1 Frédéric Delsuc,* Mark Scally,†Fl Ole Madsen,§ Michael J. Stanhope,†|| Wilfried W. De Jong,§¶ François M. Catzeflis
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MOLECULAR PHYLOGENY OF LIVING XENARTHRANS AND THE IMPACT OF CHARACTER AND TAXON SAMPLING ON THE PLACENTAL TREE ROOTING. Frédéric Delsuc,* Mark Scally,fl Ole Madsen,§ Michael J. Stanhope, Wilfried W. de Jong,§$ Fran%ois M. Catzeflis,* Mark S. Springer,fl and Emmanuel J. P. Douzery* *La,oratoire de Paléontologie, Paléo,iologie et Phylogénie, Institut des Sciences de l.Evolution, 0niversité Montpellier II, Montpellier, France 1ueen.s 0niversity of 2elfast, 2iology and 2iochemistry, 37 Lis,urn Road, 2elfast, 2T3 72L, 0nited 7ingdom flDepartment of 2iology, 0niversity of California, Riverside, California 32521, 0SA §Department of 2iochemistry, 0niversity of Nijmegen, PO 2ox 3101, 6500 H2 Nijmegen, The Netherlands 2ioinformatics, AlaxoSmith7line, 1250 South Collegeville Road, 0P13C5, Collegeville Pennsylvania 13C26, 0SA $Institute for 2iodiversity and Ecosystems Dynamics, 0niversity of Amsterdam, The Netherlands Author for correspondence and reprintsD Emmanuel J. P. Douzery La,oratoire de Paléontologie, Paléo,iologie et Phylogénie E CC06C Institut des Sciences de l.Evolution 0MR 555C / CNRS, 0niversité Montpellier II Place EugGne 2ataillon, 3C 035 MONTPELLIER Cedex 05 E France Tel.D 33 C 67 1C C8 63 / FAID 33 C 67 1C 36 10 E-mailD douzeryKisem.univ-montp2.fr Running titleD Molecular phylogeny of living xenarthrans 1 ABSTRACT Extant xenarthrans Larmadillos, anteaters and slothsM are among the most derived placental mammals ever evolved. South America Nas the cradle of their evolutionary history. During the Tertiary, xenarthrans experienced an extraordinary radiation Nhile South America remained isolated from other continents. The 13 living genera are relicts of this earlier diversification and represent one of the four major clades of placental mammals. SeOuences of the three independent protein-coding nuclear markers α22 adrenergic receptor LADRA22M, ,reast cancer suscepti,ility L2RCA1M, and von Wille,rand Factor LPWFM Nere determined for 12 of the 13 living xenarthran genera. Comparative evolutionary dynamics of these nuclear exons using a likelihood frameNork revealed contrasting patterns of molecular evolution. All codon positions of 2RCA1 Nere shoNn to evolve in a strikingly similar manner, and third codon positions appeared less saturated Nithin placentals than those of ADRA22 and PWF. Maximum likelihood and 2ayesian phylogenetic analyses of a C7 placental data set rooted ,y three marsupial outgroups resolved the phylogeny of Ienarthra Nith some evidence for tNo radiation events in armadillos and provided a strongly supported picture of placental interordinal relationships. This topology Nas fully compati,le Nith recent studies dividing placentals into the Southern Hemisphere clades Afrotheria and Ienarthra and a monophyletic Northern Hemisphere clade L2oreoeutheriaM composed of Laurasiatheria and Euarchontoglires. Partitioned likelihood statistical tests of the position of the root, under different character partition schemes, identified three almost eOually likely hypotheses for early placental divergencesD a ,asal Afrotheria, an Afrotheria Q Ienarthra clade or a ,asal Ienarthra LEpitheria hypothesisM. We took advantage of the extensive sampling realized Nithin Ienarthra to assess its impact on the location of the root on the placental tree. 2y resampling taxa Nithin Ienarthra, the conservative Shimodaira-HasegaNa likelihood ,ased test of alternative topologies Nas shoNn to ,e sensitive to ,oth character and taxon sampling. 2 7eyNordsD Ienarthran phylogeny E Taxon and character sampling E Placentals E Evolutionary dynamics E Nuclear markers E Maximum Likelihood and 2ayesian phylogenetics. 3 INTRODUCTION Living xenarthrans are represented ,y three morphologically distinct lineagesD armored armadillos, toothless anteaters, and phyllophagous tree-sloths. The 30 living species of the order Ienarthra LWetzel 1385R PizcaSno 1335M are relics of an impressive South-American Tertiary radiation that gave ,irth to giant extinct forms like glyptodonts and ground-dNelling sloths LPatterson and Pascual 1372M. The monophyly of the order is strongly supported ,y numerous morphological LEngelmann 1385R Patterson, Segall, and Turn,ull 1383R Patterson et al. 1332R Rose and Emry 1333R Aaudin 1333M and molecular Lde Jong et al. 1385R van Dijk et al. 1333R Delsuc et al. 2001M synapomorphies. Morphological LEngelmann 1385R Patterson et al. 1332M and molecular LDelsuc et al. 2001R Madsen et al. 2001R Murphy et al. 2001aM studies unam,iguously supported the division of Ienarthra into tNo su,ordersD Cingulata represented ,y armadillos LDasypodidaeM, and Pilosa represented ,y anteaters LPermilinguaD MyrmecophagidaeM plus sloths LFolivoraD Megalonychidae and 