Review Article |
Corresponding author: Thomas E. Williamson ( thomas.williamson@state.nm.us ) Academic editor: Kristofer M. Helgen
© 2014 Thomas E. Williamson, Stephen L. Brusatte, Gregory P. Wilson.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Williamson TE, Brusatte SL, Wilson GP (2014) The origin and early evolution of metatherian mammals: the Cretaceous record. ZooKeys 465: 1-76. https://doi.org/10.3897/zookeys.465.8178
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Metatherians, 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. Our understanding of this group has increased greatly over the past 20 years, with the discovery of new specimens and the application of new analytical tools. Here we provide a review of the phylogenetic relationships of metatherians with respect to other mammals, discuss the taxonomic definition and diagnosis of Metatheria, outline the Cretaceous history of major metatherian clades, describe the paleobiology, biogeography, and macroevolution of Cretaceous metatherians, and provide a physical and climatic background of Cretaceous metatherian faunas. 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. Metatherians were widespread over Laurasia during the Cretaceous, with members present in Asia, Europe, and North America by the early Late Cretaceous. In particular, they were taxonomically and morphologically diverse and relatively abundant in the Late Cretaceous of western North America, where they have been used to examine patterns of biogeography, macroevolution, diversification, and extinction through the Late Cretaceous and across the Cretaceous-Paleogene (K-Pg) boundary. Metatherian diversification patterns suggest that they were not strongly affected by a Cretaceous Terrestrial Revolution, but they clearly underwent a severe extinction across the K-Pg boundary.
Cretaceous, Metatheria , Mammalia , Boreosphenida , Deltatheroida , Marsupialiformes , dentition, osteology, phylogeny, paleobiology, macroevolution, paleoenvironment, biogeography
Metatherian mammals, which include the extant marsupials, are the second most diverse major clade of living mammals (~334 species;
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. In particular, new fossils from Asia have shed light on the origin and evolution of Theria (Eutheria + Metatheria), the earliest metatherians and the divergence between the eutherian and metatherian clades, and the early metatherian skull and postcranial skeleton (
These discoveries have provided important new insight into the evolution and paleobiogeography of metatherians. There has been a tremendous upsurge in studies using analytical cladistic methods to clarify phylogenetic relationships within Metatheria (
This paper is meant to supplement the excellent review of metatherians by
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
Mammaliaformes underwent multiple episodes of diversification through the Mesozoic, resulting in several now extinct lineages (
Once Mammalia originated, several fundamental lineages split from each other during the early stages of mammalian evolution. According to several phylogenetic analyses (
Most Mesozoic mammal fossils consist of fragmentary jaws and teeth, which largely explains the intense emphasis that paleontologists place on the evolution of the mammalian dentition. One of the most distinctive and important features that arose in some mammaliaforms is precise molar occlusion. The upper and lower molars of some basal mammaliaforms (e.g., kuehneotheriids) are nearly triangular and have a loosely interlocking fit. From such teeth, basal cladotherians (e.g., Amphitherium; Fig.
The final step towards the first tribosphenic molar was the acquisition of a molar talonid basin, which appears to have happened with the acquisition of the protocone (
This two-cusped talonid morphology was modified further in derived tribosphenic mammals. The appearance of the lingual talonid cusp (entoconid) of the lower molar, which helped to close the lingual side of the talonid to form a basin (
Recent studies in experimental developmental biology (e.g.,
Theria is a clade of boreosphenidan mammals that is defined as the most recent common ancestor of extant marsupials and placentals and all of its descendants. The only extant members of boreosphenidans can be grouped into two sister clades, the Metatheria (living marsupials and their close fossil relatives) and Eutheria (living placentals and their close fossil relatives). The most recent and comprehensive molecular clock divergence estimates place the origin of Theria approximately 170–190 million years ago (e.g.,
We follow the stem-based definition of
Many of the anatomical features that are used to distinguish living Metatheria (marsupials) and Eutheria (placentals) are based on aspects of “soft anatomy” that do not commonly preserve in fossils and do not have reliable osteological correlates (
Although the vast majority of features distinguishing metatherians and eutherians relate to soft tissues, there are limited characters of the dentition, cranium, and postcranial skeleton that diagnose Metatheria (or very proximal groups on the phylogeny). The possession of these features is usually taken as strong evidence that a fossil in question belongs to Metatheria.
