ISSN 0031�0301, Paleontological Journal, 2014, Vol. 48, No. 4, pp. 426–446. © Pleiades Publishing, Ltd., 2014.Original Russian Text © A.O. Averianov, A.V. Lopatin, 2014, published in Paleontologicheskii Zhurnal, 2014, No. 4, pp. 83–104.

426

The finding at the end of the 18th century in Aus�tralia, Tasmania, and New Guinea of Recentmonotremes, or egg�laying mammals (Monotremata)was one of the greatest zoological discoveries. In manyfeatures of physiology, reproduction, and morphology,such as oviparity, imperfect thermoregulation, pres�ence of cloaca, and the structure of chromosomes,these surprising animals are intermediate between rep�tiles and therian mammals (marsupials and placen�tals). On the other hand, extant platypus and echidnasare characterized by an extremely specialized mode oflife (swimming and feeding on benthic invertebrates inthe first and digging and feeding on soil invertebratesin the second). Such a specialization had a great effecton the monotreme structure, complicating the recog�nition of actually plesiomorphic characters inheritedfrom ancestors. Perhaps, this is the only mammalgroup, the phylogenetic position of which was treatedwithin such a wide range, from sister group of marsu�

pials (Gregory, 1947) to independent origin from“eotherapsids” (Ivakhnenko, 2009) (see also Table 1).The present study analyzes osteological and myologi�cal characters of monotremes, the development ofwhich is possible to trace in fossil material.

The following abbreviations are used below:(AMNH) American Museum of Natural History, NewYork, United States; (IVPP) Institute of Paleontologyand Paleoanthropology, Beijing, China; (NMV)Museum Victoria (former National Museum of Victo�ria), Melbourne, Australia; (ZIN) Zoological Instituteof the Russian Academy of Sciences, Saint Petersburg,Russia.

DENTITION

Pliocene and Recent echidnas lack teeth. Adultplatypuses use horn grinding pads instead of teeth and,therefore, it was long believed that platypuses also lack

On the Phylogenetic Position of Monotremes (Mammalia, Monotremata)

A. O. Averianova and A. V. Lopatinb

aZoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg, 199034 RussiaDepartment of Sedimentary Geology, Geological Faculty, St. Petersburg State University,

16 liniya VO 29, St. Petersburg, 199178 Russiae�mail: dzharakuduk@mail.ru

bBorissiak Paleontological Institute, Russian Academy of Sciences, Profsoyuznaya ul. 123, Moscow, 117997 Russia

e�mail: alopat@paleo.ruReceived March 12, 2013

Abstract—Henosferida from the Middle–Upper Jurassic of Western Gondwana is the most probable sistergroup for monotremes. They share the derived pretribosphenic structure of lower molars combined with thepresumably absent protocone on the upper molars and the plesiomorphic retention of postdentary bones andpseudangular process of the lower jaw. In addition, the two groups share the dental formula with three molarsand the position of the Meckel’s groove, which passes ventral to the mandibular foramen. In the course ofsubsequent evolution, monotremes acquired the mammalian middle ear with three auditory ossicles inde�pendently of therian mammals and multituberculates. Jurassic Laurasian Shuotheriidae are probably a sistergroup of the Gondwanian clade Henosferida + Monotremata. The Jurassic shuotheriid Pseudotribos shows agreat plesiomorphic similarity to monotremes in the structure of the pectoral girdle, with a large interclavicleimmovably connected to the clavicle. In the lineages leading to therian mammals and multituberculates, thepectoral girdle changed probably independently and in parallel in connection with the establishment of theparasagittal posture of the forelimbs (reduction of the interclavicle, mobile articulation of the interclaviclewith clavicle, reduction of the procoracoid, and development of a supraspinous fossa of the scapula) and for�mation of the mammalian middle ear with three auditory ossicles.

Keywords: Mammalia, Monotremata, origin, Mesozoic

DOI: 10.1134/S0031030114040042

“Roots of monotremes go back to primitive docodonts or,more likely, to archaic triconodonts.”

L.P. Tatarinov (2001)

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

ON THE PHYLOGENETIC POSITION OF MONOTREMES 427

teeth. True teeth were recognized in platypus only atthe end of the 19th century (Poulton, 1888, 1889;Thomas, 1890; Stewart, 1892; Wilson and Hill, 1907).This discovery gave rise to a hope that the study of den�tal morphology in this animal will be useful for resolu�tion of the complicated question of the origin ofmonotremes (Thomas, 1890, p. 131). However, theteeth of platypus have shown a rather unusual mor�phology and allowed various treatments. They wereconsidered similar to the teeth of multituberculates,xenarthrans, or desmostylians (Cope, 1888;Ameghino, 1908; Abel, 1926).

Wilson and Hill (1907) were the first to examine indetail the development of teeth in platypus. Theyfound out tooth germs of four postcanines in each jaw

and designated them as V, W, X, Y/w, x, y, z. The firstupper tooth and the last lower tooth do not have ana�logues in the opposite jaw. The teeth V and w are non�functional dental germs. There are three functioningteeth in the upper jaw (W, X, Y) and three in the man�dible (x, y, z). The authors cited assumed that W/w arethe last premolars and X, Y/x, y, z are molars. Theseteeth were regarded as “quasipermanent” (in adults,teeth are replaced by a horn beak). In addition, fiverudimentary deciduous teeth were revealed in each jawhalf; they were resorbed at an early ontogenetic stage.According to an alternative point of view, which hasbecome widely accepted, the functional teeth of platy�pus are deciduous, while problematic rudiments

Table 1. Phylogenetic relationships of Monotremata, based on morphological data (mostly works based on the cladisticprinciples are given). The composition of the clade Monotremata differs depending on authors; in the wide sense, it in�cludes the extinct taxa Ausktribosphenida, Henosferida, and Shuotheriidae

Sister group for Monotremata References

Metatheria (Gregory, 1947; Kühne, 1973, 1977)

Tribosphenida (Archer et al., 1985; Kielan�Jaworowska et al., 1987)

Multituberculata + Theria (Rowe, 1988)

Theria (Wible, 1991; Bininda�Emonds et al., 2007; Averianov and Lopatin, 2011)

Cladotheria (Kielan�Jaworowska, 1992; Rougier et al., 2007b; Gurovich, Beck, 2009)

Polytomy with Multituberculata and (Symmetrodonta, Eutriconodonta, Cladotheria)

(Wible et al., 1995)

Multituberculata, Eutriconodonta, Trechnotheria

(Rougier et al., 1996a; Rich et al., 2005a; Luo et al., 2007a; Ji et al., 2009; Luo, 2011; Meng et al., 2011)

Polytomy with Multituberculata and Cladotheria (Fox, Meng, 1997)

Multituberculata + Trechnotheria (Hu et al., 1997; Ji et al., 1999; Woodburne, 2003; Woodburne et al., 2003)

Trechnotheria (Luo et al., 2001a; Rougier et al., 2011; O’Leary et al., 2013)

Polytomy with Multituberculata and Theria (Luo et al., 2001b)

Multituberculata (Wang et al., 2001; Meng et al., 2003; Hu et al., 2005)

(Eutriconodonta + (Multituberculata + Trechnotheria)) (Ji et al., 2002; Luo et al., 2002, 2007a, 2012; Rauhut et al., 2002; Kielan�Jaworowska et al., 2004; Luo and Wible, 2005; Rowe et al., 2008; Yuan et al., 2013; Zheng et al., 2013; Zhou et al., 2013)

Polytomy with Eutriconodonta, Multituberculata and Cladotheria

(Ji et al., 2006)

Multituberculata, Symmetrodonta, Cladotheria (Li, Luo, 2006)

Polytomy with Morganucodonta, Docodonta and ((Eutriconodonta + (Multituberculata + Trechnotheria))

(Meng et al., 2006)

(Multituberculata + (Eutriconodonta + Trechnotheria)) (Luo et al., 2007b)

Multituberculata + Cladotheria (Luo, 2011; Rowe et al., 2011)

428

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

AVERIANOV, LOPATIN

belong to a “predeciduous” tooth generation (Leche,1910).

Subsequently, Green (1937) investigated the devel�opment of teeth in platypus and established the for�mula of rudimentary teeth as I0, C1, P1–2, M1–3/i1–5, c1, p1–2, m1–3. Most of the tooth germs areresorbed during embryogenesis and only three upperand three lower molars erupt and, in approximatelyone�month�old animal, they are shed and replaced byhorn plates. According to Green (1937), functionalteeth of platypus are P2, M1–2/m1–3. This formula ispresently generally accepted (Woodburne, 2003).According to an alternative point of view (Wester�gaard, 1983), these teeth are DP2–4/dp3–4, m1. Inthe Miocene platypus Obdurodon dicksoni, function�ing teeth were P1–2, M1–2/p1–2, m1–3 (Musserand Archer, 1998). The similarity of teeth with thesame position in living platypus and Obdurodon sug�gests that Green correctly treated the dental formulaof platypus. Premolars of Obdurodon probably corre�spond to P4–5/p4–5 of therian mammals and theupper premolar of platypus is P5. In all monotremeshaving teeth, the small premolars sharply differ fromlarge molars.

Green (1937) proposed that there are tooth germsof the teeth replacing the first cheek teeth in the upperand lower jaws. Based on this, Kühne (1973, 1977)revised the dental formula of platypus as P1, M1–4/p1, m1–4, because only the first of the five teeth isreplaced. He believed that the presence of four molars

and replaced premolar is a synapomorphy ofMonotremata and Marsupialia (hypothesis Marsupi�onta). Gregory (1947) adhered to the idea that thepresence of only one deciduous tooth in each jaw is ashared character of monotremes and marsupials.According to recent data, the first cheek teeth of platy�pus are not replaced during embryogenesis (Luckettand Zeller, 1989).

The postcanine formula with five premolars andthree molars could have been initial for monotremes(platypuses have lost anterior premolars and M3). Thesame formula is known for Jurassic Henosferida (Mar�tin and Rauhut, 2005; Rougier et al., 2007b),Shuotheriidae (Luo et al., 2007b), and pretribosphenicmammals, in particular, Peramus (McKenna, 1975;Prothero, 1981; Averianov et al., 2010a). Multituber�culata have only two molars in each jaw and the lastpremolars are usually larger than the first molars,sharply differing from monotremes.

As indicated above, functioning teeth were presentin Oligocene–Miocene platypuses of the genusObdurodon (Woodburne and Tedford, 1975; Archeret al., 1992, 1993; Musser and Archer, 1998). The dis�covery of the Early Cretaceous monotreme Steropodonin Australia (Archer et al., 1985), similar but moreprimitive in dental structure than Obdurodon, allowedthe characters of dentition to be used for reconstruc�tion of the phylogenetic position of monotremes.Archer et al. (1985) treated the teeth of Steropodon astribosphenic and associated the origin of monotremeswith Aegialodontidae, the earliest known tribosphenicmammals. Kielan�Jaworowska et al. (1987) believethat the teeth of Steropodon are not tribosphenic andmonotremes evolved from more primitive pretri�bosphenic mammals, such as the Early CretaceousPeramus. Woodburne (2003) has recently come to asimilar conclusion concerning the origin ofmonotremes from pretribosphenic mammals. Tatar�inov (2001) and Agadjanian (2003), on the contrary,think that monotremes are similar in the structuraltooth pattern to docodonts and, hence, phylogeneti�cally related to this group. Pascual and Goin (2001)came to a similar conclusion.

It is rather difficult to compare the teeth of Sterop�odon and docodonts (Fig. 1). The similarity in lowermolars is restricted to three characters: (1) crowns areexpanded transversely; (2) labial cusps are higher thanlingual cusps; and (3) the highest labial cusp is con�nected by transverse crests to two lingual cusps. How�ever, in docodonts, this high cusp is posterior of twolabial cusps, whereas that of Steropodon is anterior. Itis important that, in docodonts, the labial edge of thecrown is closed by a longitudinal crest connecting thecusps a, b, and d, whereas in Steropodon, the valleybetween labial cusps is open labially (Fig. 1). Althoughthe molars of docodonts are externally similar to theteeth of tribosphenic mammals (see Butler, 1988), they

a= protoconid

d = hypooconid

hypooconulid

entoconidb c

= paraconid = metaconid

Tribosphenida

B = stylocone

metastyle

С = metacone

protocone

А = paracone b = paraconidc = metaconid

entoconid

a

b c

d

BC

A X Yg

Holotheria

Morganucodonta

Docodonta

a

a

b

b

c

c

dB

B

a = protoconid d = hypooconid

C

C

A

A

g

Labialside

Anteriorside

Fig. 1. Structural pattern of the main molar types of mam�mals (black color shows lower teeth of the right side, graycolor shows upper teeth of the left side). The main toothcusps are designated by capital (A, B, C) and lowercase(a, b, c, d) letters for the upper and lower teeth, respec�tively. At the top right of the figure, the lower molar of theEarly Cretaceous monotreme Steropodon galmani Archeret al., 1985 is shown (after Kielan�Jaworowska et al., 2004,text�fig. 6.5C1, reverse).

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

ON THE PHYLOGENETIC POSITION OF MONOTREMES 429

occlude differently. In docodonts, food particles wereinitially cut by longitudinal crests of crowns (B–A–C inthe upper tooth and b–a–d in the lower tooth) and, atthe moment of the maximum occlusion, the highestlabial cusp of the upper tooth (A) is located labial tothe lower teeth (Jenkins, 1969, text�fig. 3; Butler,1988, text�figs. 5, 6; Pfretzschner et al., 2005, text�fig. 5). In pretribosphenic and early tribosphenicmammals, food particles were initially cut by trans�verse crests of crowns (preparacrista–paracristid andpostmetacrista–protocristid) and, at the maximumocclusion, the highest labial cusp (paracone or cusp A)enters the hypoflexid, a widely labially open embra�sure between the talonid and trigonid (see, e.g.,Crompton, 1971; Fox, 1975; Crompton and Kielan�Jaworowska, 1978; Kielan�Jaworowska et al., 1987).Tatarinov (2001, p. 87) incorrectly proposed that thisspace is occupied by the protocone.

