Multituberculata

Description

The multituberculates had a cranial and dental anatomy superficially similar to rodents such as mice and rats, with cheek-teeth separated from the chisel-like front teeth by a wide tooth-less gap (the diasteme). Each cheek-tooth displayed several rows of small cusps (or tubercles, hence the name) that operated against similar rows in the teeth of the jaw; the exact homology of these cusps to therian ones is still a matter of debate. However, unlike rodents which have ever-growing teeth, multituberculates still underwent through dental replacement patterns typical to most mammals (though in at least some species the lower incisors continued to erupt long after the root's closure. Multituberculates are notable for the presence of a massive fourth lower premolar, the plagiaulacoid; other mammals, like Plesiadapiformes and diprotodontian marsupials, also have similar premolars in both upper and lower jaws, but in multituberculates this tooth is massive and the upper premolars aren't modified this way. In basal multituberculates all three lower premolars were plagiaulacoids, increasing in size posteriorly, but in Cimolodonta only the fourth lower premolar remained, with the third one remaining only as a vestigial peg-like tooth, and in several taxa like gondwanatherians and taeniolabidoideans the plagiaulacoid disappeared entirely or was reconverted into a molariform tooth.

Unlike rodents and similar therians, multituberculates had a palinal jaw stroke (front-to-back), instead of a propalinal (back-to-front) or transverse (side-to-side) one; as a consequence, their jaw musculature and cusp orientation is radically different. Palinal jaw strokes are almost entirely absent in modern mammals (with the possible exception of the dugong), but are also present in haramiyidans, argyrolagoideans and tritylodontids, the former historically united with multituberculates on that basis. Multituberculate mastication is thought to have operated in a two stroke cycle: first, food held in place by the last upper premolar was sliced by the bladelike lower pre-molars as the dentary moved orthally (upward). Then the lower jaw moved palinally, grinding the food between the molar cusp rows.

During the Cretaceous and Paleocene, the multituberculates radiated into a wide variety of morphotypes, including the squirrel-like arboreal ptilodonts. The peculiar shape of their last lower premolar is their most outstanding feature. These teeth were larger and more elongated than the other cheek-teeth and had an occlusive surface forming a serrated slicing blade. Though it can be assumed that this was used for crushing seeds and nuts, it is believed that most small multituberculates also supplemented their diet with insects, worms, and fruits. Tooth marks attributed to multituberculates are known on Champsosaurus fossils, indicating that at least some of these mammals were scavengers.

A ptilodont that throve in North America was Ptilodus. Thanks to the well-preserved Ptilodus specimens found in the Bighorn Basin, Wyoming, we know that these multituberculates were able to abduct and adduct their big toes, and thus that their foot mobility was similar to that of modern squirrels, which descend trees head first.

In Europe, another family of multituberculates were equally successful—the Kogaionidae, first discovered in Haţeg, Romania. They also developed an enlarged blade-like lower premolar. The Hainina, the most successful genus, was originally believed to be a ptilodont. However, more detailed analysis of this genus revealed a smaller number of dental cusps and a retained fifth premolar—a unique combination of primitive and advanced features indicating that Hainina were related to some Jurassic genera and that enlarged, blade-like premolars were acquired independently in Europe and North America.

Another group of multituberculates, the taeniolabids, were heavier and more massively built, indicating that they lived a fully terrestrial life. The largest specimens weighted probably as much as 100 kg, making them comparable in size to large rodents like Castoroides. They reached their highest diversity in Asia during the late Cretaceous and Paleocene, which suggests that they originated from there.

The structure of the pelvis in the Multituberculata suggests that they gave birth to tiny helpless, underdeveloped young, similar to modern marsupials, such as kangaroos.

At least two lineages developed hypsodonty, in which tooth enamel extends up beyond the gumline: lambdopsalid taeniolabidoideans and sudamericid gondwanatheres. The latter, having been around already during the Cretaceous, are the earliest known lineage of grazing mammals. A species from the Katsuyama Dinosaur Forest Geopark may offer an even earlier example of grass-eating adaptations as it dates from the Lower Cretaceous at about 120 million years.

About 80 genera of Multituberculata are known, including Lambdopsalis, Ptilodus and Meniscoessus. In the northern hemisphere, during the late Cretaceous, more than half of typical land mammalian species were multituberculates.

Classification

In their 2001 study, Kielan-Jaworowska and Hurum found that most multituberculates could be referred to two suborders: "Plagiaulacida" and Cimolodonta. The exception is the genus Arginbaatar, which shares characteristics with both groups.

"Plagiaulacida" is paraphyletic, representing the more primitive evolutionary grade and possibly the more derived Gondwanatheria. Its members are the more basal Multituberculata, though gondwanatherians are rather derived. Chronologically, they ranged from perhaps the middle Jurassic (unnamed material), until the lower Cretaceous. This group is further subdivided into three informal groupings: the allodontid line, the paulchoffatiid line, and the plagiaulacid line.

Gondwanatheria is a monophyletic group that was diverse in the Late Cretaceous of South America, India, Madagascar and possibly Africa and occurs onwards into the Cenozoic of South America and Antarctica. Though their identity as multituberculates has been disputed, most recent phylogenetic studies recover them as the sister group to cimolodonts. There are two major families, Ferugliotheriidae and Sudamericidae, with a few taxa like Greniodon and Groeberia being uncertainly placed. Patagonia is the youngest multituberculate known, occurring in the Miocene of Argentina.

