Multituberculates were the longest-lived order of mammals except for monotremes, recorded with certainty from Upper Jurassic through upper Eocene sediments, a time-span of more than 100 million years (from about 155 to 40 Ma). They have no living descendants. Isolated upper second molars from the Middle Jurassic (Bathonian) of England, assigned to the new genera Kermackodon and Hahnotherium, have recently been identified as multituberculate based on wear and inferred occlusal relationships (Butler and Hooker, 2005). This finding extends the range of the group back another 10 million years. As noted previously, multituber-culates may be related to Late Triassic and Jurassic hara-miyidans, and the two groups are sometimes united in the Allotheria to reflect this relationship. Multituberculates were abundant in many Mesozoic and Early Cenozoic faunas of the northern continents. Recent discoveries have extended their Mesozoic range into northern Africa and South America, although they are still very rare from those regions (and the African teeth may instead belong to haramiyidans, according to Butler and Hooker, 2005). All were small, mostly shrew- to rat-sized, the largest reaching the size of a beaver.

The anatomy of multituberculates has been reviewed by Hahn (1978), Clemens and Kielan-Jaworowska (1979), Krause and Jenkins (1983), and Kielan-Jaworowska et al. (2004), among others. Multituberculates are distinguished by their unique dental complex, which includes in the lower jaw a single enlarged, somewhat rodentlike incisor separated from the cheek teeth by a diastema, no canine, one to four bladelike lower premolars with oblique ridges joined to apical serrations, and molars with multiple low cusps arranged in two longitudinal rows (Figs. 4.8, 4.9). In some multituberculates, including taeniolabidoids and djadochtatheres, the lower incisor is very large and has enamel essentially restricted to the labial half of the tooth. The upper series has one to three incisors, I2 enlarged, usually no canine, and premolars and molars with two or three longitudinally arranged rows of cusps separated by longitudinal grooves. M2 is medially offset relative to M1 in all but the most primitive forms. Consequently the central groove of M2 occludes with the lingual cusp row of M2, whereas the groove of M1 occludes with the buccal cusp row of M1 (Butler and Hooker, 2005). All known multituberculates are dentally so derived that it has not been possible to determine the homologies of the cusps with those of therians. The incisors and the anterior premolars were diphyodont (with deciduous precursors), but only the most primitive multituberculates (Paulchoffatiidae) are known to have had both deciduous and permanent P4. In all others, the bladelike, deciduous P4 seems to have been retained throughout life, and erupted in a unique way, by rotating anterodorsally about 90° into position (Greenwald, 1988).

Analysis of tooth morphology and microwear indicates that most multituberculates had a unique two-stroke masticatory cycle (Krause, 1982). First, food held in place by the last upper premolar was sliced by the bladelike lower pre-molar(s) as the dentary moved orthally (upward). Then the lower jaw moved palinally (backward), grinding the food between the molar cusp rows. Molar occlusion usually occurred bilaterally, although the unfused symphysis probably allowed occasional unilateral occlusion (Wall and Krause, 1992; Gambaryan and Kielan-Jaworowska, 1995). Unlike in most therians, there was no transverse component in the grinding stroke. The second part of the chewing cycle is superficially like the grinding phase in rodents (which is also often bilateral), but in the latter the chewing stroke is propalinal (forward). Although multituberculates have often been considered herbivorous analogues of rodents, considerations of body size and microwear suggest that they were omnivores that consumed a variety of items, including seeds, nuts, and small invertebrates.

The lower jaw of multituberculates is typically short and deep. It is derived compared to that of many other Mesozoic mammals in consisting entirely of the dentary, which articulates with the squamosal; there are no postdentary bones, except for a vestigial coronoid bone in one of the earliest forms, the plagiaulacid Kuehneodon. The symphysis is unfused, which allowed the dentaries to move independently from each other to a considerable extent. The dentary lacks an angular process.