Metatherians differ from eutherians in their dental formula and tooth replacement pattern. The metatherian pattern of tooth replacement is postulated to be intimately related to the metatherian reproductive process, which includes an extended period of lactation with nipple fixation following birth of extremely altricial young (
In recent years, there has been a growing consensus that the plesiomorphic dental pattern for Theria consists of seven to eight postcanine teeth, consisting of four to five premolars and three molars. Many Cretaceous eutherian mammals retain this plesiomorphic dental formula, but the ancestral placental mammal has reduced the premolar number to four, based on a loss of the P3/p3 position (the P3/p3 is variably present in stem therians and early eutherians) (
The dentition mesial to P4 is not functionally replaced in Marsupialia. Some workers have argued that vestigial deciduous incisors and canines develop, but are resorbed before eruption of permanent teeth in some marsupials (
Discrete synapomorphies of Metatheria. A list of metatherian synapomorphies recovered by recent higher-level phylogenetic analyses of mammals is given in Table
Potential synapomorphies of Metatheria.
List of synapomorphies for Metatheria after
Dental: |
1) Absence of tooth replacement in the P2, p2, P5, and p5 tooth positions. The retention of the dP5 is responsible for the sharp break in the “premolar”-molar series that has been considered distinctive for Metatheria (e.g., |
2) Lateral divergence of lower canines |
3) dp5 cristid obliqua (=ectolophid) very trenchant |
Skull: |
1) Presence of a posterior masseteric shelf on the dentary |
2) Ventral exposure of the presphenoid |
3) Angular process that is equal to half but less than the length of the dentary ramus |
Postcranial: |
1) Presence of a capitular tail on the humerus |
2) Testes that descend through the body wall to the scrotum |
3) A small vermis in the cerebellum |
4) Presence of a prehensile tail (convergently develops in many placental mammal groups including rodents, primates, carnivorans) |
1) Posterior most mental foramen at ultimate premolar first molar junction or more posterior |
2) Labial mandibular foramen |
3) Condyloid crest absent |
4) Meckelian groove absent |
5) Coronoid facet absent |
6) Palatal process of premaxilla reaches nearly or to canine alveolus |
7) Glenoid fossa troughlike |
8) Lacrimal foramen exposed on face |
9) |
Several major clades of Cretaceous metatherians have been recognized. Sinodelphys from the Early Cretaceous of China is widely considered to be a basal metatherian, sister taxon to all remaining Cretaceous–Recent forms (
Sinodelphys szalayi is based on a partial skeleton compressed on a shale slab. It was originally described as an Early Cretaceous metatherian by
The metatherian identification of Sinodelphys has not been confidently corroborated by subsequent phylogenetic analyses, often because it is excluded. Sinodelphys was not included in some recent phylogenetic analyses of metatherians because the researchers had not examined the holotype specimen (
We provisionally accept Sinodelphys as a basal metatherian, noting that it does share some features with other metatherians, and most published phylogenetic analyses recover it as a metatherian. If Sinodelphys is one of the earliest diverging metatherian lineages, then it may not be surprising that it lacks certain derived character states that are seen in all later metatherians (such as the inflected angular process and the characteristic metatherian tooth formula). In this scenario, some characters long considered metatherian hallmarks are actually diagnostic of a slightly less inclusive clade that does not include Sinodelphys, and possibly other early-diverging metatherians. Although we accept Sinodelphys as most likely belonging to Metatheria, this must be corroborated by additional phylogenetic analyses that include a large swath of Mesozoic mammals and a broad sampling of dental and non-dental characters.
Deltatheroidans were long regarded as eutherians (
The sister taxon to Deltatheroida is a large clade that includes most remaining metatherians, including crown Marsupialia. The nomenclature of this clade and its major subclades has a confusing history in the literature, with different authors using various names and various taxonomic groupings, many of which are paraphyletic or polyphyletic based on more recent phylogenetic analyses. The non-deltatheroidan Cretaceous metatherians were placed in Ameridelphia in the influential review of
More recently,
There is a stem grade of early-diverging marsupialiforms that do not fit easily into the major Cretaceous marsupialiform clades. Taxa that appear to populate this grade, based on recent phylogenetic studies, including Adelodelphys, Sinbadelphys, Kokopellia, Arcantiodelphys, Anchistodelphys, Aenigmadelphys, Eoalphadon, Apistodon, Iugomortiferum, and Bistius. Bistius was considered to possibly represent a stem therian by
Recent phylogenetic analyses of Cretaceous metatherian taxa find little resolution of the relationships of the most basal marsupialiform taxa and only weak support for many proposed clades within Marsupialiformes. The Stagodontidae may be a monophyletic group, but inclusion of Pariadens is only weakly supported (
Stagodontids are a small clade that includes the Campanian Eodelphis and the Maastrichtian Didelphodon, both from North America. This clade was defined by
Stagodontids are the largest metatherians of the Mesozoic and in all faunas where they are present they are the among the largest therian species. They are also commonly recognized in the fossil record by their distinctive teeth. The premolars are massive and inflated (
Unequivocal stagodontids are known only from the middle Campanian through Maastrichtian of North America (
The Pediomyidae is one of the few marsupialiform clades that is strongly supported by explicit synapomorphies and high tree-support values in phylogenetic analyses (
Pediomyids first appear in the Santonian Milk River Formation of Alberta (
Glasbius is one of the most dentally distinctive Cretaceous metatherians (
Glasbius has been found as a close relative or member of Pediomyidae by several phylogenetic analyses, including the analysis of
The taxon Glasbiidae was not defined by
Herpetotheriidae was defined by
Unequivocal herpetotheriids are relatively common in the fossil record of North America after the Cretaceous-Paleogene boundary. There is some evidence, however, for more basal herpetotheriids in the Cretaceous.
