Earliest modern bandicoot and bilby (Marsupialia, Peramelidae and Thylacomyidae) from the Miocene of the Riversleigh World Heritage Area, northwestern Queensland, Australia

ABSTRACT Recent molecular phylogenies of peramelemorphians suggest that thylacomyids (bilbies) and peramelids (modern bandicoots) diversified sometime in the late Oligocene or early Miocene. Until now, however, the earliest fossil evidence of thylacomyids and peramelids was from the Australian Pliocene. Here we describe the oldest peramelid and thylacomyid from the middle Miocene of the Riversleigh World Heritage Area, northwestern Queensland. The peramelid, Crash bandicoot, gen. et sp. nov., is represented by a single maxilla containing M1–3 that exhibits peramelid synapomorphies, including development of a metaconular hypocone, an incomplete centrocrista, and well-developed anterior cingulum. The thylacomyid, Liyamayi dayi, gen. et sp. nov., is represented by M2 and m1, which show thylacomyid synapomorphies including a conical entoconid, a conical stylar cusp B (StB) and StD, and reduced distance between the metastyle and StD. The results of our phylogenetic analysis indicate that both species are part of crown-group Peramelemorphia. SUPPLEMENTAL DATA—Supplemental materials are available for this article for free at www.tandfonline.com/UJVP


INTRODUCTION
Peramelemorphians (bandicoots and bilbies) are small-to medium-sized omnivorous, terrestrial marsupials present in diverse modern habitats from rainforest to deserts in Australia, New Guinea, and surrounding islands. Modern bilbies are represented by two (one extant but vulnerable and one recently extinct) desert-adapted (but not -restricted) species, whereas modern bandicoots are far more speciose and ecologically diverse. They are characterized by having syndactylous hind limbs (a derived feature shared with diprotodontians) and polyprotodonty (a plesiomorphic condition shared with dasyuromorphians, notoryctemorphians, and extant ameridelphids). On morphological grounds, all bandicoots have traditionally been regarded to be members of the Peramelidae; however, Archer and Kirsch (1977) argued that the bilbies (species of Macrotis and Ischnodon) merited being treated as a family distinct from peramelids and peroryctids. Groves and Flannery (1990) proposed that the eight modern genera constituted just two families: Peroryctidae (species of Peroryctes, Microperoryctes, Rhynchomeles, and Echymipera) and Peramelidae (species of Macrotis, Ischnodon, Chaeropus, Perameles, and Isoodon). This latter taxonomic arrangement was supported by the morphological analysis of Travouillon et al. (2010), which included Miocene taxa from the Riversleigh World Heritage Area (WHA) of northwestern Queensland (Fig. 1) described by Muirhead (2000) as members of the Yaralidae, an extinct family of peramelemorphians.

Body Mass Estimates
Tooth lengths and widths were measured for each specimen (Table 1). These were then used to estimate individual body mass using Myers' (2001) regression equations, which correlate dental variables with marsupial body mass. We used the highest possible ranked equation from the 'all species excluding dasyuromorphians' data set from Myers (2001:

Phylogenetic Analysis
We used the data matrix by Travouillon et al. (2013) and Gurovich et al. (2013), revised from Travouillon et al.'s (2010) matrix, to assess the phylogenetic relationships within Peramelemorphia of the two species described here. The matrix comprises 42 taxa and 156 qualitative morphological characters, of which 33 are cranial and 123 dental (see Supplementary Data 1 and 2). Several characters from Travouillon et al.'s (2010) matrix were deleted (to be replaced by more comprehensive characters) and some modified (see Supplementary Data 1). Because they represent putative morphoclines, 71 characters were ordered in all analyses (see Supplementary Data 1). The matrix was completely rescored to avoid repeating mistakes that may have been present in earlier iterations of this matrix. The following fossil bandicoots were added to the analysis: cf. Peroryctes tedfordi, cf. P. sp., Perameles sobbei, P. bowensis, P. allinghamensis, Ischnodon australis, Yarala burchfieldi, Y. kida, Galadi speciosus, G. grandis, G. amplus, G. adversus, and Bulungu palara. These species were omitted from previous studies because they contained too much missing data and some of them weren't yet described. Microperoryctes ornata was removed from the matrix because specimens used to score this taxon previously have subsequently been reassigned by Australian Museum staff to Microperoryctes longicauda (Sandy Ingleby, pers. comm.). In addition to the fossil dasyuromorphians Barinya wangala and Mutpuracinus archibaldi and the early Eocene stem australidelphan Djarthia murgonensis, five extant outgroup species from the family Dasyuridae were added: Dasyurus hallucatus, Dasyuroides byrnei, Phascogale tapoatafa, Antechinus stuartii, and Sminthopsis macroura.