Fig. 4.8. Multituberculate skulls: (A) ptilodontoid; (B, C) taeniolabidoids; (D) djadochtathere. Skull lengths are indicated. (From Kielan-Jaworowska and Hurum, 1997.)

The skull is typically low and broad, with a short, rather wide snout and well-developed zygomatic arches, which consist mainly of the maxilla and squamosal. The jugal, previously thought to be absent, has been identified on the medial side of the arch in several multituberculates (Hop-son et al., 1989). The orbit lacked a bony floor, and the eyes were directed laterally. Elements earlier believed to be plesio-morphic tabular and ectopterygoid bones have since been shown to be parts of the mastoid and alisphenoid, respectively (Kielan-Jaworowska et al., 1986; Hurum, 1998). In fact, no mammal has been shown to have tabular bones. Endo-cranial casts show that the olfactory bulbs of multitubercu-lates were relatively very large. The slightly curved cochlea is also primitive; it resembles that of Morganucodon more than the bent cochlea of monotremes, and differs markedly from the coiled cochlea of marsupials and placentals (Kielan-Jaworowska and Hurum, 2001). The lateral wall of the braincase, however, composed of a reduced alisphenoid and enlarged anterior lamina, is a derived condition shared with monotremes (Hopson and Rougier, 1993). Moreover, multi-tuberculates are seemingly advanced in having three middle-ear ossicles arranged like those in living mammals (Miao and Lillegraven, 1986; Hurum et al., 1996; Rougier et al., 1996b). Whether they are homologous with those of other mammals or evolved independently, however, is a matter of contention.

The postcranial skeleton, known in only a few forms, indicates that multituberculates had epipubic ("marsupial") bones and that the limbs were abducted, probably resulting

Forelimb Contention
Fig. 4.9. Multituberculate lower jaws. "Plagiaulacida" is equivalent to Plagiaula-coidea as used in this chapter. (From Kielan-Jaworowska and Hurum, 2001.)

in a sprawling stance (Kielan-Jaworowska and Gambaryan, 1994; Gambaryan and Kielan-Jaworowska, 1997). At least one multituberculate, the Late Cretaceous djadochtathere Bulganbaatar, may have had a mobile pectoral girdle and more advanced, parasagittal forelimb posture like that of higher therians, based on a specimen with articulated fore-limbs (Sereno and McKenna, 1995). But Gambaryan and Kielan-Jaworowska (1997) challenged this interpretation, which appears to conflict with other evidence. As further discussed below, the few known skeletons display considerable diversity: some multituberculates were specialized for arboreal life, whereas others were terrestrial, and still others were fossorial.

Multituberculates have traditionally been classified in three suborders or superfamilies: Plagiaulacoidea (essentially a primitive grade of Mesozoic multituberculates), and the probably monophyletic Ptilodontoidea and Taeniolabi-doidea (Clemens and Kielan-Jaworowska, 1979; Simmons, 1993). A fourth monophyletic subdivision was recently recognized: Djadochtatherioidea (=Djadochtatheria, hereafter called djadochtatheres), which includes nearly all Late Cretaceous multituberculates of Mongolia (Kielan-Jaworowska and Hurum, 1997, 2001). The last three groups comprise the monophyletic Cimolodonta (McKenna and Bell, 1997; Kielan-Jaworowska and Hurum, 2001). Although plagiaula-coids are grouped essentially by primitive characters, cimo-lodonts are united by several synapomorphies, including the loss of I1, loss of P12, and great reduction or loss of P3 (Kielan-Jaworowska and Hurum, 2001). All cimolodonts have prismatic enamel, whereas most plagiaulacoids lacked prisms. However, the prismatic enamel of cimolodonts almost surely evolved independently from that of therian mammals.

The classification of multituberculates has been especially mercurial in recent years (see the historical review by Kielan-Jaworowska and Hurum, 2001), probably owing chiefly to two factors—the rapid accumulation of new discoveries and the exploration of relationships using cladistic methods. Several new classifications have been proposed in the past decade, but there is currently no generally accepted arrangement. Although most classifications are more or less consistent with the groups listed above, the placement of both genera and higher taxa varies (see, for example, Kielan-Jaworowska et al., 2004).