This clade was defined by
The phylogenetic analysis of
As for the vast majority of Cretaceous mammals, Cretaceous metatherians are usually represented by isolated teeth. Therefore, most phylogenetic analyses and taxonomic arrangements rely heavily on dental characters, especially size and relative size, shape, and position of various tooth features (Fig.
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. In addition, some taxa are represented only by small samples, in some cases only a few fragmentary teeth. Therefore, the range of morphological variation within some taxa is poorly understood. This, no doubt, partly explains why there is considerable disagreement and skepticism surrounding some identifications of some taxa and the validity and taxonomic decisions regarding synonymies of other taxa (see
Metatherians underwent a substantial radiation during the Late Cretaceous, and while several Cretaceous metatherians are known from the Late Cretaceous of Europe and Asia (e.g.,
The interrelationships of most major metatherian subclades are unresolved. Several recent cladistic analyses have looked at the higher-level phylogenetic relationships of mammals and have included some Cretaceous and Paleogene metatherian taxa (
The revised analysis presented here includes 95 taxa and 83 characters. It adds three non-metatherian taxa to those included in the
We added five new characters (characters 7, 15, 51, 52, and 68; see Suppl. material
Minor changes or corrections were made to the scoring of some taxa from the
We conducted a parsimony analysis using TNT v. 1.1, September 2013 (
Parts of our strict consensus tree (Fig.
The topology of the strict consensus tree is similar to that recovered by
As in the previous analysis by
Species of Nortedelphys do not fall within Herpetotheriidae or any other Paleogene metatherian taxon, contra
A strong link exists between the enigmatic latest Cretaceous Glasbius and the early Paleocene Roberthoffstetteria, in agreement with previous suggestions (
Strict consensus of 2008 trees of 500 steps calculated using TNT (
The crania and postcrania of Cretaceous metatherians are poorly known. Most taxa are represented only by teeth and jaw fragments. Only two specimens that include articulated skulls and partial skeletons have been described: the stem marsupialiform Asiatherium from the Campanian of Mongolia (
The specimens of Asiatherium and Sinodelphys include nearly complete skulls that provide some of the only information on Cretaceous metatherian cranial anatomy. A nearly complete skull from Gulin Tsav (or Guriliin Tsav), Mongolia, the “Guriliin Tsav Skull” (
The skulls of Asiatherium and Sinodelphys are relatively crushed, making reconstruction problematic. Extant didelphid marsupials and some early Paleocene taxa retain many plesiomorphic therian features and their skulls closely resemble the limited fossil cranial material of Cretaceous metatherians in many respects, meaning that they can be used as a guide for reconstructing Cretaceous metatherian skull morphology (
The skulls of Cretaceous metatherians have a pronounced postorbital constriction of the cranium when seen in dorsal view, a braincase with well-developed sagittal and nuchal crests and high and robust zygomatic arches. However, these sagittal and nuchal crests were probably not as highly developed as they are in the living didelphid Didelphis, which is similar in size to Didelphodon, the largest Cretaceous metatherian (
The mammalian palate has incisive foramina situated within the premaxilla, and these are particularly large in metatherians compared to basal eutherians, extending posteriorly to the premaxillary-maxillary suture. In addition, many basal metatherians have two pairs of large palatine vacuities. The larger of these is anterior to the anterolateral part of the maxillary-palatine suture, and there is a smaller pair on the maxillary-palatine suture, at the posterolateral margins of the palatal exposure of the palatine. 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. An alisphenoid bulla is present in the undescribed Guriliin Tsav skull, Asiatherium, Didelphodon, and many extant marsupials, suggesting that it may be a feature that evolved at or near the base of Metatheria, potentially as a synapomorphy uniting the clade. However, it is lacking in Pucadelphys and Mayulestes, possibly indicating that it has evolved multiple times within Marsupialia (
Ear region. The incorporation of postdentary bones into the basicranial region of the braincase is one of the most extraordinary examples of morphological evolution in the fossil record (see
Extant placental and marsupial mammals possess very different basicranial vasculature (
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.
