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Phylogeny of the Rodent Genus Isothrix (Hystricognathi, Echimyidae) and its Diversification in Amazonia and the Eastern Andes

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Abstract

Efforts to clarify the affinities of the torós or brush-tailed rats (Isothrix) and document the radiation of these distinctive echimyids have been limited. The discovery of a new Andean species prompted a reanalysis of Isothrix and its relatives. Prior morphological analyses of skulls, mandibles, teeth, and external characters permitted robust diagnosis but offered little resolution of within- or between-group relationships. Analyses of mitochondrial cytochrome b sequences (798 bp), which are available for numerous echimyids, confirm the monophyly of recognized genera, including Isothrix, and resolve a number of interspecific relationships. Strikingly, the Andean toró (Isothrix barbarabrownae) is consistently recovered as sister to the remaining species. These are allied into three clades: I. sinnamariensis + I. pagurus in the lower Amazon Basin and Guianan Shield, I. orinoci + I. negrensis in the Rio Negro and Río Orinoco drainages, and I. bistriata across much of the western and southern Amazon Basin. However, the addition of a new basal taxon does not aid in identifying the sister taxon of Isothrix. These relationships are confirmed in combined analyses of cyt-b with sequence variation in the mitochondrial control region (D-loop; 450 bp) and in the nuclear RAG1 gene (1,072 bp). Analyses identify the Andes, or proto-Andes, as an important theater for the group’s evolution and may offer an explanation for the luxuriant fur of this genus. However, neither the biogeographic history of Isothrix nor the remarkable pelage evolution of the Echimyidae can be understood until the deeper nodes within the arboreal spiny rats (Echimyinae) are more fully resolved.

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References

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Auto Control 19:716–723

    Article  Google Scholar 

  • Albert JS, Lovejoy TE, Crampton WGR (2006) Miocene tectonism and the separation of cis- and trans-Andean river basins: evidence from Neotropical fishes. J S Am Earth Sci 21:14–27

    Article  Google Scholar 

  • Baker ML, Wares JP, Harrison GA, Miller RD (2004) Relationships among the families and orders of marsupials and the major mammalian lineages based on recombination activating gene-1. J Mammal Evol 11:1–16

    Article  Google Scholar 

  • Bates JM, Zink RM (1994) Evolution into the Andes: molecular evidence for species relationships in the genus Leptopogon. Auk 111:507–515

    Google Scholar 

  • Bonvicino CR, de Menezes AREAN, de Oliveira JA (2003) Molecular and karyologic variation in the genus Isothrix (Rodentia, Echimyidae). Hereditas 139:206–211

    Article  PubMed  CAS  Google Scholar 

  • Brooks DR, McLennan DA (1991) Phylogeny, ecology, and behavior: a research program in comparative biology. University of Chicago Press, Chicago

    Google Scholar 

  • Brumfield RT, Edwards SV (2007) Evolution into and out of the Andes: a Bayesian analysis of historical diversification in Thamnophilus antshrikes. Evol 61:346–367

    Article  CAS  Google Scholar 

  • Burns KJ, Naoki K (2004) Molecular phylogenetics and biogeography of Neotropical tanagers in the genus Tangara. Mol Phylogenet Evol 32:838–854

    Article  PubMed  CAS  Google Scholar 

  • Carvalho GAS, Salles LO (2004) Relationships among extant and fossil echimyids (Rodentia: Hystricognathi). Zool J Linn Soc 142:445–477

    Article  Google Scholar 

  • Costa LP (2003) The historical bridge between the Amazon and the Atlantic Forest of Brazil: a study of molecular phylogeography with small mammals. J Biogeogr 30:71–86

    Article  Google Scholar 

  • Costa LP, Leite YLR, da Fonseca GAB, da Fonseca MT (2000) Biogeography of South American forest mammals: endemism and diversity in the Atlantic Forest. Biotropica 32:872–881

    Google Scholar 

  • Cracraft J (1985) Historical biogeography and patterns of differentiation within the South American avifauna: areas of endemism. In: Buckley PA, Foster MS, Morton ES, Ridgely RS, Buckley FG (eds) Neotropical ornithology. American Ornithologists Union, Washington DC, pp 49–84

