–535.
de Paula Couto C. 1952a. Fossil mammals from the beginning of the Cenozoic in Brazil. Marsupialia: Didelphidae.
American Museum Novitates 1567: 1–26.
de Paula Couto C. 1952b. Fossil mammals from the beginning of the Cenozoic in Brazil. Marsupialia: Polydolopidae
and Borhyaenidae. American Museum Novitates 1559: 1–27.
de Paula Couto C. 1952c. A new name for Mirandaia riberoi
Paula Couto, 1952. Journal of Mammalogy 33: 503.
de Paula Couto C. 1961. Marsupiais fósseis do Paleoceno do
Brazil. Anais da Academia Brasileira de Ciências 33: 312–
333.
de Paula Couto C. 1962. Didelphídeos fósiles del Paleoceno
de Brazil. Revista del Museo Argentino de Ciencias Naturales ‘Bernadino Rivadavia’, Ciencias Zoologicas 112: 135–
166.
Phillips MJ, Lin Y-H, Harrison GL, Penny D. 2001. Mitochondrial genomes of a bandicoot and a brushtail possum
confirm the monophyly of australidelphian marsupials. Proceedings of the Royal Society of London Series B 268: 1533–
1538.
Phillips MJ, MacLenachan PA, Down C, Gibb GC,
Penny D. 2006. Combined mitochondrial and nuclear
protein-coding DNA sequences resolve the Interrelations of
the major Australasian marsupial radiations. Systematic
Biology 55: 122–137.
Reig OA, Kirsch JAW, Marshall LG. 1987. Systematic
relationships of the living and Neocenozoic American
‘opossum-like’ marsupials (suborder Didelphimorphia), with
comments on the classification of these and of the Cretaceous and Paleogene New World and European metatherians. In: Archer M, ed. Possums and opossums: studies in
evolution. Sydney: Surrey Beatty & Sons and the Royal
Zoological Society of New South Wales, 1–89.
Rougier GW, Bonaparte JF. 1988. La pared lateral del
cráneo de Vincelestes neuquenianus (Mammalia, Eupantotheria) y su importancia en el estudo de los mamíferos
mesozoicos. V Jornadas Argentina de Paleontología de
Vertebrados Resumenes: 14–15.
Rougier GW, Wible JR. 2006. Major changes in the ear
region and basicranium of early mammals. In: Carrano M,
Gaudin TJ, Blob R, Wible JR, eds. Amniote paleobiology:
phylogenetic and functional perspectives on the evolution of
mammals, birds and reptiles. Chicago, IL: University of
Chicago Press, 269–311.
Rougier GW, Wible JR, Hopson JA. 1992. Reconstruction
of the cranial vessels in the Early Cretaceous mammal
Vincelestes neuquenianus: implications for the evolution of
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
the mammalian cranial vascular system. Journal of Vertebrate Paleontology 12: 188–216.
Rougier GW, Wible JR, Hopson JA. 1996. Basicranial
anatomy of Priacodon fruitaensis (Triconodontidae, Mammalia) from the Late Jurassic of Colorado, and a reappraisal
of mammaliaform interrelationships. American Museum
Novitates 3183: 1–38.
Rougier GW, Wible JR, Novacek MJ. 1996. Middle-ear
ossicles of the multituberculate Kryptobaatar from the Mongolian Late Cretaceous: implications for mammaliamorph
relationships and the evolution of the auditory apparatus.
American Museum Novitates 3187: 1–43.
Rougier GW, Wible JR, Novacek MJ. 1998. Implications
of Deltatheridium specimens for early marsupial history.
Nature 396: 459–463.
Rougier GW, Wible JR, Novacek MJ. 2004. New specimen
of Deltatheroides cretacicus (Metatheria, Deltatheroidea)
from the Late Cretaceous of Mongolia. Bulletin of Carnegie
Museum of Natural History 36: 245–266.
Sánchez-Villagra MR. 2001a. Ontogenetic and phylogenetic
transformations of the vomeronasal complex and nasal floor
elements in marsupial mammals. Zoological Journal of the
Linnean Society 131: 459–479.
Sánchez-Villagra MR. 2001b. The phylogenetic relationships of argyrolagid marsupials. Zoological Journal of the
Linnean Society 131: 481–496.
Sánchez-Villagra MR, Ladevèze S, Horovitz I, Argot C,
Hooker JJ, Macrini T, Martin T, Moore-Fay S, de
Muizon C, Schmelzle T, Asher RJ. 2007. Exceptionally
preserved North American Paleogene metatherians: adaptations and discovery of a major gap in the opossum fossil
record. Proceedings of the Royal Society, Biology Letters 3:
318–322.
Sánchez-Villagra MR, Schmelzle T. 2007. Anatomy and
development of the bony inner ear in the woolly opossum,
Caluromys philander (Didelphimorphia, Marsupialia).
Mastozoología Neotropical 14: 53–60.
Sánchez-Villagra MR, Wible JR. 2002. Patterns of evolutionary transformation in the petrosal bone and some basicranial features in marsupial mammals, with special
reference to didelphids. Journal of Zoological Systematics
and Evolutionary Research 40: 26–45.
Segall W. 1970. Morphological parallelisms of the bulla and
auditory ossicles in some insectivores and marsupials. Fieldiana: Zoology, 51: 169–205.
Sorenson MD, Franzosa EA. 2007. TreeRot, Version 3.
Boston, MA: Boston University.
Springer MS. 1997. Molecular clocks and the timing of the
placental and marsupial radiations in relation to the
Cretaceous-Tertiary boundary. Journal of Mammalian Evolution 4: 285–302.
Springer MS, Kirsch JAW, Case JA. 1997. The chronicle of
marsupial evolution. In: Givnish TJ, Sytsma KJ, eds.
Molecular evolution and adaptative radiation. New York,
NY: Cambridge University Press, 129–161.
Springer MS, Westerman M, Kavanagh JR, Burk A,
Woodburne MO, Kao DJ, Krajewski C. 1998. The origin
of the Australasian marsupial fauna and the phylogenetic
773
affinities of the enigmatic monito del monte and marsupial
mole. Proceedings of the Royal Society of London. Series B.
Biological Sciences 265: 2381–2386.
Swisher CC III, Wang Y-Q, Wang X-L, Xu X, Wang Y. 1999.
Cretaceous age for the feathered dinosaurs of Liaoning,
China. Nature 400: 58–61.
Swofford DL. 2002. PAUP*. Phylogenetic analysis using parsimony (*and other methods), Version 4. Sunderland, MA:
Sinauer Associates.
Szalay FS. 1982a. A new appraisal of marsupials phylogeny
and classification. In: Archer M, ed. Carnivorous marsupials. Sydney: Royal Zoological Society of New South Wales,
621–640.
Szalay FS. 1982b. Phylogenetic relationships of the marsupials. Geobios mémoire spécial 6: 177–190.
Szalay FS. 1994. Evolutionary history of the marsupials and
an analysis of osteological characters. Cambridge; New York,
NY: Cambridge University Press.
Szalay FS, Sargis EJ. 2001. Model-based analysis of postcranial osteology of marsupials from the Paleocene of Itaboraí (Brazil) and the phylogenetics and biogeography of
Metatheria. Geodiversitas 23: 139–302.
Van der Klaauw CJ. 1931. The auditory bulla in some fossil
mammals, with a general introduction to this region of the
skull. Bulletin of the American Museum of Natural History
LXII: 1–352.
Voit M. 1909. Das primordialcranium des kaninchens unter
berücksichtigung der deckknochen. Ein beitrag zur morphologie des säugetierschädels. Anatomische Hefte 38: 425–
616.
Voss RS, Jansa SA. 2003. Phylogenetic studies on didelphid
marsupials II. Nonmolecular data and new IRBP sequences:
separate and combined analyses of didelphine relationships
with denser taxon sampling. Bulletin of the American
Museum of Natural History 276: 1–82.
Wible JR. 1986. Transformations in the extracranial course
of the internal carotid artery in mammalian phylogeny.
Journal of Vertebrate Paleontology 6: 313–325.
Wible JR. 1987. The eutherian stapedial artery: character
analysis and implications for superordinal relationships.
Zoological Journal of the Linnean Society 91: 107–135.