The lower molar structure of Steropodon corre�sponds to the pretribosphenic pattern, which isobserved, for example, in Peramus (Kielan�Jaworowska et al., 1987; Woodburne, 2003); foodobjects were cut by transverse rather than longitudinalcrests of the crown; the teeth have a three�cuspid trig�onid, two�cuspid talonid without a basin, and widevalley between the trigonid and talonid bordered bythe protocristid, a rudiment of the distal metacristid(near the metaconid apex), and cristid obliqua. Thepresence in Steropodon of a wide hypoflexid, rudimen�tary distal metacristid, and underdeveloped cristidobliqua strongly suggests that monotremes evolvedfrom pretribosphenic mammals which lacked a proto�cone on the upper teeth. In monotremes, the proto�cone has not developed (Woodburne, 2003; Davis,2011); therefore, their teeth cannot be regarded as tri�bosphenic. Pascual and Goin (2001; see also Pascualet al., 2002) deny the presence of a hypoflexid in Ste�ropodon, because respective region is shallower andhas an enamel bottom, i.e., a true incisure is absent.However, a decrease in depth of the hypoflexid andexpansion of the crown between the trigonid and tal�onid are possible to explain by a significant decrease inheight of the paracone in monotremes compared toPeramus, which is evident in Obdurodon and Pale�ocene Monotrematum (Pascual et al., 2002).

The pseudotribosphenic teeth with the talonidpositioned anterior to the trigonid are observed notonly in docodonts (Averianov et al., 2010b), but also inShuotheriidae (Luo et al., 2007b), which retain post�dentary bones in the lower jaw, like docodonts.

Apart from the lineage leading to therian mam�mals, the pretribosphenic teeth (with the talonidlocated posterior to the trigonid) independently devel�oped in Henosferida, a mammal group at a lower orga�nization level (with postdentary bones in the lowerjaw) from the Jurassic of Argentina (Rauhut et al.,2002; Martin and Rauhut, 2005; Rougier et al., 2007b;

Averianov and Lopatin, 2011). This group possiblyalso includes Ambondro from the Middle Jurassic ofMadagascar (Flynn et al., 1999), the lower jaw struc�ture of which is not known. In henosferids, the talonidis relatively small, but has a distinct basin. However,the last lacks a trace of wear, which is treated as a resultof the absence of the protocone on upper molars ofhenosferids (Martin and Rauhut, 2005; Rougier et al.,2007b). This makes henosferids close to monotremes.Since the most ancient known monotremes (Teinolo�phos) had postdentary bones in the lower jaw (Richet al., 2005a, 2005b), it seems plausible to derivepretribosphenic teeth of monotremes from that ofHenosferida rather than ancestors of therian mam�mals. This conclusion does not contradict the data onthe dental formula of monotremes.

MIDDLE EAR AND LOWER JAW

The jaw joint and middle ear structure has alwaysbeen regarded as a fundamental morphological char�acter of mammals. In contrast to reptiles, the lowerjaw of mammals consists of the single bone (dentary,dentale), which is articulated with the squamosal ofthe braincase. Postdentary bones forming the jaw jointin reptiles are transformed in mammals into auditoryossicles of the middle ear: the articulare is malleus andthe quadratum is incus. Even in mammalian ances�tors, these postdentary bones were probably connectedwith tympanic membrane and participated in soundconduction. The earliest stem mammals (Morganuc�odonta) had a double jaw joint, old “reptilian” andnew “mammalian”. In more advanced Mesozoicmammals (Docodonta, Kuehneotherium, Shuothe�ridia, and Henosferida), articular function of postden�tary bones was probably already lost, but they stillretained a groove for postdentary bones in the dentary.This groove was lost in Eutriconodonta and Symmetr�odonta, the auditory ossicles (malleus and incus) ofwhich performed only the sound�conducting func�tion, were attached to the Meckel’s cartilage con�nected by its cranial end to the Meckel’s groove in thedentary, but these ossicles were not yet located at thebase of the braincase (Luo et al., 2007a; Ji et al., 2009;Luo, 2011; Meng et al., 2011). Thus, these animals didnot have a definitive mammalian middle ear, which isformed in ontogeny of extant mammals after reduc�tion of embryonic Meckel’s cartilage and displace�ment of auditory ossicles from the jaw joint to thebraincase base. The Meckel’s cartilage, which isretained at the definitive stage in symmetrodonts andeutriconodonts, is usually treated ossifying (Wanget al., 2001; Meng et al., 2003), although histologicalproofs of this statement has not been provided. It isprobable that the cartilage was mineralized during fos�silization.

430

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

AVERIANOV, LOPATIN

Two hypotheses for the evolution of the middle earin Mesozoic mammals have been developed. Accord�ing to the first, in Eutriconodonta and Symmetro�donta, the Meckel’s cartilage and malleus and incusattached to it are an evolutionary heterochrony, i.e.,preservation of pedomorphic (embryonic) conditionof these structures in adults (Luo et al., 2007a; Ji et al.,2009; Luo, 2011). According to the alternativehypothesis, these groups show an intermediate mor�phological stage of transformation of the middle ear,which recapitulates in embryogenesis of living mam�mals (Wang et al., 2001; Meng et al., 2003, 2011; Aver�ianov and Lopatin, 2011).

According to Luo and his adherents, in the courseof evolution, mammals repeatedly showed pedomor�phoses and activation of genes responsible for reduc�tion of the Meckel’s cartilage (Luo et al., 2007a,2007b; Luo, 2011). This hypothesis is intended toexplain the topology of cladogram accepted by thisauthor as a phylogenetic hypothesis for Mesozoicmammals (Fig. 2).

According to Luo, the first mammal whichacquired the definitive mammalian middle ear isHadrocodium wui from the Early Jurassic of China,which is represented by the only skull 12 mm of length(IVPP, no. V8275) (Luo et al., 2001b; Rowe et al., 2011).Computer tomography of this specimen is available fromthe online library of University of Texas (http://digi�morph.org/specimens/Hadrocodium_wui/). The smallsize of the skull naturally raises the question of theindividual age of this animal. According to Luo et al.(2001b), specimen IVPP, no. V8275 is a skull of adultor subadult because of the presence of the followingcharacters: (1) a large postcanine diastema; (2) wearfacets on the molariform teeth; (3) completely func�tioning articulation between the squamosal and den�tary; (4) absence of the Meckel’s groove. Computertomography of this specimen has not revealed germs of

unerupted teeth (Rowe et al., 2011). Some otherauthors (Wang et al., 2001; Meng et al., 2003) believethat specimen IVPP, no. V8275 should be assigned to ayoung animal based on the following characters:(1) small size; (2) erupting first upper postcanine;(3) presence of only two molariform teeth; (4) largedistance between m2 and the coronoid process;(5) large promontory; (6) relatively large volume of thebraincase; and (7) thin and low dentary. The study ofaccessible computer tomography of this specimeninclines us to adhere to the second point of view. Thepreservation of the specimen suggests that incompleteossification of the bones is not improbable. The medialand ventral surfaces of the dentary have large lacunasprobably for a dental plate. Apparently, the replace�ment of teeth in this specimen has not yet begun;therefore, teeth germs are not preserved. The recentformation of erupted teeth is supported by the widelyopen pulp canals of p2. It is likely that the absence ofMeckel’s groove (and groove for postdentary bones?)is accounted for by incomplete ossification of the den�tary. Luo et al. (2001b: p. 1535) describe the medialside of the dentary as having “a smooth periosteal sur�face.” However, they do not provide photographsillustrating this statement. The structure of the “pseu�dangular” process of the dentary is similar to that ofMorganucodonta and Docodonta, enables us to pre�dict the recognition of a groove for postdentary bonesin an older individual of Hadrocodium wui, if it isfound.

Even taking specimen IVPP, no. V8275 for anadult, it remains problematic to treat it. If this is anadult, the above juvenile features should be treated aspedomorphic. In this case, it is surprising why such apedomorphic taxon lacks a Meckel’s cartilage withauditory ossicles attached to it. Luo believes that, in“pedomorphic” eutriconodonts from the Lower Cre�taceous of China, the dentary is much more peramor�phic in structure compared to Hadrocodium (Luoet al., 2007a; Meng et al., 2011). The hypothesis ofLuo cannot explain this logical contradiction. In ouropinion, the presence of a mammalian middle ear inHadrocodium is not established with certainty.

Our phylogenetic analysis (Averianov and Lopatin,2011) has shown paraphyly of “Australosphenida”sensu Luo et al. (2001a). Jurassic GondwanianHenosferida and Laurasian Shuotheriidae, whichretain the groove for postdentary bones and, hence,lack a definitive mammalian middle ear, are sister taxa.For Early Cretaceous Australian Ausktribosphenida,the presence of the groove for postdentary bones wasnoted (Kielan�Jaworowska et al., 1998, 2004; Luoet al., 2001a, 2002; Luo, 2011), although otherresearchers did not confirm this (Rougier et al., 2007b;Averianov and Lopatin, 2011). Ausktribosphenos hasMeckel’s groove connected to the mandibular fora�men and a small fossa posterior to the mandibular

Sinoconodon

Morganucodon

Hadrocodium

Eutriconodonta

Multituberculata

Zhangheotheriidae

Metatheria

Eutheria

Pseudotribos

Henosferus

Ausktribosphenos

Teinolophos

Monotremata

DMME

OMC

OMC

DMME

DMME

DMME

Fig. 2. Phylogenetic relationships of Mesozoic mammalsafter Luo (2011). Definitive mammalian middle ear(DMME) appeared independently four times and ossifiedMeckel’s cartilage (OMC) did two times.

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

ON THE PHYLOGENETIC POSITION OF MONOTREMES 431

foramen, which corresponds to the pterygoid fossa ofsymmetrodonts (see Lopatin et al., 2005) rather thanpostdentary groove. In primitive mammals with a truepostdentary groove (Morganucodon, Kuehneotherium,Shuotherium, Docodonta), this groove is much longerand deeper, subdivided by a diagonal crest and limitedfrom above by an overhanging medial crest (Kermacket al., 1973; Luo et al., 2002; Averianov et al., 2005).Ausktribosphenos lacks similar structures and, in Bish�ops, both Meckel’s groove and fossa posterior to themandibular foramen are reduced.

According to the majority of recent phylogeneticanalyses, Ausktribosphenida is a sister group forMonotremata. In this connection, it is extremelyimportant to judge the lower jaw structure in Creta�ceous monotremes, Steropodon and Teinolophos,which was treated differently (see discussion of Luoet al., 2002; Bever et al., 2005; Rich et al., 2005a,2005b; Rougier et al., 2005, 2007b; Rowe et al., 2008).New specimens of Teinolophos distinctly show thepresence of the groove for postdentary bones in thistaxon (T. Rich, personal communication). In addi�tion, Teinolophos and Steropodon have a Meckel’sgroove, a rudiment of which is retained in the Mioceneplatypus Obdurodon (Rougier et al., 2007b; Roweet al., 2008; Luo, 2011). This raises the question as towhether or not this groove contained the Meckel’s car�tilage and whether it was connected to the articulare,or auditory ossicles were located separately at thebraincase base.

According to Luo (Luo, 2011; see Fig. 2), thedefinitive mammalian middle ear was formed inde�pendently in four mammal lineages: Hadrocodium,Multituberculata, Theria, and Monotremata. Accord�ing to our hypothesis, this occurred three times: inMultituberculata, Monotremata, and Theria.

An important character of ausktribosphenids(Ausktribosphenos and Bishops) is the presence of atrue angular process of the lower jaw. This process isnot homologous to the “pseudangular” process ofMorganucodonta and Docodonta, which has an inci�sure for the external lamina (angular wing) of theangular bone. The true angular process is not con�nected to the angular bone and is probably formed inconnection with intensified work of the internal ptery�goid and external masticatory muscles, which was inturn caused by the amplification of transverse compo�nent of masticatory movements of the lower jaw(Patterson, 1956; Jenkins et al., 1983; Jenkins, 1984;Crompton and Sun, 1985; Gow, 1986; Crompton andLuo, 1993; Hopson, 1994; Averianov et al., 2005. Forthe alternative point of view, see Parrington, 1959;Kermack et al., 1973; Gambaryan and Kielan�Jaworowska, 1995; Kielan�Jaworowska, 1997; Luoet al., 2001a, 2002; Kielan�Jaworowska et al., 2004).The presence of the true angular process of the lower

jaw is a key synapomorphy of Cladotheria (Prothero,1981; Averianov et al., 2013).

In the Early Cretaceous monotreme Teinolophos,the shape and position of the angular process areapproximately the same as in ausktribosphenids.However, a similar posterior position is also observedin the “pseudangular” process of henosferids, which isassociated with the groove for postdentary bones andhas a fossa for the external lamina of the angular boneon the lingual side (Martin and Rauhut, 2005; Rougieret al., 2007b). The presence in Teinolophos of a groovefor postdentary bones suggests that its angular processis the “pseudangular” process, which is nonhomolo�gous to the angular process of the dentary of Cladothe�ria. Among extant monotremes, the same process isreduced in platypus, but its rudiment is retained inechidnas in connection with the specialization of theirjaw apparatus (see below).

An important character shared by Henosferida andMonotremata is the position of the Meckel’s groove.In the overwhelming majority of mammals having aMeckel’s groove, it is associated with the mandibularforamen (which provides passage inside the dentaryfor the alveolaris inferior nerve, a derivative of themandibular ramus of the trigeminal nerve (V3), andblood vessels). In forms that lack a Meckel’s cartilageat the adult stage, the presence of this relationship isevidenced by the sphenomandibulare ligament, whichis formed of remains of the dorsal part of the Meckel’scartilage and attached to the dentary on sides of themandibular foramen (Standring, 2008). In the EarlyCretaceous monotreme Teinolophos, the Meckel’sgroove passes ventral to the mandibular foramen (Richet al., 2005a, 2005b). A similar position of theMeckel’s groove is observed in Henosferus (Rougieret al., 2007b). In Asfaltomylos, it is impossible to rec�ognize the presence and position of the Meckel’sgroove because of poor preservation of the only speci�men (Martin and Rauhut, 2005). In shuotheriids, theMeckel’s groove is associated with the mandibularforamen (Chow and Rich, 1982; Luo et al., 2007b).

AUDITORY OSSICLES

The auditory ossicles of monotremes are distin�guished by the structure from many other living mam�mals (Doran, 1878; Gregory, 1947; Hopson, 1966;Kuhn, 1971; Allin, 1975; Fleischer, 1978; Zeller, 1993;Meng and Wyss, 1995; Wible and Hopson, 1995;Agadjanian, 2003; Ivakhnenko, 2009). The malleushas two large processes and a large body (pars transver�salis). The longer and more massive anterior process(homologue of the prearticular of synapsids) is con�nected (partially fused) over a significant extent to aflat ectotympanicum. The anterior process of themalleus, which is connected to the ectotympanicum,and the manubrium of the malleus form an almost

432

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

AVERIANOV, LOPATIN

closed ring, with the tympanum stretched inside it.The incus is small, flat, located dorsal to the malleus.The stapes is cylindrical, not perforated by the stape�dialis artery. The malleus, ectotympanicum, incus,and tympanum are located in a plane at an angle of25°–30° to the horizontal.

