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Bandicoots” (Peramelemorphia: Marsupialia) Based on Sequences for five Nuclear Genes

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Bandicoots” (Peramelemorphia: Marsupialia) Based on Sequences for five Nuclear Genes Available online at www.sciencedirect.com Molecular Phylogenetics and Evolution 47 (2008) 1–20 www.elsevier.com/locate/ympev A timescale and phylogeny for ‘‘Bandicoots” (Peramelemorphia: Marsupialia) based on sequences for five nuclear genes Robert W. Meredith a,*,1, Michael Westerman b,1, 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 Received 26 October 2006; revised 31 December 2007; accepted 4 January 2008 Available online 12 January 2008 Abstract Relationships among the living and recently extinct genera of bandicoots (Marsupialia: Peramelemorphia) have proven difficult to discern. Previous phylogenetic studies have used only morphology or mitochondrial DNA and have reported conflicting results in regards to their relationships. Most phylogenetic reconstructions recognize a basal split between the bilby Macrotis (Thylacomyidae) and the Peramelidae. The Peramelidae is composed of the Peramelinae (Isoodon and Perameles), Echymiperinae (Echymipera and Micr- operoryctes), and Peroryctinae (Peroryctes). Within Peramelidae, Echymipera and Microperoryctes usually group together to the exclu- sion of Peroryctes. This clade is sister to the Peramelinae. Placement of the recently extinct pig-footed bandicoot (Chaeropus: Chaeropodidae) has been ambiguous. We address the interrelationships and estimate times of divergence for the living bandicoot genera using a 6 kilobase concatenation consisting of protein-coding regions of five nuclear genes (ApoB, BRCA1, IRBP, Rag1, and vWF). We analyzed this concatenation using maximum parsimony, maximum likelihood, and Bayesian methods and estimated times of divergence using two Bayesian relaxed molecular clock methods. In all concatenated analyses, all nodes associated with the Peramelemorphia were robustly supported (bootstrap support percentages = 100; posterior probabilities = 1.00). Macrotis was recovered as basal to the remain- ing living bandicoots. Within the Peramelidae, Echymipera and Microperoryctes grouped to the exclusion of Peroryctes and this clade was sister to the Peramelinae. Only Rag1 amplified for Chaeropus; analyses based on this gene provide moderate support for an asso- ciation of Chaeropus plus Peramelidae to the exclusion of Macrotis. Both relaxed clock Bayesian methods suggest that the living ban- dicoots are a relatively recent radiation originating sometime in the late Oligocene or early Miocene with subsequent radiations in the late Miocene to early Pliocene. Ó 2008 Elsevier Inc. All rights reserved. Keywords: Marsupial; Bandicoot; Peramelemorphia; Phylogeny; Relaxed molecular clock; Bilby; Fossil 1. Introduction shared with all South American species and the Austral- asian carnivorous species; and they share the derived con- Taxonomic relationships of bandicoots (Order Peram- dition of having syndactylous hind feet (fusion of 2nd elemorphia) to other Australasian marsupials are poorly and 3rd pedal digits) with all Australasian Diprotodontia. understood. Bandicoots exhibit a mosaic of primitive and Furthermore, relationships within the order have proven derived characters. They are unique among marsupials in difficult to ascertain. having a complex allantoic placenta; they retain the plesio- Bensley (1903) argued for two distinct lineages of living morphic polyprotodont dentition, a condition that is bandicoots, one comprising the bilbies (Macrotis) and one comprising all other genera. This separation of bilbies from other living bandicoots has been supported by a number of * Corresponding authors. Fax: +1 909 787 4826. workers (see Archer and Kirsch, 1977; Westerman et al., E-mail addresses: [email protected] (R.W. Meredith), [email protected] (M.S. Springer). 1999). The bilbies (including the fossil form, Ischnodon 1 These authors contributed equally to this work. australis) have been accorded either familial or subfamilial 1055-7903/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2008.01.002 2 R.W. Meredith et al. / Molecular Phylogenetics and Evolution 47 (2008) 1–20 status (Thylacomyidae or Thylacomyinae). The six other of bandicoot taxa. Furthermore, only Kirsch et al. (1997) living bandicoot genera are usually grouped into one fam- and Westerman et al. (1999) have employed molecular dat- ily (Peramelidae) comprising three subfamilies—Perorycti- ing methods to infer the evolutionary history of bandicoots nae (Peroryctes), Echymiperinae (Echymipera, (Table 1). These studies employed fossil-calibrated molecu- Microperoryctes, and Rhynchomeles), and Peramelinae lar clocks to either DNA hybridization data (Kirsch et al., (Isoodon and