Cimolodonta is, apparently, a natural (monophyletic) suborder. This includes the more derived Multituberculata, which have been identified from the lower Cretaceous to the Eocene. The superfamilies Djadochtatherioidea, Taeniolabidoidea, Ptilodontoidea are recognized, as is the Paracimexomys group. Additionally, there are the families Cimolomyidae, Boffiidae, Eucosmodontidae, Kogaionidae, Microcosmodontidae and the two genera Uzbekbaatar and Viridomys. More precise placement of these types awaits further discoveries and analysis.

Taxonomy

Based on the combined works of Mikko's Phylogeny Archive and Paleofile.com.

Suborder †Plagiaulacida Simpson 1925

Evolutionary history

The multituberculates existed for about 166 or 183 million years, and are often considered the most successful, diversified, and long-lasting mammals in natural history. They first appeared in the Jurassic, or perhaps even the Triassic, survived the mass extinction in the Cretaceous, and became extinct in the early Oligocene epoch, some 35 million years ago. The oldest known species in the group is Indobaatar zofiae from the Jurassic of India, some 183 million years ago, and the youngest are two species, Ectypodus lovei and an unnamed possible neoplagiaulacid, from the late Eocene/Oligocene Medicine Pole Hills deposits of North Dakota. If gondwanatheres are multituberculates, then the clade might have survived even longer into the Colhuehuapian Miocene in South America, in the form of Patagonia peregrina.

Extinction

The extinction of multituberculates has been a topic of controversy for several decades. After at least 88 million years of dominance over most mammalian assemblies, multituberculates reached the peak of their diversity in the early Palaeocene, before gradually declining across the final stages of the epoch and the Eocene, finally disappearing in the early Oligocene (mid-Miocene if gondwanatherians are multituberculates). Traditionally, the extinction of multituberculates has been linked to the rise of rodents (and, to a lesser degree, earlier placental competitors like hyopsodonts and Plesiadapiformes), which supposedly competitively excluded multituberculates from most mammalian faunas.

However, the idea that multituberculates were replaced by rodents and other placentals has been criticised by several authors. For one thing, it relies on the assumption that these mammals are "inferior" to more derived placentals, and ignores the fact that rodents and multituberculates have co-existed for at least 15 million years. According to some researchers, multituberculate "decline" is shaped by sharp extinction events, most notably after the Tiffanian, where a sudden drop in diversity occurs. Finally, the youngest known multituberculates do not exemplify patterns of competitive exclusion; the Oligocene Ectypodus is a rather generalistic species, rather than a specialist. This combination of factors suggests that, rather than gradually declining due to pressure from rodents and similar placentals, multituberculates simply could not cope with climatic and vegetation changes, as well as the rise of new predatory eutherians, such as miacids.

More recent studies show a mixed effect. Multituberculate faunas in North America and Europe do indeed decline in correlation to the introduction of rodents in these areas. However, Asian multituberculate faunas co-existed with rodents with minimal extinction events, implying that competition was not the main cause for the extinction of Asiatic multituberculates. As a whole, it seems that Asian multituberculates, unlike North American and European species, never recovered from the KT event, which allowed the evolution and propagation of rodents in the first place.

Competition between gondwanatherians and rodents and/or other Glires is untested, with a wide span of time between the youngest representatives of the former in India, Africa and Madagascar in the Maastrichtian and the first representatives of the latter in the Palaeocene, Eocene and Oligocene respectively. Co-existence between both groups is currently confirmed only in South America, Patagonia peregrina is thought to have been forced into a specialised fossorial niche by competition with rodents and argyrolagoidean paucituberculate marsupials, but another clade, Groeberiidae, attained its peak diversity in the mid-Oligocene, after the arrival of rodents.

Geographic distribution

Multituberculates are mostly known from the northern continents (Laurasia), but there are various records from the southern continents (Gondwana). The group Gondwanatheria, known from Argentina, Antarctica, Madagascar, India, and possibly Tanzania, has been referred to the order in the past and, while this placement remains controversial, most recent phylogenetic studies recover them as multituberculates outside but close to Cimolodonta. Two genera, Hahnodon and Denisodon, are known from the Early Cretaceous of Morocco, but they may instead be haramiyidans. Multituberculates have also been recorded from the Late Cretaceous of Madagascar and Argentina, but this material has not been described in detail. An Australian multituberculate, Corriebaatar, is known from a single tooth. Indobaatar is known from the Kota Formation of India - then part of eastern Gondwanna - and is the oldest known multituberculate.

In the late Cretaceous, multituberculates were widespread and diverse in the northern hemisphere, and possibly across most southern landsmasses as well, making up more than half of the mammal species of typical faunas. Although several lineages became extinct during the faunal turnover at the end of the Cretaceous, multituberculates as a whole managed very successfully to cross the Cretaceous–Paleogene boundary and reached their peak of diversity during the Paleocene. They were an important component of nearly all Paleocene faunas of Europe and North America, and of some late Paleocene faunas of Asia. Multituberculates were also most diverse in size during the Paleocene, ranging from the size of a very small mouse to that of a beaver. However, in Asia, Palaeocene and Eocene multituberculates compose a very small percentage of the overall local mammalian fauna, having never managed to recover from the KT event in the same way that their North American and European counterparts did. Gondwanatheres are common in the Late Cretaceous of Madagascar and India, the Paleocene and Eocene of Seymour Island, and occur in South America from the Late Cretaceous to the Miocene.