Wible described several isolated petrosals from the Bug Creek Anthills of Montana, some of which he assigned to Cretaceous metatherians (
Mandible. The dentary of most Cretaceous metatherians has a shallow, horizontally oriented, and unfused mandibular symphysis. The canines diverge laterally, which is a synapomorphy of metatherians that was identified in the analysis by
Metatherians typically have several mental foramina on the mandible, and the posterior-most one is located below a position between p4 and dp5 (following the tooth terminology of
Associated partial postcranial skeletons (Fig.
Axial skeleton. Little is known of the Cretaceous metatherian axial skeleton as it is only incompletely preserved in two specimens, the holotypes of Asiatherium and Sinodelphys. Asiatherium was found to lack an anticlinal vertebra and has two fused sacral vertebrae (
Scapula. Damaged scapulae are preserved with the partial skeletons of Asiatherium and Sinodelphys. The scapula of Asiatherium (Fig.
Clavicle. A robust clavicle is preserved in both Asiatherium and Sinodelphys.
Humerus. Asiatherium and Sinodelphys both preserve humeri. In Asiatherium (Fig.
The three distal humerus fragments from the Bissekty Formation (Fig.
Radius and ulna. The head of the radius of Asiatherium (Fig.
Carpus. The carpals of both Sinodelphys and Asiatherium (Figs
Pelvis. Asiatherium possesses rod-shaped ilia and epipubic bones (Fig.
Femur. The femur of Asiatherium (Fig.
Fibula. The fibula of Asiatherium (Fig.
Tarsus. Associated tarsals of a Cretaceous metatherian are known only for Sinodelphys. (Fig.
The astragalus of Cretaceous metatherians is distinct from other mammals because the neck is asymmetrical, with the navicular facet of the astragalus extending medially along the length of the neck (Fig.
The calcaneus of Cretaceous metatherians (Fig.
The navicular of Sinodelphys (Fig.
Skull of Monodelphis brevicaudata, modified from
Right petrosal Type A (Protolambda) after
Humerus and carpi of Cretaceous metatherians. A Distal humerus of unidentified metatherian (cf. Sulestes?) from the Bissetky Locale, Uzbekistan after
Partial femora of unidentified metatheria (cf. Sulestes?) from the Bissetky Locale, Uzbekistan after
Tarsus of the Cretaceous stem therian Eomaia and Cretaceous metatherians. A–F isolated calcaneum (A–C) (cf. Sulestes?) from the Bissetky Locale, Uzbekistan in dorsal (A), ventral (B), and distal (C) views after
The most recent molecular clock analyses estimate the marsupial-placental split between ~140 and 190 million years ago, depending on the tree topology, calibrations, and rate models used (
Many of these molecular clock studies also estimate the origin of Marsupialia.
Juramaia sinensis was recently described as the oldest eutherian mammal, and therefore the oldest therian as well (
The oldest proposed metatherian, Sinodelphys szalayi, is Early Cretaceous in age (ca. 124–131 million years old [
The first appearance of marsupialiforms (i.e., non-deltatheroidan metatherians) in North America is near the Albian-Cenomanian boundary, at the base of the Late Cretaceous, approximately 100 million years ago (
The oldest unequivocal crown marsupials appear in the early Paleocene with Peradectes and other taxa (
Both molecular clock estimates and fossil evidence (if correctly identified) currently agree that the metatherian-eutherian split, and therefore the origin of Metatheria, occurred by 160 million years ago. Crown-group metatherians (Marsupialia) probably originated within the 10 million years before the Cretaceous-Paleogene boundary, although their oldest unequivocal fossils are from the earliest Paleocene and molecular clocks cannot completely rule out a post-Cretaceous origin. Both deltatheroidans and marsupialiforms first appear in the fossil record in the middle part of the Cretaceous, but these are minimum divergence estimates.