    Google Scholar 

  • Cracraft J, Prum RO (1988) Patterns and processes of diversification: speciation and historical congruence in some Neotropical birds. Evol 42:603–620

    Article  Google Scholar 

  • Croft DA (2001) Cenozoic environmental change in South America as indicated by mammalian body size distributions (cenograms). Divers Distrib 7:271–287

    Article  Google Scholar 

  • Darlu P, Lecointre G (2002) When does the Incongruence Length Difference test fail. Mol Biol Evol 19:432–437

    PubMed  CAS  Google Scholar 

  • da Silva MNF (1998) Four new species of spiny rats of the genus Proechimys (Rodentia: Echimyidae) from the western Amazon of Brazil. Proc Biol Soc Wash 111:436–471

    Google Scholar 

  • Douzery E, Randi E (1997) The mitochondrial control region of Cervidae: evolutionary patterns and phylogenetic content. Mol Biol Evol 14:1154–1166

    PubMed  CAS  Google Scholar 

  • Eberhard JR, Bermingham E (2004) Phylogeny and biogeography of the Amazona ochrocephala (Aves: Psittacidae) complex. Auk 121:318–332

    Article  Google Scholar 

  • Emmons LH (1993) On the identity of Echimys didelphoides Desmarest, 1817 (Mammalia: Rodentia: Echimyidae). Proc Biol Soc Wash 106:1–4

    Google Scholar 

  • Emmons LH (2005) A revision of the genera of arboreal Echimyidae (Rodentia: Echimyidae, Echimyinae), with descriptions of two new genera. In: Lacey EA, Myers P (eds) Mammalian diversification from chromosomes to phylogeography (a celebration of the career of James L. Patton), Univ Calif Publ Zool 133:247–308

  • Farris JS, Kallersjo M, Kluge AG, Bult C (1995) Testing significance of incongruence. Cladistics 10:315–319

    Article  Google Scholar 

  • Fjeldså J (2000) The relevance of systematics in choosing priority areas for global conservation. Environ Conserv 27:67–75

    Article  Google Scholar 

  • Fjeldså J, Rahbek C (2006) Diversification of tanagers, a species rich bird group, from lowlands to montane regions of South America. Integr Comp Biol 46:72–81

    Article  Google Scholar 

  • Fooden J, Aimi M (2005) Systematic review of the Japanese macaques, Macaca fuscata (Gray, 1870). Fieldiana Zool New Ser 1533:1–200

    Google Scholar 

  • Frailey CD, Campbell KE Jr (2004) Paleogene rodents from Amazonian Peru: the Santa Rosa local fauna. In: Campbell KE Jr (ed) The Paleogene mammalian fauna of Santa Rosa, Amazonian Peru, Nat Hist Mus Los Angeles County Sci Ser 40:71–130

  • Galewski T, Mauffrey J-F, Leite YLR, Patton JL, Douzery EJP (2005) Ecomorphological diversification among South American spiny rats (Rodentia; Echimyidae): a phylogenetic and chronological approach. Mol Phylogenet Evol 34:601–615

    Article  PubMed  CAS  Google Scholar 

  • Hackett SJ (1996) Molecular phylogenetics and biogeography of tanagers in the genus Ramphocelus (Aves). Mol Phylogenet Evol 5:368–382

    Article  PubMed  CAS  Google Scholar 

  • Haffer J (1969) Speciation in Amazonian forest birds. Science 165:131–137

    Article  PubMed  Google Scholar 

  • Hall JPW, Harvey DJ (2002) The phylogeography of Amazonia revisited: new evidence from riodinid butterflies. Evol 56:1489–1497

    Google Scholar 

  • Hasegawa M (1990) Phylogeny and molecular evolution in Primates. Jpn J Gen 65:243–265

    Article  CAS  Google Scholar 

  • Hennig W (1966) Phylogenetic systematics. University of Illinois Press, Urbana

    Google Scholar 

  • Hoey KA, Wise RR, Adler GH (2004) Ultrastructure of echimyid and murid rodent spines. J Zool 263:307–315

