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Systematic Biology This article was downloaded by:[University of California Riverside] On: 27 September 2007 Access Details: [subscription number 768495051] Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Systematic Biology Publication details, including instructions for authors and subscription information: http://www.informaworld.com/smpp/title~content=t713658732 The Adequacy of Morphology for Reconstructing the Early History of Placental Mammals Mark S. Springer a; Angela Burk-Herrick a; Robert Meredith a; Eduardo Eizirik b; Emma Teeling c; Stephen J. O'Brien d; William J. Murphy e a Department of Biology, University of California, Riverside, Riverside, CA, USA b Faculdade de Biociencias, PUCRS, Porto Allegre, RS, Brazil c School of Biological and Environmental Sciences, University College Dublin Belfield, Dublin, Ireland d Laboratory of Genomic Diversity, National Cancer Institute-Frederick, Frederick, MD, USA e Department of Veterinary Integrative Biosciences, Texas A&M University, College Station, TX, USA First Published on: 01 August 2007 To cite this Article: Springer, Mark S., Burk-Herrick, Angela, Meredith, Robert, Eizirik, Eduardo, Teeling, Emma, O'Brien, Stephen J. and Murphy, William J. (2007) 'The Adequacy of Morphology for Reconstructing the Early History of Placental Mammals', Systematic Biology, 56:4, 673 - 684 To link to this article: DOI: 10.1080/10635150701491149 URL: http://dx.doi.org/10.1080/10635150701491149 PLEASE SCROLL DOWN FOR ARTICLE Full terms and conditions of use: http://www.informaworld.com/terms-and-conditions-of-access.pdf This article maybe used for research, teaching and private study purposes. Any substantial or systematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material. 2007 ember ept S 27 Points of View 34 03: : Syst. Biol. 56(4):673–684, 2007 t Copyright c Society of Systematic Biologists A ! ISSN: 1063-5157 print / 1076-836X online DOI: 10.1080/10635150701491149 The Adequacy of Morphology for Reconstructing the Early History of Placental Mammals Riverside] MARK S. SPRINGER,1 ANGELA BURK-HERRICK,1 ROBERT MEREDITH,1 EDUARDO EIZIRIK,2 EMMA TEELING,3 STEPHEN J. O’BRIEN,4 AND WILLIAM J. MURPHY5 ornia 1Department of Biology, University of California, Riverside, Riverside, CA 92521, USA; E-mail: [email protected] (M.S.S.) 2 Calif Faculdade de Biociencias, PUCRS, Porto Allegre, RS 90619-900, Brazil 3School of Biological and Environmental Sciences, University College Dublin Belfield, Dublin 4, Ireland of 4Laboratory of Genomic Diversity, National Cancer Institute–Frederick, Frederick, MD 21702, USA y 5Department of Veterinary Integrative Biosciences, Texas A&M University, College Station, TX 77843-4458, USA Universit [ y: B Mammalian anatomists and paleontologists working moplastic constellations of taxa that have evolved in- primarily with osteological data have long been in- dependently in separate geographic venues rather than trigued with the problem of eutherian diversification, monophyletic assemblages that descended from a com- including both interordinal relationships and the tim- mon ancestor. ing of the placental mammal radiation (McKenna, 1975; Scotland et al. (2003) argued for a more limited role Downloaded Novacek, 1992). Cladistic analyses of morphological for morphology-based phylogenetic analyses in recon- characters for placental mammal orders have suggested structing the tree of life. Other authors (Jenner, 2004; a variety of superordinal hypotheses (Table 1). Molecular Wiens, 2004; Smith and Turner, 2005) have offered de- trees based on single gene segments were often in conflict tailed critiques of Scotland et al.’s (2003) main thesis and with each other and with morphology, but larger nuclear maintain the view that morphological data remain “cru- gene data sets that include longer and/or multiple gene cial in reconstructing the phylogeny of the earth’s biota” segments have converged on a well-supported superor- (Smith and Turner, 2005:171). In particular, Wiens (2004), dinal tree topology that divides placental orders into four Jenner (2004), and Smith and Turner (2005) all note the major groups: Afrotheria, Xenarthra, Laurasiatheria, and importance of morphological data for reconstructing re- Euarchontoglires (Madsen et al., 2001; Murphy et al., lationships of fossil taxa. We also recognize the primacy 2001a, 2001b; Scally et al., 2001; Amrine-Madsen et al., of morphological data for reconstructing relationships