Wible JR. 1990. Petrosals of Late Cretaceous marsupials
from North America, and a cladistic analysis of the petrosal
in therian mammals. Journal of Vertebrate Paleontology 10:
183–205.
Wible JR. 2003. On the cranial osteology of the short-tailed
opossum Monodelphis brevicaudata (Didelphidae, Marsupialia). Annals of Carnegie Museum 72: 137–202.
Wible JR, Hopson JA. 1993. Basicranial evidence for early
mammal phylogeny. In: Szalay FS, Novacek MJ, McKenna
MC, eds. Mammal phylogeny: Mesozoic differentiation, multituberculates, monotremes, early therians, and marsupials.
New York, NY: Springer-Verlag, 45–62.
Wible JR, Hopson JA. 1995. Homologies of the prootic canal
in mammals and non-mammalian cynodonts. Journal of
Vertebrate Paleontology 15: 331–356.
Wible JR, Rougier GW, Novacek MJ, McKenna MC.
2001. Earliest eutherian ear region: a petrosal referred to
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
774
S. LADEVÈZE and C. DE MUIZON
Prokennalestes from the Early Cretaceous of Mongolia.
American Museum Novitates 3322: 1–44.
Woodburne MO, Case JA. 1996. Dispersal, vicariance, and
the Late Cretaceous to Early Tertiary land mammal biogeography from South America to Australia. Journal of Mammalian Evolution 3: 121–161.
Wroe S. 1997. A reexamination of proposed morphology-based
synapomorphies for the families of Dasyuromorphia
(Marsupialia): Part I, Dasyuridae. Journal of Mammalian
Evolution 4: 19–52.
Wroe S. 1999. The geologically oldest dasyurid, from the
Miocene of Riversleigh, north-west Queensland. Palaeontology 42: 501–527.
Wroe S, Ebach M, Ahyong S, de Muizon C, Muirhead J.
2000. Cladistic analysis of dasyuromorphian (Marsupialia)
phylogeny using cranial and dental characters. Journal of
Mammalogy 81: 1008–1024.
LIST
OF THE
APPENDIX 1
56 BASICRANIAL AND 89
DENTAL
CHARACTERS USED IN THE PARSIMONY ANALYSIS
Some character states are revised for Pucadelphys
and Andinodelphys, as to the observations of Rougier,
et al. (1998), Wroe, et al. (2000), Wible, et al. (2001).
Most of the studied dental characters were used
and discussed in a previous analysis by Ladevèze and
Muizon (2007).
Basicranial characters
1. Complete wall separating cavum supracochleare
from cavum epiptericum: absent (0) or present
(1). References: Wible (1990, ch. 2), Wible &
Hopson (1993, ch. 6), Rougier, Wible & Hopson
(1996, ch. 40), Rougier, Wible & Novacek (1996,
ch. 40), Rougier et al. (1998, ch. 128), Wible et al.
(2001, ch. 128), Luo et al. (2002, ch. 203),
Sánchez-Villagra and Wible (2002, ch. 11),
Ladevèze (2004, ch. 1; 2007b, ch. 1), Ladevèze
and Muizon (2007, ch. 118).
2. Cavum epiptericum floored by: petrosal (0), petrosal and alisphenoid (1), or primarily or exclusively by alisphenoid (2). References: Wible &
Hopson (1993, ch. 4), Rougier et al. (1996a, b, ch.
35), Rougier et al. (1998, ch. 109), Wible et al.
(2001, ch. 109), Ladevèze (2007b, ch. 2),
Ladevèze and Muizon (2007, ch. 119).
3. Fossa subarcuata: smaller than its aperture (i.e.,
conical shape) (0) or larger than its aperture
(i.e., spherical shape) (1). Reference: Ladevèze
(2004, ch. 2; 2007b, ch. 3), Ladevèze and Muizon
(2007, ch. 120).
4. Posterior exposure of the pars mastoidea: elongated (0) or rounded and bulbous due to the
excavation of the fossa subarcuata (1). Reference: Ladevèze (2004, ch. 3; 2007b, ch. 4),
Ladevèze and Muizon (2007, ch. 121).
5. Expansion of the crista petrosa that forms a thin
lamina covering the anterolateral part of the
fossa subarcuata: absent (0) or present (1). References: Ladevèze (2007b, ch. 5), Ladevèze and
Muizon (2007, ch. 122).
6. Anterior lamina of petrosal exposure on lateral
braincase wall: present and large (0), or rudimentary (1), or absent (2). References: Wible
(1990, 14), Wible & Hopson (1993, ch. 1, 2),
Rougier et al. (1998, ch. 108), Wible et al. (2001,
ch. 108), Ladevèze (2004, ch. 5; 2007b, ch. 6),
Ladevèze and Muizon (2007, ch. 123).
7. Anterior lamina of petrosal: shows a large
depression that may have received a part of
temporal lobe of the brain (0) or shows no
depression (1). References: Ladevèze (2004, ch.
6; 2007b, ch. 7), Ladevèze and Muizon (2007, ch.
124).
8. Internal acoustic meatus and fossa subarcuata:
subequal and separated by a sharp wall (0),
internal acoustic meatus narrower than fossa
subarcuata and separated from the latter by a
thick shelf of bone (1), or fossa subarcuata
shallow and plainly narrower than internal
acoustic meatus (2). References: Ladevèze
(2007b, ch. 8), Ladevèze and Muizon (2007, ch.
125).
9. Internal acoustic meatus: deep with thick prefacial commissure (0) or shallow with thin prefacial commissure (1). References: Rougier et al.
(1998, ch. 153), Wible et al. (2001, ch.153),
Ladevèze (2004, ch. 8; 2007b, ch. 9), Ladevèze
and Muizon (2007, ch. 126).
10. Deep groove for internal carotid artery excavated on anterior pole of promontorium: absent
(0) or present (1). References: Muizon et al.
(1997), Rougier et al. (1998, ch. 148), Wible et al.
(2001, ch. 148), Sánchez-Villagra and Wible
(2002, ch. 16), Horovitz and Sánchez-Villagra
(2003, ch. 220), Ladevèze (2004, ch. 10; 2007b,
ch. 10), Ladevèze and Muizon (2007, ch.
127).
11. Deep and large fossa for the tensor tympani
muscle excavated on the anterolateral aspect of
promontorium, creating a battered ventral
surface of the promontorium: absent (0) or
present (1). References: Wible (1990, ch. 12), Luo
et al. (2002, ch. 221), Ladevèze (2007b, ch. 11),
Ladevèze and Muizon (2007, ch. 128).
12. Epitympanic wing of petrosal: absent (0) or
present (1). References: Rougier et al. (1998, ch.
122); Wible et al. (2001, ch. 122), Ladevèze
(2007b, ch. 12), Ladevèze and Muizon (2007, ch.
129).
13. Epitympanic wing of petrosal: flat (0), undulated
(1), or confluent with bulla (2). References:
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
14.
15.
16.
17.
18.
19.
20.
Rougier et al. (1998, ch. 122); Wible et al. (2001,
ch. 122), Ladevèze (2007b, ch. 12), Ladevèze and
Muizon (2007, ch. 129).
Lateral flange: large and lateral to promontorium (0) or greatly reduced or absent (1). References: Wible (1990, ch. 3), Rougier et al. (1996a,
b, ch. 29), Rougier et al. (1998, ch. 126), Wible
et al. (2001, ch. 126), Ladevèze (2007b, ch. 14),
Ladevèze and Muizon (2007, ch. 131).
Tympanic sinus formed in the lateral trough (or
lateral expansion of the pars canalicularis):
absent (0) or present (1). Reference: Ladevèze
and Muizon (2007, ch. 162).
Broad shelf of bone surrounding fenestra
cochleae and making a separation between it
and aqueductus cochleae: absent (0) or present
(1). References: Ladevèze (2007b, ch. 16),
Ladevèze and Muizon (2007, ch. 132).
Rostral tympanic process of petrosal: absent (0)
or present as a distinct crest or erected process
(1). References: Wible (1990, ch. 9), Rougier et al.
(1998, ch. 130), Wible et al. (2001, ch. 130),
Ladevèze (2007b, ch. 17), Ladevèze and Muizon
(2007, ch. 133). The presence of a low and tiny
ridge or tubercle, anterolateral to the fenestra
vestibuli is not regarded as equivalent to the
development of a tympanic process, since it is
not a process, i.e., a raised shelf of bone.