    Article  Google Scholar 

  • Huchon D, Delsuc F, Catzeflis FM, Douzery EJP (1999) Armadillos exhibit less genetic polymorphism in North America than in South America: nuclear and mitochodrial data confirm a founder effect in Dasypus novemcinctus (Xenarthra). Mol Ecol 8:1743–1748

    Article  PubMed  CAS  Google Scholar 

  • Hughes C, Eastwood R (2006) Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proc Natl Acad Sci USA 103:10334–10339

    Article  PubMed  CAS  Google Scholar 

  • Lara MC, Patton JL (2000) Evolutionary diversification of spiny rats (genus Trinomys, Rodentia: Echimyidae) in the Atlantic Forest of Brazil. Zool J Linn Soc 130:661–686

    Google Scholar 

  • Lara MC, Patton JL, da Silva MNF (1996) The simultaneous diversification of South American echimyid rodents (Hystricognathi) based on complete cytochrome b sequences. Mol Phylogenet Evol 5:403–413

    Article  PubMed  CAS  Google Scholar 

  • Leite YLR (2003) Evolution and systematics of the Atlantic tree rats, genus Phyllomys (Rodentia, Echimyidae), with description of two new species. Univ Calif Publ Zool 132:1–118

    Google Scholar 

  • Leite YLR, Patton JL (2002) Evolution of South American spiny rats (Rodentia, Echimyidae): the star-phylogeny hypothesis revisited. Mol Phylogenet Evol 25:455–464

    Article  PubMed  CAS  Google Scholar 

  • Lim BK, Engstrom MD, Lee TEJ, Patton JC, Bickham JW (2004) Molecular differentiation of large species of fruit-eating bats (Artibeus) and phylogenetic relationships based on the cytochrome b gene. Acta Chiropt 6:1–12

    Google Scholar 

  • Lim BK, Engstrom MD, Patton JC, Bickham JW (2006) Systematic relationships of the Guianan brush-tailed rat (Isothrix sinnamariensis) and its first occurrence in Guyana. Mammalia 70:120–125

    Article  Google Scholar 

  • Maddison WP, Knowles LL (2006) Inferring phylogeny despite incomplete lineage sorting. Syst Biol 55:21–30

    Article  PubMed  Google Scholar 

  • Mares MA, Ojeda RA (1982) Patterns of diversity and adaptation in South American hystricognath rodents. In: Mares MA, Genoways HH (eds) Mammalian biology in South America. Pymatuning Laboratory of Ecology, University of Pittsburgh, Pittsburgh, pp 393–432

    Google Scholar 

  • Matisoo-Smith E, Robins JH (2004) Origins and dispersals of Pacific peoples: evidence from mtDNA phylogenies of the Pacific rat. Proc Natl Acad Sci USA 101:9167–9172

    Article  PubMed  CAS  Google Scholar 

  • McKenna DD, Farrell BD (2006) Tropical forests are both evolutionary cradles and museums of leaf beetle diversity. Proc Natl Acad Sci USA 109:10947–11095

    Article  CAS  Google Scholar 

  • McKenna MC, Bell SK (1997) Classification of mammals: above the species level. Columbia University Press, New York

    Google Scholar 

  • Moscarella RA, Aguilera M, Escalante AA (2003) Phylogeography, population structure, and implications for conservation of white-tailed deer (Odocoileus virginianus) in Venezuela. J Mamm 84:1300–1315

    Article  Google Scholar 

  • Myers N (2003) Biodiversity hotspots revisited. BioSci 53:916–917

    Article  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  PubMed  CAS  Google Scholar 

  • Nelson G, Platnick N (1981) Systematics and biogeography: cladistics and vicariance. Columbia University Press, New York

    Google Scholar 

  • Nores M (1999) An alternative hypothesis for the origin of Amazonian bird diversity. J Biogeogr 26:475–486

    Article  Google Scholar 

  • Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D’Amico JA, Itoua I, Strand HE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR (2001) Terrestrial ecoregions of the world: a new map of life on Earth. BioSci 51:933–938

    Article  Google Scholar 

  • Patterson B, Wood AE (1982) Rodents from the Deseadan Oligocene of Bolivia and the relationships of the Caviomorpha. Bull Mus Comp Zool Harv Univ 149:371–543