of 2003). Analyses of independent molecular and genomic extinct taxa. However, the failure of morphological data data sets, specifically whole mitochondrial genomes and alone to recover a tree compatible with the four-clade in- rare genomic changes (RGCs), are congruent with this terordinal partitioning of placental mammals raises se- four-clade classification (Hudelot et al., 2003; Waddell rious doubts about the ability of current morphological and Shelley, 2003; Murphy et al., 2004; Reyes et al., 2004; cladistic studies to accurately reconstruct relationships Springer et al., 2004, 2005; Gibson et al., 2005; Kriegs for extinct forms. et al., 2006; Nishihara et al., 2006; Kjer and Honeycutt, Correlated character evolution related to diet and/or 2007). For example, Nishihara et al. (2006) found six, nine, locomotion in independent lineages is perhaps the most and nine L1 retroposon insertions supporting the mono- dangerous pitfall of morphological cladistics, where in- phyly of Afrotheria, Euarchontoglires, and Laurasiathe- stead the implicit assumption is that morphological char- ria, respectively. acters evolve independently of each other in separate Whereas nuclear, mitochondrial, and RGC data cor- lineages. This assumption may be warranted for some roborate each other in supporting the four major clades, characters, but there are also studies of the genetics of only Xenarthra had been previously hypothesized based skeletal variation in mammals that provide evidence for on morphology. In addition, the morphology-based positively and negatively correlated traits in skeletal size clades Altungulata, Anagalida, Archonta, Edentata, and shape. Chase et al. (2002) examined variation in Lipotyphla, Ungulata, and Volitantia (Table 1) are all in- the canid skeleton and found that individuals with rel- compatible with the four-clade classification of mammals atively small pelvic girdles and lumbar vertebrae also derived from molecular and genomic data. The molec- tend to have large attachment sites for jaw and neck ular/genomic tree also suggests that morphology-based muscles, relatively large posterior faces, and small an- groups of placental orders (Novacek, 2001) are often ho- terior faces. More generally, this finding implies that the 673 2007 674 SYSTEMATIC BIOLOGY VOL. 56 ember ABLE ept T 1. Superordinal groups based on morphological data. related to gliding (Dermoptera) and powered flight (Chi- S roptera) have evolved independently in a highly corre- Superordinal group Taxa 27 lated fashion in these two taxa. Gunnell and Simmons Altungulata Paenungulata, Perissodactyla (2005) provide a cogent ecological explanation: that mor- 34 Anagalida Glires, Macroscelidea phological similarities shared by these taxa were de- 03: Archonta Dermoptera, Chiroptera, Primates, Scandentia : rived independently due to the demands of an arboreal t Edentata Xenarthra, Pholidota A Glires Rodentia, Lagomorpha environment. Lipotyphla Afrosoricida, Eulipotyphla The emerging molecular and genomic consensus of Paenungulata Hyracoidea, Proboscidea, Sirenia four major groups of placental mammals has impli- Tethytheria Proboscidea, Sirenia Ungulata Altungulata, Cetartiodactyla, Tubulidentata cations for early placental biogeography as Afrothe- ria and Xenarthra are of putative Gondwanan origin Riverside] Volitantia Dermoptera, Chiroptera based on the fossil record of constituent orders whereas Laurasiatheria and Euarchontoglires are of putative ornia Laurasian origin (Eizirik et al., 2001; Madsen et al., 2001). size and strength of the pelvic and head-neck muscu- Molecular dating analyses with relaxed clock methods Calif loskeletal systems are inversely correlated (Chase et al., suggest that the four superordinal groups all diverged of 2002). Chase et al. (2002) also found that metrics of skull from each other in the Cretaceous (Hasegawa et al., y and limb length are inversely correlated with metrics of 2003, Springer et al., 2003; van Rheede et al., 2006; skull width and height. Carrier et al. (2005) found a neg- Murphy et al., 2007). By contrast, Asher et al. (2003, ative correlation between the size of the pelvis and di- 2005) and Meng et al. (2003) concluded that molecular Universit mensions of distal limb bones. This negative correlation studies that place interordinal divergences in the Creta- [ represents a functional trade-off between high-speed, ceous (Hasegawa et al., 2003; Springer et al., 2003)
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