Parsimony Analysis
A parsimony analysis was performed using PAUP * 4.0b10 (Swofford, 2002) using a two-stage search strategy following Worthy et al. (2006) and Beck et al. (2008). An initial search comprising 1000 heuristic replicates, saving 10 trees per replicate, was followed by a second heuristic search within the saved trees. Multiple most parsimonious trees produced were summarized using strict consensus. Bootstrap values for each node were calculated using 1000 bootstrap replicates of 10 random addition sequence replicates. Decay indices were also calculated using TreeRot.v3 (Sorenson and Franzosa, 2007).
A second analysis was performed repeating the same steps but with a 'molecular scaffold' as a 'backbone' constraint. For the backbone, relationships among extant peramelemorphians were constrained to reflect the molecular phylogeny of Westerman et al. (2012). Only taxa analyzed by Westerman et al. (2012) were included in the molecular scaffold, and only those clades that received ≥70% partitioned maximum likelihood bootstrap support and ≥0.95 partitioned Bayesian posterior probability in the analyses of Westerman et al. (2012:table 2) were enforced as monophyletic. The five extant dasyurid outgroup taxa were also included in the molecular scaffold, with their relationships constrained to match those recovered by Krajewski et al. (2007:fig. 5) and Westerman et al. (2008: fig. 2). The molecular scaffold topology is included in Supplementary Data 3.
Etymology-Named after Crash Bandicoot, the popular video game character created by Andy Gavin and Jason Rubin, with a related inference that this was the start of a new radiation of more modern bandicoots that 'crashed' through to dominate younger, drier ecosystems of Australia. The genus is here assigned masculine gender.
Type Locality and Age-Alan's Ledge 1990 Site (AL90), Riversleigh World Heritage Area, northwestern Queensland, Australia. AL90 Site is interpreted to be part of Riversleigh's Faunal Zone C and as such middle Miocene in age Arena, 2004;Travouillon et al., 2006Travouillon et al., , 2011.

Description
The M1 is longer than wide (Fig. 2). Stylar cusp A (StA) is a low cusp on the anterobuccal corner of the tooth. A crest runs from the tip of StA posteriorly and ends at the anterior flank of StC. StC (Fig. 2B) is on the parastylar region of M1, directly posterior to StA. StB, if present, is indistinguishable from StC. The preparacrista is curved and connects StC to the paracone anterolingually. The postparacrista runs from the paracone posterobuccally, almost parallel to the preparacrista, and ends at the base of the posterolingual flank of StC. It does not form a centrocrista with the premetacrista. Instead, a small bridge connects the parastylar region to the metastylar region at the ectoloph and probably represents a remnant of the centrocrista, a condition also seen in Peroryctes broadbenti (see Aplin et al., 2010). The metacone is situated posterolingual to the paracone. The metacone is the tallest cusp on the crown, followed in decreasing order by StD, paracone, StC, metastyle, StA, protocone, and metaconular hypocone. The premetacrista, which is longer than the postparacrista, runs from the metacone anterolingually and ends at the base of the anterolingual flank of StD. The postmetacrista, the longest crest on the crown, connects the metacone to metastyle posterobuccally. A stylar crest connects the metastyle to the tip of StD anteriorly (Fig.  2B). StE, if present, is not distinguishable from this stylar crest. StD is a large round cusp directly buccal to the metacone. StD1 is absent. The protocone is posterolingual to the paracone. The preprotocrista runs from the protocone anterobuccally and ends at the lingual flank of StA, forming a complete anterior cingulum. The postprotocrista is almost straight and connects the protocone to the metaconular hypocone posteriorly. This crest then continues posterobuccally to end below the postmetacrista, past the midpoint between the metacone and metastyle, forming a posterior cingulum. The metaconular hypocone is large and is level with the protocone lingually.
The morphology of M2 is similar to that of M1 except as follows (see Fig. 2A and B). The crown is much wider, elongating the preparacrista, postparacrista, premetacrista, postmetacrista, and preprotocrista. StA is taller, on the parastylar shelf, and connects to the paracone via the preparacrista. StC is absent. Instead, StB is a large conical cusp, located posterior to StA. StB remains taller and bigger than StA. A short crest runs from the tip of StB anterolingually to the base of StB. A small crest is also present on the posterior side of StB and may represent a remnant of StC. StE is present as a small cusp on the stylar crest midway between the metastyle and StD. StD1 is a miniscule cusp and directly anterior to StD. A short crest connects StD1 anterolingually to the bridge connecting the parastylar and metastylar regions. The anterior cingulum is a larger shelf that is widest just lingual to StA. The metaconular hypocone is smaller than in M1 but more cusplike on the lingual margin of the tooth. The postprotocrista ends at base of the posterior flank of the metacone; hence, the posterior cingulum is incomplete.
The morphology of M3 is similar to that of M2 except as follows (Fig. 2). The crown is wider than long, with the protocone and paracone positioned more lingually. StA is taller, almost level with StD. The preparacrista is straighter and longer. StB is smaller, but StC is present as a small cusp directly posterior to StB. The parastylar and metastylar regions are not connected by a bridge because the ectoloph is breached. StE is absent and no stylar crest connects the metastyle to StD. StD is smaller. StD1 is absent. The metaconular hypocone is smaller.
Measurements of Crash bandicoot are presented in Table 1.
Generic Etymology-'Liya' is from the Waanyi word in the Riversleigh District of northwestern Queensland meaning round and 'mayi' meaning tooth (Breen, 1985), in reference to the rounded shape of the teeth and cusps. The genus is here given masculine gender.
Specific Etymology-The species name honors geologist and palaeontologist Dr. Robert Day, who generously supported this research.