After discovery of auditory ossicles in Multituber�culata (Miao and Lillegraven, 1986), it was proposedthat they are rather similar in structure to auditory oss�icles of monotremes. These data are based on severalspecimens of Lambdopsalis bulla Chow et Qi, 1978from the Paleocene–Eocene of China (Meng, 1992;Meng and Wyss, 1995). In particular, the stapes of thisanimal is cylindrical, with a slitlike foramen, whichprobably was not passage for the stapedialis artery(Meng, 1992), as in monotremes. Other features sharedwith monotremes are (1) the ectotympanicum posi�tioned almost horizontally (at an angle of 25°–30°) andcoming in contact with the pterygoid; (2) the flat incussimple in shape and located dorsal to the malleusinstead of posterior to it, as in therians; (3) the malleushaving a massive anterior process partially fused withthe ectotympanicum and a large pars transversalis.

The discovery of auditory ossicles in other multitu�berculate taxa (Hurum et al., 1995; Rougier et al.,1996b; Wible and Rougier, 2000) and reexaminationof original materials of Lambdopsalis resulted in signif�icant reappraisal of this concept (Rougier et al.,1996b). The connection between the ectotympanicumand pterygoid in Lambdopsalis was regarded as anartefact; this contact is sometimes absent in echidnasand is not characteristic of platypus. In Kryptobaatar,the stapes is forked rather than cylindrical, pierced bythe stapedial foramen (Rougier et al., 1996b). In somemultituberculate taxa from the Upper Cretaceous ofNorth America, the presence of a forked stapespierced by the stapedialis artery was reconstructedbased on the groove for this artery on the promonto�rium, which forms an incisure in the margin of thefenestra vestibuli (Rougier et al., 1992; Wible andHopson, 1995). On the other hand, cylindrical stapesis typical for Pholidota among placentals and manymarsupials (Novacek and Wyss, 1986; Gaudin et al.,1996). The malleus with a massive anterior processarticulated with the ectotympanicum and large parstransversalis occurs not only in monotremes and mul�tituberculates, but also in many archaic marsupialsand placentals (Doran, 1878; Fleischer, 1978).

In the Early Cretaceous eutriconodont Yanocon�odon, the structure of the malleus and incus was recon�structed almost identical to that of platypus (Luo et al.,2007a). According to this reconstruction, the incus isflat and positioned dorsal to the malleus, as inmonotremes. The difference from the monotremedesign is only the articulation of the malleus and ecto�tympanicum with the Meckel’s cartilage, which isretained in adults. However, this reconstruction seems

incorrect and is based on a too peremptory interpreta�tion of poorly preserved and very incomplete frag�ments of auditory ossicles (Meng et al., 2011). InLiaoconodon, another eutriconodont from the LowerCretaceous of China (Meng et al., 2011), the auditoryossicles are much better preserved. In this taxon, theincus was positioned posterior to the malleus and hada hinged articulation with it.

The peculiar structure of auditory ossicles ofmonotremes suggests that the mammalian middle earcould have independently developed in monotremesand therian mammals, which is supported by the rec�ognition of the groove for postdentary bones in theearliest known monotreme Teinolophos from theLower Cretaceous of Australia (Rich et al., 2005a).

BRAINCASE

The lateral wall of the braincase of monotremesessentially differs in structure from that of therianmammals, which is traditionally used in phylogeneticreconstruction (Watson, 1916; Kermack and Mussett,1958; Kermack, 1963; Hopson, 1964; Kermack andKielan�Jaworowska, 1971; Crompton and Jenkins,1979; Kielan�Jaworowska et al., 1986, 2004; Hopsonand Rougier, 1993; Wible and Hopson, 1993, 1995;Rougier and Wible, 2006).

In nonmammalian cynodonts, most of the lateralwall of the braincase is formed of the ascending pro�cess of the alisphenoid (or epipterygoid), which islocated between the orbital depression providing pas�sage for the orbital branch of the trigeminal nerve (V1)and a large trigeminal foramen, an exit for the maxil�lary (V2) and mandibular (V3) branches of the trigem�inal nerve (Fig. 3a). The trigeminal foramen is locatedat the boundary between the alisphenoid and anteriorlamina of the prootic, which is ossification of the audi�tory capsule. There is a well�developed, posteriorlydirected quadrate ramus of the alisphenoid. The squa�mosal does not participate in the formation of the pri�mary braincase wall; its anterior process comes in con�tact with the auditory capsule and anterior lamina ofthe prootic.

In stem mammals (Morganucodonta, Doc�odonta), the anterior lamina of the prootic is consid�erably anteroposteriorly extended; therefore, thetrigeminal foramen is divided into two for separateexits of V2 and V3 branches of the trigeminal nerve(Figs. 3b, 4a).

The braincase structure was investigated in detail inVincelestes from the Lower Cretaceous of Argentina(Fig. 3c), which is usually assigned to pretribosphenicmammals (Rougier et al., 1992; Hopson and Rougier,1993; Kielan�Jaworowska et al., 2004; Macrini et al.,2007). According to recent data, this taxon belongs tobasal radiation of Cladotheria (Averianov et al., 2013).Vincelestes generally retains the plesiomorphic struc�

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

ON THE PHYLOGENETIC POSITION OF MONOTREMES 433

ture of the braincase wall, which is characteristic ofMorganucodon (Figs. 3b, 4a). At this evolutionarystage, derived characters are an increase in size of thealisphenoid and reduction of its quadrate ramus. Theanterior lamina of the prootic also participated in theformation of the braincase wall in the symmetrodontMaotherium (Ji et al., 2009).

In extant therian mammals (Metatheria and Euth�eria), the anterior lamina of the prootic is completelylost (Fig. 3d). It is preserved in reduced form in theEarly Cretaceous eutherian Prokennalestes fromMongolia (Wible et al., 2001). Most of the lateral wallof the braincase is formed by the expanded alisphe�noid, which contains the foramen for the mandibular

(a)

(b)

(c)

(d)

?

al

pras

as

oc

foqr

V1

V2

V3

?

(e)

Fig. 3. Transformations of the braincase wall in the evolution of mammals (after Hopson and Rougier, 1993, text�fig. 6): (a) initialstate characteristic of nonmammalian cynodonts; (b) stem mammals (Morganucodonta, Docodonta); (c) basal cladotherianVincelestes; (d) therian mammals (Metatheria, Eutheria); (e) Monotremata, Multituberculata, and probably Eutriconodonta.White arrow in (d, e) shows the direction of growth of membrana spheno�obturatoria: (d) from the ala temporalis in Theria or(e) towards the ala temporalis in Monotremata. Designations: (al) anterior lamina of the prootic (= lamina obturans);(as) alisphenoid; (fo) fenestra ovalis; (oc) auditory capsule; (pras) ascending process of the alisphenoid or ala temporalis, embry�onic predecessor of the alisphenoid (shown by dotted line); (qr) quadrate ramus of the alisphenoid; (V1, V2, V3) orbital, maxillary,and mandibular branches of the trigeminal nerve.

434

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

AVERIANOV, LOPATIN

branch of the trigeminal nerve (V3). The pars squa�mosa appears to participate in the formation of thebraincase wall and adjoin anteriorly the alisphenoid(Fig. 4c).

Monotremes, multituberculates, and probablyeutriconodonts are probably characterized by a differ�ent structure of the braincase wall. In this case, thealisphenoid is strongly reduced, forms only the lateralwall of the cavum epiptericum (cavity of the trigemi�nal ganglion) and most of the braincase wall is formedof the anterior lamina of the prootic (Fig. 3e). Thislamina is formed during embryogenesis by the fusionof embryonic obturator plate (lamina obturans) withthe ear capsule, which is a cartilaginous predecessor ofthe petrosal (Watson, 1916; Kuhn, 1971; Zeller, 1989;Hopson and Rougier, 1993). The anterior lamina ofthe petrosal is bordered anteriorly by the orbitosphe�noid and contains a foramen for the mandibularbranch of the trigeminal nerve (V3). The cranial part ofthe squamosal overlies the surface of the petrosal andoccipitals and does not form the primary braincasewall (Fig. 4b). This distinction in the braincase wallstructure of therian and nontherian mammals was pre�viously the basis for division of mammals into the sub�classes Theria and Prototheria (Kermack, 1963; Hop�son, 1964; Kermack and Kielan�Jaworowska, 1971).However, as later embryological studies have shown,the braincase walls of monotremes and therian mam�mals are homologous and formed by ossification of themembrana spheno�obturatoria (Presley and Steel,1976; Presley, 1980, 1981; Kuhn and Zeller, 1987;

Maier, 1987, 1989; Zeller, 1989). The only differenceis the fact that, at later embryological stages, this ossi�fication is fused with either the auditory capsule toform the anterior lamina of the petrosal (Monotrem�ata), or with the ascending process of the alisphenoidto form its wing (Theria). The condition characteristicof living monotremes is possible to derive from boththe condition of stem mammals (Fig. 3b) and the levelof basal Cladotheria (Fig. 3c); this is designated inFig. 3 by arrows with question marks.

The idea of fundamental difference betweenmonotremes and therian mammals in the braincasewall structure has recently been revived by Ivakhnenko(2009). In his opinion, the basic distinction is the factthat the therian alisphenoid results from the fusionduring embryogenesis of the epipterygoid with ossifiedsphenobturator membrane, whereas the “alisphe�noid” of monotremes (anterior lamina of the prootic)does not include the epipterygoid, which is retained asa rudiment at the base of the anterior lamina. How�ever, according to the embryological data (Presley andSteel, 1976; Presley, 1980, 1981; Kuhn and Zeller,1987; Maier, 1987, 1989; Zeller, 1989), the elementsforming the braincase wall of therian and oviparousmammals are homologous (Fig. 4). The ascendingprocess of the epipterygoid, which in adult cynodontsand stem mammals forms the anterior braincase part(Fig. 4a), is lost in extant monotremes and stronglyreduced in therian mammals, so that the epipterygoid isonly represented by its quadrate ramus (Figs. 4b, 4c). Inliving monotremes, the epipterygoid is formed ofsmall neomorphic ascending lamina, which growsbetween the exits of the V2 and V3 nerves based on theanterior end of the quadrate ramus of the epipterygoid(Fig. 4b). Among living therian mammals, some mar�supials retain a reduced cartilaginous ascending pro�cess anterior to the exit of the V2 nerve (Fig. 4c). Othertherians develop instead of it a neomorphic laminaascendens between the exits of the V2 and V3 nerves(Fig. 4c), as in monotremes. The only difference is thefact that, in therians, epipterygoid remains are fusedwith the lamina obturans to form a large alisphenoidand, in monotremes, the lamina obturans is fused withthe auditory capsule to form the anterior lamina of thepetrosal, while epipterygoid remains are separate. Thisdifference is accounted for by the direction of ossifica�tion of the lamina obturans: in the anterior direction inmonotremes and in the posterior direction in therians(white arrow in Figs. 3d, 3e). Cartilaginous germs canfuse only at early stages of ossification; therefore, asthis process is accomplished at the anterior braincaseend, the epipterygoid (alisphenoid) of monotremes isnot included in the braincase and, in therians, the pro�cess of ossification begins from the inclusion of epip�terygoid remains.

The primary braincase of mammals is formed ofcartilage (chondrocranium) and pachymeninx (dura

(a)

(b)

prassqlo

per

qr

V1

V2

V3

ept

pras

sqlo

perV1

V2

V3

V1

V2

sq

lo

V3

per

aslaslas as

(c)

Fig. 4. Homology of embryonic elements composing thelateral braincase wall in (a) stem mammals,(b) monotremes, and (c) therian mammals (after Hopsonand Rougier, 1993, text�fig. 4). Designations: (ept) epip�terygoid; (las) lamina ascendens; (lo) lamina obturans;(per) periotic; (pras) ascending process of the epiptery�goid, embryonic predecessor of the epipterygoid (shownby dotted line); (sq) squamosal. For other designations, seeFig. 3.

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

ON THE PHYLOGENETIC POSITION OF MONOTREMES 435

mater). In connection with an increase in brain size,different mammal groups independently formed thesecondary, more lateral cerebral envelope (De Beer,1937; Moore, 1981; Kuhn and Zeller, 1987; Wible andRougier, 2000). The new extradural space between theprimary and secondary walls of the braincase isreferred to as the cavum epiptericum (Gaupp, 1902,1905). It contains the ganglia of the trigeminal andfacial nerves and other cranial nerves and blood ves�sels. The vessels and cranial nerves come from thebraincase into the cavum epiptericum or back throughthe fissures between vertical columns (pila) of thechondrocranium (Fig. 5). Mammalian ancestors, likeextant sauropsids, probably had three pila, i.e., thepreoptica, metoptica, and antotica pila (De Beer,1926, 1937; Starck, 1967, 1978; Kuhn, 1971; Moore,1981; Kuhn and Zeller, 1987; Zeller, 1989; Fig. 5a).Mammal groups are distinguished by the pattern ofreduction of vertical cartilaginous pila (Fig. 5). Inmonotremes, the metoptic pilum has disappeared(Fig. 5c); marsupials has lost the metoptic and antoticpila (Fig. 5d); and placentals lack the antotic pilum(Fig. 5e) (Gaupp, 1908; De Beer, 1937; Starck, 1967;Kuhn, 1971; Kuhn and Zeller, 1987; Maier, 1987;Zeller, 1989; Wible and Rougier, 2000). It is notewor�thy that multituberculates retain a primitive structureof the chondrocranium with three vertical pila, as sau�ropsids (Fig. 5b; Wible and Rougier, 2000). This sug�gests that the stems of therian mammals andmonotremes diverged later than multituberculatesbranched off. This conclusion contradicts the inclu�sion of Multituberculata in the crown group of Mam�malia, which is shown in the majority of recent phylo�genetic hypotheses (Luo et al., 2002; Kielan�Jaworowska et al., 2004; Yuan et al., 2013; Zhou et al.,2013).

