A Pre-neogene Phalangerid Possum from South Australia

-Phalangeridae is one of the most widely dispersed families of possums (Marsupialia, Dirprotodontia) in the Australasian region, extending from Tasmania in the southeast to Sulawesi of the Greater Sunda Islands of Indonesia in the northwest. Yet this one family of possums has generated the most morphological and biochemical phylogenetic uncertainties of any family within Order Diprotodontia. The various phylogenetic relationships for the family have led to different biogeographic models in regard to the site of origin and directions of dispersal for taxa within the family. The recovery of a maxilla from faunal zone B of the late Oligocene Etadunna Formation at Lake Palankarinna, South Australia (ca. 25 mya), results in the oldest known phalangerid to date, some ten million years older than the numerous Middle Miocene fossil phalangerids described from Riversleigh, Queensland. Whereas the Riversleigh phalangerids are similar enough to modern taxa to have originally been included in modern genera, the Etadunna specimen has morphologies that are very plesiomorphic for the family. These include a bladed P3 with a central main cusp that has denticles posteriorly, but no ridges; P3 aligned with tooth row; M1 with parastyle shear aligned with blade of P3; and M2 and M3 more square in occlusal outline. Autapomorphic character states include an infraorbital canal anterior to the second premolar, lack of an intraorbital groove, and the opening of the lacrimal canal inside the orbit. With substantial molecular time-of-divergence data now available, plus the addition of this new pre-Neogene phalangerid from South Australia, a new biogeographic model for site of origin and dispersal can be offered where phalangerids originate in Australia, diversify and give rise to the cuscus subfamilies, which disperse to New Guinea and then to Indonesia. INTRODUCTION The Australian possum family Phalangeridae, which includes cuscuses and brush-tailed possums, is the most widely distributed Australasian marsupial family with approximately two-dozen recognized extinct and extant species that range over most of Australia (including Tasmania), New Guinea, and northwestward to the Celebes Islands (Flannery, 1994; Hamilton and Springer, 1999; Osborne and Christidis, 2002; Springer et al., 1990; Fig. 1). This one family has generated the most phylogenetic and taxonomic uncertainties of any family within Order Diprotodontia, whether those phylogenies are based on morphological data or on biochemical data (e.g., Flannery et al., 1987; George, 1987; Groves, 1987a; Norris, 1994; Springer et al., 1990; Kirsch and Wolman, 2001; Ruedas and Morales, 2005). The various phylogenetic relationships for the family have led to different biogeographic models in regard to the site of origin (Australia or Sulawesi in the Celebes) and directions of dispersal (Australia to the Celebes or from the Celebes to Australia), for taxa within the family (e.g., Flannery et al., 1987 or Ruedas and Morales, 2005). Late Oligocene deposits in South Australia from the Etadunna and Wipajiri formations in the Lake Eyre Basin, and from the Namba Formation in the Frome Basin, have produced a wide range and the earliest records of most of the extinct and extant possum families (Fig. 2). Burramyidae, Ektopodontidae, Miralinidae, Pilkipildridae, and Pseudocheiridae have all been recovered from deposits of the Etadunna Formation, yet there had been no positive sign that Phalangeridae was present at all (see the series of papers in Archer, 1987, or those cited in Woodburne et al., 1993). The absence of phalangerids in the late Oligocene had been confusing considering that the earlier molecular studies (e.g., Springer et al., 1990; Springer, 1997), which produced divergence time data from molecular sequences, indicated that the phalangerid lineage should be present by the Eocene. Figure 1. Distribution of Phalangeridae subfamilies proposed by Ruedas and Morales (2005). Distributions based on Flannery (1994). Figure 2. Locality map for outcrops of the Etadunna Formation and the contemporaneous Namba Formation (black triangles), which have produced late Oligocene-aged marsupial fossils (Etadunna Formation outcrops indicated by arrows pointing to triangles). Eocuscus sarastamppi was recovered from informal faunal zone B, representing the Ditjimanka local fauna, at Lake Palankarinna (middle triangle). The inset list indicates the local faunas from the Etadunna Formation in stratigraphic