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An Emerging Consensus in the Evolution, Phylogeny, And An emerging consensus in the evolution, phylogeny, and systematics of marsupials and their fossil relatives (Metatheria) Eldridge, MDB, Beck, RMD, Croft, DA, Travouillon, KJ and Fox, BJ http://dx.doi.org/10.1093/jmammal/gyz018 Title An emerging consensus in the evolution, phylogeny, and systematics of marsupials and their fossil relatives (Metatheria) Authors Eldridge, MDB, Beck, RMD, Croft, DA, Travouillon, KJ and Fox, BJ Type Article URL This version is available at: http://usir.salford.ac.uk/id/eprint/51430/ Published Date 2019 USIR is a digital collection of the research output of the University of Salford. Where copyright permits, full text material held in the repository is made freely available online and can be read, downloaded and copied for non-commercial private study or research purposes. Please check the manuscript for any further copyright restrictions. For more information, including our policy and submission procedure, please contact the Repository Team at: [email protected]. An emerging consensus in the evolution, phylogeny and systematics of marsupials and their fossil relatives (Metatheria) Invited review for the Centenary of the American Society of Mammologists to be published in Journal of Mammalogy in 2019 Mark D.B. Eldridge1, Robin M.D. Beck2, Darin A. Croft3, Kenny J. Travouillon4, Barry J. Fox5 1 Australian Museum Research Institute, Australian Museum, 1 William Street, Sydney, New South Wales 2010, Australia. 61 2 9320 6320 [email protected] 2 School of Environment and Life Sciences, University of Salford, Manchester M5 4WT, United Kingdom 44 161 295 4994 [email protected] 3 School of Medicine, Case Western Reserve University, Cleveland, Ohio, USA. 1-216-368- 5268 [email protected] 4 Western Australian Museum, Locked Bag 49, Welshpool DC, WA, 6986 Australia. E-mail: [email protected] 5 School of Biological, Earth and Environmental, University of New South Wales, Sydney, New South Wales 2052, Australia. 61 2 49449710 [email protected] 1 ABSTRACT Marsupials and their fossil relatives, which collectively comprise the Metatheria, have been of scientific interest for centuries, with many aspects of their evolution and systematics subject to intense research and debate. Here we review progress over the last 25 years, which has included the description of many new species (modern and fossil), and major improvements in understanding of their phylogenetic relationships, as well as the overall evolutionary history and biogeography of Marsupialia (crown-clade) and Metatheria (total- clade). Significant advances have included the deployment of increasingly sophisticated molecular, morphological and total evidence analyses, which have resolved most previously disputed relationships amongst and within the modern marsupial orders. A broad systematic consensus is now emerging, although several major areas of contention remain, particularly among fossil metatherians. New modern species continue to be described at an impressive rate, with almost 50 named in last 25 years, and many more await discovery. There has also been an explosion in the discovery and description of fossil marsupials and non-marsupial metatherians (~270 species), principally from Australasia and the Americas but also from Antarctica, Europe and Asia. Most are represented by dental specimens only, but some consist of complete and well-preserved material, which has led to major improvements in our understanding of the evolution of cranial and postcranial morphology. Improvements in the fossil record and advances in methods for inferring divergence times have helped clarify when and where key events occurred in metatherian evolution and the patterns of subclade diversification. We also have improved understanding of biogeographical relationships among metatherians on different landmasses. Despite enormous progress, numerous key uncertainties remain due to major gaps in the fossil record (e.g. Antarctica, late Cretaceous and early Paleogene of Australia) and a comparative lack of studies that directly combine 2 molecular and fossil data. Future advances will largely depend on improvements in the fossil record and studies that better integrate neontological and palaeontological evidence. 