Conservation Genetics

, Volume 12, Issue 4, pp 1035–1048

Molecular phylogenetics of an endangered species: the Tamaulipan woodrat (Neotoma angustapalata)

  • Duke S. Rogers
  • Rafael N. Leite
  • Rustin J. Reed
Research Article

Abstract

Neotoma angustapalata (Tamaulipan woodrat) is a large cricetid rodent found only in southwestern Tamaulipas and northeastern San Luis Potosí, Mexico. This species currently is listed as endangered due to habitat alteration, its restricted distribution, and relative rarity. Previous taxonomic assessments have allied N. angustapalata with N. albigula (now encompassing N. leucodon), N. mexicana or N. micropus. We sequenced portions of the mitochondrial cytochrome b gene from two skin samples of the Tamaulipan woodrat, including one of two topotypes. We estimated genealogical relationships between N. angustapalata and other species of Neotoma using maximum likelihood and Bayesian inference. In general, our results confirm the phylogeny of woodrats as proposed previously but we also recovered major genetic differentiation within what currently is recognized as N. mexicana and N. albigula. Our data document that the Tamaulipan woodrat is genetically indistinguishable from geographically adjacent haplotypes of N. leucodon. However, mitochondrial introgression from N. leucodon cannot be ruled out inasmuch as we were not able to obtain nuclear sequence data for N. angustapalata. Morphological analyses document that both male and female Tamaulipan woodrats differ morphologically from N. leucodon. Given that the Tamaulipan woodrat is diagnosable morphologically and occurs in habitat that differs from N. leucodon, we recognize N. angustapalata as a species-level entity.

Keywords

Cytochrome b Endangered species General lineage concept Molecular systematics Neotoma angustapalata N. leucodon Principal components analysis 