The oldest probable metatherian, Sinodelphys, comes from the Lower Cretaceous lagerstätten of the Yixian Formation of northeastern China (Tables
Following Sinodelphys, the next earliest metatherians in the fossil record are the Early Cretaceous delatatheroidans Oklatheridium and Atokatheridium from eastern Oklahoma, USA (
Marsupialiforms first appear in North America near the Albian-Cenomanian boundary (
The entire North American record of Late Cretaceous metatherians (Tables
This North American record for the Mesozoic is unequaled for its sampling density, broad geographic span, and great temporal depth (
Important records of Cretaceous metatherians are also known from Asia and Europe (Tables
Europe |
Font-de-Benon quarry, Archingeay-Les Nouillers (Cenomanian, Late Cretaceous), Charente-Maritime, southwestern France ( |
Valkenburg Member, Maastricht Formation (late Maastrichtian, Late Cretaceous), southern Limburg, The Netherlands ( |
Asia |
Yixian Formation, China (Barremian, Early Cretaceous) |
Jehol fauna ( |
Bissekty Formation, Kyzylkum Desert, Uzbekistan (Turonian, Late Cretaceous) |
Bissekty local fauna ( |
Darbasa Formation, southern Kazakhstan (Campanian, Late Cretaceous) |
Grey Mesa locality ( |
Barun Goyot Formation, Umuni Gobi, Mongolia (Campanian, Late Cretaceous) |
Udan Sayr locality ( |
Nemegt Formation, Omnogov, Mongolia (Maastrichtian, Late Cretaceous) |
Gurlin Tsav, Mongolia ( |
Djadokhta Formation, Mongolia (Campanian, Late Cretaceous) |
Ukhaa Tolgod and Kholbot localities, Mongolia ( |
Bayn Dzak, Mongolia ( |
North America |
Alaska |
Prince Creek Formation, Alaska (early Maastrichtian, Late Cretaceous) |
Colville River ( |
Pediomys Point local fauna ( |
Alberta and Saskatchewan, Canada |
Milk River Formation, southern Alberta, Canada (late Santonian, Late Cretaceous) |
Upper Milk River ( |
Oldman Formation, southern Alberta, Canada (Campanian, Late Cretaceous) |
South Saskatchewan River ( |
Dinosaur Park Formation, southern Alberta, Canada (late Campanian, Late Cretaceous) |
“Oldman Formation” ( |
Horseshoe Canyon Formation, southern Alberta, Canada (early Maastrichtian, Late Cretaceous) |
Drumheller local fauna ( |
St. Mary River Formation, Alberta and northwestern Montana (early Maastrichtian, Late Cretaceous) |
Scabby Butte local fauna ( |
Lundbreck locality ( |
Shell Hell locality ( |
Scollard Formation, Alberta (late Maastrichtian, Late Cretaceous) |
Trochu local fauna ( |
Frenchman Formation, Saskatchewan (late Maastrichtian, Late Cretaceous) |
Wounded Knee local fauna ( |
Gryde local fauna ( |
quarry ( |
Montana and North Dakota |
Judith River Formation (late Campanian, Late Cretaceous) |
Type fauna ( |
Two Medicine Formation (late Campanian, Late Cretaceous) |
Egg Mountain ( |
Hell Creek Formation, Montana and North Dakota (late Maastrichtian, Late Cretaceous) |
Garfield and McCone Counties, assorted localities ( |
Muddy Tork local fauna, Williston Basin, Montana (Hunter et al. 1997) |
Ekalaka local faunas, Montana ( |
Localities in the Little Missouri badlands, Montana and North Dakota ( |
South Dakota |
Fox Hills Formation, South Dakota (late Maastrichtian, Late Cretaceous) |
Iron Lightning local fauna ( |
Hell Creek Formation, South Dakota (late Maastrichtian, Late Cretaceous) |
Joe Painter Quarry ( |
Eureka Quarry ( |
Wyoming |
“Mesa Verde Formation” (late Campanian, Late Cretaceous) |
Bighorn Basin local fauna ( |
Wind River Basin local fauna ( |
Lance Formation, Wyoming (late Maastrichtian, Late Cretaceous) |
Localities near Mule Creek Junction ( |
Localities in Lance Creek drainage, type Lance Formation ( |
Hewitt’s Foresight ( |
Black Butte Station ( |
Ferris Formation, Wyoming (late Maastrichtian, Late Cretaceous) |
Localities in Hanna Basin ( |
Utah |
Cedar Mountain Formation (Albian-Cenomanian) |
Mussentuchit local fauna, southern Utah ( |
Dakota Formation fauna (late Cenomanian, Late Cretaceous) |
Kaiparowits and Paunsaugunt figaus, southern Utah ( |
Smoky Hollow Member, Straight Cliffs Formation (Turonian, Late Cretaceous) |
Kaiparowits and Paunsaugunt figaus, southern Utah (Cifelli 1990c; |
John Henry Member, Straight Cliffs Formation (Coniacian-Santonian, Late Cretaceous) |
Kaiparowits and Paunsaugunt figaus, southern Utah ( |
Wahweap Formation (early-middle Campanian, Late Cretaceous) |
Kaiparowits Plateau ( |
Kaiparowits Formation (late Campanian, Late Cretaceous) |
Kaiparowits Plateau ( |
Iron Springs Formation fauna, southern Utah (Turonian – Santonian, Late Cretaceous) |
Pine Valley Mountains ( |
North Horn Formation, Utah (late Maastrichtian, Late Cretaceous) |