Rostral tympanic process of petrosal: does not
extend as a tympanic wing (0), forms an anterolaterally directed wing, sometimes contacting
the ectotympanic, that does not extend on the
whole length of the promontorium (1), or forms
an anterolaterally directed wing, sometimes contacting the ectotympanic, that does extend on
the whole length of the promontorium (2). References: Sánchez-Villagra and Wible (2002, ch.
7), Horovitz and Sánchez-Villagra (2003, ch.
215), Ladevèze (2007b, ch. 18), Ladevèze and
Muizon (2007, ch. 134).
Hypotympanic sinus of the petrosal: absent (0)
or present (1). References: Wroe (1999), Wroe
et al. (2000, ch. 65). This character describes the
petrosal contribution to the hypotympanic sinus
of the alisphenoid, and differs from the character
15 of the present analysis.
Tympanic aperture of hiatus Fallopii: ventral
(0), dorsal (1), or intermediate (2). References:
Sánchez-Villagra and Wible (2002, ch. 12), Horovitz and Sánchez-Villagra (2003, ch. 218),
Ladevèze (2007b, ch. 20), Ladevèze and Muizon
(2007, ch. 135). The floor and roof of the cavum
epiptericum are of interest to delimitate the
position of the hiatus Fallopii (Sánchez-Villagra
and Wible 2002). If the floor of the cavum epiptericum does extend further anteriorly than the
21.
22.
23.
24.
25.
26.
775
roof, the hiatus Fallopii is considered as having
a dorsal position (e.g., Pucadelphys, Andinodelphys, and Petrosal Types I, II, V, VI, VII). In
extant didelphids, the anterior lamina has
totally disappeared and the hiatus opens on the
anteromedial edge of the bone (i.e., the floor and
the roof of the cavum epiptericum are at the
same level; intermediate position of SánchezVillagra and Wible 2002). A ventral aperture of
the hiatus Fallopii occurs in Perameles and
Echymipera, where the roof of the cavum epiptericum extends further anteriorly than the
floor.
Stylomastoid foramen: absent (0) or present (1).
References: Archer (1976), Wroe et al. (2000, ch.
54), Ladevèze (2007b, ch. 21), Ladevèze and
Muizon (2007, ch. 136).
Inferior petrosal sinus: intrapetrosal (0) or
between petrosal, basisphenoid and basioccipital
(1) or endocranial (2). References: Rougier et al.
(1996a, b, ch. 42), Rougier et al. (1998, ch. 151),
Wible et al. (2001, ch. 151), Ladevèze (2004, ch.
17; 2007b, ch. 22), Ladevèze and Muizon (2007,
ch. 137).
Mastoid exposure: large (0), narrow (1), or
reduced pars mastoidea, internal to the braincase and wedged between the squamosal and
exoccipital (2). References: Ladevèze (2004, ch.
18; 2007b, ch. 23), Ladevèze and Muizon (2007,
ch. 138).
Mastoid tympanic process: large vertical process
(0), large, slanted, and nodelike process, projecting ventrally and extended posteriorly on the
mastoid, from the posteromedial border of the
stylomastoid notch (1), small, nodelike, and ventrally directed process, forming a distinct posterior wall of the stylomastoid notch (2), or
indistinct to absent (3). References: Wible (1990,
ch. 7), Rougier et al. (1998, ch. 131), Wroe et al.
(2000, ch. 67), Wible et al. (2001, ch. 131),
Ladevèze (2004, ch. 19; 2007b, ch. 24), Ladevèze
and Muizon (2007, ch. 139).
Caudal tympanic process of petrosal: absent (0)
or present (1). References: Wible (1990, ch. 8),
Wible & Hopson (1993, ch. 26), Rougier et al.
(1996a, b, ch. 18), Rougier et al. (1998, ch. 132),
Wible et al. (2001, ch. 132), Luo et al. (2002, ch.
200), Ladevèze (2007b, ch. 25), Ladevèze and
Muizon (2007, ch. 140). As for the character of
the rostral tympanic process of petrosal (ch. 17),
the presence of a low and tiny ridge or tubercle,
in the area of the caudal tympanic process, is not
regarded as a tympanic process.
Caudal tympanic process of petrosal: forms a
small crest that does not wholly floor the postpromontorial sinus (0) or forms an expanded
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
776
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
S. LADEVÈZE and C. DE MUIZON
lamina that floors the postpromontorial sinus
(1). Reference: Ladevèze (2004, ch. 20; 2007b, ch.
26), Ladevèze and Muizon (2007, ch. 141).
Petrosal plate: absent (0) or present (1). References: Wible (1990, ch. 8), Sánchez-Villagra and
Wible (2002, ch. 8), Horovitz and SánchezVillagra (2003, ch. 216), Ladevèze (2004, ch. 21;
2007b, ch. 27), Ladevèze and Muizon (2007, ch.
142).
Fossa incudis and epitympanic recess: continuous (0) or separated by a distinct ridge (1).
References: Rougier et al. (1998, ch. 137), Wible
et al. (2001, ch. 137), Ladevèze (2007b, ch. 28),
Ladevèze and Muizon (2007, ch. 143).
Tympanic crest (“petrosal crest” of Archer, 1976;
Muizon, 1999): absent (0) or present (1). References: Archer (1976), Muizon (1999), ch. 15),
Ladevèze (2004, ch. 23; 2007b, ch. 29), Ladevèze
and Muizon (2007, ch. 144).
Petrosal contribution to the lateral wall of the
epitympanic recess: absent (0) or present (1).
References: Ladevèze (2007b, ch. 30), Ladevèze
and Muizon (2007, ch. 145).
Petrosal contribution to the lateral wall of the
epitympanic recess: massive, large shelf of bone,
sometimes rounded (0), raised and triangular
(1), or forming a thin lamina (2). References:
Ladevèze (2004, ch. 24; 2007b, ch. 31), Ladevèze
and Muizon (2007, ch. 146).
Prootic canal: present (0) or absent (1). References: Wible (1990, ch. 17), Wible & Hopson
(1993, ch. 18), Wible & Hopson (1995), Wroe
et al. (2000, ch. 77), Sánchez-Villagra and Wible
(2002, ch. 9, 10), Ladevèze (2004, ch. 25; 2007b,
ch. 32), Ladevèze and Muizon (2007, ch. 147).
Prootic canal: large with endocranial opening (0)
or reduced with intramural opening (1). References: Wible (1990, ch. 18), Wible & Hopson
(1993, ch. 19), Rougier et al. (1998, ch. 124),
Wible et al. (2001, ch. 124), Ladevèze (2004, ch.
26; 2007b, ch. 33), Ladevèze and Muizon (2007,
ch. 148).
Imprint of the transverse sinus bifurcation on
the petrosal: absent (0) or present (1). Reference:
Ladevèze (2004, ch. 27; 2007, ch. 34), Ladevèze
and Muizon (2007, ch. 149).
Foramina on the sigmoid sinus and/or prootic
sinus, apparently connecting both vessels (i.e.,
sigmoid sinus vein): absent (0) or present (1).
References: Ladevèze (2007b, ch. 35), Ladevèze
and Muizon (2007, ch. 150).
Vascular groove adjacent to prootic sinus sulcus,
on the mastoid (i.e., prootic sinus vein or connection): absent (0) or present (1). References:
Ladevèze (2007b, ch. 36), Ladevèze and Muizon
(2007, ch. 151).
37. Posttemporal sulcus on the squamosal surface of
the petrosal: present (0) or absent (1). References: Wible & Hopson (1995), Rougier et al.
(1998, ch. 144), Wible et al. (2001, ch. 144),
Sánchez-Villagra and Wible (2002, ch. 13), Horovitz and Sánchez-Villagra (2003, ch. 219),
Ladevèze (2007b, ch. 37), Ladevèze and Muizon
(2007, ch. 152).
38. Posttemporal notch/foramen: present (0) or
absent (1). References: Wible (1990, ch. 24),
Rougier et al. (1998, ch. 144), Wible et al. (2001,
ch. 144), Luo et al. (2002, ch. 251), SánchezVillagra and Wible (2002, ch. 14), Ladevèze
(2004, ch. 29; 2007b, ch. 38), Ladevèze and
Muizon (2007, ch. 153).