References

  1. Akaike H (1974) The new look at the statistical model identification. IEEE Trans Autom Control 19:716–723CrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  3. Alvarez T (1963) The recent mammals of Tamaulipas, Mexico. Univ Kansas Publ Mus Nat Hist 14:363–473Google Scholar
  4. Álvarez-Castañeda ST, Castro-Arellano I (2008) Neotoma angustapalata. In: IUCN 2009 IUCN Red List of Threatened Species. Version 2009.1. Available via http://www.iucnredlist.org
  5. Arellano E, González-Cozátl FX, Rogers DS (2005) Molecular systematics of middle American harvest mice Reithrodontomys (Muridae), estimated from mitochondrial cytochrome b gene sequences. Mol Phylogenet Evol 37:529–540Google Scholar
  6. Baker RH (1951) Mammals from Tamaulipas, Mexico. Univ Kansas Publ Mus Nat Hist 5:207–218Google Scholar
  7. Baker JR, Bradley RD (2006) Speciation in mammals and the genetic species concept. J Mammal 87:643–663PubMedCrossRefGoogle Scholar
  8. Baker RH, Greer JK (1962) Mammals of the Mexican state of Durango. Publ Mus Michigan State Univ Biol Ser 2:25–154Google Scholar
  9. Barome PO, Lymberakis P, Monnerot M, Gatun JC (2001) Cytochrome b sequences reveal Acomys minous (Rodentia, Muridae) paraphyly and answer the question about the ancestral karyotype of Acomys dimidiatus. Mol Phylogenet Evol 18:37–46PubMedCrossRefGoogle Scholar
  10. Birney EC (1973) Systematics of three species of woodrats (genus Neotoma) in Central North America. Misc Publ Univ Kansas Mus Nat Hist 58:1–173Google Scholar
  11. Burgio G, Baylac M, Heyer E, Montagutelli X (2009) Genetic analysis of skull shape variation and morphological integration in the mouse using interspecific recombinant congenic strains between C57BL/6 and mice of the Mus spretus species. Evolution 63:2668–2686PubMedCrossRefGoogle Scholar
  12. Burt WH (1939) A new woodrat (Neotoma mexicana) from the lava beds of southern New Mexico. Occas Pap Mus Zool Univ Mich 400:1–3Google Scholar
  13. Burt WH, Barkalow FS (1942) A comparative study of the bacula of wood rats (subfamily Neotominae). J Mammal 23:287–297CrossRefGoogle Scholar
  14. Cantú C, Wright RG, Scott JM, Strand E (2004) Assessment of current and proposed nature reserves of Mexico based on their capacity to protect geophysical features and biodiversity. Biol Conserv 115:411–417CrossRefGoogle Scholar
  15. Castro-Arellano I (2005) Ecological patterns of the small mammal communities at El Cielo Biosphere Reserve, Tamaulipas, Mexico. Dissertation, Texas A&M UniversityGoogle Scholar
  16. Cheverud JM, Routman EJ, Duarte FAM, van Swinderen B, Cothram K, Perel C (1996) Quantitative trait loci for murine growth. Genetics 142:1305–1319PubMedGoogle Scholar
  17. CONABIO (1999) Ecorregiones de México, escala 1:100000. CCA-Conabio, México. Available via http://www.conabio.gob.mx
  18. Cracraft J (1983) Species concepts and speciation analysis. In: Johnson RF (ed) Current ornithology. Plenum Press, New York, pp 159–187Google Scholar
  19. Davis WB, Robertson JL (1944) The mammals of Culberson County, Texas. J Mammal 25:254–273CrossRefGoogle Scholar
  20. de Queiroz K (1998) The general lineage concept of species, species criteria, and the process of speciation: a conceptual unification and terminological recommendations. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, New York, pp 57–75Google Scholar
  21. de Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886PubMedCrossRefGoogle Scholar
  22. Degnan SM (1993) The perils of single gene trees: mitochondrial versus single-copy nuclear DNA variation in white-eyes (Aves: Zosteropidae). Mol Ecol 2:219–225CrossRefGoogle Scholar
  23. Demboski JR, Cook JA (2001) Phylogeography of the dusky shrew, Sorex monticolus (Insectivora, Soricidae): insight into deep and shallow history in northwestern North America. Mol Ecol 10:1227–1240 Google Scholar
  24. Dice LR (1929) Description of two new pocket mice and a new woodrat from New Mexico. Occas Pap Mus Zool Univ Mich 203:1–4Google Scholar
  25. Edwards CW, Bradley RD (2001) Molecular phylogenetics of the Neotoma floridana species group. J Mammal 82:791–798CrossRefGoogle Scholar
  26. Edwards CW, Bradley RD (2002a) Molecular systematics and historical phylobiogeography of the Neotoma mexicana species group. J Mammal 83:20–30CrossRefGoogle Scholar
  27. Edwards CW, Bradley RD (2002b) Molecular systematics of the genus Neotoma. Mol Phylogenet Evol 25:489–500PubMedCrossRefGoogle Scholar
  28. Edwards SV, Arctander P, Wilson AC (1991) Mitochondrial resolution of a deep branch in the genealogical tree for perching birds. Proc Royal Soc London B 243:99–107CrossRefGoogle Scholar
  29. Edwards CW, Fulhorst CF, Bradley RD (2001) Molecular phylogenetics of the Neotoma albigula species group: further evidence of a paraphyletic assemblage. J Mammal 82:267–279CrossRefGoogle Scholar
  30. Escalante T, Espinosa D, Morrone JJ (2003) Using parsimony analysis of endemicity to analyze the distribution of Mexican land mammals. Southwestern Nat 48:563–578CrossRefGoogle Scholar
