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A Phylogeny of Diprotodontia (Marsupialia) Based on Sequences for five Nuclear Genes

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A Phylogeny of Diprotodontia (Marsupialia) Based on Sequences for five Nuclear Genes Molecular Phylogenetics and Evolution 51 (2009) 554–571 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev A phylogeny of Diprotodontia (Marsupialia) based on sequences for five nuclear genes Robert W. Meredith a,*, Michael Westerman b, Mark S. Springer a,* a Department of Biology, University of California, 900 University Avenue, Riverside, CA 92521, USA b Department of Genetics, La Trobe University, Bundoora, Vic. 3083, Australia article info abstract Article history: Even though the marsupial order Diprotodontia is one of the most heavily studied groups of Australasian Received 22 September 2008 marsupials, phylogenetic relationships within this group remain contentious. The more than 125 living Revised 19 January 2009 species of Diprotodontia can be divided into two main groups: Vombatiformes (wombats and koalas) Accepted 16 February 2009 and Phalangerida. Phalangerida is composed of the kangaroos (Macropodidae, Potoroidae, and Hyp- Available online 26 February 2009 siprymnodontidae) and possums (Phalangeridae, Burramyidae, Petauridae, Pseudocheiridae, Tarsipedi- dae, and Acrobatidae). Much of the debate has focused on relationships among the families of possums Keywords: and whether possums are monophyletic or paraphyletic. A limitation of previous investigations is that Marsupial no study to date has investigated diprotodontian relationships using all genera. Here, we examine dipro- Diprotodontia Fossil todontian interrelationships using a nuclear multigene molecular data set representing all recognized Phylogeny extant diprotodontian genera. Maximum parsimony, maximum likelihood, and Bayesian methods were Relaxed molecular clock used to analyze sequence data obtained from protein-coding portions of ApoB, BRCA1, IRBP, Rag1, and Ancestral state reconstructions vWF. We also applied a Bayesian relaxed molecular clock method to estimate times of divergence. Diprot- odontia was rooted between Vombatiformes and Phalangerida. Within Phalangerida, the model-based methods strongly support possum paraphyly with Phalangeroidea (Burramyidae + Phalangeridae) group- ing with the kangaroos (Macropodiformes) to the exclusion of Petauroidea (Tarsipedidae, Acrobatidae, Pseudocheiridae, and Petauridae). Within Petauroidea, Tarsipedidae grouped with both Petauridae and Pseudocheiridae to the exclusion of Acrobatidae. Our analyses also suggest that the diprotodontian gen- era Pseudochirops and Strigocuscus are paraphyletic and diphyletic, respectively, as currently recognized. Dating analyses suggest Diprotodontia diverged from other australidelphians in the late Paleocene to early Eocene with all interfamilial divergences occurring prior to the early Miocene except for the split between the Potoroidae and Macropodidae, which occurred sometime in the mid-Miocene. Ancestral state reconstructions using a Bayesian method suggest that the patagium evolved independently in the Acrobatidae, Petauridae, and Pseudocheiridae. Ancestral state reconstructions of ecological venue suggest that the ancestor of Diprotodontia was arboreal. Within Diprotodontia, the common ancestor of Macro- podidae was reconstructed as terrestrial, suggesting that tree kangaroos (Dendrolagus) are secondarily arboreal. Ó 2009 Elsevier Inc. All rights reserved. 1. Introduction oleonids, commonly known as marsupial lions, and herbivorous diprotodontids, among which are the largest known marsupials Of the seven extant marsupial orders, Diprotodontia is the larg- from any time period (Long et al., 2002). est and most ecologically diverse. More than 125 living diproto- The name Diprotodontia was coined by Owen in 1866 for Aus- dontian species are currently recognized. Most diprotodontians tralian diprotodont marsupials (Aplin and Archer, 1987). Dip- are herbivorous, but there are also forms specialized for nectari- rotodonty, a state in which the lower medial incisors are vory, folivory, and insect-omnivory (Aplin and Archer, 1987). Loco- enlarged and procumbent, occurs in all diprotodontians and is motory specializations include arboreality, bipedal locomotion, widely considered a diagnostic morphological synapomorphy for fossoriality, and gliding. When fossil taxa are considered, Diprot- the group (Kirsch, 1977; Aplin and Archer, 1987). A superficial cer- odontia is even more diverse and includes the carnivorous thylac- vical thymus gland has also been reported as a diagnostic diproto- dontian character by Yadav (1973), who examined 51 diprotodontian taxa, including representatives of all diprotodon- * Corresponding authors. Fax: +1 909 787 4826. tian families (sensu Wilson and Reeder, 2005) except