Thomas E. Williamson; Stephen L. Brusatte; Gregory P. Wilson

“ Because of the pervasiveness of sampling bias, it is very difficult to rigorously study how metatherians were distributed across the Cretaceous globe and how intercontinental dispersals and continental breakup may have affected their evolution. Many previous authors have proposed complex, and in some cases grand, biogeographic narratives based on very limited fossil evidence, sometimes the discovery of a single new tooth. Such scenarios are tempting to consider, but exceedingly difficult to test. ”

“ We follow the stem-based definition of [38] , in which Metatheria is defined as all mammals more closely related to living marsupials (such as kangaroos and opossums) than to living placentals (such as humans and hedgehogs) and monotremes. According to most recent phylogenetic analyses ( [9] ; [10] ; [12] ) , Metatheria includes basal stem taxa (e.g., Sinodelphys) , the Deltatheroida, and Marsupialiformes, with the latter group consisting of the Marsupialia (crown group metatherians) plus stem metatherians more closely related to Marsupialia than to Deltatheroida ( [25] ) . ”

“ Teeth of metatherians form an intricate functional complex that is intimately related to diet ( [111] ) and tooth size is highly correlated with mass of the animal ( [112] ) .
Although teeth can usually be used to confidently distinguish metatherians from other mammals and give some insight into body size and diet, there are difficulties associated with using teeth for higher-level metatherian taxonomy and phylogeny. Some of the differences used to distinguish teeth of various taxa are subtle. ”

“ Metatherians are a clade of boreosphendian mammals that must have originated by the Late Jurassic, but the first unequivocal metatherian fossil is from the Early Cretaceous of Asia. Metatherians have the distinctive tightly interlocking occlusal molar pattern of tribosphenic mammals, but differ from Eutheria in their dental formula and tooth replacement pattern, which may be related to the metatherian reproductive process which includes an extended period of lactation followed by birth of extremely altricial young. ”

“ In North America, metatherians were far more numerous and taxonomically diverse than were eutherian mammals, the stem placental mammalian group that is dominant across most of the world today.
Our understanding of metatherian evolution during the Mesozoic and into the early Paleogene has grown rapidly over the past 20 years with the discovery of new fossils and the application of new analytical tools. ”

“ We review the phylogenetic relationships of metatherians with respect to other mammals and the taxonomic definition and diagnosis of Metatheria, the Cretaceous history of major metatherian clades and the paleobiology and macroevolution of Cretaceous metatherians, and the physical and climatic background and biogeography of Cretaceous metatherian faunas. ”

“ Therefore, it is also unclear which taxa may be the closest relatives to Maastrichtidelphys, which leaves open the question of when, and between where, any potential dispersal events may have occurred. High-latitude dispersal in the latest Cretaceous is certainly plausible, and there is some evidence from the fossil record of dinosaurs and other organisms that this likely occurred, particularly between North America and Asia (e.g., [230] ) . But testing whether mammals also employed such routes will require much better fossil sampling and better resolved phylogenies. ”

“ Only two clades, the one containing Glasbius and Roberthoffstetteria and the other containing Ectocentrocristus and Herpetotheriidae, show well resolved relationships with sister taxa on either side of the K-Pg boundary. However, the taxa bracketing the boundary are either found on different continents (Glasbius, Roberthoffstetteria) or are separated by a significant temporal gap (Ectocentrocristus, Golerdelphys) . This analysis supports the conclusion that metatherians underwent a profound extinction event at the end of the Cretaceous. ”

“ There have been some suggestions that some latest Cretaceous metatherians from North America may have occupied an unusual aquatic habitat. Based on the morphology of isolated tarsal bones, [128] suggested that stagodontids had remarkably flexible feet that could rotate in a wide arc, which he regarded as a characteristic of aquatic animals. However, [22] criticized this hypothesis, noting that flexible feet are also commonly seen in non-aquatic taxa such as climbers and gliders. ”

“ It may be that Glasbius was one of the earliest mammals with a frugivorous (or nearly frugivorous) diet. Such a diet would have been suitable for the high energy requirements of a small (<50 gram) metatherian, and would have been possible in a Late Cretaceous world where flowering plants were diversifying ( [38] ) .
Cretaceous paleobiogeography
As with many fossil groups, the greatest handicap in studying the biogeography and distribution of Cretaceous metatherians is their patchy fossil record (Fig. 14; Tables 3–4) . ”