DEPRESSORS OF THE LOWER JAW

One of the most fundamental arguments in favor ofthe hypothesis about a large phylogenetic distancebetween Monotremata and Theria is differences inmuscles lowering the mandible in these groups. In the�rian mammals, the lower jaw depressor is the digastricmuscle (musculus digastricus), which is complex inorigin: its anterior belly developed from jaw musclesand was innervated by the mandibular branch of thetrigeminal nerve (V3), while the posterior belly devel�oped from hyoid muscles and was innervated by thefacial nerve (VII). In monotremes, the depressor of thelower jaw (m. detrahens mandibulae) is a derivative ofjaw muscles and is innervated by the mandibularbranch of the trigeminal nerve (V3) (Adams, 1919;Hopson, 1966; Parrington, 1974; Tatarinov, 2001;Diogo et al., 2008). In extant nonmammalian tetra�pods, the mandibular depressor in the narrow sense(m. depressor mandibulae) developed from hyoidmuscles (innervated by the VII nerve).

Even Gregory (1947) presumed that the specificityof jaw muscles of monotremes is determined by theirspecialization. Actually, the mechanism for mouthopening in monotremes essentially differs from that oftherian mammals. It was described in detail in echidna(Murray, 1981). Its rostrum is covered by a dense con�necting tissue sheath and the mouth end can open onlyslightly, for approximately 5 mm. The mouth is openby rotation of the posterior part of the jaw rami aroundtheir longitudinal axis, which results in slight loweringof the anterior end of the dentaries, rather than by low�ering the mandible. This rotation is provided by alter�

eaen II III IV V VI ps

ev oa pv VII

nc oc

(a)

pv

pp pm pan

ips VII

pp pan

pvpp ps

(b)

(c)

(d)

(e) pp

ais pis ips cev

pm

Fig. 5. Scheme of embryonic chondrocranium in (a) gen�eralized sauropsid, (b) multituberculate, (c) monotreme,(d) marsupial, and (e) placental. Designations: (ais) ante�rior intercavernous sinus; (cev) capsuloparietal vein;(ea) ethmoid artery; (en) ethmoid; (ev) ethmoid vein;(ips) inferior petrosal sinus; (nc) nasal capsule; (oa) orbitalartery; (oc) auditory capsule; (pan) pila antotica; (pis) pos�terior intercavernous sinus; (pm) pila metoptica; (pp) pilapreoptica; (ps) prootic sinus; (pv) hypophysiorbital vein;(II) optic nerve; (III) oculomotor nerve; (IV) trochlearnerve; (V) trigeminal nerve; (VI) abducent nerve;(VII) facial nerve.

436

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

AVERIANOV, LOPATIN

nating work of the medial and lateral pterygoid mus�cles, while contraction of the detrahens mandibulaemuscle has a minor effect on mouth opening (Murray,1981). The function of the detrahens mandibulaemuscle of echidna is probably retention of the man�dibular condyle in the jaw joint, as the dentary rotates.The peculiarity of the jaw apparatus of echidna is con�nected with feeding on social insects, which areground on the palate by the dorsal side of tongue.Hence, echidnas lack teeth; the bone palate is verylong; and the dentary is reduced to a narrow rodlikestructure. In these features, the skull of echidna isamazingly convergently similar to the skull of anteat�ers (Myrmecophagidae). Anteaters also lack m. digas�tricus in the form characteristic of other therian mam�mals; its anterior belly forms the anterior part of thesternomandibularis muscle, connecting the lower jawwith the manubrium of the sternum and the posteriorpart is retained as a primitive interhyoideus muscle(Reiss, 1997).

In contrast to echidna, the platypus can open themouth within a wider range. However, it is evidentthat, in platypus, the mechanism for mouth opening issimilar to that of echidnas and differs from simple sag�ittal movements typical of other mammals, because itsjaws are tightly connected by the horny cover formingthe beak. The platypus feeds mostly on aquatic inver�tebrates with relatively soft integument, which isground by horny plates replacing in ontogeny provi�sional (embryonic) teeth. The dentary of platypus isalso reduced, although to a lesser extent than inechidna. It retains a rudimentary coronoid processand masseteric fossa. It is possible to assume that

platypus also opens its mouth by twisting the mandib�ular rami in the posterior part. It is important that, inplatypus, the anterior part of jaws is covered by a beak,which interferes with placing here the mylohyoideusmuscle and anterior part of the digastricus muscle,which are displaced posteriorly. In fact, the digastricmuscle of platypus shows approximately the samestate as in anteaters; the posterior belly is not differen�tiated (not separated from the styloideus muscle,according to Diogo et al., 2008) and, hence, a com�plete digastric complex is absent (Fig. 6). Thus, theleast hypothetical scenario implies that ancestors ofMammalia had only the digastricus anterior muscle.The detrahens mandibulae muscle probably alsoexisted in common ancestors of Recent mammals inthe form of a separate fascicle of the m. adductor man�dibulae externus (Edgeworth, 1935; Kemp, 1979,1980a). If this is the case, it was lost in ancestors ofTheria and, in monotremes, it was transformed into anew depressor of the lower jaw, since the formerdepressor (digastricus muscle) could not functionunder condition of rigid connection of the jaws.

POSTCRANIAL SKELETON

In nonmammalian cynodonts, stem mammals(Morganucodonta), and multituberculates, cervicalribs have a mobile synovial articulation with vertebrae(Kühne, 1956; Jenkins, 1970, 1971; Jenkins and Par�rington, 1976; Kemp, 1980b; Rowe, 1988; Kielan�Jaworowska and Gambaryan, 1994). In extant andCretaceous therian mammals, cervical ribs are fusedwith vertebrae (Rowe, 1988; Kielan�Jaworowska et al.,2004). Among therians, this fusion was first recordedin Juramaia from the Middle or Upper Jurassic ofChina (Luo et al., 2011). In Recent monotremes, cer�vical vertebrae and ribs are fused, but retain suturesbetween them for a long time (Lessertisseur andSaban, 1967, text�fig. 348), disappearing in old ani�mals. This circumstance results in confusion in thedetermination of condition of this character inmonotremes. It is usually believed that the fusion iscomplete (Kielan�Jaworowska and Gambaryan, 1994;Kielan�Jaworowska et al., 2004). Sometimes, it isremarked that, in platypus, the fusion is complete, but,in the Tachyglossidae, it has not yet been reached (Huet al., 1997). Our examination shows that, in specimenZIN, no. 19957 of Tachyglossus aculeatus, cervical ribsare completely fused with vertebrae, without a trace ofsuture. In Early Cretaceous eutriconodonts(Jeholodens, Yanoconodon) and symmetrodonts(Zhangheotherium, Maotherium), cervical ribs wereconsidered to be isolated (nonfused), although thesestructures have not been described in detail (Hu et al.,1997; Ji et al., 1999; Luo et al., 2007a; Ji et al., 2009).It remains uncertain whether they retain synovialarticulation of ribs and cervical vertebrae or connec�tion is sutural. All or most of known specimens of

os dentalem. mylohyoideus p. profunda

m. mylohyoideus p. superficialis

m. digastricus anterior

m. masseter

m. detrahens mandibulae

m. styloideus

m. cleidomastoideusm. omohyoideusm. sternomastoideusm. sternothyroideus

Fig. 6. Jaw and cervical musculature of the platypus Orni�thorhynchus anatinus (Shaw, 1799), ventral view (afterDiogo et al., 2008, text�fig. 9A).

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

ON THE PHYLOGENETIC POSITION OF MONOTREMES 437

these taxa are young or subadult animals; this may bethe cause of incomplete fusion. The basal cladotherianVincelestes is encoded in matrices as having the cervi�cal ribs fused with vertebrae; however, a description ofits postcranial skeleton has not been published.

The vertebral column of monotremes consists of7 cervical, 15–18 thoracic, 1–5 lumbar, 2–4 sacral,and 11–20 caudal vertebrae (Lessertisseur and Saban,1967; Narita and Kuratani, 2005; Asher et al., 2011;Buchholtz et al., 2012). The ratio and total number ofthoracic and lumbar vertebrae widely vary, on averagethere are 19, but may be from 17 to 20. The posteriorthoracic vertebrae are determined by the presence offloating ribs. Platypus has from one to three (on aver�age two) lumbar vertebrae; echidna has from two tofive (on average three; Asher et al., 2011).

The presacral vertebrae lacking free ribs are distin�guished in the lumbar region of the vertebral column(Romer, 1956, 1970). Therefore, by definition, it isimpossible to find lumbar vertebrae with ribs or lumbarribs. In nonmammalian cynodonts, the presacral ver�tebrae, which correspond to the lumbar vertebrae ofmammals, had movably articulated ribs (Jenkins,1970, 1971). In some basal mammals, a large numberof lumbar vertebrae has been recorded because ofincorrect inclusion in this region of vertebrae withmobile ribs. In the Jurassic docodont Castorocauda,seven lumbar vertebrae have been recorded, six ante�rior of which have large mobile ribs (Ji et al., 2006). Inthe Early Cretaceous eutriconodont Yanoconodon,eight lumbar vertebrae have been determined, only thelast of them lacks a movably articulated rib (Luo et al.,2007a). In the other Early Cretaceous eutriconodontJeholodens, seven lumbar vertebrae and mobile lumbarribs are determined (Ji et al., 1999); it is uncertainwhether or not this taxon had a presacral vertebrawithout a mobile rib. “Lumbar” ribs were also recog�nized in the Early Cretaceous eutriconodont Gobicon�odon (Jenkins and Schaff, 1988). Among symmetro�donts, seven lumbar vertebrae are known for Maothe�rium (Rougier et al., 2003; Ji et al., 2009); all of themlack mobile ribs. Another symmetrodont, Zhanghe�otherium, has five lumbar vertebrae, which also lackribs (Hu et al., 1997; Luo and Ji, 2005; Li and Luo,2006). On the contrary, in the symmetrodont Akidol�estes, six lumbar vertebrae have been recognized, firstfive of which have mobile ribs (Li and Luo, 2006;Chen and Luo, 2013). In the Jurassic pseudotri�bosphenic mammal Pseudotribos, 16 thoracic verte�brae were determined, the last three of which havefloating ribs, and six lumbar vertebrae, two anterior ofwhich have mobile ribs (Luo et al., 2007b). Inharamiyids, seven (Arborharamiya) or nine (Megaco�nus) lumbar vertebrae have been determined, some ofwhich had mobile ribs (Zheng et al., 2013; Zhou et al.,2013). In Arborharamiya, the number of presacral ver�tebrae without mobile ribs has not been indicated;

Megaconus probably had five vertebrae of this sort,judging from the published reconstruction (Zhouet al., 2013, text�fig. 1a). The Jurassic multitubercu�late Rugosodon had six lumbar vertebrae withoutmobile ribs (Yuan et al., 2013). Cretaceous and Paleo�gene multituberculates had seven or eight lumbar ver�tebrae, also without ribs (Krause and Jenkins, 1983;Kielan�Jaworowska and Gambaryan, 1994).

The above review shows that docodonts and eutri�conodonts apparently had one true sacral vertebra.One sacral vertebra was also in the enigmatic diggingmammal Fruitafossor from the Upper Jurassic ofNorth America (Luo and Wible, 2005). The number ofsacral vertebrae increased to four in Pseudotribos, fromsix to eight in multituberculates, and from five to sevenin symmetrodonts (except for Akidolestes). A largenumber of lumbar vertebrae without ribs is also knownin the basal cladotherians Vincelestes and Henkelothe�rium and Cretaceous therian mammals (Kielan�Jaworowska et al., 2004). Thus, the small number oflumbar vertebrae in monotremes (on average two orthree) is a plesiomorphic condition.

In monotremes, the interclavicle or suprasternum(interclavicula, seu episternum) is large, movably con�nected to the sternum and immovably, to the clavicle.The interclavicle is formed by the fusion of the pairedlateral pars desmalis interclaviculae of dermal originand unpaired medial pars chondralis interclaviculaeformed by ossification of cartilage (Cave, 1970;Klima, 1987). In living therian mammals, the parsdesmalis is completely lost, so that it is not recognizedeven in embryogenesis (Klima, 1987). The pars chon�dralis is fused with the manubrium of the sternum. Inmarsupials, the clavicle is connected to the sternum byan intermediate element (praeclavium), which isembryonic germ of the procoracoid (Klima, 1987).

Among Mesozoic mammals, the interclavicle islarge and immovably connected to the clavicle inMorganucodonta and the shuotheriid Pseudotribos(Jenkins and Parrington, 1976; Luo et al., 2007b). Theinterclavicle is present in the docodont Haldanodon,but the character of connection with the clavicle is notknown (Martin, 2005). In multituberculates, theeutriconodonts Jeholodens and Yanoconodon, sym�metrodonts Zhangheotherium, Maotherium, and Aki�dolestes, the interclavicle is strongly reduced and mov�ably articulated with the clavicle, although it is stillpreserved as an independent element (Ji et al., 1999;Sereno, 2006; Luo et al., 2007a; Ji et al., 2009; Chenand Luo, 2013). In Cretaceous basal cladotherians(Vincelestes), the interclavicle is fused with the manu�brium of the sternum and the clavicle is movably con�nected to the sternum (Kielan�Jaworowska et al.,2004). The development of mobile articulation of theclavicle and interclavicle/sternum is connected with theacquisition of the parasagittal position of forelimbs,which apparently occurred independently in different

438

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

AVERIANOV, LOPATIN

mammal lineages. This presumable homoplasydecreases the phylogenetic value of this character.

The spine of the scapula passing into the acromionis a process for articulation with the clavicle, which islocated in monotremes on the anterior margin of thebone and, hence, the prescapular fossa (fossasupraspinalis) is usually undeveloped. A rudimentarysupraspinous fossa is occasionally present in platypusas an individual variation (Luo and Wible, 2005, text�fig. 3A). In therian mammals, the scapular spinepasses in the middle of the bone between large supras�pinous and infraspinous fossae. Among nonmamma�lian cynodonts, a rudimentary supraspinous part of thescapula is only present in tritylodontids at the vertebraledge of the scapula (Sues and Jenkins, 2006). In Mor�ganucodonta and Docodonta, the supraspinous fossais absent (Jenkins and Parrington, 1976; Martin,2005). Among multituberculates, the supraspinousfossa is probably absent in North American forms(McKenna, 1961; Krause and Jenkins, 1983). Asiaticforms had a rudimentary supraspinous fossa locatednear of the glenoid articulation (Kielan�Jaworowskaet al., 2004; Sereno, 2006, text�fig. 10.3; Hurum andKielan�Jaworowska, 2008, text�fig. 4A2). A rudimen�tary supraspinous fossa is described, but not desig�nated in figures of the Jurassic mammal Fruitafossor(Luo and Wible, 2005). A well�developed supras�pinous fossa reaching the glenoid articulation ispresent in the eutriconodonts Gobiconodon andJeholodens, symmetrodonts Zhangheotherium andAkidolestes, and basal cladotherians Vincelestes andHenkelotherium (Jenkins and Schaff, 1988; Krebs,1991; Hu et al., 1997; Ji et al., 1999; Chen and Luo,2013). In these forms, the supraspinous fossa is usuallynarrow, at most half as wide as the infraspinous fossa,although in Jeholodens, both fossae are almost equal inwidth (Ji et al., 1999). In Cretaceous therian mam�mals, the supraspinous fossa is as wide as, or somewhatwither than the infraspinous fossa (Kielan�Jaworowska et al., 2004). The development of thesupraspinous fossa of the scapula is apparently alsoconnected with parasagittalization of limbs.