for Hyp- E-mail addresses: [email protected] (R.W. Meredith), mark. [email protected] (M.S. Springer). siprymnodontidae, and found that this feature was present in all 1055-7903/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2009.02.009 R.W. Meredith et al. / Molecular Phylogenetics and Evolution 51 (2009) 554–571 555 diprotodontians but not in other marsupials. However, Yadav iformes. As a result, Phalangeriformes consisted of only the Aus- (1973) did not include Dromiciops gliroides in his study. The pres- tralasian possums. Within Phalangeriformes, Kirsch et al. (1997) ence or absence of the superficial cervical thymus in D. gliroides grouped Burramyidae and Phalangeridae in Superfamily Phalange- is of special interest given Kirsch et al.’s (1991) hypothesis that roidea and the remaining Australasian possums (Pseudocheiridae, D. gliroides and Diprotodontia are sister taxa. A Diprotodon- Petauridae, Acrobatidae, Tarsipedidae) in Superfamily Petauroidea. tia + Dromiciops clade was also suggested by Drummond et al. Wilson and Reeder (2005) provide one of the most recent marsu- (2006). More recently, Haynes (2001) found evidence for a deep pial classifications and recognize the three suborders of Kirsch cervical thymus in two species of Isoodon and suggested that ban- et al. (1997). Kear and Cooke (2001) and Wilson and Reeder dicoots may be intermediate between other polyprotodont marsu- (2005) also recognize Macropodidae, Potoroidae, and Hyp- pials and Diprotodontia. The presence of the fasciculus aberrans, siprymnodontidae as distinct families within Macropodiformes. which connects the cerebral hemispheres, has also been suggested Resolving higher-level relationships within Diprotodontia has as a diagnostic diprotodontian character (Abbie, 1937). The fascic- proved difficult. Aplin and Archer (1987), Flannery (1987), and ulus aberrans occurs in all diprotodontians that were investigated Springer and Woodburne (1989) found morphological support by Abbie (1937), who as noted by Aplin and Archer (1987), even for a Macropodiformes + Phalangeriformes (sensu Kirsch et al., coined the name Duplicicommissurala to replace Diprotodontia 1997) clade. Horovitz and Sánchez-Villagra (2003) recovered a sis- based on this putative diagnostic character. However, there remain ter group relationship between Vombatiformes and Macropodifor- important gaps in taxonomic sampling for this character including mes (sensu Kirsch et al., 1997) with this collective group nested Tarsipes and burramyids (Aplin and Archer, 1987; Luckett, 1994). inside of a paraphyletic Phalangeriformes. Nilsson et al. (2004), The intermediate placement of bandicoots between polyprotodont Asher et al. (2004), and Beck et al. (2008) also found support for and diprotodontian marsupials has also been suggested based on a Vombatiformes + Macropodiformes clade. In contrast, Szalay the presence of the syndactylous condition exhibited by both and Sargis (2006), Weisbecker and Sánchez-Villagra (2006), and Diprotodontia and Peramelemorphia (= Syndactyla) (e.g. Jones, Weisbecker and Archer (2008) suggest that this association is spu- 1923; Szalay, 1994; Weisbecker and Nilsson, 2008). However, Syn- rious and results from convergent/parallel changes associated dactyla has been rejected in almost all recent molecular, morpho- with the terrestrial plantigrade locomotion exhibited by both logical, and combined analyses although Szalay and Sargis (2001, groups. Single-copy DNA–DNA hybridization studies (e.g. Springer 2006) still favor this grouping. and Kirsch, 1991; Springer et al., 1997; Kirsch et al., 1997) pro- Even with only a few diagnostic morphological characters that vided some support for the monophyly of Phalangeriformes, but occur broadly across Diprotodontia, morphological cladistic stud- were unable to resolve relationships between Phalangeriformes, ies almost always recover this order as monophyletic (e.g. Archer, Macropodiformes, and Vombatiformes. Analyses of mitochondrial 1984; Aplin and Archer, 1987; Luckett, 1994; Marshall et al., 1990; rRNA gene sequences (Kavanagh et al., 2004) consistently failed to Springer et al., 1997; Horovitz and Sánchez-Villagra, 2003). Molec- recover Phalangeriformes. Osborne et al.’s (2002) analysis of mito- ular studies are in solid agreement with morphology in supporting chondrial ND2 and ND2 + 12S rRNA gene sequences returned diprotodontian monophyly (Baverstock, 1984; Baverstock et al., inconclusive results for both Phalangeriformes and Phalangerifor- 1987, 1990; Springer and Kirsch, 1991; Kirsch et al., 1997; Colgan, mes + Macropodiformes. Nilsson et al. (2004) analyzed sequences 1999; Amrine-Madsen et al., 2003; Baker et al., 2004; Kavanagh from complete mitochondrial genomes and obtained strong sup- et al., 2004; Nilsson et al., 2004; Munemasa et al., 2006; Phillips port
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