Localities in North Horn Mountain and in South Dragon Canyon ( |
Colorado |
Williams Fork Formation, Colorado (late Campanian-early Maastrichtian) |
Rio Blanco local fauna ( |
Laramie Formation, northeastern Colorado (late Maastrichtian, Late Cretaceous) |
Cheyenne Basin assemblages ( |
Site in Weld County ( |
Baja California Del Norte, Mexico |
El Gallo Formation (late Campanian, Late Cretaceous) ( |
New Mexico |
Fruitland and lower Kirtland Formation, San Juan Basin (late Campanian, Late Cretaceous) |
Hunter Wash local fauna, Bisti/De-na-zin Wilderness Area, San Juan Basin ( |
Fossil Forest, San Juan Basin ( |
Willow Wash local fauna (Flynn 1986) |
Naashoibito Member, Kirtland Formation, New Mexico (late Maastrichtian, Late Cretaceous) |
Alamo Wash local fauna, San Juan Basin (Flynn 1986; |
Oklahoma |
Antlers Formation, Texas and Oklahoma (Aptian-Albian, Early Cretaceous) |
Tomato Hill local fauna ( |
Texas |
Aguja Formation, West Texas (late Campanian, Late Cretaceous) |
Terlingua local fauna ( |
New Jersey |
Marshalltown Formation, New Jersey (Campanian, Late Cretaceous) |
Ellisdale Site ( |
Distribution of Cretaceous metatherian taxa. Numbers correspond to localities listed in Table
Taxon | Localities |
---|---|
Adelodelphys muizoni | 25 |
Aenigmadelphys archeri | 30 |
Albertatherium primum | 10 |
Albertatherium secundum | 10 |
Alphadon attaragos | 22, 30 |
Alphadon eatoni | 32 |
Alphadon halleyi | 12, 17, 18, 22, 28?, 30, 36, 38? |
Alphadon marshi | 15, 16, 19, 21?, 23, 33, 37 |
Alphadon perexiguus | 38 |
Alphadon sahni | 12, 17, 22, 30, 36 |
Alphadon wilsoni | 15, 19, 23, 33, 36? |
Anchistodelphys archibaldi | 29 |
Anchistodelphys delicatus | 27 |
Apistodon exiguus | 10, 28?, 29? |
?Aquiladelphis laurae | 29 |
Aquiladelphis incus | 10, 33 |
Aquiladelphis minor | 10, 36 |
Arcantiodelphys marchandi | 1 |
Asiatherium reshetovi | 6 |
Atokatheridium boreni | 38 |
Bistius bondi | 36 |
Dakotadens morrowi | 26 |
Deltatheridium pretrituberculare | 8 |
Deltatheroides cretacicus | 8 |
Didelphodon coyi | 13 |
Didelphodon vorax | 15, 16, 19, 20?, 23 |
Ectocentrocristus foxi | 17, 36? |
Eoalphadon clemensi | 26 |
Eoalphadon lillegraveni | 26 |
Eoalphadon woodburnei | 26 |
Eodelphis browni | 12 |
Eodelphis cutleri | 12, 17 |
Glasbius intricatus | 23, 37? |
Glasbius twitchelli | 16, 19 |
Hatcheritherium alpha | 23 |
Iqualadelphis lactea | 10, 28 |
Iugomortiferum thoringtoni | 29 |
Kokopellia juddi | 25 |
?Leptalestes cooki | 14?, 19, 23, 33, 34, 36? |
Leptalestes krejcii | 14?, 15, 16, 19, 21, 23 |
Leptalestes prokrejcii | 11, 12, 17, 18, 36 |
Leptalestes toevsi | 14 |
Maastrichtidelphys meurismeti | 2 |
Nanocuris improvida | 15, 19, 23 |
Nortedelphys jasoni | 15, 16, 19, 21, 23, 34 |
Nortedelphys magnus | 15, 19, 23 |
Nortedelphys minimus | 19, 23 |
Oklatheridium szalayi | 38 |
Pariadens kirklandi | 26 |
Pariadens mckennai | 25 |
Pediomys elegans | 9, 12, 15, 16, 21, 23, 35 |
Protalphadon foxi | 19 |
Protalphadon lulli | 21?, 22, 23, 24, 39 |
?Protolambda clemensi | 12, 17, 18, 22 |
Protolambda florencae | 19, 21, 23 |
Protolambda hatcheri | 12?, 15, 16?, 19, 21, 23, 32, 34 |
Sinbadelphys schmidti | 25 |
Sinodelphys szalayi | 3 |
Sulestes karakshi | 4 |
Turgidodon lillegraveni | 30, 38? |
Turgidodon madseni | 30 |
Turgidodon petiminis | 16 |
Turgidodon praesagus | 11, 12, 17 |
Turgidodon rhaister | 14?, 15, 19, 23 |
Turgidodon russelli | 11, 12, 14, 17, 29?, 33, 36 |
Varalphadon creber | 10, 29? |
Varalphadon crebreforme | 29 |
Varalphadon wahweapensis | 29, 30 |
The “Gurlin Tsav Skull” | 7 |
Body mass is significantly correlated with dental dimensions in extant mammals. As such, predictive formulae have been developed to estimate body mass in fossil metatherians. These formulae rely on the area of the dp5 (traditionally m1) as estimated by the product of length and width of the crown (
Reconstructing the postures, locomotor abilities, and habitat preferences of most fossil metatherians is exceedingly difficult, because most extinct taxa are known only from isolated jaws and teeth. Nevertheless, the rare postcranial fossils of Cretaceous metatherians give some insight into their locomotory paleobiology. The small skeleton of the oldest recognized metatherian, Sinodelphys, possesses features seen in living mammals that climb, leading
The locomotor habits of deltatheroidans are difficult to reconstruct due to the lack of associated skeletal material for this clade.
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) (
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,
Compared to locomotion, reconstructing the diet of Cretaceous metatherians is more straightforward, because tooth morphology can often give clear insights into feeding behavior and preferences (
