NATURE | VOL 409 | 4 JANUARY 2001 | www.nature.com 53 articles Dual origin of tribosphenic mammals Zhe-Xi Luo*, Richard L. Cifelli² & Zo®a Kielan-Jaworowska³ *Section of Vertebrate Paleontology, Carnegie Museum of Natural History, Pittsburgh, Pennsylvania 15213, USA ² Oklahoma Museum of Natural History, 2401 Chautauqua, Norman, Oklahoma 73072, USA ³ Institute of Paleobiology, Polish Academy of Sciences, ulica Twarda 51/55, PL-00-818 Warszawa, Poland ............................................................................................................................................................................................................................................................................ Marsupials, placentals and their close therian relatives possess complex (tribosphenic) molars that are capable of versatile occlusal functions. This functional complex is widely thought to be a key to the early diversi®cation and evolutionary success of extant therians and their close relatives (tribosphenidans). Long thought to have arisen on northern continents, tribosphenic mammals have recently been reported from southern landmasses. The great age and advanced morphology of these new mammals has led to the alternative suggestion of a Gondwanan origin for the group. Implicit in both biogeographic hypotheses is the assumption that tribosphenic molars evolved only once in mammalian evolutionary history. Phylogenetic and morphometric analyses including these newly discovered taxa suggest a different interpretation: that mammals with tribosphenic molars are not monophyletic. Tribosphenic molars evolved independently in two ancient (holotherian) mammalian groups with different geographic distributions during the Jurassic/Early Cretaceous: an australosphenidan clade endemic to Gondwanan landmasses, survived by extant monotremes; and a boreosphenidan clade of Laurasian continents, including extant marsupials, placentals and their relatives. Because most mammals are only represented in the fossil record by their teeth, dental evidence has prominently ®gured in interpreting the relationships of early mammals. The highly distinctive tribo- sphenic molars, capable of both shearing (sphen) and grinding (tribein) occlusal functions, are the most important dental feature of marsupials and placentals (extant therians) and their close fossil relatives, collectively known as tribosphenidans 1 . The tribosphenic molar has been used to distinguish these therians from other Mesozoic mammals 1±4 , including stem holotherians such as ``sym- metrodonts'' and ``eupantotheres'' 3,4 , and from living monotremes. The traditional view that tribosphenic molars arose in the Early Cretaceous, and that the early diversi®cation of therians took place on northern continents 5 , has been challenged by recent discoveries on Gondwanan landmasses. Ambondro, from Madagascar, has fully tribosphenic molars 6 yet is of Middle Jurassic age, and is therefore some 25 Myr older than the earliest northern therians. Ausktribosphenos, a tribosphenic mammal from the Early Creta- ceous of Australia, is thought to have been a placental, possibly even a member of the living hedgehog family 7,8 . Thus, these new fossils have important implications for reconstructing the paleobiogeo- graphy and timing of divergence of the main extant mammalian groups. Here we re-evaluate the phylogenetic relationships of these newly discovered mammals, with respect to other Mesozoic and extant mammal groups. Phylogenetic relationships Parsimony analysis of the available evidence from the dentition and mandible (Fig. 1; also see Methods) places the tribosphenic mam- mals Ambondro 6 and Ausktribosphenos 7,8 , together with the earliest known monotreme Steropodon 6 (Australia, Early Cretaceous), in a monophyletic group, which we term the Australosphenida (concept modi®ed from Ausktribosphenida 7 ; see `Systematic Palaeontol- ogy'). This group is characterized by a well-developed, continuous mesial cingulid that wraps around and extends to the lingual side of the trigonid (Fig. 2); a mesiodistally short, buccolingually broad talonid; and reduced height of the trigonidÐat least when com- pared with other Jurassic/Early Cretaceous holotherians. Notably, Ausktribosphenos retains plesiomorphies of the jaw as seen in stem mammals 9 , and we provisionally recognize some of these primitive characters to be preserved also in Steropodon. By contrast, the Boreosphenida, a clade of northern mammals with tribosphenic molars 10±12 (Fig. 1), have distinctive cingulid cuspules (cuspule e, cuspule f, or both) but lack a continuous mesial cingulid. The mesial cingulid does not wrap around or extend to the lingual side of the molars. Furthermore, boreosphenidans and proximal relatives, such as Henkelotherium, are more derived in that they have a mandibular angle far more posteriorly positioned than australosphenidans, Kuehneotherium, morganucodontids and Sinoconodon. Further dental apomorphies are consistent with the monophyly of australosphenidans. For example, Steropodon 13 and Ausktribosphenos 7 both have the `twinned' paraconid and metaco- nid, and a well-developed lingual cusp on the talonid (Fig. 2). Ambondro 6 and Ausktribosphenos 7,8 share an unusual feature in which the premolars seem to be molariform, with a distinctive triangulation of the three main cusps and a prominent lingual cingulid. The posterior part of the premolar is buccolingually wide. This derived feature is shared by Obdurodon dicksoni 14 (Australia, Miocene), an ornithorhynchid monotreme 14,15 widely accepted to be a relative of Steropodon (in which the premolar is not pre- served 13 ). None of these derived premolar features of fossil ornitho- rhynchids, Ambondro and Ausktribosphenos is present in the earliest known eutherians 10,11 , metatherians 12 , nor stem taxa of the northern tribosphenidans 16±18 . They are also absent in a wide variety of non-tribosphenic (eupantothere) mammals including Peramus 17 and Henkelotherium 18 . Australosphenidans may have af®nities with the northern holo- there Shuotherium 19±21 (Fig. 1), some unknown early ``symmetro- donts'' 9 , or the holotherian Dryolestidae 14 . However, by any previous interpretation they are independent from boreospheni- dans and their proximal relatives, including Henkelotherium 19 and pre-tribosphenic Peramus 17,22 . The clade of Ausktribosphenos, Ambondro and the monotreme Steropodon (Fig. 1), as inferred from mandibular and postcanine tooth morphology, is consistent with the phylogenies established by independent studies of basicranial 23,24 and postcranial 25±27 features of the main Mesozoic mammal groups documented by well-preserved fossils. In our expanded analysis (Fig. 1b), we added the cranial and postcranial features for those better-preserved taxa (for example, Morganucodon, Jeholodens and Henkelotherium). The simultaneous analysis (Fig. 1b) of cranial and postcranial data, together with the dental and mandibular characters, corroborates the australosphe- nidan clade and the boreosphenidan clade. Hence, the hypothesis of a diphyletic origin for tribosphenic mammals is supported by morphological characteristics other than teeth and mandibles. Independent multivariate analysis of the shape of the lower molar shows that Ausktribosphenos and Steropodon are grouped together © 2001 Macmillan Magazines Ltd