39. Primary foramen ovale bounded by: lamina
obturans/petrosal (0), alisphenoid and petrosal
(1), alisphenoid or alisphenoid and squamosal
(2). References: Gaudin, Wible, Hopson & Turnbull (1996), Wroe (1997), Rougier et al. (1998, ch.
111), Muizon (1999), ch. 7), Wroe et al. (2000, ch.
50), Wible et al. (2001, ch. 111), Horovitz and
Sánchez-Villagra (2003, ch. 194), Ladevèze
(2004, ch. 30; 2007b, ch. 41), Ladevèze and
Muizon (2007, ch. 157).
40. Secondary foramen ovale: absent (0) or present
(1). References: Archer (1976), Gaudin et al.
(1996), Wroe (1997), Wroe et al. (2000, ch. 51, 52,
53), Ladevèze (2004, ch. 31; 2007b, ch. 42),
Ladevèze and Muizon (2007, ch. 158).
41. Alisphenoid tympanic process: absent (0) or
present (1). References: Rougier et al. (1998, ch.
121), Wible et al. (2001, ch. 121), Ladevèze
(2004, ch. 32; 2007b, ch. 43), Ladevèze and
Muizon (2007, ch. 159).
42. Alisphenoid tympanic process well developed
and encloses a hypotympanic sinus: absent (0) or
present (1). References: Springer et al. (1997, ch.
62), Wroe et al. (2000, ch. 57), Luo et al. (2002,
ch. 222), Horovitz and Sánchez-Villagra (2003,
ch. 185), Ladevèze (2007b, ch. 44), Ladevèze and
Muizon (2007, ch. 160).
43. Alisphenoid tympanic process: does not cover the
alisphenoid hypotympanic sinus in external
view (0) or extends posteriorly to reach posterior
limit of the alisphenoid hypotympanic sinus in
ventral view (1). References: Springer et al.
(1997, ch. 62), Wroe et al. (2000, ch. 57), Luo
et al. (2002, ch. 222), Horovitz and SánchezVillagra (2003, ch. 185), Ladevèze (2007b, ch.
45), Ladevèze and Muizon (2007, ch. 161).
44. Hypotympanic sinus: absent (0), formed by squamosal, petrosal, and alisphenoid (1), or formed
by alisphenoid and petrosal or present wholly
within alisphenoid (2). References: Muizon
(1994), Rougier et al. (1998, ch. 140), Wroe et al.
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
(2000, ch. 56), Wible et al. (2001, ch. 140), Luo
et al. (2002, ch. 223), Ladevèze (2007b, ch. 46).
Transpromontorial sulcus: present (0) or absent
(1). References: Wible (1986), Rougier et al.
(1998, ch. 146), Wible et al. (2001, ch. 146), Luo
et al. (2002, ch. 220), Ladevèze (2004, ch. 9;
2007b, ch. 39), Ladevèze and Muizon (2007, ch.
154).
Sulcus for stapedial artery: present (0) or absent
(1). References: Wible (1987), Wible (1990, ch.
16), Rougier et al. (1998, ch. 147), Wible et al.
(2001, ch. 147), Luo et al. (2002, ch. 219), Horovitz and Sánchez-Villagra (2003, ch. 221),
Ladevèze (2004, ch. 35; 2007b, ch. 40), Ladevèze
and Muizon (2007, ch. 155).
Tubal foramen just posterior and ventral to the
foramen ovale: absent (0) or present (1). References: Wroe (1997, 1999), Wroe et al. (2000, ch.
70), Ladevèze (2004, ch. 36; 2007b, ch. 47),
Ladevèze and Muizon (2007, ch. 167).
Tympanic cavity partially or entirely enclosed by
bony structures (i.e, auditory bulla): absent (0)
or present (1). Reference: Ladevèze (2007b, ch.
48).
Auditory bulla formed by: alisphenoid (0),
alisphenoid and petrosal (1), or fused alisphenoid and petrosal (2). Reference: Ladevèze
(2007b, ch. 49).
Transverse canal: absent (0) or present (1). References: Archer (1976), Wroe (1999), Rougier
et al. (1998, ch. 104), Muizon (1999), ch. 8), Wroe
et al. (2000, ch. 63), Wible et al. (2001, ch. 104),
Sánchez-Villagra and Wible (2002, ch. 1), Horovitz and Sánchez-Villagra (2003, ch. 196, 197),
Ladevèze (2007b, ch. 50), Ladevèze and Muizon
(2007, ch. 168).
Squamosal epitympanic sinus: absent (0) or
present (1). References: Archer (1976), Wroe
(1999), Wroe et al. (1998), Wroe et al. (2000, ch.
55), Ladevèze (2004, ch. 38; 2007b, ch. 51),
Ladevèze and Muizon (2007, ch. 169).
Medial process of squamosal in tympanic cavity:
absent (0) or present (1). References: Muizon
et al. (1997), Muizon (1999), ch. 1), Rougier et al.
(1998, ch. 141), Wroe et al. (2000, ch. 59), Wible
et al. (2001, ch. 141), Horovitz and SánchezVillagra (2003, ch. 199), Ladevèze (2007b, ch.
52), Ladevèze and Muizon (2007, ch. 170).
Jugular foramen very large, at least three times
larger than the fenestra cochleae: absent (0) or
present (1). References: Rougier et al. (1996a, b,
ch. 14), Rougier et al. (1998, ch. 149), Wible et al.
(2001, ch. 149), Ladevèze (2007b, ch. 53),
Ladevèze and Muizon (2007, ch. 171).
Jugular foramen: confluent with opening for
inferior petrosal sinus (0) or separated from
777
opening for inferior petrosal sinus (1). References: Rougier et al. (1998, ch. 150), Wible et al.
(2001, ch. 150), Ladevèze (2007, ch. 54),
Ladevèze and Muizon (2007, ch. 172).
55. Mastoid-squamosal fusion: absent (0) or present
(1). References: Rougier et al. (1998, ch. 154),
Wible et al. (2001, ch. 154), Ladevèze (2007b, ch.
54).
56. Cochlear coiling: absent or less than 300° (0), or
fully coiled (more than 360°) (1). References:
Rougier et al. (1998, ch. 129), Wible et al. (2001,
ch. 129), Luo et al. (2002, ch. 194), Horovitz and
Sánchez-Villagra (2003, ch. 222), Ladevèze
(2007b, ch. 55), Ladevèze and Muizon (2007, ch.
156).
General Dentition
57. Number of premolars: 5 (0), 4 (1), 3 (2), or less
than 3 (3). References: Rougier et al. (1998, ch.
1), Wible et al. (2001, ch. 1), Ladevèze and
Muizon (2007, ch. 1). Ordered.
58. Premolar cusp form: sharp, uninflated (0) or
inflated, with apical wear strongly developed.
References: Wible et al. (2001, ch. 2).
59. Tall, trenchant premolar: in last PM position (0),
in penultimate PM position (1), or absent (2)
(upper dentition considered when possible). References: Rougier et al. (1998, ch. 3), Wible et al.
(2001, ch. 3), Luo et al. (2003, ch.38), Ladevèze
and Muizon (2007, ch. 2).
60. Number of molars: 4 (0), 3 (1), or none (2).
References: Springer et al. (1997, ch. 4), Rougier
et al. (1998, ch. 4), Wible et al. (2001, ch. 4),
Horovitz and Sánchez-Villagra (2003, ch. 152),
Ladevèze and Muizon (2007, ch. 3). Ordered.
61. Molar cusp form: sharp, gracile (0), inflated,
robust (1), or low and robust, molars bunodont
(2).
62. Size of molars increasing posteriorly: absent (0),
moderate posterior increase (1), or marked posterior increase (2) (< jaw: all M, > jaw: all bust
the last). References: Marshall & KielanJaworowska (1992), Rougier et al. (1998, ch. 6),
Wible et al. (2001, ch. 6), Ladevèze and Muizon
(2007, ch. 4).
63. Number of postcanine tooth family: 8 or more
(0), 7 (1), or < 7 (2). References: Rougier et al.
(1998, ch. 7), Wible et al. (2001, ch. 7), Ladevèze
and Muizon (2007, ch. 5). Ordered.