Deltatheroidans were probably predominantly carnivorous. They are relatively large in size, exhibit enlarged temporalis muscle attachment sites on the skull, possess large canines, and have hypertrophied upper and lower molar shearing blades accentuating postvallum/prevallid shear (enlarged paracristids on the lower molars and metacrista on the upper molars) and reduced talonid basins reflecting de-emphasis of crushing (
Small-bodied Cretaceous marsupialiforms were probably mostly insectivorous, based on their fairly conservative molar structure and teeth that appear well suited for both shearing and crushing. These taxa include various basal marsupialiforms (such as “alphadontids”), small pediomyids, and potential Cretaceous herpetotheriids and peradectids (Fig.
Large pediomyids are also probably roughly analogous to mid-to-large-sized extant didelphids, but exhibit somewhat more pronounced adaptations for crushing (larger protocone and talonid basin) relative to most other Cretaceous metatherians. Taxa such as Pediomys and Protolambda (Fig.
Stagodontids exhibit some of the most unusual premolars among Cretaceous metatherians, indicating that they had a distinctive diet. These taxa are particularly large from their first appearance in the Albian-Cenomanian (Pariadens) (
The other Cretaceous metatherians with a highly unusual dentition are the species of Glasbius (Figs
As with many fossil groups, the greatest handicap in studying the biogeography and distribution of Cretaceous metatherians is their patchy fossil record (Fig.
Regardless, this imperfect North American record is considerably better than the very poorly sampled Asian and European Late Cretaceous records. Metatherians clearly lived in these regions, but very few specimens are known (e.g., only two Cretaceous metatherian taxa are known from Europe, one from only a single tooth). Unequivocal metatherians have yet to be found in the Cretaceous of Africa (
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. Undoubtedly, as the metatherian fossil record improves and metatherian phylogeny becomes better resolved, more explicit cladistic biogeographic methods will enable biogeographic patterns to be proposed and tested with increased rigor. 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.,
Such a scenario is certainly congruent with the known fossil record, but as outlined above, this fossil record is biased. Just because the oldest and most basal currently known metatherian is from Asia is not particularly strong evidence that the clade must have originated there. Sinodelphys was found in the Yixian Formation, as part of a spectacularly preserved fauna that was killed, transported, and buried quickly by pyroclastic debris flows (
Once metatherians originated, they spread to various regions around the globe. The diversity of Cretaceous metatherians in North America, and to a lesser extent in Asia and Europe, indicates that most of their early diversification was centered in the northern continents. The lack of unequivocal Cretaceous metatherians in the southern continents is potentially due to sampling biases, as the Gondwanan latest Cretaceous fossil record is nowhere near as densely preserved or sampled as that in the northern continents. But, assuming that the lack of southern metatherian fossils either represents genuine absence or extreme rarity compared to the northern continents, then the Cretaceous metatherian radiation can be considered a predominantly Holarctic story. It is worth noting that
There has been intense debate in the literature regarding how metatherians spread across the northern continents during their Cretaceous evolution. Several dispersal events probably occurred, but number and timing of these events is uncertain, due to the incomplete metatherian record, the lack of radiometric dates for most fossils, and poor resolution of metatherian phylogeny. At least one inter-continental interchange event must explain the distribution of deltatheroidans in North America and Asia (e.g.,
Deltatheroidans were first discovered in the Late Cretaceous of Mongolia by the American Museum of Natural History’s Central Asiatic Expeditions in the 1920s (
However, more recent discoveries show that early deltatheroidans were present in the middle Cretaceous of North America (e.g.,
In terms of the European Cretaceous metatherians, these taxa are so rare, and their phylogenetic positions are so poorly resolved, that it is difficult to comment on their biogeographic implications.