“ Despite the slight downtrend in stem marsupialiform richness and the low likelihood of marsupial diversification during the late Late Cretaceous, metatherians remained numerically abundant members of mammalian local faunas in North America. ”

“ The taxon Mammalia consists of numerous extinct lineages as well as three extant clades: the monotremes (egg-laying mammals) , marsupials (“pouched” mammals that give live birth to relatively altricial young) , and placentals (mammals that give live birth to precocial young) . Here, we follow the crown-group definition of Mammalia, which circumscribes the clade as the most recent common ancestor of living monotremes, marsupials, and placentals, and all its descendants (sensu [39] ) . ”

“ At a minimum, this taxon indicates that Europe was part of the early evolutionary story of metatherians. However, the phylogenetic analysis by [25] recovered Arcantiodelphys in a large polytomy, whereas it was excluded from [30] comprehensive phylogeny because of its incompleteness, meaning that it is uncertain which taxa are the closest relatives of this rare European early metatherian. Therefore, it is difficult to hypothesize about potential dispersal events or other biogeographic scenarios that may explain Europe’s role in early metatherian diversification, a point recognized by [25] . ”

“ Such preservational modes are rare, which explains why small-bodied mammals and feathered dinosaurs are not commonly found elsewhere in the Mesozoic. Sinodelphys, therefore, probably provides a lucky glimpse into early metatherian anatomy and paleoenvironments, but not necessarily an accurate picture of the ancestral metatherian. This common ancestor could have lived almost anywhere, given the notoriously sporadic global fossil record of the late Early–early Middle Jurassic, when metatherians are estimated to have originated (see above) . ”

“ For the time being, however, we are restricted to discussing general biogeographic patterns based on a fairly literal reading of the fossil record, with a skeptical eye always on the lookout for sampling biases.
One particular question of interest in the literature has been the ancestral “area of origin” of Metatheria. For much of the last century, it was explicitly stated or implicitly assumed that metatherians, including crown marsupials, originated and first diversified in North America, based on the great diversity of Late Cretaceous metatherian fossils (e.g., [69] ; [227] ; [228] ) . ”

“ Furthermore, because of the uneven nature of fossil preservation and unequal collecting efforts, certain metatherian faunas (e.g., those of the Maastrichtian portion of the Hell Creek Formation of Montana and nearby states; Table 3) have been much better sampled than others (e.g., Hanna Basin, Cheyenne Basin, Denver Basin, San Juan Basin, Big Bend region) .
Regardless, this imperfect North American record is considerably better than the very poorly sampled Asian and European Late Cretaceous records. ”

“ Coniacian eutherian-dominated mammalian local faunas of middle Asia (Uzbekistan) sharply contrast with the pattern from North America ( [239] ) and speak to a biogeographically complex story that remains largely untold.
Across the K-Pg boundary, metatherian richness dropped from 25 species in the late Maastrichtian to 23 in the early Paleocene (Danian) . However, this rather modest dip aggregates two very divergent patterns: in North America, richness plummeted to 8 species (66% decline) , while it surged to 15 species and at least nine families in South America. ”

“ To assess broad-scale patterns in these data, we plotted species richness through time relative to geography and higher-level taxonomy (Fig. 15) . Given that the Cretaceous fossil record of mammals suffers from temporal and geographic sampling biases (see discussion above) , we hope that these diversity patterns (i) will be interpreted cautiously and (ii) will serve to stimulate field research in intervals and regions of apparent low diversity.
Metatherian richness during the late Early Cretaceous (Barremian–Albian) was paltry, never exceeding two species in any time bin. ”

“ Stagodontids are a small clade that includes the Campanian Eodelphis and the Maastrichtian Didelphodon, both from North America. This clade was defined by [30] as the most inclusive clade (stem-based) containing Didelphodon vorax, but not Glasbius intricatus, Dakotadens morrowi, Turgidodon praesagus, Herpetotherium fugax, Peradectes elegans, Pediomys elegans, or Didelphis virginiana.
Stagodontids are the largest metatherians of the Mesozoic and in all faunas where they are present they are the among the largest therian species. ”