In monotremes, the articular fossa of the shouldergirdle is formed by the scapula and “posterior” cora�coid (metacoracoid) completely fused with it (Vick�aryous and Hall, 2006). The metacoracoid adjoins themanubrium of the sternum and interclavicle; it ishomologous to the coracoid process (processus cora�coideus) of the scapula of therian mammals, in whichthe metacoracoid has lost contact with the sternum.The “anterior” coracoid (procoracoid, or epicora�coid) is retained as a separate element connected by asuture with the metacoracoid and overlying the dorsalside of the interclavicle. Among Mesozoic mammals,a free procoracoid is only recorded in Morganuc�odonta (Jenkins and Parrington, 1976). The conditionof this element in Shuotheriidae is not known (Luo

et al., 2007b). The shoulder girdle of Pseudotribos issimilar in structure to that of monotremes and, hence,the presence of a procoracoid in shuotheriids is ratherprobably. In the docodont Haldanodon, multitubercu�lates, the eutriconodonts Gobiconodon, Jeholodens,and Yanoconodon, symmetrodonts Zhangheotherium,Maotherium, and Akidolestes, basal cladotheriansFruitafossor, Vincelestes, and Henkelotherium, andCretaceous therian mammals, the procoracoid isabsent (Ji et al., 1999, 2002, 2009; Luo and Wible,2005; Martin, 2005; Li and Luo, 2006; Sereno, 2006;Luo et al., 2007a). In marsupials, the procoracoid issometimes preserved as a separate element (pre�clavium) movably articulated by its medial end withthe manubrium of the sternum and the lateral end isconnected to the clavicle (Klima, 1987).

In monotremes and marsupials, the pelvic girdlecontains epipubic, or prepubic (“marsupial”) bones(epipubis, seu prepubis). They are not directly relatedto the pouch, since they are present in both sexes andspecies lacking a pouch (platypus). Their function isconnected with locomotion and breathing (Reilly andWhite, 2003; Reilly et al., 2009, 2010). Among Meso�zoic mammals, epipubic bones are recorded in multi�tuberculates, the shuotheriid Pseudotribos, eutricon�odonts Gobiconodon, Jeholodens, and Yanoconodon,zhangheotheriids Zhangheotherium and Maotherium,spalacotheriids Akidolestes, basal cladotherian Hen�kelotherium, Cretaceous Eutheria, and Metatheria(Kielan�Jaworowska, 1969, 1975; Krause and Jenkins,1983; Jenkins and Schaff, 1988; Krebs, 1991; Kielan�Jaworowska and Gambaryan, 1994; Hu et al., 1997;Novacek et al., 1997; Ji et al., 1999, 2002, 2009;Kielan�Jaworowska et al., 2004; Li and Luo, 2006;Luo et al., 2007a, 2007b). Among nonmammaliancynodonts, epipubic bones are only recognized in tri�tylodontids (Kühne, 1956). It remains uncertainwhether or not they were present in Morganucodonta(Jenkins and Parrington, 1976; Kemp, 1983; Evans,1984).

Males of the three living monotreme genera have aspur on the hind limb. The spur of platypus is moststrongly developed. The spur contains a duct of thepoisonous gland, opening in the shin region. In femaleplatypus and echidnas, spurs are rudimentary. Thespur is a horny spine (cornu calcaris) on a special bone(os calcaris). This bone is articulated with the astraga�lus and tibia. The presence of a spur is a primitive char�acter presumably typical for all early mammals withlaterally positioned limbs (Hurum et al., 2006).Among Mesozoic mammals, the spur is recorded inharamiyids, multituberculates, the eutriconodontGobiconodon, and symmetrodonts Zhangheotherium,Maotherium, and Akidolestes (Hurum et al., 2006;Chen and Luo, 2013; Yuan et al., 2013; Zhou et al.,2013).

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

ON THE PHYLOGENETIC POSITION OF MONOTREMES 439

PHYLOGENETIC POSITION OF MONOTREMES

The analysis of the main morphological features ofmonotremes has outlined a set of characters recon�structed for their direct ancestors: (1) the dental for�mula includes three molars; (2) molars are of pretri�bosphenic type, without a protocone; (3) the dentaryhas a groove for postdentary bones; (4) the Meckel’sgroove is not associated with the mandibular foramen;(5) the dentary has a “pseudangular” process; (6) theincus is flat, located dorsal to the malleus; (7) thechondrocranium retains the pila antotica; (8) the lat�eral braincase wall is formed by the anterior lamina ofthe prootic; (9) at most two or three lumbar vertebraeare present; (10) the interclavicle is large, movablyarticulated with the sternum and immovably, with theclavicle; (11) the procoracoid is present; (12) the scap�ula lacks a supraspinous fossa; (13) the metatarsal spuris present.

Therian mammals (Theria) are most remote fromthis state. They have one character shared with ances�tors of monotremes, the dental formula with threemolars. In addition, Early Cretaceous Eutheria whichretain the Meckel’s groove, it is usually not associatedwith the mandibular foramen (Kielan�Jaworowskaand Dashzeveg, 1989; Ji et al., 2002).

It is hardly probable that Early Cretaceous Austra�lian Ausktribosphenida, which are regarded as themost probable sister group of Monotremata in themajority of phylogenetic hypotheses (Luo et al.,2001a, 2002; Kielan�Jaworowska et al., 2004), couldhave been ancestral to this group (Rich et al., 2002).The characters shared by Ausktribosphenida andMonotremata include the dental formula with threemolars and the pretribosphenic structure of molars,probably without the protocone. In Ausktribosphenos,the Meckel’s groove is associated with the mandibularforamen, whereas in Bishops, it is reduced and passesventral to the foramen (Rich et al., 1997, 1999, 2001).Ausktribosphenids are more advanced in comparisonwith presumable ancestors of monotremes in theabsence of a groove for postdentary bones and thepresence of true angular rather than “pseudangular”process of the dentary.

The Dryolestida have more than three molars, themolars are not pretribosphenic in structure, a groovefor postdentary bones and “pseudangular” process ofthe dentary are absent, the Meckel’s groove is associ�ated with the mandibular foramen, five lumbar verte�brae, interclavicle and procoracoid are absent, thescapula has a large supraspinous fossa (Krebs, 1991;Kielan�Jaworowska et al., 2004). In addition, dryoles�tids are more advanced in comparison withmonotremes in the structure of the internal ear: thecochlear canal is longer, turning for 270° (Ruf et al.,2009; Luo et al., 2012).

The Spalacotheriidae also have more than threemolars. The dentary lacks a groove for postdentarybones and angular process. The Meckel’s groove iscompletely reduced in advanced forms; in Spalacothe�rium, it is associated with the mandibular foramen.The postcranial skeleton is only known for Akidolestes(Li and Luo, 2006; Chen and Luo, 2013). Its shouldergirdle is advanced in structure: the interclavicle issmall, immovably articulated with the sternum, andmobile relative to the clavicle; the procoracoid isabsent; the scapula has a large supraspinous fossa. Inthe description of Akidolestes, six lumbar vertebrae,five anterior of which have mobile ribs, are mentioned(Li and Luo, 2006; Chen and Luo, 2013). Thus, thistaxon has one true lumbar vertebra. The metatarsalspur is present.

The Zhangheotheriidae are also characterized bydetachment of postdentary bones from the lower jawand more than three molars. The molars are nontri�bosphenic. The dentary lacks an angular process. InZhangheotherium, the Meckel’s groove probablypasses ventral to the mandibular foramen (Luo and Ji,2005). Zhangheotherium and Maotherium have five andseven lumbar vertebrae. The shoulder girdle is similarin structure to that of Akidolestes (Hu et al., 1997; Luoand Ji, 2005; Chen and Luo, 2013). The metatarsalspur is present.

Eutriconodonta is an artificial group. TheAmphilestidae, Gobiconodontidae, and Jeholodon�tidae are apparently close to ancestors of Trechnothe�ria (Rougier et al., 2007a; Gaetano and Rougier, 2011;Averianov et al., 2013). The Triconodontidae probablybelong to a more basal radiation of mammals; in somefeatures, they are close to multituberculates (Kielan�Jaworowska et al., 2004). Eutriconodonts usually havemore than three molars, with longitudinally posi�tioned cusps, nontribosphenic. Postdentary bones areseparated from the lower jaw; in Jeholodontidae, theycould be attached to the Meckel’s cartilage at the adultstage (Luo et al., 2007a; Meng et al., 2011). The incusis located posterior to the malleus (Meng et al., 2011).The dentary lacks an angular process. The Meckel’sgroove is not associated with the mandibular foramen,at least in some forms. The braincase wall of Tricon�odontidae has a large anterior lamina of the prootic(Kermack, 1963). For the Jeholodontidae, seven(Jeholodens) or eight (Yanoconodon) lumbar vertebrae,only posterior of which lacks mobile ribs, have beendescribed (Ji et al., 1999; Luo et al., 2007a). Theshoulder girdle of Jeholodontidae is of the advancedtype, as in contemporaneous Zhangheotheriidae andAkidolestes. In Gobiconodon and Jeholodens, the scap�ula has a large supraspinous fossa (Jenkins and Schaff,1988; Ji et al., 1999). The metatarsal spur is present, atleast in Gobiconodon (Hurum et al., 2006).

The Multituberculata are close to Monotremata inthe structure of auditory ossicles. In particular, their

440

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

AVERIANOV, LOPATIN

incus is small, flat, and located dorsal to the malleus(Meng and Wyss, 1995). The anterior lamina of theprootic participates in the formation of the braincasewall. The supraspinous fossa of the scapula is rudi�mentary or absent. The metatarsal spur is present. Inother characters under consideration, multitubercu�lates sharply differ from monotremes. Multitubercu�lates do not have more than two molars of a specificstructure with two or three rows of longitudinal cusps.Even in the earliest Jurassic multituberculates, post�dentary bones are completely separated from the den�tary and the Meckel’s groove is completely reduced(Yuan et al., 2013). The dentary lacks an angular pro�cess. The number of lumbar vertebrae is six in Jurassicforms and seven or eight in Cretaceous–Paleogeneforms (Krause and Jenkins, 1983; Kielan�Jaworowskaand Gambaryan, 1994; Yuan et al., 2013). The inter�clavicle is strongly reduced and movably connected tothe clavicle (Sereno, 2006). The procoracoid is absent.

The Docodonta have more than three molars of amore advanced structure than in monotremes, with afunctional analogue of the protocone. The similarityto monotremes involves the presence of the groove forpostdentary bones, “pseudangular” process, one lum�bar vertebra (Castorocauda), and interclavicles(Haldanodon), the structure of which remains unknown(Martin, 2005), and also the absence of a supraspinousfossa of the scapula. The Meckel’s groove is associatedwith the mandibular foramen. The procoracoid isabsent (Haldanodon).

Among the main clades of Mesozoic mammals,Jurassic Gondwanian Henosferida most closelyapproach the state ancestral for monotremes. Thesimilarity to Monotremata involves the dental formulawith three molars, pretribosphenic structure ofmolars, apparently without a protocone, the dentarywith a groove for postdentary bones and “pseudangu�lar” process, and Meckel’s groove, which passes ven�tral to the mandibular foramen (Martin and Rauhut,2005; Rougier et al., 2007b). Unfortunately, the struc�ture of the skull and postcranial skeleton of henosfer�ids is not known. All other accessible characters com�pletely coincide with the state reconstructed for ances�tors of monotremes.

The Shuotheriida are close to Monotremata in thestructure of the shoulder girdle with a large interclavi�cle immovably connected to the clavicle and the pres�ence on the dentary of only three molars and groovefor postdentary bones (Chow and Rich, 1982; Luoet al., 2007b). However, the structure of molars ispseudotribosphenic, with the anterior talonid andfunctional analogue of the protocone (Wang et al.,1998; Luo et al., 2007b). The Meckel’s groove is asso�ciated with the mandibular foramen. The “pseudan�gular” process of the dentary is strongly reduced,almost absent. Four lumbar vertebrae are present(Pseudotribos).

The Morganucodonta, as the earliest monotremes,have a groove for postdentary bones on the lower jaw,“pseudangular” process of the dentary, a large inter�clavicle immovably connected to the clavicle, a proc�oracoid, and lack a supraspinous fossa of the scapula(Kermack et al., 1973; Jenkins and Parrington, 1976).The differences from monotremes include the number(more than three) and pretribosphenic structure ofmolars and the position of Meckel’s groove, which isassociated with the mandibular foramen.

The above review shows that henosferids from theMiddle–Upper Jurassic of Argentina and, probably,Madagascar (Flynn et al., 1999; Rauhut et al., 2002;Martin and Rauhut, 2005; Rougier et al., 2007b) arethe best candidates for the ancestor of Monotremata.This hypothesis is attractive because of suitable geo�logical age of Henosferida (the earliest monotremesare dated Early Cretaceous) and their geographicalposition in Gondwanian supercontinent, wheremonotremes probably emerged. New paleontologicaldata are required to gain a better understanding of thephylogenetic position of monotremes.

To summarize it should be noted that, of all hypoth�eses for the phylogenetic position of monotremes, thevariant reconstructed here most closely corresponds tothe concept developed by Tatarinov (2001) based onother arguments and implying that this group branchedoff between morganucodonts and docodonts.

ACKNOWLEDGMENTS

We are grateful to T. Rich (Queen VictoriaMuseum, Melbourne, Australia) for discussions onthe origin of monotremes, E. Buchholtz (WellesleyCollege, Wellesley, United States) and A.N. Kuz�netsov (Moscow State University, Moscow, Russia) foradvice on the lumbar vertebrae of monotremes. We arealso grateful to A.N. Kuznetsov for reviewing thepaper and many remarks that allowed us to improvethe text.

This study was supported by the Board of the Presidentof Russian Federation (project no. MD�802.2009.4),Russian Foundation for Basic Research (projectnos. 07�04�00393, 10�04�01350, and 13�04�01401),and the Program of the Presidium of the RussianAcademy of Sciences “Problems of the Origin of Lifeand Formation of the Biosphere.”