3 INTRODUCTION Although the marsupials (crown-clade metatherians) represent a much smaller radiation than their placental (crown-clade eutherian) counterparts, they have fascinated Western science ever since their discovery in the 16th and 17th Centuries (Tyndale-Biscoe 2005). This is due to a variety of factors, including their ancient evolutionary divergence, their current almost exclusively Gondwanan distribution, their distinctively specialized reproductive biology, and the many examples of convergent evolution between them and placentals (Weisbecker and Beck 2015). Although modern marsupials are confined to the Americas and Australasia, metatherian fossils are known from every continent (Beck in press). Metatherians diverged from eutherians at least 125 million years ago, and perhaps 160 million years ago or earlier (Luo et al. 2011; Bi et al. 2018). Metatherians appear to have been confined to Laurasia until at least the latest Cretaceous, before dispersing into Gondwana, presumably from North America to South America (Case et al. 2005; Beck 2017a). Gondwanan metatherians, including crown-clade marsupials, diversified enormously over the course of the Cenozoic (Long et al. 2002; Goin et al. 2016), in contrast to the far more limited diversity observed in Laurasian (non-marsupial) metatherians that survived the K-Pg mass extinction (Crochet 1980; Korth 2008; Bennett et al. 2018b). Today, marsupials are more diverse in Australasia (Australia, New Guinea and Wallacea) than they are in the Americas, with four orders, 18 families, and >248 species in the former region compared to three orders, three families, and >111 species in the latter (Wilson and Mittermeier 2015) (Table 1). In the Americas, most diversity is found in South and Central America; only a single species (Didelphis virginiana) occurs north of Mexico (Wilson and Mittermeier 2015), the result of a recent (<1 Ma) dispersal event (Woodburne 2010). Although the fossil record is far from complete, both Australasia and South America once hosted a far more extensive marsupial fauna (Long et al. 2002; Goin et al. 2016) (Table 1). 4 Since their discovery by Western science, much debate and controversy has surrounded systematics, taxonomy, and evolution of marsupials, with many different techniques employed to unravel their relationships including anatomy (cranial, dental and postcranial osteology, as well as soft tissue morphology), chromosomes, proteins, and DNA (Tyndale- Biscoe 2005). A revolution during recent decades in genetic/genomic methods and computing power has seen many increasingly large and sophisticated molecular studies examining relationships within modern marsupials. These studies have progressed from examining single genes (e.g. Retief et al. 1995; Jansa and Voss 2000), to 5-10 genes (e.g. Meredith et al. 2009b; Potter et al. 2012), to whole mitochondrial genomes (Phillips et al. 2001; Nilsson et al. 2003), and now partial nuclear genomes comprising thousands of loci (Duchêne et al. 2018; Nilsson et al. 2018). Whole nuclear genome sequences of marsupials are now also beginning to accumulate (Mikkelsen et al. 2007; Renfree et al. 2011; Murchison et al. 2012; Feigin et al. 2017; Johnson et al. 2018). The greater information content and power of these analyses, as well as improved taxon sampling, have transformed our understanding of modern marsupial relationships; a consensus is now emerging, with higher order systematics beginning to stabilize. In addition, these molecular techniques have proved instrumental in the recognition of additional, often morphologically cryptic, species (e.g. Baker et al. 2014; Potter et al. 2014). As well as revolutionary developments in molecular techniques, there have been major advances in our knowledge of the morphology of marsupials and other metatherians, and in phylogenetic analyses that incorporate morphological data. This is partly the result of dramatic improvements in the fossil record of marsupials and other metatherians in recent years. These have included the discovery of numerous new taxa (see below), some of them known from extremely well-preserved remains, in a few cases even including ontogenetic 5 series (Marshall et al. 1995; Sánchez-Villagra et al. 2007; Black et al. 2010; Ladevèze et al. 2011; Black et al. 2012c; Travouillon et al. 2015b; Maga and Beck 2017). The increasing use of screen-washing techniques has greatly improved the recovery of more fragmentary fossils, particularly isolated teeth and partial jaws (Goin et al. 2010). However, numerous major gaps remain in the metatherian fossil record, and most taxa are known only from dental remains. Particularly frustrating is the near total lack of Australian fossil sites preserving mammals from the early Paleogene, as this is the period during which the Australian marsupial radiation probably began to diverge (Meredith et al. 2011; Mitchell et al. 2014; Duchêne et al. 2018). Currently, only the early Eocene Tingamarra Local Fauna is known from this period in Australia (Godthelp et al. 1999; Long et al. 2002; Beck et al. 2008b). Our knowledge of the comparative morphology (particularly the skull and postcranial skeleton) of modern marsupials has improved thanks to monographs, taxonomic studies, and new phylogenetic analyses incorporating morphological
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