order and the informal faunal zone with which they are associated. The Kutjamarpu local fauna has an asterisk, as it is from the Wipajiri Formation, which unconformably overlies the Etadunna Fm. and would represent an additional faunal level (“F”) younger than those of the Etadunna Formation (after Woodburne et al., 1993). Here we report on the first record of a phalangerid from the Etadunna Formation and, thus far, the oldest record of a phalangerid from Australia. This record is based on a maxilla with P3-M3 found by one of us (JP) in a buff-colored clay layer in a deposit representing informal faunal zone B of the Etadunna Formation at Lake Palankarinna and the Ditjimanka local fauna (Woodburne et al., 1993). Dental morphology clearly places the specimen within Phalangeridae (semilophate occlusal pattern of the upper molars, molar shape, premolar number), whereas cranial features and other dental features indicate that this late Oligocene species is the sister-taxon to all other phalangerids. The late Oligocene presence of phalangerids in central South Australia, the diversity of trichosurine phalangerids from the middle Miocene deposits of northern Queensland (Crosby, 2007), plus data from a recent nuclear gene molecular study by Meredith et al. (2008), all indicate a change from the prevailing biogeographical model of Flannery et al. (1987) to a newer model where Australia is the site of origin for the family followed by subsequent dispersal to the Celebes. Definitions and Institutional Abbreviations--Dental nomenclature follows Luckett (1993), where premolars (P-upper and p-lower) are numbered 1-3 and molar designation is M1-4 (upper molars) and m1-4 (lower molars). Molar occlusal surface terminology for diprotodontian marsupials follows that of Woodburne et al. (1987) and is illustrated in Figure 3. Anatomical directions are L (left) and R (right); measurements are in millimeters. SAM, South Australia Museum, Adelaide, South Australia; QM, Queensland Museum, Brisbane, Queensland. Figure 3. Diagram of the holotype of Eocuscus sarastamppi, SAM P44324, illustrating the dental terminology and locations used herein. Additional terminology; preparacrista and postparacrista are the crests anterior and posterior to the paracone; premetacrista and postmetacrista are the crests anterior and posterior to the metacone; preprotocrista and postprotocrista are the crests anterior and posterior to the protocone; premetaconular crista and postmetaconular crista are the crests anterior and posterior to the metaconule; and the centrocrista is composed of the postparacrista anteriorly and the premetacrista posteriorly. SYSTEMATIC PALEONTOLOGY Cohort AUSTRALIDELPHIA Szalay 1982 Order DIPROTODONTIA Owen, 1866 Family PHALANGERIDAE Thomas, 1888 EOCUSCUS gen. nov. Etymology--Eo-, Greek for dawn, representing the earliest known member of the family of cuscuses and brush-tail possums; -cuscus, aboriginal word in reference to a phalangerid possum. Type species-Eocuscus sarastamppi sp. nov. Diagnosis-As for the holotype and the only known species. Eocuscus sarastamppi sp. nov. (Figs. 4 and 5; Table1) Etymology--In honor of Dr. Sara K. Stampp, former provost at Saint Mary’s College of California, under whose auspices the project resulting in the collection of the holotype received funding. Locality and Age-Holotype recovered from lacustrine to fluviatile deposits of the Etadunna Formation, Lake Palankarinna, Lake Eyre Basin of South Australia; specifically from the SAM Quarry, bottom of the white clay unit above the sandy unit at the base of the quarry wall, faunal zone B, Ditjimanka local fauna of late Oligocene age (ca. 25 mya, Woodburne et al., 1993). Holotype-SAM P44324, right maxilla with P3-M3. Diagnosis-Eocuscus sarastamppi gen. et sp. nov. is distinguished from other phalangerid possums, both extant and extinct, by the following eleven unique autapomorphic (A) or plesiomorphic (P) character states (where character state polarities have been determined by the distribution of character states within phalangerid possums and within other possum families): 1) P3 bladed with a central main cusp having denticles present on posterior crest, but without vertical ridges on buccal and lingual faces (P); 2) P3 aligned with tooth row and not set obliquely to it (P); 3) M1 with parastyle shear aligned with blade of P3 (P); 4) M2 and M3 more square (i.e., wider per length) in occlusal outline (P); 5) infraorbital canal anterior to second premolar (A): 6) lack of intraorbital groove on