Upper Incisors
64. Number of upper incisors: 5 (0), less than 5 (1),
or none (2). References: Springer et al. (1997, ch.
1), Rougier et al. (1998, ch. 8), Wroe et al. (2000,
ch. 1), Wible et al. (2001, ch. 8), Horovitz and
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
778
65.
66.
67.
68.
S. LADEVÈZE and C. DE MUIZON
Sánchez-Villagra (2003, ch. 150), Ladevèze and
Muizon (2007, ch. 6).
Shape of upper incisors: peg shaped (0), spatulate (1). References: Reig, Kirsch & Marshall
(1987, ch. 20), Springer et al. (1997, ch. 29),
Wroe et al. (2000, ch. 2), Horovitz and SánchezVillagra (2003, ch. 165), Ladevèze and Muizon
(2007, ch. 7).
Upper incisor arcade shape: U-shape (0), broad
V-shape (1), long, narrow V-shape (2). References: Springer et al. (1997, ch. 25), Horovitz
and Sánchez-Villagra (2003, ch. 161), Ladevèze
and Muizon (2007, ch. 8). Ordered.
First upper incisor enlarged, anteriorly projecting, separated from I2 by small diastema (0),
subequal or smaller than remaining incisors,
without diastema (1), or lost (2). References:
Muizon et al. (1997), Rougier et al. (1998, ch. 9),
Wible et al. (2001, ch. 9), Ladevèze and Muizon
(2007, ch. 9).
Size of upper I3 vs. I2: I3>I2 (0), I3 = I2 (1), I3<I2
(2). References: Springer et al. (1997, ch. 30),
Horovitz and Sánchez-Villagra (2003, ch. 166),
Ladevèze and Muizon (2007, ch. 10). Ordered.
Upper Premolars
69. First upper premolar with diastema: absent (0)
or present (1). References: Rougier et al. (1998,
ch. 11), Wible et al. (2001, ch. 11), Luo et al.
(2003, ch.39), Ladevèze and Muizon (2007, ch.
11).
70. First upper premolar procumbent: absent (0) or
present (1). References: Rougier et al. (1998, ch.
11), Wible et al. (2001, ch. 11), Luo et al. (2003,
ch.39), Ladevèze and Muizon (2007, ch. 12).
71. Posterolingual cuspule on the last upper premolar: absent (0) or present (1). Reference: Wroe
et al. (2000, ch. 7), Ladevèze and Muizon (2007,
ch. 13).
72. Shape of the last upper premolar: transversally
compressed in occlusal view (0) or bulbous and
ovate in occlusal view (1). References: Reig et al.
(1987, ch. 24), Wroe et al. (2000, ch. 6), Ladevèze
and Muizon (2007, ch. 14).
Upper Molars
73. Third upper molar proportions: as long as wide
(0), longer than wide (1), or wider than long (2).
74. Upper molar outline in occlusal view: triangular
or semi-triangular (0), or rectangular or semisquare (1). References: Springer et al. (1997, ch.
5), Horovitz and Sánchez-Villagra (2003, ch.
153), Ladevèze and Muizon (2007, ch. 15).
75. Relative sizes of M2 (antepenultimate molar)
and M3 (penultimate molar): M2 longer or subequal in length to M3 (0) or M2 shorter than M3
76.
77.
78.
79.
80.
81.
82.
83.
84.
85.
(1). References: Marshall (1987, ch. 3), Reig
et al. (1987, ch. 3), Ladevèze and Muizon (2007,
ch. 16).
Last upper molar width relative to penultimate
upper molar: subequal (0) or smaller (1). References: Rougier et al. (1998, ch. 41), Wible et al.
(2001, ch. 41), Ladevèze and Muizon (2007, ch.
17).
Stylar shelf uniform in width (0), slightly
reduced labial to paracone (1), strongly reduced
labial to paracone (2), or strongly reduced or
absent (3) (penultimate molar considered when
present). References: Rougier et al. (1998, ch.
17), Wible et al. (2001, ch. 17), Ladevèze and
Muizon (2007, ch. 18).
Postmetacrista weakly developed (0) or strongly
developed, with a large metastylar area on
upper molars, and with paraconid enlarged and
metaconid reduced on lower molars (1). References: Cifelli (1993), Rougier et al. (1998, ch. 18,
32), Wible et al. (2001, ch. 18, 32), Ladevèze and
Muizon (2007, ch. 19).
Deep ectoflexus present on one or more teeth (0),
or upper molars without a distinct ectoflexus (1).
Reference: Voss & Jansa (2003, ch. 59),
Ladevèze and Muizon (2007, ch. 20).
Parastylar hook: absent (0), or present (1).
Stylar cusp A distinct but smaller than B (0),
subequal to larger than B (1), or very small to
indistinct (2) (penultimate molar considered
when available). References: Rougier et al.
(1998, ch. 20), Wroe et al. (2000, ch. 16), Wible
et al. (2001, ch. 20), Ladevèze and Muizon (2007,
ch. 21).
Stylar cusp B small (0), vestigial to absent (1),
large but less than paracone (2), larger than
paracone (3) (penultimate upper molar considered when available). References: Rougier et al.
(1998, ch. 22), Wroe et al. (2000, ch. 17), Wible
et al. (2001, ch. 22), Ladevèze and Muizon (2007,
ch. 22).
Stylar cusp C on penultimate upper molar:
absent (0) or present (1). References: Rougier
et al. (1998, ch. 23), Wroe et al. (2000, ch. 21),
Wible et al. (2001, ch. 23), Ladevèze and Muizon
(2007, ch. 23).
Stylar cusp D on penultimate upper molar:
present (0) or absent (1). Reference: Wroe et al.
(2000, ch. 18), Ladevèze and Muizon (2007, ch.
24).
Relative size of stylar cusp B and stylar cusp D
on M2: B smaller or subequal to D (0), or B
larger than D (1). References: Rougier et al.
(1998, ch. 24), Wroe et al. (2000, ch. 19), Wible
et al. (2001, ch. 24), Ladevèze and Muizon (2007,
ch. 25).
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
86. Stylar cusp E: absent or poorly developed (0) or
well developed (1). References: Rougier et al.
(1998, ch. 25), Wible et al. (2001, ch. 25), Luo
et al. (2003, ch. 110), Ladevèze and Muizon
(2007, ch. 26).
87. Position of the stylar cusp E relative to cusp D
or ‘D-position’: E more lingual to D or
‘D-position’ (0), or E distal to or at same level as
D or ‘D-position’ (1). References: Rougier et al.
(1998, ch. 25), Wible et al. (2001, ch. 25), Luo
et al. (2003, ch. 110), Ladevèze and Muizon
(2007, ch. 27).
88. Metacone size relative to paracone: noticeably
smaller (0), subequal (2), or noticeably larger (3)
(second upper molar considered when available).
References: Reig et al. (1987, ch. 5), Springer
et al. (1997, ch. 7), Rougier et al. (1998, ch. 27),
Asher (1999, ch. 41), Wroe et al. (2000, ch. 8),
Wible et al. (2001, ch. 27), Luo et al. (2002, ch.
81), Horovitz and Sánchez-Villagra (2003, ch.
155), Ladevèze and Muizon (2007, ch. 28).
89. Metacone position relative to paracone: labial
(0), approximately at same level (1), or lingual
(2). References: Rougier et al. (1998, ch. 28),
Wible et al. (2001, ch. 28), Ladevèze and Muizon
(2007, ch. 29).
90. Metacone and paracone shape: conical, with
labial face concave (0), or not conical, with labial
face flat or convex (1). References: Rougier et al.
(1998, ch. 29), Wible et al. (2001, ch. 23),
Ladevèze and Muizon (2007, ch. 30).
91. Metacone and paracone bases: adjoined (0) or
separated (1). References: Rougier et al. (1998,
ch. 30), Wible et al. (2001, ch. 30), Ladevèze and
Muizon (2007, ch. 31).
92. Metacone on last upper molar: present and distinct from metastylar corner of tooth (0), present
but not distinct from metastylar corner of tooth
(1), or absent (2). Reference: Wroe et al. (2000,
ch. 9), Ladevèze and Muizon (2007, ch. 32).