    Google Scholar 

  • Patterson BD (1992a) Mammals in the Royal Natural History Museum, Stockholm, collected in Brazil and Bolivia by A. M. Olalla during 1934–1938. Fieldiana Zool New Ser 66:1–48

    Google Scholar 

  • Patterson BD (1992b) A new genus and species of long-clawed mouse (Rodentia: Muridae) from temperate rainforests of Chile. Zool J Linn Soc 106:127–145

    Article  Google Scholar 

  • Patterson BD, Velazco P (2006) A distinctive new cloud-forest rodent (Hystricognathi: Echimyidae) from the Manu Biosphere Reserve, Peru. Mastozool Neotrop 13:175–191

    Google Scholar 

  • Patton JL, da Silva MNF (1997) Definition of species of pouched four-eyed opossums (Didelphidae, Philander). J Mamm 78:90–102

    Article  Google Scholar 

  • Patton JL, da Silva MNF, Malcolm JR (1994) Gene geneology and differentiation among arboreal spiny rats (Rodentia: Echimyidae) of the Amazon Basin: a test of the riverine barrier hypothesis. Evol 48:1314–1323

    Article  Google Scholar 

  • Patton JL, da Silva MNF, Malcolm JR (2000) Mammals of the Rio Juruá and the evolutionary and ecological diversification of Amazonia. Bull Am Mus Nat Hist 244:1–306

    Article  Google Scholar 

  • Patton JL, Emmons LH (1985) A review of the genus Isothrix (Rodentia, Echimydae). Am Mus Novitates 2817:1–14

    Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:917–918

    Article  Google Scholar 

  • Ramos VA, Aleman A (2000) Tectonic evolution of the Andes. In: Cordani U, Milani EJ, Thomaz Filho A, Navas CA, Campos Neto MC (eds) Tectonic evolution of South America. International Geology Congress, Rio de Janeiro, pp 635–685

    Google Scholar 

  • Reig OA (1981) Teoría del origen y desarrollo de la fauna de mamíferos de America del Sur. Monogr Naturae. Mus Munic Cien Nat “Lorenzo Scaglia” 1:1–162

    Google Scholar 

  • Reig OA (1986) Diversity patterns and differentiation of high Andean rodents. In: Vuilleumier F, Monasterio M (eds) High altitude tropical biogeography. Oxford University Press, New York, pp 404–439

    Google Scholar 

  • Rivera PC, Ittig REG, Fraire HJR, Levis S, Gardenal CN (2007) Molecular identification and phylogenetic relationships among the species of the genus Oligoryzomys (Rodentia, Cricetidae) present in Argentina, putative reservoirs of hantaviruses. Zool Scripta 36:231–239

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Smith MF, Patton JL (1993) The diversification of South American murid rodents: evidence from mitochondrial DNA sequence data for the akodontine tribe. Biol J Linn Soc 50:149–177

    Article  Google Scholar 

  • Steppan SJ, Adkins RM, Spinks PQ, Hale C (2005) Multigene phylogeny of the Old World mice, Murinae, reveals distinct geographic lineages and the declining utility of mitochondrial genes compared to nuclear genes. Mol Phylogenet Evol 37:370–388

    Article  PubMed  CAS  Google Scholar 

  • Steppan SJ, Storz BL, Hoffmann RS (2004) Nuclear DNA phylogeny of the squirrels (Mammalia: Rodentia) and the evolution of arboreality from c-myc and RAG1. Mol Phylogenet Evol 30:703–719

    Article  PubMed  CAS  Google Scholar 

  • Stotz DF, Fitzpatrick JW, Parker TA III, Moskovits DK (1996) Neotropical birds: ecology and conservation. University of Chicago Press, Chicago

    Google Scholar 

  • Swofford D (2002) PAUP* 4.0b10: Phylogenetic analysis using parsimony. Sinauer Associates, Sunderland

  • Teeling EC, Scally M, Kao DJ, Romagnoli ML, Springer MS, Stanhope MJ (2000) Molecular evidence regarding the origin of echolocation and flight in bats. Nature 403:188–192

    Article  PubMed  CAS  Google Scholar 

  • Thomas O, St. Leger J (1926) The Godman-Thomas Expedition to Peru.–IV. Mammals collected by Mr. R. W. Hendee north of Chachapoyas, province of Amazonas, North Peru. Ann Mag Nat Hist Ser 9(18):345–349