maxillary shelf forming floor on inside of orbit (A); 7) sphenopalatine foramen does not lie within intraorbital groove (groove not present) and opens medially into nasal cavity near posterior end of maxilla (A); 8) lacrimal foramen inside orbit relatively close to floor of orbit (A); 9) lacrimal foramen formed equally by maxilla, anteroventrally, and by lacrimal, posterodorsally (A); 10) nasolacrimal canal runs horizontally in nasal cavity from lacrimal foramen to at least maxillary-premaxillary suture (A); P1 not separated from P3 by diastema (P). Description-SAM P44324, the holotype, is a right maxilla, which retains the maxilla-premaxilla suture anteriorly. The preorbital wing is broken just below the level of the orbital process of the lacrimal, and it retains some of the maxillary-palatine suture posteriorly. Much of the palatal process of the maxillary is still present, indicating that the palatal fenestra extended anteriorly to the level of the interloph valley of M2. The anterior extent of the palatine along the lateral margin of the right palatal fenestra is to the level of the anterior loph of M3. The floor of the orbit is very broad and long anteroposteriorly creating an extensive flat aspect to it. There is no intraorbital groove medial to the alveolar bone of the maxilla leading to the orbital entrance to the infraorbital canal (Fig. 4). The sphenopalatine foramen opens medially into the posterior nasal cavity through the sidewall of the maxilla at the posterior end of the maxilla near the triple junction of the maxilla, palatine, and the frontal. The opening of the nasolacrimal canal, the lacrimal foramen, is inside the orbit and the sutures for the lacrimal bone are visible. The anteroventral half of the circular lacrimal foramen is formed from the maxilla, and the maxillary-lacrimal sutures can be traced indicating that there is an equal contribution to the lacrimal foramen by the lacrimal bone, as it would form the posterodorsal border of the foramen. The lacrimal foramen is low on the orbit margin, as the dorsal margin of the jugal and the maxilla process of the zygomatic arch do not rise very far above the floor of the orbit. There are only 4.0 mm of vertical distance from the floor of the orbit at the opening of the infraorbital canal to the level of the lacrimal foramen. This is only half the vertical distance between those same anatomical features in extant phalangerids. A broad groove on the internal surface of the maxilla within the anterior nasal cavity begins at the lacrimal foramen and extends anteriorly to the maxillary-premaxillary suture where the specimen ends. This internal groove indicates the path of the nasolacrimal canal within the nasal cavity. The canal is nearly horizontal along its entire length, and only slightly higher at the lacrimal foramen than at the anterior end of the maxilla. This near horizontal orientation of the nasolacrimal canal differs from the condition for extant taxa and presumably extinct taxa such as the mid-Miocene Onirocuscus from Riversleigh, where the lacrimal foramen is much higher than the palate resulting in a substantial vertical drop in the nasolacrimal canal before it becomes horizontal. The anterior portion of the jugal, which is only ~5 mm in length, remains attached to the base of the maxillary process of the zygomatic arch. Dentally, P3 and M1 through M3 are present. Alveoli for the C and P1 are present anterior to P3, as is the alveolus for a tri-rooted M4 (Fig. 5). P1--There are two circular alveoli anterior to P3, with the anterior of the two having the greater diameter. There is no diastema between the posterior alveolus and P3, but there is a diastema between the canine alveolus and the anterior of the two premolar alveoli (see below for a discussion on the determination that these two alveoli represent those for a P1). Figure 4. Comparison of the anterior orbital region of the holotype of Eocuscus sarastamppi (SAM P44324; left in dorsal view) and the extant species of Brushtail Possum, Trichosurus vulpecula (right). As shown here for Trichosurus and all extant phalangerids, plus all Neogene phalangerids, the sphenopalatine foramen lies in a groove, which leads to the orbital opening of the infraorbital canal as indicated by the arrow. Eocuscus lacks the groove leading to the infraorbital canal (indicated by the long arrow) and the sphenopalatine foramen (indicated by the short arrow) opens to the posterior nasal cavity further posteriorly at the triple junction of the maxillary, palatine