“ At least one inter-continental interchange event must explain the distribution of deltatheroidans in North America and Asia (e.g., [2] ; [21] ; [12] ; [27] ) , another must account for the presence of the Asian Asiatherium interspersed among North America taxa in the phylogeny ( [30] ) , and one or two others are necessary to explain how the European taxa Maastrichtidelphys ( [24] ) and Arcantiodelphys ( [25] ) are nested among North American (and possibly Asian) taxa in the phylogeny. The issues surrounding Deltatheroida and the European taxa deserve further comment. ”

“ Abstract AbstractMetatherians, which comprise marsupials and their closest fossil relatives, were one of the most dominant clades of mammals during the Cretaceous and are the most diverse clade of living mammals after Placentalia. ”

“ In particular, Pucadelphys and Mayulestes from the early Paleocene of Bolivia are useful models for approximating the cranial anatomy of Cretaceous taxa, although they are probably more closely related to extant Marsupialia than to any Cretaceous taxon ( [32] ; [9] ; [33] ) . Their skulls have both been described in detail (Pucadelphys: [126] ; Marshall and Muizon] ; Mayulestes [66] ) , as has the skull of the extant didelphid Monodelphis brevicaudata (the red-legged short-tailed opossum) ( [124] ) . ”

“ Eutherians possess a basicranial vasculature in which the prootic sinus and the lateral head vein completely disappear by adulthood. A new vein, the capsuloparietal emissary vein, leaves the cranial cavity through the capsuloparietal foramen and exits the skull through the postglenoid foramen ( [122] ) . In extant marsupials, and evidently also in some Cretaceous metatherians ( [122] ) , the posterior or tympanic portion of the lateral head vein becomes reduced during ontogeny and in most extant taxa, is totally lacking in the adult ( [122] , [124] ; [35] ) . ”

“ Therefore, if some or all of these specimens belong to deltatheroidans, they may indicate that this clade was largely scansorial or arboreal.
Living didelphids are widely considered to be good analogs for Cretaceous non-deltatheroidan metatherians. This is somewhat problematic, however, because living didelphids are capable of a great variety of locomotor habits, and range from being mostly terrestrial (e.g., Metachirus) to arboreal (e.g., Caluromys) ( [38] ) . Such variety may have also been present in Cretaceous taxa. ”

“ Fossils may help us to better understand the evolution of this basicranial vasculature in metatherians and other early mammals. The mammalian basicranial region, especially the petrosal bone, can preserve osteological correlates associated with each vessel of the basicranial vasculature, meaning that their presence or absence can be assessed in well-preserved fossils. ”

“ It was provisionally assigned to Deltatheroida by Szalay and Trofimov, but other workers (e.g., [2] ; [11] ) have found it to be near the base of Marsupialiformes and possibly related to stagodontids. Partial skulls are known for several Late Cretaceous metatherian taxa, including the Asian deltatheroidans Deltatheridium and Sulestes ( [2] ; [11] ) . Although metatherians were more species rich and evidently numerically abundant in the Late Cretaceous of North America relative to Asia (at least based on the known fossil record) , the North American specimens are more fragmentary. ”

“ However, these are variably present in basal metatherians, living marsupials, and basal eutherians, so it is not clear if these are a synapomorphy of Metatheria or just a feature seen in many (but not all) species. The pterygoids of metatherians are not fused to the alisphenoids as they are in eutherians. Metatherians have a relatively larger alisphenoid than do eutherians. In some taxa, the alisphenoid contributes to the glenoid fossa and in others it extends posteriorly to form a tympanic process that partially conceals the petrosal as an alisphenoid bulla. ”

“ In contrast, metatherians declined in richness to 25 species leading up to the K-Pg boundary (Fig. 15) and, along with other non-multituberculates, declined in morphological disparity ( [245] ) . In light of how well sampled this interval is relative to other parts of the Cretaceous (see [149] ) , it would appear that the richness pattern is evolutionarily meaningful for at least North America and thus supports the claim by [38] :427) that “marsupials declined in generic diversity during the Campanian–Maastrichtian of North America.” ”

“ In living didelphids, the enlarged hamate, triquetrum, and scaphoid in the carpus are thought to be related to increased capacity for gripping ( [9] ) .
Pelvis. Asiatherium possesses rod-shaped ilia and epipubic bones (Fig. 7) . ”