Perameles). Peroryctines and echymiperines 1997) or mitochondrial 12S rRNA gene sequences (Wes- differ from peramelines in a number of derived cranial terman et al., 1999). On average, the mitochondrial point characters including a tube-like foramen rotundum and estimates of divergence time for the bandicoot subfamily are essentially forest-dwelling animals either limited to and family nodes were seven million years younger than New Guinea (Microperoryctes, Peroryctes, Rhynchomeles), the DNA hybridization estimates. or nearly so (Echymipera). Within this grouping, the Peror- Parametric (e.g., Thorne et al., 1998; Kishino et al., yctinae is regarded as being very divergent from the 2001) and semi-parametric (e.g., Sanderson, 2002) dating Echymiperinae (see Nowak and Dickman, 2005; Wilson methods are becoming increasingly common given that and Reeder, 2005). The peramelines are mainly an Austra- they allow for relaxation of the molecular clock and gener- lian group whose members share few, if any, derived char- ally perform better than strict molecular clock methods acter states. Indeed, Perameles is often considered to have (Yang and Rannala, 2006; Smith et al., 2006; Benton and the most plesiomorphic dentition of any modern Donoghue, 2007). Of considerable interest are reliable cal- bandicoot. ibration points. Benton and Donoghue (2007) suggest that There have been major difficulties in ascertaining the minimum constraints require (1) a fossil with well-sup- taxonomic relationships of the recently extinct pig-footed ported apomorphies of the given group; (2) a correct phy- bandicoot, Chaeropus ecaudatus. Few specimens of this logenetic tree; and a (3) well-dated fossil-bearing stratum. highly specialized, cursorial, semi-arid adapted herbivo- When these conditions are satisfied, the probability of a rous species were ever collected and few fossil remains have later divergence can be considered zero and the constraint been described. It has several unique derived characters can be treated as a ‘‘hard” bound (Benton and Donoghue, and Tate (1948) pointed out that Chaeropus was taxonom- 2007). When these conditions are not satisfied, ‘‘soft” ically remote from other genera. Groves and Flannery bounded constraints may be more appropriate. Maximum (1990) suggested that Chaeropus shares a number of constraints are much more controversial and difficult to derived character states with Macrotis that were often specify (Benton and Donoghue, 2007; Benton and Ayala, ignored or overlooked. For example, thylacomyids differ 2003; Hedges and Kumar, 2004; Reisz and Mu¨ller, 2004). from peramelines and peroryctines in that although they Reisz and Mu¨ller (2004) and Mu¨ller and Reisz (2005) sug- show four principal cusps, the metacone has shifted lin- gest phylogenetic bracketing. Benton and Donoghue (2007) gually and the two principal external cusps are relatively suggest a pluralistic approach that uses both ‘‘phylogenetic larger (see Rich, 1991). Chaeropus also has lingual metaco- bracketing” and considers ‘‘the absence of fossils from nids compared to other bandicoots (see Wright et al., 1991) underlying deposits” (p. 28). In addition, maximum and and ‘‘the cusps of the buccal tier [metacone and paracone] minimum constraints should be ‘‘fully substantiated” so and the crests associated with these, are major features of that any refinements in geological dates, the discovery of the tooth” (p. 232), suggesting that it may be related to new fossils, or changes in diagnostic apomorphies can be thylacomyids. incorporated into new analyses. Soft and hard bounded Westerman et al. (1999) summarized the molecular stud- analyses will recover similar estimates if the molecular data ies on bandicoot relationships. Molecular studies have con- and fossil constraints are not in ‘‘conflict” with one another sistently demonstrated a large difference between Macrotis (Yang and Rannala, 2006). Analyses employing soft (Thylacomyidae) and other bandicoots. They have also bounded constraints will out perform hard bounded analy- consistently demonstrated not only a large difference ses when poor constraints are used. Soft bounded con- between the Peramelinae (Isoodon + Perameles) and the mainly New Guinean Peroryctinae and Echymiperinae, but also that the Peroryctinae is very distinct from the Table 1 Echymiperinae. Previously estimated divergence dates in millions of years for the Peramelemorphia The mitochondrial DNA sequencing studies of Wes- terman et al. (1999) included sequences from a spirit-pre- DNA 12S rRNA hybridizationa Transversionsb served museum specimen of the extinct Chaeropus ecaudatus. This study favored Chaeropus as the sister taxon Node Peramelinae 12.36 1.75 to all other bandicoots but statistical tests failed to reject a Echymiperinae 10.51 5.26 Chaeropus + Macrotis
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