93. Centrocrista: straight (0) or V-shaped (1). References: Reig et al. (1987, ch. 1), Springer et al.
(1997, ch. 8), Rougier et al. (1998, ch.31), Wroe
et al. (2000, ch. 10), Wible et al. (2001, ch. 31),
Luo et al. (2002, ch. 82), Horovitz and SánchezVillagra (2003, ch. 156), Ladevèze and Muizon
(2007, ch. 33).
94. Preparacrista: moderately to well-developed (0),
short and blade-like (1), or short, rounded and
virtually absent (2). References: Marshall (1987,
ch. 8).
95. Orientation of preparacrista on M1: forms a
nearly perpendicular angle with respect to the
long axis of the tooth (0), or oblique relative to
the long axis of the tooth (1). References: Wroe
et al. (2000, ch. 12).
779
96. Relative lengths of M3 and M4 preparacristae
(penultimate and ultimate upper molars): M4
preparacrista shorter than or equal to that of
M3 (0), or M4 preparacrista longer than that of
M3 (1). Reference: Wroe et al. (2000, ch. 13),
Ladevèze and Muizon (2007, ch. 34).
97. Conules: absent (0), small, without cristae (1), or
strong, labially placed, with wing-like cristae
(2). References: Cifelli (1993), Rougier et al.
(1998, ch. 35), Wible et al. (2001, ch. 35),
Ladevèze and Muizon (2007, ch. 35).
98. Hypocone: absent (0), or present (1).
99. Trigon basin on upper molars: absent (0) or
present (1). References: Reig et al. (1987, ch. 10),
Rougier et al. (1998, ch. 36), Wible et al. (2001,
ch. 36), Ladevèze and Muizon (2007, ch. 36).
100. Protocone on upper molars: small, anteroposteriorly compressed (0), somewhat expanded
anteroposteriorly (1), or large with posterior
portion expanded (2). References: Reig et al.
(1987, ch. 10), Rougier et al. (1998, ch. 36), Wible
et al. (2001, ch. 36), Ladevèze and Muizon (2007,
ch. 37).
101. Procumbent protocone: absent (0) or present (1).
References: Rougier et al. (1998, ch. 37), Wible
et al. (2001, ch. 37), Ladevèze and Muizon (2007,
ch. 38).
102. Protocone height: low (0) or tall, approaching
para- and/or metacone height (1). References:
Rougier et al. (1998, ch. 38), Wible et al. (2001,
ch. 38), Ladevèze and Muizon (2007, ch.
39).
103. Paracingulum: absent (0), interrupted between
stylar margin and paraconule (1), or continuous
(2) (penultimate molar considered when available). References: Rougier et al. (1998, ch. 26),
Wible et al. (2001, ch. 26), Ladevèze and Muizon
(2007, ch. 40).
104. Preprotocrista does not (0) or does (1) extend
labially past base of paracone and form a paracingulum (double rank prevallum/postvallid
shearing). References: Cifelli (1993), Rougier
et al. (1998, ch. 33), Wible et al. (2001, ch. 33),
Ladevèze and Muizon (2007, ch. 41).
105. Postprotocrista does not (0) or does (1) extend
labially past base of metacone and form a metacingulum (double rank prevallum/postvallid
shearing). References: Cifelli (1993), Rougier
et al. (1998, ch. 34), Wible et al. (2001, ch. 34),
Ladevèze and Muizon (2007, ch. 42).
106. Precingulum on M1-3: absent (0) or present (1).
References: Rougier et al. (1998, ch. 39), Wroe
et al. (2000, ch. 24), Wible et al. (2001, ch. 39),
Ladevèze and Muizon (2007, ch. 43).
107. Postcingulum on M1-3: absent (0) or present (1).
References: Rougier et al. (1998, ch. 39), Wroe
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
780
S. LADEVÈZE and C. DE MUIZON
et al. (2000, ch. 25), Wible et al. (2001, ch. 39),
Ladevèze and Muizon (2007, ch. 44).
Lower Incisors
108. Number of lower incisors: 4 (0), less than 4 (1).
References: Springer et al. (1997, ch. 2), Rougier
et al. (1998, ch. 42), Wroe et al. (2000, ch. 26),
Wible et al. (2001, ch. 42), Luo et al. (2002, ch.
105), Horovitz and Sánchez-Villagra (2003, ch.
151), Ladevèze and Muizon (2007, ch. 45).
109. Staggered lower incisor (i3 of Hershkovitz,
1982): absent (0) or present (1). References:
Rougier et al. (1998, ch. 43), Wroe et al. (2000,
ch. 29), Wible et al. (2001, ch. 43), Horovitz and
Sánchez-Villagra (2003, ch. 172), Ladevèze and
Muizon (2007, ch. 46).
110. Bilobed i3: absent (0) or present (1). Reference:
Wroe et al. (2000, ch. 27), Ladevèze and Muizon
(2007, ch. 47).
111. Lower incisors and/or canines semi procumbent
or procumbent (i.e., forming an angle with the
jaw of 45° at least): absent (0) or present (1).
References: Springer et al. (1997, ch. 33), Luo
et al. (2002, p. 115), Horovitz and SánchezVillagra, 2003, ch. 167), Ladevèze and Muizon
(2007, ch. 48).
Lower Canine
112. Fossa for the lower canine: absent (0), reduced to
a small cupule (1), or large (2). References:
Rougier et al. (1998, ch. 81), Wroe et al. (2000,
ch. 46), Wible et al. (2001, ch. 81), Ladevèze and
Muizon (2007, ch. 49).
113. Anterolateral process of the maxilla: wholly
forms the border of the fossa for the lower
canine (0), partially forms the border of the fossa
for the lower canine (i.e., with premaxillae) (1),
or absent (2). References: Rougier et al. (1998,
ch. 81), Wroe et al. (2000, ch. 46), Wible et al.
(2001, ch. 81), Ladevèze and Muizon (2007, ch.
50).
Lower Premolars
114. First lower premolar oriented in line with jaw
axis (0) or oblique (1). References: Marshall
(1987, ch. 16), Rougier et al. (1998, ch. 45), Wible
et al. (2001, ch. 45), Ladevèze and Muizon (2007,
ch. 51).
115. Second lower premolar: smaller than 3rd premolar (0), subequal in size (1) or larger than 3rd
premolar (2). References: Marshall (1987, ch.
14-15), Rougier et al. (1998, ch. 46), Wroe et al.
(2000, ch. 43), Wible et al. (2001, ch. 46),
Ladevèze and Muizon (2007, ch. 52).
116. Shape of p3 (ultimate premolar): trenchant and
narrow transversely (0), somewhat inflated and
ovoid in occlusal view (1), enormous, bulbous,
and has a distinct crushing function (2). Reference: Marshall (1987, ch. 13), Ladevèze and
Muizon (2007, ch. 53).
Lower Molars
117. Trigonid configuration on m1-3: open, i.e. the
angle formed by protocristid and paracristid
approximates 90° (0), more acute, i.e. the angle
formed by protocristid and paracristid approximates 45° (1), or anteroposteriorly compressed,
i.e. protocristid and paracristid are subparallel
(2). References: Cifelli (1993), Rougier et al.
(1998, ch. 48), Wible et al. (2001, ch. 48),
Ladevèze and Muizon (2007, ch. 54).
118. Shape of m2-4 trigonids: wider than long (0), or
as wide as long (1), or longer than wide (2).
Reference: Reig et al. (1987, ch. 13), Ladevèze
and Muizon (2007, ch. 55).
119. Number of cusps on m4 talonid: 3 cusps (0), 2
cusps (1), or 1 cusp (2). Reference: Wroe et al.
(2000, ch. 44), Ladevèze and Muizon (2007,
ch. 56).
120. Relative sizes and shapes of m3 and m4 talonids: talonid of m4 similar in size and shape to
that of m3 (0), or talonid of m4 reduced and
narrower than that of m3 (1). Reference: Reig
et al. (1987, ch. 16), Ladevèze and Muizon (2007,
ch. 57).
121. Talonid width relative to trigonid on m1-3: very
narrower, subequal in width to base of metaconid, and at the lingual half or 2/3 of the
protocristid (0), narrower (1), or subequal to
wider (2). References: Springer et al. (1997, ch.