2radypodidaeM. HoNever, Nhereas the phylogeny of living pilosans is Nell resolved LAaudin and 2ranham 1338R Delsuc et al. 2001R AreenNood et al. 2001M, this is not the case for cingulates. Armadillos are the most diversified xenarthrans and comprise 21 extant species classified in eight genera LWetzel 1385R PizcaSno 1335M. This ecologically and morphologically diverse group contains enigmatic taxa like the dNarf su,terranean pink-fairy armadillos Lgenus ChlamyphorusM and the endangered giant armadillo LPriodontes maximusM. Some striking adaptations can ,e found in armadillos. Three-,anded armadillos LTolypeutesM developed a uniOue anti-predator strategy ,y entirely rolling up into a ,all, and nine-,anded armadillos LDasypusM are the only verte,rates to reproduce ,y o,ligate monozygotic polyem,ryony LLoughry et al. 1338M. NotNithstanding these fascinating peculiarities, phylogenetic studies on armadillos are still scarce LAuth 1361R Engelmann 1385R Patterson, Segall, and Turn,ull 1383R Cetica et al. 1338R Delsuc et al. 2001M and relationships among the eight living genera remain unclear. C Solving the phylogenetic position of the order Ienarthra Nithin Mammalia is of primary importance to understand the morphological and ,iogeographical processes that shaped the early stages of placental evolution. Indeed, despite their highly specialized morphology, xenarthrans retain anatomical and physiological characters thought to ,e primitive for placental mammals LMc7enna 1375M. This composite morphology, mixing ancestral and derived characters, has made the orderTs position Nithin placentals very difficult to assess LEngelmann 1385R Aaudin et al. 1336M. 2ased on the retention of numerous UarchaicU features, morphologists LAregory 1310R Mc7enna 1375R Novacek 1332R Shoshani and Mc7enna 1338M have long proposed that Ienarthra represents the sister-group to all other eutherians there,y named Epitheria. HoNever, morphological synapomorphies defining epitherians are Neak and their phylogenetic distri,ution is eOuivocal LAaudin et al. 1336M. Early studies of complete mitochondrial genomes did not support a ,asal position for Ienarthra LArnason, Aull,erg, and Janke 1337M. More recent analysesVincluding a larger taxon samplingVsuggested a sister-group relationship ,etNeen the nine-,anded armadillo LDasypus novemcinctusM and representatives of the African clade LWaddell et al. 1333R Cao et al. 2000R Mouchaty et al. 2000aM. HoNever, complete mitochondrial genome analyses appear to ,e affected ,y insufficient taxon samplingVespecially Nithin IenarthraVlikely responsi,le for long-,ranch attraction and rooting artifacts LWaddell et al. 1333M, and suffer from saturation in the deepest parts of the tree LCao et al. 2000R Springer et al. 2001M. 2y contrast tNo recent independent analyses ,ased on the large concatenation of mainly nuclear genes for a ,road taxon sampling of eutherian mammals have shoNn that the order Ienarthra on its oNn represents one of the major clades of placentals LMadsen et al. 2001R Murphy et al. 2001a, ,M. These studies provided convincing evidence for an arrangement of placental orders into four major cladesD IM Afrotheria, IIM Ienarthra, IIIM Euarchontoglires and IPM Laurasiatheria, emphasizing the crucial influence of tectonic events in their early differentiation. A close relationship ,etNeen the Northern Hemisphere clades III and IP has ,een proposed Li. e. 5 U2oreoeutheriaU R Springer and de Jong 2001M Nith either Afrotheria or Ienarthra as the most ,asal clade, suggesting a Southern Hemisphere origin for eutherian mammals LEizirik, Murphy, and OT2rien 2001R Madsen et al. 2001M. In fact, the relationships ,etNeen these four clades directly depend on the unsta,le position of the root. Recent application of the 2ayesian approach LYang and Rannala 1337R Huelsen,eck et al. 2001M to this pro,lem using a large character sampling supported a ,asal position of Afrotheria LMurphy et al. 2001,M. HoNever, in this study, Ienarthra suffers from poor taxonomic representation Lonly three taxaM relative to the other three major clades that include eight LAfrotheriaM, 11 LEuarchontogliresM, and 20 LLaurasiatheriaM taxa. Here Ne present a study including the ,roadest taxonomic representation so far considered in a molecular approach to xenarthran phylogeny. We constructed a supermatrix of C7 placental taxa and three marsupial outgroups, including 12 of the 13 living xenarthran genera, for three genetically independent protein-coding nuclear genesD α22 Adrenergic receptor LADRA22M, 2reast Cancer Suscepti,ility exon 11 L2RCA1M, and von Wille,rand Factor exon 28 LPWFM representing a total of 5130 aligned nucleotide sites. Choice of these nuclear markers Nas guided ,y their Nide use for inferring the phylogeny of placental mammals LSpringer et al. 1337R Stanhope et al. 1338a, ,R Madsen et al. 2001M and their resolving