and frontal bones. Figure 5. Holotype of Eocuscus sarastamppi, SAM P44324, a right maxilla with P3-M3 present, plus the alveoli for double-rooted P1 and M4. A) Occlusal view, note the extended parastyle and lack of anterior cingulum on M1; B) Occlusal view, to complete a steropair of the dentition; and C) Labial view, note the continuous shearing surface from P3 onto the parastyle of M1, also note the opening of the lacrimal foramen which is inside the border of the orbit, the maxilla contributes to the anteroventral half of the foramen, while the lacrimal bone contributes to the posterodorsal half of the foramen. The scale is marked in millimeters. P3--The third premolar is aligned with the arch of the upper molar arcade. The blade of P3 has its shearing angle continued on the anteroposterior bladed paracone. P3 has a single central cusp with a crest descending to the crown, both anteriorly and posteriorly, and the cusp extends well past the occlusal level of M1 creating a dagger-like shape in lateral view. There are three small cuspules or denticles posterior to the central cusp along the steeply inclined posterior crest. There are no vertical ridges associated with the cuspules. The anterior crest curves lingually and creates a concave space on the anterolingual face of the tooth, whereas the anterobuccal face is convex. The tooth is widest in occlusal aspect below the central cusp. It then narrows posteriorly in a slightly shorter distance than the anterior half of the tooth. A posterolingual ridge descends from the posterior crest at a point where the posterior crest contacts the parastyle of M1. This ridge continues along the crown margin trending in an anterolingual direction, creating a lingual cingulum that extends anteriorly for two-thirds the crown length. M1--This tooth is rectangular in occlusal outline. There is an extreme height differential between the buccal cusps and the lingual cusps, which is independent of wear. The paracone and metacone are tall and are at the labial margin of the tooth. Their respective labial faces are rounded with a slight ectoflexus between them. In contrast, the lingual faces of the paracone and metacone are vertical and flattened, and with their associated cristae, present a bladed appearance, anteroposteriorly. The preparacrista is oriented anteriorly and continues the shearing effect of the P3 in a carnassial notch-like morphology. The preparacrista has two cuspules along the crest, one halfway along and the second almost at its anterior terminus. The centrocrista between the paracone and metacone is linear and anteroposteriorly oriented. The centrocrista acts as a bladed crest on the posterior face of the paracone and the anterior face of the metacone as two cusps adjacent to each other. There is a larger cuspule on the premetacrista portion of the centrocrista. The postmetacrista has a kink near the apex of the lingually oriented metacone, and then bends at a right angle resulting in a longer posterior segment; it is thus parallel to, but offset lingually from, the centrocrista and preparacrista. At the corner of the metastyle is a small stylar cusp in the E position. The protocone is a low, conical cusp with a low transverse ridge that extends from near the apex of the protocone to the base of the paracone. The ridge then extends partially up the lingual face of the paracone forming the typical semilophate morphology seen in the phalangerids and other diprotodontians. There is no preprotocrista nor is there an anterior cingulum. These latter characters are the result of the bladed paracone and its continuation of the shearing surface of P3. The metaconule is fully hypertrophied to make the fourth cusp in the posterolingual position equal in size to the protocone and like that cusp, it is low and conical. A more robust ridge than present in the paraloph connects the metacone to the metaconule, which begins at the kink in the postmetacrista and continues transversely to the metaconule. At the midpoint of the ridge is a distinct swelling indicating the position of the neometaconule. The postmetaconular crista continues around the posterior margin of the tooth to form a posterior cingulum. M2--The second molar is distinctly wider than M1, both anteriorly and posteriorly, but shorter because it lacks the anteriorly expanded parastyle. As with M1, there is a distinct stylar cusp present along the buccal margin. The stylar cusp on M2 is anterior to the paracone in the position of a stylar cusp A, whereas on M1 