Plagiaulacoids include the oldest and most primitive multituberculates—families Paulchoffatiidae, Allodontidae, Plagiaulacidae, and a few others (Kielan-Jaworowska and Hurum, 2001; Kielan-Jaworowska et al., 2004). They are best known from Late Jurassic and Early Cretaceous sites in Europe and North America. In addition, several Early Cretaceous forms from Asia and one tooth from northern Africa have been described in recent years. Plagiaulacoidea is a paraphyletic assemblage (including successive sister taxa of later multituberculates), hence it is not surprising that its composition is particularly unstable—for example, regarding the proper familial allocation of various genera and even which families belong here. The dental formula is 3.0-1.4-5.2/1.0.3-4.2. I2 is multicusped and the largest of the upper incisors, I3 may also be large and multicusped, and several genera retain the upper canine (Hahn, 1977, 1993). The three or four lower premolars form a bladelike cutting edge, with the anteriormost premolar smallest and lowest. In paulchoffatiids, unlike later multituberculates, the pre-molars usually were not markedly larger than the molars. Heavy apical wear in some of them suggests that these teeth were used for grinding. A row of basal cuspules is developed on the buccal surface of the posterior lower premolars. A reduced jugal bone was still present, as was a vestigial coronoid, which is absent in later multituberculates. All the cranial nerves entering the orbit apparently passed through a single large sphenorbital fissure. These features suggest that paulchoffatiids are the most primitive multituberculates. However, allodontids are plesiomorphic in having a small I3, smooth enamel, a premolar formula of 5/4, and well-separated cusps on the lower molars. Nevertheless, their lower premolars are more derived than those of paulchoffatiids (Kielan-Jaworowska et al., 2004). One bizarre plagiaulacoid, Early Cretaceous Arginbaatar from Asia, had an unusually large P4 that rotated anteriorly over the two more anterior premolars, gradually pushing them out of the jaw as the animal aged (Kielan-Jaworowska et al., 1987b).


The Asian djadochtatheres are united by several apo-morphic cranial features relating mainly to the anatomy of the frontal and lacrimal bones. Unlike many other multituberculates, most of the dozen djadochtathere genera are known from skulls and often postcranial skeletons as well (Fig. 4.10). The skull is short and broad and, in several genera, triangular in superior view. The cheek teeth have fewer cusps and P4 has fewer ridges than in ptilodontoids and tae-niolabidoids (Kielan-Jaworowska and Hurum, 1997). Some forms retain cervical ribs. According to Kielan-Jaworowska and Gambaryan (1994), both the forelimbs and the hind limbs of djadochtatheres were held in a primitive abducted, sprawling posture, and the feet were abducted about 30° from the sagittal plane. These authors also identified an incipient supraspinous fossa in djadochtatheres, but it is much less developed than in therians. Long spinous processes of the lumbar vertebrae imply well-developed erector spinae muscles, as are found in mammals with jumping ability. Djadochtatheres were terrestrial animals that evidently progressed by an asymmetrical gait punctuated by occasional jumps.


Ptilodontoids are first known from the Late Cretaceous and survived until the late Eocene. They were the most diverse early Cenozoic multituberculates, with 15 of the

Fig. 4.10. Skeleton and restoration of the djadochtathere Nemegtbaatar. (From Kielan-Jaworowska and Gambaryan, 1994.)

16 genera known from Paleocene or early Eocene strata. They ranged in size from a small mouse to a squirrel (Sciu-rus). The two or three families are known from North America, Europe, and Asia. Ptilodontoids had a longer, more slender lower incisor than in plagiaulacoids (Fig. 4.11). There are at most four upper premolars and only one or two lower premolars. P3, when present, is reduced to a single-rooted peg, whereas P4 is elongate, and P4 is large and bladelike, its crown usually extending well above the molars and bearing 8 to 16 serrations. The upper molars often have cingula or an extra row of cusps compared to plagiaulacoids. The first molars are longer than the second molars.

