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A Phylogeny and Timescale for the Evolution of Pseudocheiridae (Marsupialia: Diprotodontia) in Australia and New Guinea

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A Phylogeny and Timescale for the Evolution of Pseudocheiridae (Marsupialia: Diprotodontia) in Australia and New Guinea J Mammal Evol DOI 10.1007/s10914-010-9129-7 ORIGINAL PAPER A Phylogeny and Timescale for the Evolution of Pseudocheiridae (Marsupialia: Diprotodontia) in Australia and New Guinea Robert W. Meredith & Miguel A. Mendoza & Karen K. Roberts & Michael Westerman & Mark S. Springer # The Author(s) 2010. This article is published with open access at Springerlink.com Abstract Pseudocheiridae (Marsupialia: Diprotodontia) is opsinae (Pseudochirops+Petropseudes), respectively, and a family of endemic Australasian arboreal folivores, more for an association of Pseudocheirinae and Hemibelidinae to commonly known as ringtail possums. Seventeen extant the exclusion of Pseudochiropsinae. Within Pseudochiropsinae, species are grouped into six genera (Pseudocheirus, Petropseudes grouped more closely with the New Guinean Pseudochirulus, Hemibelideus, Petauroides, Pseudochir- Pseudochirops spp. than with the Australian Pseudochirops ops, Petropseudes). Pseudochirops and Pseudochirulus are archeri, rendering Pseudochirops paraphyletic. New Guinean the only genera with representatives on New Guinea and species belonging to Pseudochirops are monophyletic, as are surrounding western islands. Here, we examine phyloge- New Guinean species belonging to Pseudochirulus. Molecular netic relationships among 13 of the 17 extant pseudocheirid dates and ancestral reconstructions of geographic provenance species based on protein-coding portions of the ApoB, combine to suggest that the ancestors of extant New Guinean BRCA1, ENAM, IRBP, Rag1, and vWF genes. Maximum Pseudochirops spp. and Pseudochirulus spp. dispersed from parsimony, maximum likelihood, and Bayesian methods Australia to New Guinea ∼12.1–6.5 Ma (Pseudochirops) and were used to estimate phylogenetic relationships. Two ∼6.0–2.4 Ma (Pseudochirulus). Ancestral state reconstructions different relaxed molecular clock methods were used to support the hypothesis that occupation of high elevations estimate divergence times. Bayesian and maximum parsi- (>3000 m) is a derived feature that evolved on the terminal mony methods were used to reconstruct ancestral character branch leading to Pseudochirops cupreus, and either evolved states for geographic provenance and maximum elevation in the ancestor of Pseudochirulus forbesi, Pseudochirulus occupied. We find robust support for the monophyly of mayeri, and Pseudochirulus caroli, with subsequent loss in P. Pseudocheirinae (Pseudochirulus+Pseudocheirus), Hemi- caroli, or evolved independently in P. mayeri and P. forbesi. belidinae (Hemibelideus + Petauroides), and Pseudochir- Divergence times within the New Guinean Pseudochirops clade are generally coincident with the uplift of the central cordillera and other highlands. Diversification within New Electronic supplementary material The online version of this article (doi:10.1007/s10914-010-9129-7) contains supplementary material, Guinean Pseudochirulus occurred in the Plio-Pleistocene after which is available to authorized users. the establishment of the Central Range and other highlands. : : R. W. Meredith M. A. Mendoza M. S. Springer (*) . Department of Biology, University of California, Keywords Marsupialia New Guinea Phylogenetic Riverside, CA 92521, USA bracketing . Pseudocheiridae . Relaxed molecular clocks . e-mail: [email protected] Stratigraphic bounding K. K. Roberts School of Biological, Earth and Environmental Sciences, University of New South Wales, Introduction Randwick, NSW 2031, Australia The marsupial family Pseudocheiridae (Marsupialia: Dipro- M. Westerman Department of Genetics, La Trobe University, todontia) includes six extant genera (Pseudochirulus, Bundoora, Victoria 3083, Australia Pseudocheirus, Pseudochirops, Petropseudes, Hemibeli- J Mammal Evol deus, Petauroides) and 16 to 17 (Nowak and Dickman South Australia, Victoria, and Queensland (Turnbull and 2005; Groves 2005) species commonly known as ringtail Lundelius 1970; Crosby et al. 2004). The fossil record of possums. With the exception of Petauroides, which has Gawinga is restricted to Riversleigh’s Faunal Zone B, which consistently been recognized as a genus, the other genera has been interpreted as early Miocene in age based on have variably been recognized as subgenera in Pseudochei- biocorrelation (Roberts et al. 2007). rus (e.g., Tate 1945). Pseudocheirids inhabit mainland The most comprehensive phylogenetic studies of Pseu- Australia, Tasmania, New Guinea, and islands (Japen, docheiridae are based on microcomplement fixation studies Salawatti) to the west of New Guinea, and commonly occur with albumin (Baverstock et al. 1990b), single-copy DNA- in montane rainforests. Four