13), Rougier et al. (1998, ch. 50), Wible et al.
(2001, ch. 50), Luo et al. (2002, ch. 63), Horovitz
and Sánchez-Villagra (2003, ch. 158), Ladevèze
and Muizon (2007, ch. 58). Ordered.
122. Trigonid noticeably taller than talonid: absent
(0) or present (1), Ladevèze and Muizon (2007,
ch. 59).
123. Anterior point of termination of the cristid
obliqua in m3 with respect to carnassial notch
formed by postprotocristid and metacristid:
beneath carnassial notch (0), lingual to carnassial notch (1), labial to carnassial notch (2).
References: Archer (1976b), Cifelli (1993),
Springer et al. (1997, ch. 23), Rougier et al.
(1998, ch. 51), Godthelp, Wroe & Archer (1999),
Wroe et al. (2000, ch. 40), Wible et al. (2001, ch.
51), Luo et al. (2002, ch. 47), Horovitz and
Sánchez-Villagra (2003, ch. 160), Ladevèze and
Muizon (2007, ch. 60). Ordered.
124. Hypoconulid: absent (0), in median position (1),
or lingually displaced, being closer to entoconid
(2). References: Springer et al. (1997, ch. 35),
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
125.
126.
127.
128.
129.
130.
131.
132.
133.
134.
135.
Rougier et al. (1998, ch. 52), Wroe et al. (2000,
ch. 28), Wible et al. (2001, ch. 52), Horovitz and
Sánchez-Villagra (2003, ch.168), Ladevèze and
Muizon (2007, ch. 61). Ordered.
Hypoconulid of last molar: short and erect (0) or
tall and sharply recurved (1). References:
Rougier et al. (1998, ch. 53), Wible et al. (2001,
ch. 53), Ladevèze and Muizon (2007, ch. 62).
Hypoconulid notch: present (0) or absent (1).
Reference: Wroe et al. (2000, ch. 30), Ladevèze
and Muizon (2007, ch. 63).
Entoconid: absent (0), smaller than (1), or subequal to larger than (2) hypoconid and/or hypoconulid. References: Marshall (1987, ch. 12),
Rougier et al. (1998, ch. 54), Wroe et al. (2000,
ch. 41), Wible et al. (2001, ch. 54), Ladevèze and
Muizon (2007, ch. 64).
Entoconid shape: conical (0) or rather bladed
and forming a prominent wall lingual to the
talonid basin (1). Reference: Springer et al.
(1997, ch. 20), Ladevèze and Muizon (2007, ch.
65).
Entoconid and metaconid relative positions:
distant (0), close (1), or entoconid at an extreme
posterior position (2), Ladevèze and Muizon
(2007, ch. 66).
Hypoconid: small (0), large and labially salient
(1), large but not salient labially (2). Reference:
Ladevèze and Muizon (2007, ch. 67).
Entocristid: weakly developed (0), welldeveloped and sharp (1). Reference: Ladevèze
and Muizon (2007, ch. 68).
Posthypocristid on m2: transversal (0) or not (1)
with respect to long axis of the tooth (penultimate inferior molar considered when available).
Reference: Ladevèze and Muizon (2007, ch. 69).
Labial postcingulid: absent (0) or present (1).
References: Cifelli (1993), Rougier et al. (1998,
ch. 55), Wroe et al. (2000, ch. 36), Wible et al.
(2001, ch. 55), Ladevèze and Muizon (2007, ch.
70).
Postcingulid in m4: present (0) or absent (1).
Reference: Wroe et al. (2000, ch. 37), Ladevèze
and Muizon (2007, ch. 71).
Well-developed sulcus formed by anterior cingulid: absent (0) or present (1). References: Reig
et al. (1987, ch. 19), Wroe et al. (2000, ch. 31),
Ladevèze and Muizon (2007, ch. 72).
781
136. Metaconid and paraconid positions: metaconid
at extreme lingual margin (0) or aligned with
paraconid (1). References: Rougier et al. (1998,
ch. 56), Wible et al. (2001, ch. 56), Ladevèze and
Muizon (2007, ch. 73).
137. Protocristid orientation to lower jaw axis:
oblique (0) or transverse (1). References: Rougier
et al. (1998, ch. 57), Wroe et al. (2000, ch. 35),
Wible et al. (2001, ch. 57), Ladevèze and Muizon
(2007, ch. 74).
138. Size of paraconid relative to that of protoconid in
m1: subequal (0), lower (1), or greatly reduced
(2). References: Rougier et al. (1998, ch. 58),
Wroe et al. (2000, ch. 34), Wible et al. (2001, ch.
58), Ladevèze and Muizon (2007, ch. 75).
139. Protoconid height: tallest cusp on trigonid (0) or
subequal to para- and/or metaconid (1). References: Reig et al. (1987, ch. 18), Rougier et al.
(1998, ch. 59), Wible et al. (2001, ch. 59), Luo
et al. (2003, ch. 57), Ladevèze and Muizon (2007,
ch. 76).
140. Metaconid: absent (0) or present (1). Reference:
Wroe et al. (2000, ch. 33), Ladevèze and Muizon
(2007, ch. 77).
141. Relative height of metaconid and paraconid:
metaconid lower than paraconid (0), subequal
(1), or metaconid taller than paraconid (2)
(molars other than the first considered when
available). References: Reig et al. (1987, ch. 17),
Rougier et al. (1998, ch. 60), Wible et al. (2001,
ch. 60), Luo et al. (2003, ch. 58), Ladevèze and
Muizon (2007, ch. 78).
142. Size of metaconid on m1 relative to that of the
other molars: not reduced (0) or reduced (1).
Reference: Wroe et al. (2000, ch. 32), Ladevèze
and Muizon (2007, ch. 79).
143. Relative lengths of para- and protocristids: subequal (0), paracristid > protocristid (1), or protocristid >paracristid (2), Ladevèze and Muizon
(2007, ch. 80).
144. Para- and protocristids: rounded (0), or bladed
and sharp (1). Reference: Ladevèze and Muizon
(2007, ch. 81).
145. Last lower molar size relative to penultimate
molar: subequal (0) or smaller or lost (1). References: Reig et al. (1987, ch. 14), Cifelli (1993),
Rougier et al. (1998, ch. 61), Wible et al. (2001,
ch. 6), Ladevèze and Muizon (2007, ch. 82).
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
782
S. LADEVÈZE and C. DE MUIZON
APPENDIX 2
Data matrix showing the distribution of 56 petrosal and basicranial and 89 dental characters amongst 44 taxa
Vincelestes
0000?00000 00-0000-00 00000-0000 -000000000 00-00000-0 0000003001 1021000100
2000110110 0201100000 0000000100 12000102-1 0010?10–1 -001000101 10001
Ornithorhynchus
0010000110 00-0000-00 02010-0-00 -001001000 00-01000-0 00-000???? ??????????
?????????? ?????????? ?????????? ?????????? ?????????? ?????????? ?????
Tachyglossus
10-0000210 00-1000-00 02010-0-00 -001001000 00-11100-0 00-000???? ??????????
?????????? ?????????? ?????????? ?????????? ?????????? ?????????? ?????
Prokennalestes
01?0010110 0100000-00 00????0001 0000?000?? ???0000??? ??0?010011 000???????
000010-010 0001001011 00211000?? ??01001100 1111101002 1001001101 20?00
Deltatheridium
1100020100 0101000-0- 01?1100000 -0100000?? ???0110??? ??01012000 02110?1?11
2001-10110 0200001010 0021000110 12000012?1 01110?100? ?001?10101 01111
Didelphodon
12?0020000 111100000? 00001001?? ?011?000?? ???1110??? ?0?1112120 021???????
C200110220 1102?02012 11210001?? ???1022000 2122002002 0011011011 00110
Pediomys
12?0021000 1111000-02 0100100101 00110000?? ???B110??? ???1012000 011???????
