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Molecular Evidence for Multiple Origins of Insectivora and for a New Order of Endemic African Insectivore Mammals

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Molecular Evidence for Multiple Origins of Insectivora and for a New Order of Endemic African Insectivore Mammals Proc. Natl. Acad. Sci. USA Vol. 95, pp. 9967–9972, August 1998 Evolution Molecular evidence for multiple origins of Insectivora and for a new order of endemic African insectivore mammals MICHAEL J. STANHOPE*†‡,VICTOR G. WADDELL†,OLE MADSEN§,WILFRIED DE JONG§,S.BLAIR HEDGES¶, i i i GREGORY C. CLEVEN ,DIANA KAO , AND MARK S. SPRINGER* †Queen’s University of Belfast, Biology and Biochemistry, 97 Lisburn Road, Belfast, BT9 7BL, United Kingdom; §Department of Biochemistry, University of Nijmegen, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands, and Institute for Systematics and Population Biology, University of Amsterdam, P.O. Box 94766, 1090 GT Amsterdam, The Netherlands; ¶Department of Biology, 208 Mueller Lab, Pennsylvania State University, University Park, PA 16802; and iDepartment of Biology, University of California, Riverside, CA 92521 Edited by Roy J. Britten, California Institute of Technology, Corona Del Mar, CA, and approved June 5, 1998 (received for review April 3, 1998) ABSTRACT The traditional views regarding the mamma- recently, MacPhee and Novacek (3) have reviewed the evidence lian order Insectivora are that the group descended from a single and concluded that characteristics (i) and (ii) support lipotyphlan common ancestor and that it is comprised of the following monophyly, characteristic (iii) possibly does, and (iv–vi), as cur- families: Soricidae (shrews), Tenrecidae (tenrecs), Solenodonti- rently defined, do not, leaving two to three characteristics that, in dae (solenodons), Talpidae (moles), Erinaceidae (hedgehogs and their opinion, support the order Insectivora. gymnures), and Chrysochloridae (golden moles). Here we The six families of insectivores are most often grouped into two present a molecular analysis that includes representatives of all clades of subordinal rank: the Erinaceomorpha (hedgehogs) and six families of insectivores, as well as 37 other taxa representing the Soricomorpha (all other families). Within the Soricomorpha, marsupials, monotremes, and all but two orders of placental Butler (4) suggested that the golden moles and tenrecs form a mammals. These data come from complete sequences of the clade and that moles and shrews cluster together, followed by mitochondrial 12S rRNA, tRNA-Valine, and 16S rRNA genes (2.6 solenodons. MacPhee and Novacek (3), however, proposed three kb). A wide range of different methods of phylogenetic analysis clades of subordinal rank: Chrysochloromorpha (Chrysochlori- groups the tenrecs and golden moles (both endemic to Africa) in dae), Erinaceomorpha (Erinaceidae), and Soricomorpha (Sori- an all-African superordinal clade comprised of elephants, sire- cidae, Talpidae, Solenodontidae, and Tenrecidae). This latter nians, hyracoids, aardvark, and elephant shrews, to the exclusion organization is based on their view that the Chrysochloridae is of the other four remaining families of insectivores. Statistical ‘‘spectacularly autapomorphic.’’ In their opinion, golden moles analyses reject the idea of a monophyletic Insectivora as well as show no shared derived traits with the soricomorphs and there- traditional concepts of the insectivore suborder Soricomorpha. fore should be separated from that suborder. This recommen- These findings are supported by sequence analyses of several dation echoes earlier views regarding the group that have sug- nuclear genes presented here: vWF, A2AB, and a-b hemoglobin. gested that golden moles are a separate order or suborder (5–7). These results require that the order Insectivora be partitioned A recent molecular study of mammalian phylogeny, which and that the two African families (golden moles and tenrecs) be included three insectivore families, demonstrated that golden placed in a new order. The African superordinal clade now moles are not part of the Insectivora but instead belong to a clade includes six orders of placental mammals. of endemic African mammals that also includes elephants, hyraxes, sea cows, aardvarks, and elephant shrews (8). Evidence Throughout most of this century, the placental (eutherian) mam- for this now comes from a wide range of disparate molecular loci mals with extant representation have been classified into 18 including the nuclear AQP2, vWF, and A2AB genes as well as the orders. During this period, the order Insectivora has been among mitochondrial 12S–16S rRNA genes (8, 9). The fossil record of the least stable higher taxa in Eutheria, both in terms of phylo- golden moles indicates that the geographic distribution of this genetic position and taxonomic content. Beginning with Huxley group has been restricted to