Description
Upper Dentition-The M2 is wider than it is long with the buccal and lingual sides of the tooth rounded (Fig. 3A, B). The anterior cingulum is present as a short, low shelf lingual to StA. StA is a large cusp at the most anterobuccal corner of the tooth. StA connects to the paracone posterolingually via the preparacrista. The preparacrista is almost straight, curving only a third of the way to the paracone where another crest connects the preparacrista to the tip of the large conical StB posterobuccally. This crest continues posterobuccally from the tip of StB and ends before breaching the ectoloph. StC is absent. The paracone is posterolingual to StA and anterolingual to StB. The postparacrista runs from the paracone posterobuccally to the base of the posterolingual flank of StB. The metacone, which is directly posterior to the paracone, is the tallest cusp on the crown, followed in decreasing order by StD, paracone, StB, StA, metastyle, protocone, and metaconular hypocone. The premetacrista runs from the tip of the metacone anterobuccally to the anterolingual flank of StD. The postmetacrista connects the metacone to the metastyle posterobuccally. A short stylar crest connects the metastyle to the tip of the large conical StD anteriorly. StE, if present, is indistinguishable from this stylar crest. Just anterior to StD, StD1 is absent, but in its place a short crest runs anterolingually and ends before breaching the ectoloph. The protocone is directly lingual to the paracone. The preprotocrista is short and connects the protocone to the anterolingual flank of the paracone anterobuccally. The postprotocrista runs from the protocone posterobuccally, and then curves posterolingually at the anterior base of the metaconular hypocone. This crest continues through the metaconular hypocone and ends at the posterolingual flank of this cusp. The metaconular hypocone is small and situated anterolingual to the metacone. There is no posterior cingulum.
Lower Dentition-The anterior cingulid of m1 is highly reduced, with only a small remnant present just anterior to the paraconid (Fig. 3C, D). The protoconid is the tallest cusp, followed in decreasing order by the hypoconid, metaconid, entoconid, paraconid, and hypoconulid. The trigonid is narrower than the talonid. The protoconid, paraconid, and metaconid are equidistant. The paraconid is anterobuccal to the metaconid and anterolingual to the protoconid. The hypoconid is posterobuccal to the protoconid. The cristid obliqua is a concave crest that runs from the tip of the hypoconid to the posterobuccal flank of the protoconid. A minute cusp is present on the shelf in the hypoflexid region. The oblique posthypocristid connects the hypoconid to the hypoconulid. The entoconid is a large conical cusp directly posterior to the metaconid and directly lingual to the hypoconid. A short preentocristid runs obliquely towards the protoconid from the entoconid.
Measurements of Liyamayi dayi are presented in Table 1.
The constrained parsimony analysis, enforcing a molecular scaffold as a 'backbone' constraint, recovered 478 most parsimonious trees of 864 steps. The strict consensus is illustrated in Figure 4B, with bootstrap values above branches. Again, Crash bandicoot is recovered within the crown-group Peramelemorphia, and unresolved within the same clade as in the unconstrained analysis. However, the rest of the crown group is fairly unresolved and fails to identify the relationship between Liyamayi dayi and other peramelemorphians.