00A0010220 1102102012 1121100??? ???1011001 2122002001 1110011201 20110
Mayulestes
?1?0?????1 0101100-0? 0111100011 01-?????10 00-11100-0 0111012000 0110000011
1000110220 1000012010 1021000010 1211001201 1102101002 0011101101 11010
Pucadelphys
1B10010011 1101110-01 010B100011 0010A11A10 00-01100-0 0111012000 0110001111
1210111221 1011012012 1111000010 1201001001 2122102002 1011011111 20000
Andinodelphys
1B00010111 1101110-01 0101100011 0010011110 00-01100-1 0111012000 0110000011
0210111221 1011012012 1121000010 1201001001 2122101002 0010011111 20000
Didelphis
1210021110 0101001102 0112100011 1011000011 1102110101 0001012000 0110010111
2210111221 101B010011 1121000010 0200211201 2122002101 0101111101 20100
Marmosa
1210021010 0101001102 0112100011 101100001A 1102110101 0001012000 0110010111
2210111221 1011010011 1121000010 0200201201 2122002101 0101111101 20100
Metachirus
1210021110 0101001102 0112100011 1011000011 1102110101 0000012000 0110010111
2200111221 1011010011 1121000010 0200201201 2122002101 0101111101 20100
Caenolestes
0211020010 0101001101 0103110001 1010101110 1102110101 0000012000 0011120210
230000-22? 110–?2112 1020000100 1021001011 2022002121 1000111011 21211
Dromiciops
1211121110 0121001211 11031110?1 21-?1?1120 111211112A 0000012020 0010101100
2101-0-221 1201100011 1121000000 0120011111 2122002021 1101011201 20111
Phascogale
1211121010 0101001211 1103111001 21-0111110 1112111111 1001012000 0111000200
220000-221 1110010011 1121001110 1100?01B11 2102002002 0011010101 20110
Dasycercus
12?112?010 0101001211 1103111101 ?1-????110 1112111111 1001012000 0111000200
220000-221 1110010011 1121001110 1210?0?211 2102002002 0011010101 20110
Perameles
1210021010 0101001200 0103110001 21-0001111 1112110101 1001012000 0110111110
0300010221 1112111112 1021001111 1020001011 2102012111 1101111101 20000
0100010010
??????????
??????????
–20000001
0020110101
0120101100
0020002001
0020001100
0020001001
0020001001
0120101001
0020101001
0020101001
0001013010
0020011000
00200110A0
0020112010
1001011010
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
EARLY EVOLUTION OF AUSTRALIDELPHIA IN SOUTH AMERICA
APPENDIX 2. Continued
Echymipera
?20002?210 0101001200 0?03100001 ?1-??01111 1102110101 0011012000 0111111110
1300010221 1212112112 1001001111 1020002011 2?02012111 1101111111 20?00
‘Type I’
1211020011 0101001101 0102100011 10101111?? ????11???? ?????1???? ??????????
?????????? ?????????? ?????????? ?????????? ?????????? ?????????? ?????
‘Type II’
0210020011 1101100-01 0101100011 10100000?? ????11???? ?????1???? ??????????
?????????? ?????????? ?????????? ?????????? ?????????? ?????????? ?????
‘Type III’
1211020011 0101000-02 0102100001 10100111?? ????11???? ?????1???? ??????????
?????????? ?????????? ?????????? ?????????? ?????????? ?????????? ?????
‘Type IV’
121102?010 0101000-02 01021000?1 ?1-00011?? ????11???? ?????1???? ??????????
?????????? ?????????? ?????????? ?????????? ?????????? ?????????? ?????
‘Type V’
1211020010 0101000-01 0103??0011 00101011?? ????11???? ?????1???? ??????????
?????????? ?????????? ?????????? ?????????? ?????????? ?????????? ?????
‘Type VI’
1211020011 0101001001 0102110011 10101111?? ????11???? ?????1???? ??????????
?????????? ?????????? ?????????? ?????????? ?????????? ?????????? ?????
‘Type VII’
12??020010 0101001001 01?2110001 ?01??????? ????11???? ?????1???? ??????????
?????????? ?????????? ?????????? ?????????? ?????????? ?????????? ?????
‘Type VIII’
12??020010 0101000-02 01????0001 ?01??????? ????110??? ?????1???? ??????????
?????????? ?????????? ?????????? ?????????? ?????????? ?????????? ?????
Bobbschaefferia
?????????? ?????????? ?????????? ?????????? ?????????? ??????2000 0?1???????
?????????? ?????????? ?????????? ???1012001 2122102102 1001011?01 1?111
Carolopaulacoutoia
?????????? ?????????? ?????????? ?????????? ?????????? ??????20?0 001???????
001010-221 1111?02011 1010000??? ??????1201 2102002012 1111111201 20111
Derorhynchus
?????????? ?????????? ?????????? ?????????? ?????????? ??????2??0 001???????
0310101221 11110?1012 10210????? 1??0??1101 2122102010 1111011?11 20001
Didelphopsis
?????????? ?????????? ?????????? ?????????? ?????????? ??????2120 211???????
0310111221 1011002012 1121010??? ???0022001 2122002102 1101111?11 200?1
Eobrasilia
?????????? ?????????? ?????????? ?????????? ?????????? ??????2120 ????????11
?????????? ?????????? ???????1?? 1??102???? ?????????? ?????????? ?????
Epidolops
?????????? ?????????? ?????????? ?????????? ?????????? ??????2100 201???????
230010-111 1?021?2112 0121000100 1???021021 1020-12121 100110?011 10?11
Gaylordia
?????????? ?????????? ?????????? ?????????? ?????????? ??????2120 001?????10
0310011211 1?10??1011 102??????? ???0022001 1122002012 0011111?01 21111
Guggenheimia
?????????? ?????????? ?????????? ?????????? ?????????? ??????2010 001???????
?????????? ?????????? ?????????? ???1111001 20210020C2 0001011111 21011
Itaboraidelphys
?????????? ?????????? ?????????? ?????????? ?????????? ??????20?0 111???????
031000-221 1?11??2011 1021010??? ????111201 2102102001 1111111111 20110
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784
100A001000
??????????
??????????
??????????
??????????
??????????
??????????
??????????
??????????
??????????
??20011001
??10002000
??20101010
01??0?????
0121011010
?1200?0000
??????????
??201?1010
783
784
S. LADEVÈZE and C. DE MUIZON
APPENDIX 2. Continued
Marmosopsis
?????????? ?????????? ?????????? ?????????? ?????????? ??????2000 011???????
031010-221 1?100?1011 1021110??? ???01000A1 1122002101 1111011201 20110
Minusculodelphis
?????????? ?????????? ?????????? ?????????? ?????????? ??????2020 001???????
?????????? ?????????? ?????????? 1??01?0011 21210021?1 1001000?01 2?111
Mirandatherium
?????????? ?????????? ?????????? ?????????? ?????????? ??????2010 011???????
031000-221 1?110?2012 1121000??? ???1000201 2022002102 1011010201 21111
Monodelphopsis
?????????? ?????????? ?????????? ?????????? ?????????? ??????2010 001???????
?????????? ?????????? ?????????? ????101101 2102002101 1011110201 2?11?
Patene
?????????? ?????????? ?????????? ?????????? ?????????? ??????20?0 021???????
0311-0-220 0000012010 1021000??? ?????022?? 1102?02102 101?011101 0?01?
Procaroloameghinia
?????????? ?????????? ?????????? ?????????? ?????????? ??????20?0 211???????
?????????? ?????????? ?????????? ?????12001 2022002002 1001010111 20001
Protodidelphis
?????????? ?????????? ?????????? ?????????? ?????????? ??????2000 221?????1?
0300A01210 1012000012 112101A??? ???0012001 2022002001 1011110111 21001
Zeusdelphys
?????????? ?????????? ?????????? ?????????? ?????????? ?????????? 1?????????
0200000211 1??2??0011 10100?0??? ?????????? ?????????? ?????????? ?????
??20??2001
??????????
??200?1001
??????????
0010111100
??????????
0120101010
??10??00?0
? denotes non-preservation and – is a non-applicable character state. Polymorphism: A = 0 + 1, B = 1 + 2, C = 0 + 2.
SUPPORTING INFORMATION
Additional Supporting Information may be found in the online version of this article:
Appendix S1. Institutional abbreviations.
Appendix S2. List of the fossil and extant metatherians used for measurements.
Appendix S3. List of character states distribution amongst metatherians.
Please note: Wiley-Blackwell are not responsible for the content or functionality of any supporting materials
supplied by the authors. Any queries (other than missing material) should be directed to the corresponding
author for the article.
© 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 746–784