REFERENCES

Abel, O., Neue Untersuchungen uber Desmostylus, einenMonotremen aus dem Tertiar der pazifischen Kustenre�gion, Verhandl. Kais.�Kön. Zool.–Botan. Ges. Wien, 1926,vol. 74, pp. 134–138.

Adams, L.A., A memoir on the phylogeny of the jaw musclesin Recent and fossil vertebrates, Ann. New York Acad. Sci.,1919, vol. 28, pp. 51–166.

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

ON THE PHYLOGENETIC POSITION OF MONOTREMES 441

Agadjanian, A.K., Questions of early adaptive radiation ofmammals, Paleontol. Zh., 2003, no. 1, pp. 78–91.Allin, E.F., Evolution of the mammalian middle ear,J. Morphol., 1975, vol. 147, pp. 403–436.Ameghino, F., El arco escapular de los edentados ymonotremos y el origen reptiloide de estos dos grupos demamiferos, An. Mus. Nacion. Buenos Aires Ser. 3, 1908,vol. 10, pp. 1–91.Archer, M., Flannery, T.F., Ritchie, A., and Molnar, R.E.,First Mesozoic mammal from Australia—an Early Creta�ceous monotreme, Nature, 1985, vol. 318, no. 6044,pp. 363–366.Archer, M., Jenkins, F.A., Hand, S.J., et al., Description ofthe skull and non�vestigial dentition of a Miocene platypusObdurodon dicksoni n. sp. from Riversleigh, Australia, andthe problem of monotreme origins, in Platypus and Echid�nas, Augee, M.L., Ed., Sydney: Roy. Zool. Soc. New SouthWales, 1992, pp. 15–27.Archer, M., Murray, P., Hand, S.J., and Godthelp, H.,Reconsideration of monotreme relationships based on theskull and dentition of the Miocene Obdurodon dicksoni, inMammal Phylogeny: Mesozoic Differentiation, Multituberculates,Monotremes, Early Therians, and Marsupials, Szalay, F.S.,Novacek, M.J., and McKenna, M.C., Eds., New York:Springer Verlag, 1993, pp. 75–94.Asher, R.J., Lin, K.H., Kardjilov, N., and Hautier, L., Vari�ability and constraint in the mammalian vertebral column,J. Evol. Biol., 2011, vol. 24, no. 5, pp. 1080–1090.Averianov, A.O., Archibald, J.D., and Ekdale, E.G., Newmaterial of the Late Cretaceous deltatheroidan mammalSulestes from Uzbekistan and phylogenetic reassessment ofthe metatherian–eutherian dichotomy, J. Syst. Palaeontol.,2010a, vol. 8, no. 3, pp. 301–330.Averianov, A.O. and Lopatin, A.V., Phylogeny of tricon�odonts and symmetrodonts and the origin of extant mam�mals, Dokl. Akad. Nauk, 2011, vol. 436, no. 2, pp. 276–279.Averianov, A.O., Lopatin, A.V., Skutschas, P.P., et al., Dis�covery of Middle Jurassic mammals from Siberia, ActaPalaeontol. Polon., 2005, vol. 50, no. 4, pp. 789–797.Averianov, A.O., Lopatin, A.V., Krasnolutskii, S.A., andIvantsov, S.V., New docodontans from the Middle Jurassicof Siberia and reanalysis of docodonta interrelationships,Proc. Zool. Inst. Russ. Acad. Sci., 2010b, vol. 314, no. 2,pp. 121–148.Averianov, A., Martin, T., and Lopatin, A., A new phylog�eny for basal Trechnotheria and Cladotheria and affinitiesof South American endemic Late Cretaceous mammals,Naturwissenschaften, 2013, vol. 100, no. 4, pp. 311–326.Bever, G.S., Rowe, T., Ekdale, E.G., et al., Comment on“independent” origins of middle ear bones in monotremesand “therians” (I), Science, 2005, vol. 309, no. 5740,p. 1492.Bininda�Emonds, O.R.P., Cardillo, M., Jones, K.E., et al.,The delayed rise of present�day mammals, Nature, 2007,vol. 446, no. 7135, pp. 507–512.Buchholtz, E.A., Bailin, H.G., Laves, S.A., et al., Fixedcervical count and the origin of the mammalian diaphragm,Evol. Devel., 2012, vol. 14, no. 5, pp. 399–411.Butler, P.M., Docodont molars as tribosphenic analogues(Mammalia, Jurassic), Mem. Mus. Nat. Hist. Natur. ParisSer. C, 1988, vol. 53 (Teeth Revisited: Proceedings of the

VII International Symposium on Dental Morphology,Paris, 1986), pp. 329–340.Cave, A.J.E., Observations on the monotreme interclavicle,J. Zool., 1970, vol. 160, no. 3, pp. 297–312.

Chen, M. and Luo, Z.�X., Postcranial skeleton of the Cre�taceous mammal Akidolestes cifellii and its locomotor adap�tations, J. Mammal. Evol., 2013, vol. 20, pp. 1–31.Chow, M.�C. and Rich, T.H.V., Shuotherium dongi, n. gen.and n. sp., a therian with pseudo�tribosphenic molars fromthe Jurassic of Sichuan, China, Austral. Mammal., 1982,vol. 5, pp. 127–142.

Cope, E.D., The Multituberculata monotremes, Am.Natur., 1888, no. 22, p. 259.Crompton, A.W., The origin of the tribosphenic molar,Zool. J. Linn. Soc., 1971, vol. 50, no. suppl. 1, pp. 65–87.

Crompton, A.W. and Jenkins, F.A., Origin of mammals, inMesozoic Mammals: The First Two�thirds of MammalianHistory, Lillegraven, J.A., Kielan�Jaworowska, Z., and Cle�mens, W.A., Eds., Berkeley: Univ. California Press, 1979,pp. 59–73.

Crompton, A.W. and Kielan�Jaworowska, Z., Molar struc�ture and occlusion in Cretaceous therian mammals, inStudies in the Development, Function and Evolution of Teeth,Butler, P.M. and Joysey, K.A., Eds., London: AcademicPress, 1978, pp. 249–287.Crompton, A.W. and Luo, Z.�X., Relationships of the Lias�sic mammals, Sinoconodon, Morganucodon oehleri, andDinnetherium, in Mammal Phylogeny: Mesozoic Differentia�tion, Multituberculates, Monotremes, Early Therians, andMarsupials, Szalay, F.S., Novacek, M.J., and McKenna, M.C.,Eds., New York: Springer Verlag, 1993, pp. 30–44.

Crompton, A.W. and Sun, A., Cranial structure and rela�tionships of the Liassic mammal Sinoconodon, Zool. J. Linn.Soc., 1985, vol. 85, pp. 99–119.Davis, B.M., Evolution of the tribosphenic molar pattern inearly mammals, with comments on the “dual�origin”hypothesis, J. Mammal. Evol., 2011, vol. 18, no. 4, pp. 227–244.

De Beer, G.R., Studies on the vertebrate head: II. The orb�itotemporal region of the skull, Quarter. J. Microscop. Sci.,1926, vol. 70, pp. 263–370.De Beer, G.R., The Development of the Vertebrate Skull,Oxford: Clarendon Press, 1937.

Diogo, R., Abdala, V., Lonergan, N., and Wood, B.A.,From fish to modern humans—comparative anatomy,homologies and evolution of the head and neck muscula�ture, J. Anat., 2008, vol. 213, no. 4, pp. 391–424.

Doran, A.H.G., Morphology of the mammalian ossiculaauditus, Trans. Linn. Soc. London, 1878, vol. 2, no. 7,pp. 371–497.Edgeworth, F.H., The Cranial Muscles of Vertebrates, Cam�bridge: Univ. Press, 1935.

Evans, S.E., On the question of epipubic bones in morganu�codontids, J. Paleontol., 1984, vol. 58, no. 5, p. 1339.Fleischer, G., Evolutionary principles of the mammalianmiddle ear, Adv. Anat. Embryol. Cell Biol., 1978, vol. 55,no. 5, pp. 3–70.

Flynn, J.J., Parrish, J.M., Rakotosamimanana, B., et al.,the Middle Jurassic mammal from Madagascar, Nature,1999, vol. 401, no. 6877, pp. 57–60.

442

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

AVERIANOV, LOPATIN

Fox, R.C., Molar structure and function in the Early Creta�ceous mammal Pappotherium: Evolutionary implicationsfor Mesozoic Theria, Can. J. Earth Sci., 1975, vol. 12, no. 3,pp. 412–442.Fox, R.C. and Meng, J., An X�radiographic and SEM studyof the osseous inner ear of multituberculates andmonotremes (Mammalia): Implications for mammalianphylogeny and the evolution of hearing, Zool. J. Linn. Soc.,1997, vol. 121, no. 3, pp. 249–291.Gaetano, L.C. and Rougier, G.W., New materials of Argen�toconodon fariasorum (Mammaliaformes, Triconodontidae)from the Jurassic of Argentina and its bearing on tricon�odont phylogeny, J. Vertebr. Paleontol., 2011, vol. 31, no. 4,pp. 829–843.Gambaryan, P.P. and Kielan�Jaworowska, Z., Masticatorymusculature of Asian taeniolabidoid multituberculatemammals, Acta Palaeontol. Polon., 1995, vol. 40, no. 1,pp. 45–108.Gaudin, T.J., Wible, J.R., Hopson, J.A., and Turnbull, W.D.,Reexamination of the morphological evidence for thecohort Epitheria (Mammalia, Eutheria), J. Mammal. Evol.,1996, vol. 3, no. 1, pp. 1–79.Gaupp, E., Über die Ala temporalis des Säugetierschädelsund die Regio orbitalis einiger anderer Wiebeltierschädels,Anat. Hefte, 1902, vol. 19, pp. 155–230.Gaupp, E., Neue Deutungen auf dem Gebiete der Lehrevom Säugetierschädel, Anat. Anzeiger., 1905, vol. 27,pp. 273–310.Gaupp, E., Zur Entwicklungsgeschichte und vergleichendeMorphologie des Schädels von Echidna aculeata var. Typ�ica, in Denkschriften der Medizinisch�Naturwissenschaftli�chen Gesellschaft zu Jena, 1908, vol. 6, pp. 539–788.Gow, C.E., A new skull of Megazostrodon (Mammalia, Tri�conodonta) from the Elliot Formation (Lower Jurassic) ofsouthern Africa, Palaeontol. Afr., 1986, vol. 26, pp. 13–26.Green, H.L.H.H., The development and morphology ofthe teeth of Ornithorhynchus, Phil. Trans. Roy. Soc. LondonSer. B Biol. Sci., 1937, vol. 288, no. 555, pp. 367–420.Gregory, W.K., The monotremes and the palimpset theory,Bull. Am. Mus. Natur. Hist., 1947, vol. 88, pp. 1–52.Gurovich, Y. and Beck, R.M.D., The phylogenetic affini�ties of the enigmatic mammalian clade Gondwanatheria,J. Mammal. Evol., 2009, vol. 16, no. 1, pp. 25–49.Hopson, J.A., The braincase of the advanced mammal�likereptile Bienotherium, Postilla, 1964, vol. 87, pp. 1–30.Hopson, J.A., The origin of the mammalian middle ear,Am. Zool., 1966, vol. 6, no. 3, pp. 437–450.Hopson, J.A., Synapsid evolution and the radiation of non�eutherian mammals, in Major Features of Vertebrate Evolu�tion: Short Courses in Paleontology, Prothero, D.R. andSchoch, R.M., Eds., Knoxville–Tennessee: Paleontol.Soc., 1994, pp. 190–219.Hopson, J.A. and Rougier, G.W., Braincase structure in theoldest known skull of a therian mammal: Implications formammalian systematics and cranial evolution, Am. J. Sci.,1993, vol. 293A, pp. 268–299.Hu, Y.�M., Meng, J., Wang, Y.�Q., and Li, C.�K., LargeMesozoic mammals fed on young dinosaurs, Nature, 2005,vol. 433, no. 7022, pp. 149–152.Hu, Y.�M., Wang, Y.�Q., Luo, Z.�X., and Li, C.�K., A newsymmetrodont mammal from China and its implications

for mammalian evolution, Nature, 1997, vol. 390, no. 6656,pp. 137–142.Hurum, J.H. and Kielan�Jaworowska, Z., Postcranial skel�eton of multituberculate mammal Catopsbaatar, ActaPalaeontol. Polon., 2008, vol. 53, no. 4, pp. 545–566.Hurum, J.H., Luo, Z.�X., and Kielan�Jaworowska, Z.,Were mammals originally venomous?, Acta Palaeontol.Polon., 2006, vol. 51, no. 1, pp. 1–11.Hurum, J.H., Presley, R., and Kielan�Jaworowska, Z.,Multituberculate ear ossicles, in Sixth Symposium on Meso�zoic Terrestrial Ecosystems and Biota: Short Papers, Sun, A.and Wang, Y., Eds., Beijing: China Ocean Press, 1995,pp. 243–246.Ivakhnenko, M.F., Eotherapsid hypothesis for the origin ofMonotremata, Paleontol. Zh., 2009, no. 3, pp. 3–16.Jenkins, F.A., Occlusion in Docodon (Mammalia, Doc�odonta), Postilla, 1969, vol. 139, pp. 1–24.Jenkins, F.A., Cynodont postcranial anatomy and the “pro�totherian” level of mammalian organization, Evolution,1970, vol. 24, no. 1, pp. 230–252.Jenkins, F.A., The postcranial skeleton of African cyn�odonts, Bull. Peabody Mus. Natur. Hist., 1971, vol. 36,pp. 1–216.Jenkins, F.A., A survey of mammalian origins, Univ. Ten�nessee Dep. Geol. Sci. Stud. Geol., 1984, vol. 8, pp. 32–47.Jenkins, F.A., Crompton, A.W., and Downs, W.R., Meso�zoic mammals from Arizona: New evidence on mammalianevolution, Science, 1983, vol. 222, no. 4629, pp. 1233–1235.Jenkins, F.A. and Parrington, F.R., The postcranial skele�tons of the Triassic mammals Eozostrodon, Megazostrodonand Erythrotherium, Phil. Trans. Roy. Soc. London Ser. BBiol. Sci., 1976, vol. 273, no. 926, pp. 387–431.Jenkins, F.A. and Schaff, C.R., The Early Cretaceousmammal Gobiconodon (Mammalia, Triconodonta) from theCloverly Formation in Montana, J. Vertebr. Paleontol.,1988, vol. 8, no. 1, pp. 1–24.Ji, Q., Luo, Z.�X., and Ji, S.�A., A Chinese triconodontmammal and mosaic evolution of mammalian skeleton,Nature, 1999, vol. 398, no. 6725, pp. 326–330.Ji, Q., Luo, Z.�X., Yuan, C.�X., et al., The earliest knowneutherian mammal, Nature, 2002, vol. 416, no. 6883,pp. 816–822.Ji, Q., Luo, Z.�X., Yuan, C.�X., and Tabrum, A.R., A swim�ming mammaliaform from the Middle Jurassic and eco�morphological diversification of early mammals, Science,2006, vol. 311, no. 5764, pp. 1123–1127.Ji, Q., Luo, Z.�X., Zhang, X., et al., Evolutionary develop�ment of the middle ear in Mesozoic therian mammals,Science, 2009, vol. 326, no. 5950, pp. 278–281.Kemp, T.S., The primitive cynodont Procynosuchus: Func�tional anatomy of the skull and relationships, Phil. Trans.Roy. Soc. London Ser. B Biol. Sci., 1979, vol. 285, no. 1005,pp. 73–122.Kemp, T.S., Aspects of the structure and functional anat�omy of the Middle Triassic cynodont Luangwa, J. Zool.,1980a, vol. 191, no. 2, pp. 193–239.Kemp, T.S., The primitive cynodont Procynosuchus: Struc�ture, function and evolution of the postcranial skeleton,Phil. Trans. Roy. Soc. London Ser. B Biol. Sci., 1980b,vol. 288, no. 1027, pp. 217–258.

