The origin and early evolution of metatherian mammals: the Cretaceous record

Abstract

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.

Keywords: Boreosphenida; Cretaceous; Deltatheroida; Mammalia; Marsupialiformes; Metatheria; biogeography; dentition; macroevolution; osteology; paleobiology; paleoenvironment; phylogeny.

Figure 1.

Phylogeny and diversification patterns of major mammal lineages after Luo (2007).

Figure 2.

Molar terminology and wear facet designation showing upper and lower molar tooth cusp homologies between the “symmetrodont” Kuehneotherium (A) and the metatherian Kokopellia (B) after Davis (2011a).

Figure 3.

Molar tooth nomenclature of basal metatherian right M2 (upper) and left m2 (lower). Mesial is to the right, buccal is up. Teeth are based on the Late Cretaceous metatherian Glasbius.

Figure 4.

Homologies between postcanine teeth of adult basal therian, basal metatherian, and basal eutherian mammals after O’Leary et al. (2013).

Figure 5.

Representative upper and lower molars of Cretaceous and early Paleogene metatherians. Scale bars equal 1 mm.

Figure 6.

Strict consensus of 2008 trees of 500 steps calculated using TNT (Goloboff et al. 2008) based on a taxon-character matrix of 95 taxa and 83 dental characters (CI = 0.210; RI = 0.703). Analysis conducted using a New Technology Search with a Driven Search (Sectorial Search, Ratchet, Drift, and Tree Fusing), finding minimum length 10 times. All characters are unweighted and 19 characters are additive. Numbers to the left of each node correspond to nodes in Online Suppl. material 1 listing the synapomorphies common to the 500 shortest trees. Numbers to the right of each node correspond to Bremer branch supports calculated from a pool of 30,000 suboptimal trees of up to 10 steps longer than the shortest trees obtained.

Figure 7.

Cast of holotype of Asiatherium reshetovi. A postcranial skeleton B close-up of right forelimb C ventral view of skull. Scale bars equal 1 cm.

Figure 8.

Skull of Monodelphis brevicaudata, modified from Wible (2003). Skull (A–D) and mandible (C) in dorsal (A), ventral (B), left lateral (C), and caudal (D) views. Abbreviations: an angular process; as alisphenoid; astp alisphenoid tympanic process; bo basioccipital; bs basisphenoid; coc coronoid crest; con mandibular condyle; cor coronoid process; ctpp caudal tympanic process of the petrosal; ec ectotympanic; eo exoccipital; fc fenestra cochleae; fm foramen magnum; fr frontal; ham pterygoid hamulus; inf incisive foramen; iof infraorbital foramen; ip interparietal; jf jugular foramen; ju jugal; lac lacrimal; lacf lacrimal foramen; m malleus; maf masseteric fossa; mapf major palatine foramen; mf mental foramen; mpf minor palatine foramen; mx maxilla; na nasal; oc occipital condyle; pa parietal; pal palatine; pcp paracondylar process of the exoccipital; pe petrosal; pmx premaxilla; pgp postglenoid process; ppt postpalatine torus; pptf foramen in the postpalatine torus; ps presphenoid; pt pterygoid; ptn posttemporal foramen; ptp posttympanic process; rtpp rostral tympanic process of the petrosal; so supraoccipital; sq squamosal; tl temporal line.

Figure 9.

Right petrosal Type A (Protolambda) after Wible (1990) showing reconstruction of vasculature. Abbreviations: ac aqueductus cochleae; adm arteria diploetica magna; cev capsuloparietal emissary vein; cp crista parotica; ctpp caudal tympanic process of petrosal; er epitympanic recess; fc fenestra cochleae; fi fossa incudis; fs facial sulcus; fv fenestra vestibuli; hF, hiatus Fallopii; If, lateral flange of petrosal; lhv lateral head vein; It, lateral trough of petrosal; me mastoid exposure; mp mastoid process; pc prootic canal; pcv vein ofprootic canal; pff primary facial foramen; pp paroccipital process; pr promontorium; ri ramus inferior of stapedial artery; rs ramus superior of stapedial artery; rtpp rostral tympanic process of petrosal; sa stapedial artery; sev sphenoparietal emissary vein; sf stapedius fossa; sff secondary facial foramen; sips sulcus for inferior petrosal sinus; spd sulcus for perilymphatic duct; vdm vena diploetica magna.

Figure 10.

Skeleton of Monodelphis domestica. Scale bar is 1 cm.

Figure 11.

Humerus and carpi of Cretaceous metatherians. A Distal humerus of unidentified metatherian (cf. Sulestes?) from the Bissetky Locale, Uzbekistan after Chester et al. (2010) in anterior view. Carpus of the Cretaceous stem therian Eomaia (B) and the Cretaceous metatherians Sinodelphys (C) and Asiatherium (D) after Szalay and Trofimov (1996) and Luo et al. (2003). Scale bars equal 1 mm.

Figure 12.

Partial femora of unidentified metatheria (cf. Sulestes?) from the Bissetky Locale, Uzbekistan after Chester et al. (2012). A–C right distal femur in anterior (A), posterior (B), and distal (C) views D–F right proximal femur of a possible unidentified metatherian in proximal (D), anterior (E), and posterior (F) views.

Figure 13.

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 Szalay and Sargis (2006). D–F isolated astragalus (cf. Sulestes?) from the Bissetky Locale, Uzbekistan in dorsal (D), ventral (E), and distal (F) views after Szalay and Sargis (2006). G articulated partial pes of Sinodelphys in ventral view H–I calcaneum and astragalus, respectively, of Eomaia in ventral view J–K calcaneum and astragalus of Sinodelphys, respectively, in ventral view L–M calcaneum and astragalus of Protolambda, respectively, in ventral view G–M are after Luo et al. (2003). Scale bars equal 1 mm.

Figure 14.

World map showing Late Cretaceous metatherian locales. Numbering of locales corresponds to the Cretaceous metatherian localities listed in Table 3.

Figure 15.

Taxonomic richness of Cretaceous and earliest Paleocene metatherians (see Tables 3–4, Suppl. materials 4–5 for data used to calculate values).