the stylar cusp is in the E position. There is a cuspule on a crest extending anteriorly from the metacone, which is separate from the centrocrista. If this is a stylar cusp and not a neomorphic cuspule, then the cuspule would be a stylar cusp C. The anteriorly directed parastyle is less well developed on M2 than on M1. The paracone has a conical buccal face, but the lingual face is flat and vertical as on M1. The centrocrista is not linear, as the postparacrista is oriented posterolingually, while the premetacrista is oriented posterobuccally. The metacone, like the paracone, is a more conical cusp than on M1. The postmetacrista descends from the metacone apex and about halfway down the posterior face it begins to bend lingually, eventually becoming continuous with the postmetaconular crista to form a laterally wide posterior cingulum. The protocone is pyramidal in shape because of the formation of the paraloph. Without the influence of an extended parastyle, the preand postprotocristae form a more acutely angled structure around the protocone; the preprotocrista extends buccally to the parastyle forming an anterior cingulum. The paraloph is kinked anteriorly just lingual to the apex of the paracone and then extends transversely as a raised ridge to intersect the preprotocrista just anterior to the protocone. In the middle of the paraloph is a neomorphic cusp, the neoparaconule. The metaconule is smaller than the protocone which corresponds to a smaller metacone than paracone. The premetaconular crista is short and anterobuccally directed, and it meets with the postprotocrista at the lingual margin of the interloph valley. The post metaconular crista helps form the posterior cingulum. The metaloph is slightly V-shaped anteriorly, beginning at the apex of the metacone and terminating at the metaconule. The metaloph is a robust structure with sloping anterior and posterior faces. A small cuspule is present near the midline representing a neometaconule. M3--The third molar is both shorter and narrower than M1 or M2 (Table 1). The paracone is the largest buccal cusp and is pyramidal in shape with a flattened buccal face and a pointed lingual face. The preparacrista is short, anteriorly directed, and it terminates in a cuspule in the stylar cusp A position. The postparacrista is longer, posteriorly directed, and it runs buccally to the premetacrista, which is shorter and terminates on the flank of the postparacrista forming a high wall on the labial side of the interloph valley. The paraloph is segmented with a short crest from the apex of the paracone that is truncated at a narrow anteroposteriorly oriented groove just labial to the neoparaconule. The latter has a short, lingually directed crest that terminates on the flank of the preprotocrista, just anterior to the apex of the protocone. The metacone is pyramidal in shape, like the paracone, with the buccal face flattened and the lingual face pointed. The postmetacrista is initially posteriorly directed, but bends at a right angle lingually to form, with the postmetaconular crista, the posterior cingulum. The protocone is very broad and is the largest cusp of the tooth, with the preand postprotocristae forming a very obtuse angle that is nearly linear in shape. The preprotocrista is thicker as it descends from the apex of the protocone anteriorly and then thins as it bends labially at a right angle to form the anterior cingulum. The postprotocrista is truncated and ends at the lingual opening of the interloph valley. The metaconule is conical in shape and lacks a premetaconular crista. The postmetaconular crista is labially directed and forms part of the posterior cingulum. The metaloph is much narrower mediolaterally than the paraloph, reflecting the abrupt decrease in tooth size from the M3 to M4. The metaloph is a narrow transverse ridge with low sloping anterior and posterior faces. A neometaconule occurs midway along the metaloph. M4--The morphology of this tooth is presented only by the root pattern of the alveoli posterior to the M3. The breadth across the two anterior roots indicates that the anterior half of the tooth was no wider than the posterior half of M3, while the posterior half of the M4 probably ended in a round point as there is only a single circular root to support the posterior crown of the tooth. Table 1. Measurements of the dentition of the Oligocene phalangerid, Eocuscus sarastamppi gen. et sp. nov., from the Etadunna Formation, South Australia (mm). Tooth Length Ant. Width Post. Width