    Google Scholar 

  • Van Den Bussche RA, Hudgeons JL, Baker RJ (1998) Phylogenetic accuracy, stability, and congruence: Relationships within and among the New World bat genera Artibeus, Dermanura, and Koopmania. In: Kunz TH, Racey PA (eds) Bat biology and conservation. Smithsonian Institution Press, Washington, DC, pp 59–71

    Google Scholar 

  • Vanzolini PE, Williams EE (1970) South American anoles: the geographic differentiation and evolution of the Anolis chrysolepis species group (Sauria, Iguanidae). Arquiv Zool 19:1–298

    Google Scholar 

  • Vie JC, Voloboue V, Patton JL, Granjon L (1996) A new species of Isothrix (Rodentia: Echimyidae) from French Guiana. Mammalia 60:393–406

    Google Scholar 

  • Vuilleumier F, Monasterio M (1986) High altitude tropical biogeography. Oxford University Press, New York

    Google Scholar 

  • Wiens JJ, Graham CH, Moen DS, Smith SA, Reeder TW (2006) Evolutionary and ecological causes of the latitudinal diversity gradient in hylid frogs: treefrog trees unearth the roots of high tropical diversity. Am Nat 168:579–596

    Article  PubMed  Google Scholar 

  • Woods CA (1982) The history and classification of South American hystricognath rodents: reflections on the far away and long ago. In: Mares MA, Genoways HH (eds) Mammalian biology in South America. Pymatuning Laboratory of Ecology, University of Pittsburgh, Pittsburgh, pp 377–392

    Google Scholar 

  • Woods CA, Kilpatrick CW (2005) Infraorder Hystricognathi Brandt, 1855. In: Wilson DE, Reeder DM (eds) Mammal species of the world: a taxonomic and geographic reference, 3rd ed. Johns Hopkins University Press, Baltimore, pp 1538–1600

    Google Scholar 

  • Wright S, Keeling J, Gillman L (2006) The road from Santa Rosalia: a faster tempo of evolution in tropical climates. Proc Natl Acad Sci USA 103:7718–7722

    Article  PubMed  CAS  Google Scholar 

  • Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Thesis, Department of Zoology, University of Texas at Austin, x + 115 pp

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Acknowledgements

A principal debt is owed all those who collected specimens, most recently those participating in the 1999–2001 Manu expeditions organized by Field Museum and Universidad de San Marcos and funded by FMNH, MUSM, and the NSF (DEB-9870191); S. Solari and D. Stotz deserve special thanks. We also deeply appreciate the generosity of J.L. Patton in sharing tissues, sequence, and insights from his extensive association with Echimyidae in general and Isothrix in particular. F. Catzeflis, L. Emmons, M. N. da Silva, and B. Lim also shared unpublished specimens and/or manuscripts in press with us, and M. Carleton and L. Gordon permitted us to sample USNM specimens. J. Tello and K. Feldheim of the Pritzker Laboratory provided valued technical help. Sequencing costs were borne by the Field Museum’s Barbara E. Brown Fund for Mammal Research. During this effort, the junior author was supported by the University of Illinois at Chicago, the Ellen Thorne Smith Fund (FMNH), The Lester Armour Fellowship (FMNH), and OISE-0630149 (NSF). Two anonymous reviewers provided important and insightful reviews that greatly strengthened our arguments and this presentation.

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  1. Department of Zoology, Field Museum of Natural History, 1400 S. Lake Shore Drive, Chicago, IL, 60605, USA

    Bruce D. Patterson & Paúl M. Velazco

  2. Department of Biological Sciences, University of Illinois at Chicago, 845 W. Taylor St, Chicago, IL, 60607, USA

    Paúl M. Velazco

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  1. Bruce D. Patterson
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Correspondence to Bruce D. Patterson.

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Patterson, B.D., Velazco, P.M. Phylogeny of the Rodent Genus Isothrix (Hystricognathi, Echimyidae) and its Diversification in Amazonia and the Eastern Andes. J Mammal Evol 15, 181–201 (2008). https://doi.org/10.1007/s10914-007-9070-6

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