of the five Pseudochirops DNA hybridization data (Springer et al. 1992), craniodental species and five of the seven Pseudochirulus species are characters (Springer 1993), and concatenated nuclear gene found only in New Guinea (Flannery 1995b; Fig. 1). sequences (Meredith et al. 2009a). Baverstock et al. Ringtail possums are arboreal folivores. Adaptations to (1990b) treated all pseudocheirid species except for arboreality include forcipate hands, in which the first two Petauroides volans as members of the genus Pseudochei- digits are at least partly opposable to the latter three, and a rus, but their taxonomic sampling included representatives prehensile tail. Adaptations to folivory include selenodont of all pseudocheirid genera as currently recognized by Groves molars and an enlarged cecum that acts as a fermentation (2005). Baverstock et al.’s(1990b) microcomplement fixa- chamber. In addition to extant pseudocheirid genera, extinct tion analyses provided support for three primary lineages: pseudocheirids have been referred to five genera: Paljara, Pseudochirulus+Pseudocheirus, Hemibelideus+Petaur- Pildra, Marlu, Pseudokoala, and Gawinga (Woodburne et oides, and Pseudochirops+Petropseudes (Baverstock et al. al. 1987; Bassarova and Archer 1999; Roberts et al. 2007, 1990b). Neither the New Guinean Pseudochirops spp. nor 2008, 2009). Paljara, Pildra, and Marlu are known from Pseudochirulus spp., respectively, were recovered as mono- late Oligocene to early Miocene sediments in South phyletic (Baverstock et al. 1990b). DNA-DNA hybridization Australia and Oligo-Miocene deposits of the Riversleigh analyses included representatives of all pseudocheirid World Heritage Area in Queensland (Woodburne et al. genera (sensu Groves 2005) excepting Petropseudes, and 1987; Bassarova and Archer 1999; Roberts et al. 2007). provided additional support for Pseudochirulus+Pseudo- Pseudokoala is known from Plio-Pleistocene sediments in cheirus, Hemibelideus+Petauroides, and Pseudochirops 1000 m + + 3000 m + 1000 m + + + + + + + + + ++ + + + Pseudochirops cupreus + + + + + + + + Pseudochirops albertisii + + + Pseudochirops corinnae + Pseudochirops coronatus + Pseudochirulus forbesi + Pseudochirulus mayeri +++ Pseudochirulus canescens Pseudochirulus caroli ++ ++ Pseudochirulus schlegeli + + + Fig. 1 Distribution of collecting localities for New Guinean pseudocheirids (Flannery 1995a, b) plotted on a generalized topographic map (modified from Flannery 1995b). J Mammal Evol (Springer et al. 1992; Kirsch et al. 1997). Cladistic analyses and New Guinean mammal faunas via waif dispersal of craniodental characters are generally in agreement with subsequent to the vicariant sundering of Australia and microcomplement fixation and DNA-DNA hybridization New Guinea. Tropical rainforest pseudocheirids are “ex- results and supported a sister group relationship between tremely poor dispersers” (Flannery 1995a) as a conse- Petropseudes and representative species of Pseudochirops,a quence of their largely or strictly arboreal lifestyle (Pahl et sister group relationship between Hemibelideus and Petaur- al. 1988; Laurance 1990; Laurance and Laurance 1999), oides (Springer 1993), and an association of Pseudocheirus and are therefore among the least probable candidates for with Pseudochirulus (Springer 1993). None of the cladistic waif dispersal. Australia and New Guinea remained isolated analyses of craniodental characters recovered the New from each other until the Pleistocene (Dow 1977), when Guinean Pseudochirops spp. as monophyletic (Springer eustatic lowering of sea level allowed for interchange 1993). Groves (2005), following Kirsch et al. (1997), between the Australian and New Guinean mammal faunas divided Pseudocheiridae into the subfamilies Pseudochirop- (Flannery 1988). sinae (Pseudochirops), Hemibelidinae (Hemibelideus+ If Flannery’s(1988) hypothesis is correct, we should Petauroides), and Pseudocheirinae (Pseudocheirus+Pseu- expect to find two sets of divergences dates between dochirulus+Petropseudes), although it should be noted that Australian and New Guinean taxa: (1) divergence dates whereas Groves included Petropseudes in Pseudocheirinae, that predate the Miocene and reflect the vicariant separation the taxonomic affinities of Petropseudes were not explicitly of Australia and New Guinea, and (2) divergence dates addressed in Kirsch et al.’s(1997) classification. Analyses from the latest Pliocene/Pleistocene that reflect resurgent based on concatenated nuclear DNA sequences (Meredith et land connections that developed at this time in conjunction al. 2009a) are in general agreement with microcomplement with eustatic lowering of sea level. Flannery’s(1988) fixation (Baverstock et al. 1990a, b), DNA-DNA hybrid- hypothesis was subsequently tested by Aplin et al. (1993) ization (Springer et al. 1992; Kirsch et al. 1997), and with microcomplement fixation data, and Kirsch and craniodental
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