DISCUSSION
Until now, the oldest fossil members of the family Peramelidae were the Pliocene Perameles bowensis from Big Sink and Bow LFs, New South Wales (Muirhead et al., 1997), and Chin-chilla LF, Queensland (Mackness et al., 2000), and Perameles allinghamensis from Bluff Downs LF, Queensland (Archer and Wade, 1976). The most recent molecular phylogeny of peramelemorphians (Westerman et al., 2012) suggests that peramelids diversified in the middle Miocene, and estimated that the split between the three peramelid subfamilies Peramelinae (species of Isoodon and Perameles), Peroryctinae (species of Peroryctes), and Echymiperinae (species of Echymipera, Rhynchomeles and Microperoryctes) occurred at ∼13.8 million years ago. Crash bandicoot (Fig. 2), from AL90 Site in the Riversleigh World Heritage Area, is here recognized as the oldest member of this family, and our phylogenetic analysis and shared synapomorphies (see below) suggests that it belonged to the subfamily Peramelinae. AL90 Site is estimated to be middle Miocene in age Travouillon et al., 2006Travouillon et al., , 2011 and radiometric dating for this site (work in preparation) is congruent with this assessment (Woodhead et al., 2011). This species pushes back the first occurrence of the family in the fossil record at least 5 to 10 million years earlier than previously thought. AL90 Site is considered to represent a rainforest community (Travouillon et al., 2009;Black et al., 2012) based on the high proportion of arboreal folivores within the assemblage, including five species of pseudocheirid possums, two species of phalangerid possums, one small species of koala, and the arboreal diprotodontid Nimbadon lavarackorum. The presence of C. bandicoot, the earliest peramelid, in AL90 Site suggests that peramelids evolved in rainforest before subsequently diversifying into other types of environments.
Crash bandicoot (Fig. 2) shares a number of synapomorphies with peramelines. For example, the position and development of the metaconule on M2 and 3 is similar to that of Perameles gunnii and P. bougainville; the centrocrista is incomplete on all molars and StD and StB are conical and not connected by any stylar crests; the preparacrista connects to StA on M2 and 3; and StE is absent on M3. Crash bandicoot also retains a number of plesiomorphies shared with species of the extinct genus Galadi. These include the presence of a stylar crest connecting StD to the metastyle on M1 and 2 and the absence of a posterior cingulum on M2 and 3. Travouillon et al. (2010Travouillon et al. ( , 2013) identified a number of synapomorphies (e.g., well-developed lingual shelf and larger major cusp on P3; large metaconule; incomplete centrocrista on M3; and paraconid-metaconid distance is reduced on posterior molars) shared between species of Galadi and crowngroup peramelemorphians (and C. bandicoot), suggesting a close relationship between the two clades. It is possible that C. bandicoot shared a common ancestor with species of Galadi.
Thylacomyids are distinct from all other peramelemorphians in possessing the following combination of molar synapomorphies: metaconule absent; posterior cingulum absent; conical StB and StD; lingual displacement of the metacone (although less extreme in M. leucura than M. lagotis) such that it comes to function as a topographic 'hypocone'; shortened distance between metastyle and StD; preparacrista connects paracone to base of StB; conical entoconid; markedly reduced paraconid; and presence of a cusp in the hypoflexid region. Ischnodon australis shares all lower molar synapomorphies with species of Macrotis, although the paraconid is less reduced than in Macrotis lagotis, but closer in size to Macrotis leucura (no upper dentition has yet been recovered for I. australis). Liyamayi dayi shares some of those synapomorphies with species of Macrotis and Ischnodon australis: shortened distance between metastyle and StD; posterior cingulum absent; conical StB and StD (but stylar crests are still present on both stylar cusps); preparacrista connects paracone to base of StB (but also connects to StA); conical entoconid; and presence of cusp in hypoflexid region. However, some of these features are also present in peramelids, such as species of Isoodon (shortened distance between metastyle and StD; conical StB and StD; conical entoconid; presence of cusp in hypoflexid region) and Chaeropus ecaudatus (shortened distance between metastyle and StD; conical StB and StD; conical entoconid). These features probably represent homoplasies related to similarities in diet (i.e., omnivory). The shortened distance between the metastyle and StD is seemingly more significant because it is only present in species of Macrotis, Isoodon, and Chaeropus. This distance is long in species of Perameles, all New Guinea genera, and all other fossil peramelemorphians. However, Liyamayi dayi lacks key synapomorphies linking it to species of Isoodon (presence of posterior cingulum; well-developed metaconular hypocone) or C. ecaudatus (absence of anterior cingulum; well-developed metaconular hypocone), therefore supporting its placement within thylacomyids. Liyamayi dayi exhibits many plesiomorphic features (e.g., presence of metaconule; stylar crest connecting StD to metastyle; connection of preparacrista to StA; incomplete anterior cingulum) features that might be expected to be present in a Miocene peramelemorphian. The earliest fossil notoryctid, Naraboryctes philcreaseri , retains a number of dental plesiomorphies, such as the presence of a paracone, StB, StC, and StD on the upper molars. However, the paracone in N. philcreaseri is highly reduced, and absent in all other notoryctids (species of Notoryctes). In late Cenozoic thylacomyids, the metaconule is absent, but it might be expected that a more plesiomorphic thylacomyid would retain a small metaconule as L. dayi does. Interestingly, both notoryctids and thylacomyids have modern desert-adapted species (Notoryctes and Macrotis, respectively) that evolved in rainforest.
The age of the Riversleigh deposit that has produced L. dayi is not clear. Rick's Sausage Site is an isolated deposit that occurs on the southern Gag Plateau, west of AL90 Site (Faunal Zone C, middle Miocene) and Encore Site (Faunal Zone D, early late Miocene). The fauna is as yet poorly understood but the assemblage includes the bandicoot Bulungu palara and the pseudocheirid Pildra sp. 1, which are found in Faunal Zones A-C, a pseudocheirid species, found in Faunal Zones A-D, and Wanburoo hilarus, a Miocene macropodid only found in Faunal Zone C sites Travouillon et al., 2011). The presence of the latter (also found in AL90 Site) suggests a middle Miocene age for Rick's Sausage Site.
The earliest thylacomyid, Ischnodon australis (Stirton, 1955) from the Palankarinna LF, South Australia, is Pliocene in age. However, Westerman et al. (2012) estimated a late Oligocene molecular divergence date of ∼25.8 million years for the split between thylacomyids and peramelids. The presence of a thylacomyid in the Miocene of Riversleigh would not be inconsistent with this estimate. This is around 10 million years before the occurrence of L. dayi in the Riversleigh deposits. The absence of thylacomyids in earlier Faunal Zones of Riversleigh suggests that either thylacomyids first evolved elsewhere on the continent before colonizing the Riversleigh rainforest, or that earlier Riversleigh thylacomyids had not evolved their dental synapomorphies and were dentally indistinguishable from other peramelemorphians until the middle Miocene.