The postcranial skeleton of Ptilodus (Fig. 4.12) displays numerous arboreal adaptations, including a divergent hal-lux, a long and probably prehensile tail, and tarsal modifications that facilitated hindfoot abduction and reversal, thus allowing the animal to descend trees headfirst (Plate 1.1; Jenkins and Krause, 1983). The mouse-sized neoplagiaulacids account for two-thirds of ptilodontoid genera and existed from the Late Cretaceous through the Eocene. A neopla-giaulacid from the Chadronian (latest Eocene, approximately 35 million years ago), usually identified as Ectypodus, was the last occurring multituberculate (Krishtalka et al., 1982).

Multituberculates, particularly ptilodontoids, experienced something of a resurgence during the Paleocene in western North America. In the richest Torrejonian through Clark-forkian quarry assemblages from Wyoming and Montana, multituberculates typically account for 15-20% of all mammal species and from 12-25% of the individuals represented (Rose, 1981; Krause, 1986). At Swain Quarry in southern Wyoming—perhaps the richest known Paleocene site—43% of the 28,000 mammal teeth collected belong to multituberculates, mainly ptilodontoids (Rigby, 1980). Ptilodon-toids were generally rare after the Paleocene, although they were moderately common in the early Eocene Four Mile fauna of Colorado (McKenna, 1960a) and abundant in one early Eocene quarry sample from the Bighorn Basin of Wyoming (26% of individuals; Silcox and Rose, 2001).


Taeniolabidoids (Fig. 4.8B-C) are known from the Late Cretaceous through early Eocene of North America, Asia, and Europe. Two of the three known families persisted into the Early Tertiary: Taeniolabididae are known from the Paleocene of North America and Asia, while Eucosmodon-tidae lived into the early Eocene in North America and Europe. (Survival of eucosmodontids into the Eocene, however, is based on the genera Neoliotomus and Microcosmodon, both of which were excluded from this family by Kielan-

Fig. 4.12. Ptilodus skeleton and foot. Reconstructions at left show the right hind foot in normal terrestrial stance (below) and reversed for headfirst descent from trees (above). (From Jenkins and Krause, 1983.)

First Mammals Mesozoic

Fig. 4.12. Ptilodus skeleton and foot. Reconstructions at left show the right hind foot in normal terrestrial stance (below) and reversed for headfirst descent from trees (above). (From Jenkins and Krause, 1983.)

Jaworowska and Hurum, 2001.) In these multituberculates Ij is hypsodont and in some forms possibly ever-growing, and the enamel is limited to a ventrolateral band. There are two upper incisors (I2-3). From one to four upper premolars are present, and only one or two lower premolars. P4 is typically bladelike, but in Taeniolabididae it is reduced to a small tooth with only a few apical cusps. In Eucosmodonti-dae, by contrast, P4 can have up to 15 serrations. The molars of taeniolabidoids are often as large as or larger than the pre-molars. Early Paleocene Taeniolabis was the largest known multituberculate, reaching the size of a large beaver. Some recent studies suggest that eucosmodontids are not so closely related to taeniolabidids as long believed and should be excluded from the Taeniolabidoidea (e.g., Kielan-Jaworowska and Hurum, 2001).