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

ON THE PHYLOGENETIC POSITION OF MONOTREMES 443

Kemp, T.S., The relationships of mammals, Zool. J. Linn.Soc., 1983, vol. 77, no. 4, pp. 353–384.Kermack, K.A., The cranial structure of the triconodonts,Phil. Trans. Roy. Soc. London Ser. B Biol. Sci., 1963,vol. 246, no. 727, pp. 83–103.Kermack, K.A. and Kielan�Jaworowska, Z., Therian andnon�therian mammals, Zool. J. Linn. Soc. London, 1971,vol. 50, suppl. 1, pp. 103–115.Kermack, K.A. and Mussett, F., The jaw articulation of thedocodonta and the classification of Mesozoic mammals,Proc. Roy. Soc. London Ser. B Biol. Sci., 1958, vol. 149,no. 935, pp. 204–215.Kermack, K.A., Mussett, F., and Rigney, H.W., The lowerjaw of Morganucodon, Zool. J. Linn. Soc., 1973, vol. 53,pp. 87–175.Kielan�Jaworowska, Z., Discovery of a multituberculatemarsupial bone, Nature, 1969, vol. 222, no. 5198,pp. 1091–1092.Kielan�Jaworowska, Z., Possible occurrence of marsupialbones in Cretaceous eutherian mammals, Nature, 1975,vol. 255, no. 5511, pp. 698–699.Kielan�Jaworowska, Z., Interrelationships of Mesozoicmammals, Hist. Biol., 1992, vol. 6, pp. 185–202.Kielan�Jaworowska, Z., Characters of multituberculatesneglected in phylogenetic analyses of early mammals,Lethaia, 1997, vol. 29, no. 3, pp. 249–266.Kielan�Jaworowska, Z., Cifelli, R.L., and Luo, Z.�X.,Alleged Cretaceous placental from down under, Lethaia,1998, vol. 31, no. 3, pp. 267–268.Kielan�Jaworowska, Z., Cifelli, R.L., and Luo, Z.�X.,Mammals from the Age of Dinosaurs: Origins, Evolution, andStructure, New York: Columbia Univ. Press, 2004.Kielan�Jaworowska, Z., Crompton, A.W., and Jenkins, F.A.,The origin of egg�laying mammals, Nature, 1987, vol. 326,no. 6116, pp. 871–873.Kielan�Jaworowska, Z. and Dashzeveg, D., Eutherianmammals from the Early Cretaceous of Mongolia, Zool.Scripta, 1989, vol. 18, pp. 347–355.Kielan�Jaworowska, Z. and Gambaryan, P.P., Postcranialanatomy and habits of Asian multituberculate mammals,Fossils and Strata, 1994, vol. 36, pp. 1–92.Kielan�Jaworowska, Z., Presley, R., and Poplin, C.M., Thecranial vascular system in taeniolabidoid multituberculatemammals, Phil. Trans. Roy. Soc. London Ser B Biol. Sci.,1986, vol. 313, no. 1164, pp. 525–602.Klima, M., Early development of the shoulder girdle andsternum in marsupials (Mammalia: Metatheria), Adv. Anat.Embryol. Cell Biol., 1987, vol. 109, pp. 1–91.Krause, D.W. and Jenkins, F.A., The postcranial skeleton ofNorth American multituberculates, Bull. Mus. Compar.Zool., 1983, vol. 150, pp. 199–246.Krebs, B., Das skelett von Henkelotherium guimarotae gen.et sp. nov. (Eupantotheria, Mammalia) aus dem OberenJura von Portugal, Berl. Geowiss. Abh. A Geol. Palaeontol.,1991, vol. 133, pp. 1–121.Kuhn, H.�J., Die Entwicklung und Morphologie desSchädels von Tachyglossus aculeatus, Abh. Senckenb. Natur�forsch. Ges., 1971, vol. 528, pp. 1–192.Kuhn, H.�J. and Zeller, U., The cavum epiptericum inmonotremes and therian mammals, Mammalia Depicta,1987, no. 13, pp. 51–70.

Kühne, W.G., The Liassic Therapsid Oligokyphus, London:Brit. Mus. Natur. Hist., 1956.Kühne, W.G., The systematic position of monotremesreconsidered (Mammalia), Z. Morphol. Tiere, 1973, vol. 75,no. 1, pp. 59–64.Kühne, W.G., On the Marsupionta, a reply to dr. Par�rington, J. Natur. Hist., 1977, vol. 11, pp. 225–228.Leche, W., Zur Frage nach der stammesgeschichtlichenBedeutung des Milchgebisses bei den Säugetieren: 1. Zool�ogische Jahrbücher, Abt. Syst. Okol. Geogr. Tiere, 1910,vol. 28, no. 4, pp. 449–456.Lessertisseur, J. and Saban, R., Squelette axial, in Traité dezoologie. Anatomie, systématique, biologie, vol. 16: Mam�mifères. Fasc. I. Téguments et squelette, Grassé, P.�P., Ed.,Paris: Maison et Cie, 1967, pp. 584–708.Li, G. and Luo, Z.�X., A Cretaceous symmetrodont therianwith some monotreme�like postcranial features, Nature,2006, vol. 439, no. 7073, pp. 195–200.Lopatin, A.V., Maschenko, E.N., Averianov, A.O., et al.,Early Cretaceous mammals of Western Siberia. 1. Tinodon�tidae, Paleontol. Zh., 2005, no. 5, pp. 62–72.Luckett, W.P. and Zeller, U., Developmental evidence fordental homologies in the monotreme Ornithorhynchus andits systematic implications, Z. Saugetierkunde, 1989,vol. 54, no. 4, pp. 193–204.Luo, Z.�X., Developmental patterns in Mesozoic evolutionof mammal ears, Ann. Rev. Ecol. Evol. Syst., 2011, vol. 42,pp. 355–380.Luo, Z.�X., Chen, P., Li, G., and Chen, M., A new eutri�conodont mammal and evolutionary development in earlymammals, Nature, 2007a, vol. 446, no. 7133, pp. 288–293.Luo, Z.�X., Cifelli, R.L., and Kielan�Jaworowska, Z., Dualorigin of tribosphenic mammals, Nature, 2001a, vol. 409,no. 6816, pp. 53–57.Luo, Z.�X., Crompton, A.W., and Sun, A., A new mamma�liaform from the Early Jurassic of China and evolution ofmammalian characteristics, Science, 2001b, vol. 292,no. 5521, pp. 1535–1540.Luo, Z.�X. and Ji, Q., New study on dental and skeletal fea�tures of the Cretaceous “symmetrodontan” mammalZhangheotherium, J. Mammal. Evol., 2005, vol. 12, nos. 3/4,pp. 337–357.Luo, Z.�X., Ji, Q., and Yuan, C.�X., Convergent dentaladaptations in pseudo�tribosphenic and tribosphenic mam�mals, Nature, 2007b, vol. 450, no. 7166, pp. 93–97.Luo, Z.�X., Kielan�Jaworowska, Z., and Cifelli, R.L., Inquest for a phylogeny of Mesozoic mammals, Acta Palaeontol.Polon., 2002, vol. 47, no. 1, pp. 1–78.Luo, Z.�X., Ruf, I., and Martin, T., The petrosal and innerear of the Late Jurassic cladotherian mammal Dryolestesleiriensis and implications for ear evolution in therian mam�mals, Zool. J. Linn. Soc., 2012, vol. 166, no. 2, pp. 433–463.Luo, Z.�X. and Wible, J.R., A Late Jurassic digging mam�mal and early mammalian diversification, Science, 2005,vol. 308, no. 5718, pp. 103–107.Luo, Z.�X., Yuan, C.�X., Meng, Q.�J., and Ji, Q., A Juras�sic eutherian mammal and divergence of marsupials andplacentals, Nature, 2011, vol. 476, no. 7361, pp. 442–445.Macrini, T.E., Rougier, G.W., and Rowe, T.B., Descriptionof a cranial endocast from the fossil mammal Vincelestesneuquenianus (Theriiformes) and its relevance to the evolu�

444

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

AVERIANOV, LOPATIN

tion of endocranial characters in therians, Anat. Rec., 2007,vol. 290, no. 7, pp. 875–892.

Maier, W., The ontogenetic development of the orbitotem�poral region in the skull of Monodelphis domestica (Didel�phidae, Marsupialia) and the problem of the mammalianalisphenoid, Mam. Dep., 1987, vol. 13, pp. 71–90.

Maier, W., Ala temporalis and alisphenoid in therian mam�mals, in Trends in Vertebrate Morphology, Splechtna, H. andHilgers, H., Eds., Stuttgart: Fischer, 1989, pp. 396–400.

Martin, T., Postcranial anatomy of Haldanodon exspectatus(Mammalia, Docodonta) from the Late Jurassic (Kim�meridgian) of Portugal and its bearing for mammalian evo�lution, Zool. J. Linn. Soc., 2005, vol. 145, no. 2, pp. 219–248.

Martin, T. and Rauhut, O.W.M., Mandible and dentition ofAsfaltomylos patagonicus (Australosphenida, Mammalia)and the evolution of tribosphenic teeth, J. Vertebr. Paleon�tol., 2005, vol. 25, no. 2, pp. 414–425.

McKenna, M.C., On the shoulder girdle of the mammaliansubclass Allotheria, Am. Mus. Novit., 1961, no. 2066, pp. 1–27.

McKenna, M.C., Towards a phylogenetic classification ofthe Mammalia, in Phylogeny of the Primates, Luckett, W.P.and Szalay, F.S., Eds., New York: Plenum Press, 1975,pp. 21–46.

Meng, J., The stapes of Lambdopsalis bulla (Multitubercu�lata) and transformational analyses on some stapedial fea�tures in mammaliaformes, J. Vertebr. Paleontol., 1992,vol. 12, no. 4, pp. 459–471.

Meng, J., Hu, Y.�M., Wang, Y.�Q., and Li, C.�K., The ossi�fied Meckel’s cartilage and internal groove in Mesozoicmammaliaforms: Implications to origin of the definitivemammalian middle ear, Zool. J. Linn. Soc., 2003, vol. 138,no. 4, pp. 431–448.

Meng, J., Hu, Y.�M., Wang, Y., et al., A Mesozoic glidingmammal from northeastern China, Nature, 2006, vol. 444,no. 7121, pp. 889–893.

Meng, J., Wang, Y., and Li, C.�K., Transitional mammalianmiddle ear from a new Cretaceous Jehol eutriconodont,Nature, 2011, vol. 472, no. 7342, pp. 181–185.

Meng, J. and Wyss, A.R., Monotreme affinities and low�frequency hearing suggested by multituberculate ear,Nature, 1995, vol. 377, no. 6545, pp. 141–144.

Miao, D. and Lillegraven, J.A., Discovery of three ear ossi�cles in a multituberculate mammal, Nat. Geogr. Res., 1986,vol. 2, no. 4, pp. 500–507.

Moore, W.J., The Mammalian Skull, Cambridge: Cam�bridge Univ. Press, 1981.

Murray, P.F., A unique jaw mechanism in the echidna,Tachyglossus aculeatus (Monotremata), Aust. J. Zool., 1981,vol. 29, no. 1, pp. 1–5.

Musser, A.M. and Archer, M., New information about theskull and dentary of the Miocene platypus Obdurodon dick�soni, and a discussion of ornithorhynchid relationships,Phil. Trans. Roy. Soc. London Ser. B Biol. Sci., 1998,vol. 353, no. 1372, pp. 1063–1079.

Narita, Y. and Kuratani, S., Evolution of the vertebral for�mulae in mammals: A perspective on developmental con�straints, J. Experiment. Zool. Pt B Mol. Develop. Evol., 2005,vol. 304, no. 2, pp. 91–106.

Novacek, M.J., Rougier, G.W., Wible, J.R., et al., Epipubicbones in eutherian mammals from the Late Cretaceous ofMongolia, Nature, 1997, vol. 389, no. 6650, pp. 483–486.

Novacek, M.J. and Wyss, A.R., Origin and transformationof the mammalian stapes, Contrib. Geol. Univ. WyomingSpec. Pap., 1986, no. 3, pp. 35–53.

O’Leary, M.A., Bloch, J.I., Flynn, J.J., et al., The placentalmammal ancestor and the post�K�Pg radiation of placen�tals, Science, 2013, vol. 339, no. 6120, pp. 662–667.

Parrington, F.R., The angular process of the dentary, Ann.Mag. Natur. Hist. Ser. 13, 1959, vol. 2, no. 20, pp. 505–512.

Parrington, F.R., The problem of the origin of themonotremes, J. Natur. Hist., 1974, vol. 8, no. 4, pp. 421–426.

Pascual, R. and Goin, F.J., Non�tribosphenic Gondwanamammals, and the alternative development of molars with areversed triangle cusp pattern, in Publ. Espec. Asoc. Paleontol.Argent., 2001, no. 7 (VII International Symposium onMesozoic Terrestrial Ecosystems), pp. 157–162.

Pascual, R., Goin, F.J., Balarino, L., and Udrizar, D.E.,New data on the Paleocene monotreme Monotrematumsudamericanum, and the convergent evolution of triangulatemolars, Acta Palaeontol. Polon., 2002, vol. 47, pp. 487–492.