CONCLUSIONS
The oldest peramelid and thylacomyid are described from middle Miocene deposits in the Riversleigh World Heritage Area. Although both retain a number of plesiomorphies, they display a number of apomorphies linking them to crown-group peramele-morphians. The presence of the two new species presented in this paper is congruent with the most recent peramelemorphian molecular divergence times and suggest that peramelids and thylacomyids diversified in middle Miocene rainforests. ACKNOWLEDGMENTS Support for research at Riversleigh has come from the Australian Research Council (LP0989969, LP100200486, and DP1094569 grants to M. Archer, S. J. Hand, and K. H. Black at the University of New South Wales); XSTRATA Community Partnership Program (North Queensland); the University of New South Wales; P. Creaser and the CREATE Fund; the Queensland Parks and Wildlife Service; Environment Australia; the Queensland Museum; the Riversleigh Society Inc.; Outback at Isa; Mount Isa City Council; and private supporters, including K. and M. Pettit, E. Clark, M. Beavis, and M. Dickson. Assistance in the field has come from many hundreds of volunteers as well as staff and postgraduate students of the University of New South Wales. We thank R. Day for providing funding to the University of Queensland to create a postdoctoral position for K. J. Travouillon. We thank S. Ingleby and A. Divljan from the Australian Museum, H. Janetzki from the Queensland Museum, and C. Stevenson from the Western Australian Museum for providing access to modern bandicoot specimens. We thank the University of New South Wales Palaeosciences Lab and the University of Queensland Palaeo Hub for their support and anonymous reviewers for helpful comments.