Africa throughout its temporal range (1) and later embellished by Mathew (2), insectivores have been (10, 11). The fossil record of tenrecs also suggests an African thought to possess features that rendered them closer to the origin (10, 11). This paleontological record, along with the ancestral stock of mammals. Despite this presumed central po- morphological study of Butler (4), suggests a possible common sition of insectivores in the evolutionary history of mammals, the ancestry for golden moles and tenrecs. However, it also may be composition of the group never has been widely agreed on. The that the autapomorphic qualities of golden moles reflect their prevalent morphological view (3) suggests that the following evolutionary history as a singular distinct lineage of African extant families of ‘‘insectivores’’ descended from a single common insectivores, separate from the rest of the order. At present, there ancestor and as such should be those groups that are regarded as is no published molecular phylogenetic perspective on the evo- the constituents of the order Insectivora (Lipotyphla): Soricidae lutionary history of the Tenrecidae, there is no molecular study (shrews), Tenrecidae (tenrecs), Solenodontidae (solenodons), that includes a representative from all families of insectivores, and Talpidae (moles), Erinaceidae (hedgehogs and gymnures), and there are no molecular sequence data (data banks or published Chrysochloridae (golden moles). accounts) for solenodons. Butler (4) listed six morphological characteristics that, in his Here, we report a molecular phylogenetic analysis involving all opinion, supported a monophyletic Insectivora including (i) ab- families of insectivores, using complete sequences of the mito- sence of cecum; (ii) reduction of pubic symphysis; (iii) maxillary chondrial 12S rRNA, 16S rRNA, and tRNA-Valine genes. These expansion within orbit, displacing palatine; (iv) mobile proboscis; data, along with additional sequences from four disparate nuclear (v) reduction of jugal; and (vi) hemochorial placenta. More This paper was submitted directly (Track II) to the Proceedings office. The publication costs of this article were defrayed in part by page charge Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. AF069533-40, payment. This article must therefore be hereby marked ‘‘advertisement’’ in AF076646, Y17692, and AF076478-80). accordance with 18 U.S.C. §1734 solely to indicate this fact. *These two authors contributed equally to this work. © 1998 by The National Academy of Sciences 0027-8424y98y959967-6$2.00y0 ‡To whom reprint requests should be addressed. e-mail: m.stanhope@ PNAS is available online at www.pnas.org. qub.ac.uk. 9967 Downloaded by guest on September 26, 2021 9968 Evolution: Stanhope et al. Proc. Natl. Acad. Sci. USA 95 (1998) genes, are used to examine the extent of insectivore paraphyly or two nuclear genes: exon 28 of the gene for von Willebrand factor polyphyly, the conflicting hypotheses regarding the origin of the (vWF; AF076478) and the a-2B adrenergic receptor gene family Tenrecidae, and the possibility of an African clade of (A2AB; Y17692). New sequence data were also obtained for insectivores. vWF from mole (AF076479), and hairy armadillo (AF076480). These sequences were combined with already existing data for MATERIALS AND METHODS both of these genes arising from previous studies (8, 9, 14). For The 12S rRNA, tRNA-Valine, and 16S rRNA genes were am- vWF, this included the following taxa: human, galago (Galago plified and sequenced [as described elsewhere refs. 8 and 12] from crassicaudatus; Primates), agouti (Dasyprocta agouti; Rodentia), the following taxa: tenrec (Echinops telfairi; Insectivora; rat, mole-rat (Spalax polinicus; Rodentia), African elephant, AF069540), hairy armadillo (Chaetophractus villosus; Xenarthra; Asian elephant (Elephas maximus), dugong (Dugong dugon; Si- U61080, AF069534), three-toed sloth (Bradypus tridactylus; Xe- renia), hyrax, aardvark, elephant shrew, harbor porpoise (Pho- narthra; AF038022, AF069535), tube-nosed fruit bat (Nyctimene coena phocoena; Cetacea), cow, pig (Sus scrofa; Artiodactyla), robinsoni; Chiroptera; U93061, AF069536), flying fox (Pteropus hedgehog, golden mole, white rhinoceros, horse (Equus asinus), hypomelanus; Chiroptera; U93073, AF069537), false vampire bat rabbit, pangolin, false-vampire bat, bar-backed fruit bat (Dobso- (Megaderma lyra; Chiroptera; AF069538), mole (Scalopus aquati- nia moluccensis), cat, dog (Canis familiaris; Carnivora), flying cus; Insectivora; AF069539), solenodon (Solenodon paradoxus; lemur (Cynocephalus variegatus; Dermoptera), tree shrew (Tupai Insectivora; AF076646) and capybara (Hydrochaeris hydrochaeris; glis; Scandentia), and three-toed sloth (scientific name indicated Rodentia; U61081, AF069533). These were combined with se- only when it has not been listed already for the mitochondrial
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