Skeletal remains are known for several taeniolabidoid taxa, and they indicate diverse habits. The late Paleocene taeniolabidid Lambdopsalis from Asia was fossorial. This interpretation is based on many features, including fused neck vertebrae (C2-3), a robust humerus, and a thick, keeled manubrium sterni (Kielan-Jaworowska, 1989; Kielan-Jaworowska and Qi, 1990). The incisors of Lambdopsalis had pigmented enamel, presumably indicating a hard, iron-

bearing outer layer of enamel (Akersten et al., 2002), which would have been useful if the teeth were used for digging. The skull of Lambdopsalis was wedge-shaped and had very large, inflated petrosals, superficially resembling bullae, that housed an expanded vestibular apparatus and an uncoiled cochlea. These features, as well as the structure of the auditory ossicles, suggest that Lambdopsalis was adapted for low-frequency sound reception, another indication of fossorial habits (Miao, 1988; Meng and Wyss, 1995). The morphology of the middle ear of Lambdopsalis is particularly similar to that of living monotremes, which is taken by some authors as evidence of a special relationship between them (e.g., Meng and Wyss, 1995). Other taxa traditionally considered taeniolabidoids, such as Eucosmodon, show arboreal adaptations similar to those of Ptilodus (Krause and Jenkins, 1983).

Relationships and Extinction of Multituberculates

Despite substantial knowledge of their anatomy, the ancestry of multituberculates remains enigmatic. Their highly apomorphic dentition and the possibility that haramiyids or theroteinids might be related to multituberculates suggest that they are a very ancient clade that could have originated independently from other mammals. However, the mammalian jaw joint, virtual absence of postdentary bones, di-phyodont tooth replacement, and presence of mammal-like middle-ear ossicles (Miao and Lillegraven, 1986; Meng and Wyss, 1995; Hurum et al., 1996; Rougier et al., 1996b) support their inclusion in a monophyletic Mammalia, as does the unequivocal presence of hair (Meng and Wyss, 1997). Various cranial features (e.g., cribriform plate, ossified ethmoid plate) are shared with monotremes and therians (Hu-rum, 1994). However, there remains a wide gulf between multituberculates and therians in many other aspects of their anatomy. This paradoxical association of very primitive traits with autapomorphic and derived therian-like features has made it very difficult to decipher the phyletic position of multituberculates relative to other mammals. In recent years, they have been considered a primitive offshoot of the mammalian stem (e.g., Kielan-Jaworowska, 1992; Miao, 1993; McKenna and Bell, 1997), the sister taxon of monotremes (e.g., Kemp, 1983; Wible and Hopson, 1993), the sister taxon of Theria (Rowe, 1988), or somewhere in between (e.g., Rougier et al., 1996a; Luo et al., 2002).

Why such a diverse and successful group as multituberculates became extinct remains a conundrum. Perhaps they were competitively inferior to placentals. The brains of multituberculates were relatively large among Mesozoic mammals (encephalization quotient, or EQ, between 0.37 and 0.71) but relatively much smaller than in average modern mammals (Krause and Kielan-Jaworowska, 1993; Kielan-Jaworowska and Lancaster, 2004). Although competition with condylarths, rodents, plesiadapiforms, and early eu-primates was probably a factor in their disappearance (Van Valen and Sloan, 1966; Krause, 1986), it seems unlikely to be the full explanation, as multituberculates coexisted successfully with one or more of these placental groups in several Early Tertiary faunas. Reproductive biology may also have contributed. Kielan-Jaworowska (1979) suggested that the pelvic outlet of the djadochtathere Kryptobaatar was too small to allow eggs to pass through, which may indicate that it gave birth to tiny, altricial young, as do living marsupials.

Whatever the reason for their demise, multituberculates were the most successful Mesozoic mammalian group, dispersing through most of the world. More than 40 Cretaceous genera in 12 families were listed by McKenna and Bell (1997), and at least nine more Cretaceous genera have been described since then (Kielan-Jaworowska et al., 2004). But multituberculates had declined sharply by the end of the Cretaceous: only five of the families and just four genera continued into the Paleocene. Remarkably, multituberculates radiated again in the Early Cenozoic to become abundant constituents of northern Paleocene faunas. About 30 Paleocene genera are recognized. Multituberculates diminished quickly after the Paleocene, only two families persisting into the Eocene, and just one genus beyond the early Eocene. By the end of the Eocene, the last of the multi-tuberculates had disappeared.

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