Similarly,
Metatherian faunas also provide an excellent opportunity to investigate Late Cretaceous provincialism within North America (
Yet again, however, sampling biases may be influencing the above conclusions (
Finally, metatherians may give some insight into community structure and assembly on small time scales and in local geographic regions. Precise dating and dense sampling of successions of faunas in smaller areas has revealed that presence/absence and relative abundances of metatherian taxa may have fluctuated on short time scales (ca. 250 Ka) (
The Cretaceous record of metatherians includes a total of 68 valid species (one basal metatherian, six deltatheroidans, and 61 stem marsupialiforms) from the Barremian through Maastrichtian of Europe, Asia, and North America. In Tables
Metatherian richness during the late Early Cretaceous (Barremian–Albian) was paltry, never exceeding two species in any time bin. Taxa included the basal metatherian Sinodelphys szalayi from the Barremian of China and the deltatheroidans Atokatheridium boreni and Oklatheridium szalayi from the Aptian/Albian of North America. These two deltatheroidans are the most abundant boreosphenidans in the Tomato Hill local fauna (
The KTR has been interpreted as a significant episode in the evolution of terrestrial biotas (125–80 Ma) in which the taxonomic diversification of angiosperms and the resulting new food resources spurred co-evolutionary radiations of insects and some terrestrial vertebrates (e.g., herbivorous dinosaurs;
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. A detailed review of this Paleogene radiation of South American stem marsupialiforms and marsupials is beyond the scope of this review, but see
At the K-Pg boundary, metatherians were nearly wiped out in the local section (92%); there is only a single metatherian species, Thylacodon montanensis (=Peradectes cf. P. pusillus;
Reconstruction of the phylogenetic relationships of Cretaceous and Paleogene metatherians is important for understanding the pattern of metatherian survivorship across the K-Pg boundary and the origin of the crown-clade members of Metatheria, the Marsupialia. North American metatherian faunas underwent a catastrophic decline at the boundary. The K-Pg boundary section of eastern Montana, which contains the most intensely studied latest Cretaceous terrestrial vertebrate fauna in the world, shows a drop from 11 species in the uppermost Cretaceous Hell Creek Formation to only one, Thylacodon montanensis, in the lowest Paleocene Tullock Formation (
Thanks to R. Cifelli and an anonymous reviewer for comments and to W. A. Clemens for discussions that substantially improved this paper. Support for this work was provided by the National Science Foundation (EAR 0207750 to TEW, EAR 1325544 to TEW and SLB, and EAR-1325674 to GPW) and a Marie Curie Career Integration Grant EC 630652 (SLB).
List of taxa and characters used in phylogenetic analysis.
Data type: (measurement/occurence/multimedia/etc.)
Taxon-Character Matrix with characters ordered (TNT file).
Data type: Matrix.
Characters in common on the most parsimonious trees diagnosing the nodes on the strict consensus tree in Figure
Data type: Characters.
Explanation note: Characters in common on the most parsimonious trees diagnosing the selected nodes on the strict consensus tree resulting from the analysis run with characters ordered.
Temporal ranges of Cretaceous metatherian taxa used to calculate taxonomic richness of Metatheria.
Data type: Range.
Explanation note: Temporal ranges of Cretaceous metatherian taxa used to calculate taxonomic richness of Metatheria (Suppl. material 5). Data were compiled from the Paleobiology Database (PBDB; http: //fossilworks.org/?a=home),
Data used to calculate taxonomic richness for Metatherian shown in Figure
Data type: Range.
Explanation note: Data used to calculate taxonomic richness for Metatheria shown in Figure