Patterson, B., Early Cretaceous mammals and the evolutionof mammalian molar teeth, Fieldiana. Geol., 1956, vol. 13,no. 1, pp. 1–105.

Pfretzschner, H.�U., Martin, T., Maisch, M.W., et al., Anew docodont mammal from the Late Jurassic of the Jung�gar Basin in northwest China, Acta Palaeontol. Polon., 2005,vol. 50, no. 4, pp. 799–808.

Poulton, E.B., True teeth in the young Ornithorhynchus par�adoxus, Proc. Roy. Soc. London, 1888, vol. 43, pp. 353–356.

Poulton, E.B., The true teeth and horny plates of Ornitho�rhynchus, Quart. J. Microscop. Sci., 1889, vol. 29, pp. 9–48.

Presley, R., The braincase in Recent and Mesozoic ther�apsids, Mem. Soc. Geol. France. NS, 1980, vol. 139,pp. 159–162.

Presley, R., Alisphenoid equivalents in placentals, marsupi�als, monotremes and fossils, Nature, 1981, vol. 294,no. 5842, pp. 668–670.

Presley, R. and Steel, F.L.D., On the homology of thealisphenoid, J. Anat., 1976, vol. 121, no. 3, pp. 441–459.

Prothero, D.R., New Jurassic mammals from Como Bluff,Wyoming, and the interrelationships of non�tribosphenicTheria, Bull. Am. Mus. Natur. Hist., 1981, no. 167, pp. 281–325.

Rauhut, O.W.M., Martin, T., Ortiz�Jaureguizar, E.O., andPuerta, P.F., A Jurassic mammal from South America,Nature, 2002, vol. 416, no. 6877, pp. 165–168.

Reilly, S.M., McElroy, E.J., and White, T.D., Abdominalmuscle function in ventilation and locomotion in new worldopossums and basal eutherians: Breathing and running withand without epipubic bones, J. Morphol., 2009, vol. 270,no. 8, pp. 1014–1028.

Reilly, S.M., McElroy, E.J., White, T.D., et al., Abdominalmuscle and epipubic bone function during locomotion inAustralian possums: Insights to basal mammalian condi�tions and eutherian�like tendencies in Trichosurus, J. Mor�phol., 2010, vol. 271, no. 4, pp. 438–450.

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

ON THE PHYLOGENETIC POSITION OF MONOTREMES 445

Reilly, S.M. and White, T.D., Hypaxial motor patterns and thefunction of epipubic bones in primitive mammals, Science,2003, vol. 299, no. 5605, pp. 400–402.

Reiss, K.Z., Myology of the feeding apparatus of myrme�cophagid anteaters (Xenarthra: Myrmecophagidae),J. Mammal. Evol., 1997, vol. 4, no. 2, pp. 87–117.

Rich, T.H.V., Flannery, T.F., Trusler, P., et al., A second tri�bosphenic mammal from the Mesozoic of Australia, Rec.Queen Victoria Mus., 2001, vol. 110, pp. 1–9.

Rich, T.H.V., Flannery, T.F., Trusler, P., et al., Evidence thatmonotremes and ausktribosphenids are not sistergroups,J. Vertebr. Paleontol., 2002, vol. 22, no. 2, pp. 466–469.

Rich, T.H.V., Hopson, J.A., and Musser, A.M., Indepen�dent origins of middle ear bones in monotremes and theri�ans, Science, 2005a, vol. 307, no. 5711, pp. 910–914.

Rich, T.H.V., Hopson, J.A., Musser, A.M., et al., Responseto comments on “independent origins of middle ear bonesin monotremes and therians”, Science, 2005b, vol. 309,no. 5740, p. 1492.

Rich, T.H.V., Vickers�Rich, P., Constantine, A., et al.,A tribosphenic mammal from the Mesozoic of Australia,Science, 1997, vol. 278, no. 5342, pp. 1438–1442.

Rich, T.H.V., Vickers�Rich, P., Constantine, A., et al.,Early Cretaceous mammals from Flat Rocks, Victoria, Aus�tralia, Rec. Queen Victoria Mus., 1999, vol. 106, pp. 1–29.

Romer, A.S., Osteology of the Reptiles, Chicago: Univ. Chi�cago Press, 1956.

Romer, A.S., The Vertebrate Body, Philadelphia: W.B.Saunders Co., 1970.

Rougier, G.W., Apesteguia, S., and Gaetano, L.C., Highlyspecialized mammalian skulls from the Late Cretaceous ofSouth America, Nature, 2011, vol. 479, no. 7371, pp. 98–102.

Rougier, G.W., Forasiepi, A.M., and Martinelli, A.G.,Comment on “independent origins of middle ear bones inmonotremes and therians” (II), Science, 2005, vol. 309,no. 5740, p. 1492.

Rougier, G.W., Isaji, S., and Manabe, M., An Early Creta�ceous mammal from the Kuwajima Formation (TetoriGroup), Japan, and a reassessment of triconodont phylog�eny, Ann. Carnegie Mus., 2007a, vol. 76, no. 2, pp. 73–115.

Rougier, G.W., Ji, Q., and Novacek, M.J., A new symmet�rodont mammal with fur impressions from the Mesozoic ofChina, Acta Geol. Sin., 2003, vol. 77, no. 1, pp. 7–14.

Rougier, G.W., Martinelli, A.G., Forasiepi, A.M., andNovacek, M.J., New Jurassic mammals from Patagonia,Argentina: A reappraisal of australosphenidan morphologyand interrelationships, Am. Mus. Novit., 2007b, no. 3566,pp. 1–54.

Rougier, G.W. and Wible, J.R., Major changes in the earregion and basicranium of early mammals, in Amniote Pale�obiology: Phylogenetic and Functional Perspectives on theEvolution of Mammals, Birds and Reptiles, Carrano, M.T.,Gaudin, T.J., Blob, R.W., and Wible, J.R., Eds., Chicago:Univ. Chicago Press, 2006, pp. 269–311.

Rougier, G.W., Wible, J.R., and Hopson, J.A., Reconstruc�tion of the cranial vessels in the Early Cretaceous mammalVincelestes neuquenianus: Implications for the evolution ofthe mammalian cranial vascular system, J. Vertebr. Paleontol.,1992, vol. 12, no. 2, pp. 188–216.

Rougier, G.W., Wible, J.R., and Hopson, J.A., Basicranialanatomy of Priacodon fruitaensis (Triconodontidae, Mam�malia) from the Late Jurassic of Colorado, and a reappraisalof mammaliaform interrelationships, Am. Mus. Novit.,1996a, no. 3183, pp. 1–38.Rougier, G.W., Wible, J.R., and Novacek, M.J., Middle�earossicles of Kryptobaatar dashzevegi (Mammalia, Multitu�berculata): Implications for mammaliamorph relationshipsand evolution of the auditory apparatus, Am. Mus. Novit.,1996b, no. 3187, pp. 1–43.Rowe, T.B., Definition, diagnosis, and origin of Mammalia,J. Vertebr. Paleontol., 1988, vol. 8, no. 3, pp. 241–264.Rowe, T.B., Macrini, T.E., and Luo, Z.�X., Fossil evidenceon origin of the mammalian brain, Science, 2011, vol. 332,no. 6032, pp. 955–957.Rowe, T.B., Rich, T.H.V., Vickers�Rich, P., et al., The old�est platypus and its bearing on divergence timing of theplatypus and echidna clades, Proc. Nat. Acad. Sci., 2008,vol. 105, no. 4, pp. 1238–1242.Ruf, I., Luo, Z.�X., Wible, J.R., and Martin, T., Petrosalanatomy and inner ear structures of the Late Jurassic Hen�kelotherium (Mammalia, Cladotheria, Dryolestoidea):Insight into the early evolution of the ear region in cladot�herian mammals, J. Anat., 2009, vol. 214, pp. 679–693.Sereno, P.C., Shoulder girdle and forelimb in multitubercu�lates: evolution of parasagittal forelimb posture in mam�mals, in Amniote Paleobiology: Perspectives on the Evolutionof Mammals, Birds, and Reptiles, Carrano, M.T., Blob, R.W.,Gaudin, T.J., and Wible, J.R., Eds., Chicago: Univ. Chi�cago Press, 2006, pp. 315–366.Standring, S., Gray’s Anatomy: The Anatomical Basis ofClinical Practice, 40th ed., Elsevier, 2008.Starck, D., Le crâne des mammifères, in Traité de Zoologie.Anatomie, systématique, biologie, vol. 16: Mammifères.Fasc. I. Téguments et squelette, Grassé, P.�P., Ed., Paris:Masson et Cie, 1967, pp. 405–549.Starck, D., Das evolutive Plateau Säugetier, Sonderb.Naturwiss. Vereins in Hamburg, 1978, vol. 3, pp. 7–33.Stewart, C., On a specimen of the true teeth of Ornithorhyn�chus, Quart. J. Microscop. Sci., 1892, vol. 33, pp. 229–231.Sues, H.�D. and Jenkins, F.A., The postcranial skeleton ofKayentatherium wellesi from the Lower Jurassic KayentaFormation of Arizona and the phylogenetic significance ofpostcranial features in tritylodontid cynodonts, in AmniotePaleobiology: Perspectivers on the Evolution of Mammals,Birds, and Reptiles, Carrano, M.T., Gaudin, T.J.,Blob, R.W., and Wible, J.R., Eds., Chicago: Univ. ChicagoPress, 2006, pp. 114–152.Tatarinov, L.P., Modern data on the origin of monotremes(Mammalia), Paleontol. Zh., 2001, no. 3, pp. 86–96.Thomas, O., On the dentition of Ornithorhynchus, Proc.Roy. Soc. London, 1890, vol. 46, pp. 126–131.Vickaryous, M.K. and Hall, B.K., Homology of the reptil�ian coracoid and a reappraisal of the evolution and develop�ment of the amniote pectoral apparatus, J. Anat., 2006,vol. 208, no. 3, pp. 263–285.Wang, Y., Clemens, W.A., Hu, Y., and Li, C., A probablepseudo�tribosphenic upper molar from the Late Jurassic ofChina and the early radiation of the Holotheria, J. Vertebr.Paleontol., 1998, vol. 18, no. 4, pp. 777–787.Wang, Y., Hu, Y.�M., Meng, J., and Li, C.�K., An ossifiedMeckel’s cartilage in two Cretaceous mammals and the ori�

446

PALEONTOLOGICAL JOURNAL Vol. 48 No. 4 2014

AVERIANOV, LOPATIN

gin of the mammalian middle ear, Science, 2001, vol. 294,no. 5541, pp. 357–361.

Watson, D.M.S., The monotreme skull: A contribution tomammalian morphogenesis, Phil. Trans. Roy. Soc. LondonSer. B, 1916, vol. 207, pp. 311–374.

Westergaard, B., A new detailed model for mammalian den�titional evolution, J. Zool. Syst. Evol., 1983, vol. 21, no. 1,pp. 68–87.

Wible, J.R., Origin of Mammalia: The craniodental evi�dence reexamined, J. Vertebr. Paleontol., 1991, vol. 11,no. 1, pp. 1–28.

Wible, J.R. and Hopson, J.A., Basicranial evidence for earlymammal phylogeny, in Mammal Phylogeny: Mesozoic Dif�ferentiation, Multituberculates, Monotremes, Early Theri�ans, and Marsupials, Szalay, F.S., Novacek, M.J., andMcKenna, M.C., Eds., New York: Springer Verlag, 1993,pp. 45–62.

Wible, J.R. and Hopson, J.A., Homologies of the prooticcanal in mammals and non�mammalian cynodonts,J. Vertebr. Paleontol., 1995, vol. 15, no. 2, pp. 331–356.

Wible, J.R. and Rougier, G.W., The cranial anatomy ofKryptobaatar dashzevegi (Mammalia, Multituberculata),and its bearing on the evolution of mammalian characters,Bull. Am. Mus. Natur. Hist., 2000, no. 247, pp. 1–124.

Wible, J.R., Rougier, G.W., Novacek, M.J., et al., A mam�malian petrosal from the Early Cretaceous of Mongolia:Implications for the evolution of the ear region and mam�maliamorph relationships, Am. Mus. Novit., 1995, no. 3149,pp. 1–19.

Wible, J.R., Rougier, G.W., Novacek, M.J., and McKen�na, M.C., Earliest eutherian ear region: A petrosal referredto Prokennalestes from the Early Cretaceous of Mongolia,Am. Mus. Novit., 2001, no. 3322, pp. 1–44.

Wilson, J.T. and Hill, J.P., Observations on tooth develop�ment in Ornithorhynchus, Quart. J. Microscop. Sci., 1907,vol. 51, pp. 137–165.Woodburne, M.O., Monotremes as pretribosphenic mam�mals, J. Mammal. Evol., 2003, vol. 10, no. 3, pp. 195–248.Woodburne, M.O., Rich, T.H.V., and Springer, M.S., Theevolution of tribospheny and the antiquity of mammalianclades, Mol. Phylogen. Evol., 2003, vol. 28, no. 2, pp. 360–385.Woodburne, M.O. and Tedford, R.H., The first Tertiarymonotreme from Australia, Am. Mus. Novit., 1975,no. 2588, pp. 1–11.Yuan, C.�X., Ji, Q., Meng, Q.�J., et al., Earliest evolution ofmultituberculate mammals revealed by a new Jurassic fossil,Science, 2013, vol. 341, no. 6147, pp. 779–783.Zeller, U., Die Enwicklung und Morphologie des Schadelsvon Ornithorhynchus anatinus (Mammalia: Prototheria:Monotremata), Abh. Senckenb. Naturforsch. Ges., 1989,vol. 545, pp. 1–188.Zeller, U., Ontogenetic evidence for cranial homologies inmonotremes and therians, with special reference to Orni�thorhynchus, in Mammal Phylogeny: Mesozoic Differentia�tion, Multituberculates, Monotremes, Early Therians, andMarsupials, Szalay, F.S., Novacek, M.J., and McKenna, M.C.,Eds., New York: Springer Verlag, 1993, pp. 95–107.Zheng, X., Bi, S., Wang, X., and Meng, J., A new arborealharamiyid shows the diversity of crown mammals in theJurassic Period, Nature, 2013, vol. 500, no. 7461, pp. 199–202.Zhou, C.�F., Wu, S., Martin, T., and Luo, Z.�X., A Jurassicmammaliaform and the earliest mammalian evolutionaryadaptations, Nature, 2013, vol. 500, no. 7461, pp. 163–167.

Translated by G. Rautian