Maria A. Nilsson*, Gennady Churakov, Mirjam Sommer,Ngoc Van Tran, Anja Zemann, Jürgen Brosius, Jürgen Schmitz*
Institute of Experimental Pathology (ZMBE), University of Münster, Münster, Germany
Abstract
The Australasian and South American marsupial mammals, such as kangaroos and opossums, are the closest living relatives to placental mammals, having shared a common ancestor around 130 million years ago. The evolutionary relationships among the seven marsupial orders have, however, so far eluded resolution. In particular, the relationships between the four Australasian and three South American marsupial orders have been intensively debated since the South American order Microbiotheria was taxonomically moved into the group Australidelphia. Australidelphia is significantly supported by both molecular and morphological data and comprises the four Australasian marsupial orders and the South American order Microbiotheria, indicating a complex, ancient, biogeographic history of marsupials. However, the exact phylogenetic position of Microbiotheria within Australidelphia has yet to be resolved using either sequence or morphological data analysis. Here, we provide evidence from newly established and virtually homoplasy-free retroposon insertion markers for the basal relationships among marsupial orders. Fifty-three phylogenetically informative markers were retrieved after in silico and experimental screening of ~217,000 retroposon-containing loci from opossum and kangaroo. The four Australasian orders share a single origin with Microbiotheria as their closest sister group, supporting a clear divergence between South American and Australasian marsupials. In addition, the new data place the South American opossums (Didelphimorphia) as the first branch of the marsupial tree. The exhaustive computational and experimental evidence provides important insight into the evolution of retroposable elements in the marsupial genome. Placing the retroposon insertion pattern in a paleobiogeographic context indicates a single marsupial migration from South America to Australia. The now firmly established phylogeny can be used to determine the direction of genomic changes and morphological transitions within marsupials.
Author Summary
Ever since the first Europeans reached the Australian shores and were fascinated by the curious marsupials they found, the evolutionary relationships between the living Australian and South American marsupial orders have been intensively investigated. However, neither the morphological nor the more recent molecular methods produced an evolutionary consensus. Most problematic of the seven marsupial groups is the South American species Dromiciops gliroides, the only survivor of the order Microbiotheria. Several studies suggest that Dromiciops, although living in South America, is more closely related to Australian than to South American marsupials. This relationship would have required a complex migration scenario whereby several groups of ancestral South American marsupials migrated across Antarctica to Australia. We screened the genomes of the South American opossum and the Australian tammar wallaby for retroposons, unambiguous phylogenetic markers that occupy more than half of the marsupial genome. From analyses of nearly 217,000 retroposon-containing loci, we identified 53 retroposons that resolve most branches of the marsupial evolutionary tree. Dromiciops is clearly only distantly related to Australian marsupials, supporting a single Gondwanan migration of marsupials from South America to Australia. The new phylogeny offers a novel perspective in understanding the morphological and molecular transitions between the South American and Australian marsupials.
Citation: Nilsson MA, Churakov G, Sommer M, Tran NV, Zemann A, et al. (2010) Tracking Marsupial Evolution Using Archaic Genomic Retroposon Insertions. PLoS Biol 8(7): e1000436. doi:10.1371/journal.pbio.1000436
Academic Editor: David Penny, Massey University, New Zealand
Received: January 28, 2010; Accepted: June 15, 2010; Published: July 27, 2010
Copyright: © 2010 Nilsson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by a Swedish Research Council post doc grant to MN (2007-1053), the Deutsche Forschungsgemeinschaft (DFG, SCHM 1469/3 and NI 1284/1), and the Conservation, Research and Education Opportunities (CREO), Seattle, USA. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
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