  31. Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Syst 34:397–423CrossRefGoogle Scholar
  32. Goldstein PZ, DeSalle R, Amato G (2000) Conservation genetics at the species boundary. Cons Biol 14:120–131CrossRefGoogle Scholar
  33. Gorog AJ, Sinaga MH, Engstrom MD (2004) Vicariance or dispersal? Historical biogeography of three Sunda shelf murine rodents (Maxomys surifer, Leopoldamys sabanus and Maxomys whiteheadi). Biol J Linn Soc 81:91–109CrossRefGoogle Scholar
  34. Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  35. Hall ER (1955) A new subspecies of wood rat from Nayarit, Mexico, with new name-combinations for the Neotoma micropus group. J Wash Acad Sci 45:328–332Google Scholar
  36. Hall ER (1981) The mammals of North America. John Wiley & Sons, New YorkGoogle Scholar
  37. Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 21:160–174CrossRefGoogle Scholar
  38. Hoffmeister DF, de la Torre L (1960) A revision of the woodrat Neotoma stephansi. J Mammal 41:476–491CrossRefGoogle Scholar
  39. Hooper ET (1953) Notes on mammals of Tamaulipas, México. Occas Pap Mus Zool Univ Mich 544:1–12Google Scholar
  40. Huelsenbeck JP, Imennov NS (2002) Geographic origin of human mitochondrial DNA: accommodating phylogenetic uncertainty and model comparison. Syst Biol 51:155–165PubMedCrossRefGoogle Scholar
  41. Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogeny. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  42. Huelsenbeck JP, Larget B, Miller RE, Ronquist F (2002) Potential applications and pitfalls of Bayesian inference of phylogeny. Syst Biol 51:673–688PubMedCrossRefGoogle Scholar
  43. Irwin DM, Kocher TD, Wilson AC (1991) Evolution of the cytochrome b gene of mammals. J Mol Evol 32:128–144PubMedCrossRefGoogle Scholar
  44. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120 Google Scholar
  45. Kishino H, Miyata T, Hasegawa M (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J Mol Evol 30:151–160CrossRefGoogle Scholar
  46. Koopman KF, Martin PS (1959) Subfossil mammals from the Gómez Fárias region and the tropical gradient of eastern Mexico. J Mammal 40:1–12CrossRefGoogle Scholar
  47. Leamy LJ, Routman EJ, Cheverud JM (1999) Quantitative trait loci for early- and late-developing skull characters in mice: a test of the genetic independence model of morphological integration. Amer Nat 153:201–214CrossRefGoogle Scholar
  48. Leamy LJ, Pomp D, Eisen EJ, Cheverud JM (2002) Pleiotropy of quantitative trait loci for organ weights and limb bone lengths in mice. Physiol Genomics 10:21–29PubMedGoogle Scholar
  49. Lee JC, Hsieh HM, Huang LH, Kuo YC, Wu JH, Chin SC, Lee AH, Linacre A, Tsai LC (2009) Ivory identification by DNA profiling of cytochrome b gene. Int J Legal Med 123:117–121PubMedCrossRefGoogle Scholar
  50. Luna-Vega I, Alcántara Ayala O, Espinosa Organista D, Morrone JJ (1999) Historical relationships of the Mexican cloud forests: a preliminary vicariance model applying Parsimony analysis of endemicity to vascular plant taxa. J Biogeo 26:1299–1305CrossRefGoogle Scholar
  51. Luna-Vega I, Morrone JJ, Alcácantara Ayala O, Epinosa Organista D (2001) Biogeographical affinities among Neotropical cloud forests. Plant Syst Evol 228:229–239CrossRefGoogle Scholar
  52. Martin Y, Gerlach G, Schlötterer C, Meyer A (2000) Molecular phylogeny of muriod rodents based on complete Cytochrome b sequences. Mol Phylogenet Evol 16:37–47PubMedCrossRefGoogle Scholar
  53. Mas JF, Velázquez A, Díaz-Gallegos JR, Mayorga-Saucedo R, Alcantara C, Bocco G, Castro R, Fernández T, Pérez-Vega A (2004) Assessing land/use cover changes: a nationwide multidate spatial database for Mexico. Inter J Appl Earth Observ Geoinfor 5:249–261CrossRefGoogle Scholar
  54. Masera O, Ordoñez MJ, Dirzo R (1992) Carbon emissions and sequestration in forests: case studies from seven developing countries. In: Makundi W, Sathaye J (eds) Carbon emissions from deforestation in Mexico: current situation and long term scenarios. Om: University of California, Berkeley, pp 1–49Google Scholar
  55. Matocq MD (2002) Phylogeographical structure and regional history of the dusky-footed woodrat, Neotoma fuscipes. Mol Ecol 11:229–242PubMedCrossRefGoogle Scholar
  56. Matocq MD, Shurtliff QR, Feldman CR (2007) Phylogenetics of the woodrat genus Neotoma (Rodentia: Muridae): Implications for the evolution of phenotypic variation in male external genitalia. Mol Phylogenet Evol 42:637–652PubMedCrossRefGoogle Scholar
  57. Milazzo ML, Cajimat MNB, Haynie ML, Abbott KD, Bradley RD, Fulhorst C (2008) Diversity among the Tacaribe serocomplex viruses (Family Arenaviridae) naturally associated with the white-throated woodrat (Neotoma albigula) in the southwestern United States. Vector-Borne Zoo Dis 8:523–540CrossRefGoogle Scholar
  58. Miller JR, Engstrom MD (2008) The relationships of major lineages within peromyscine rodents: a molecular phylogenetic hypothesis and systematic reappraisal. J Mammal 89:1279–1295 Google Scholar
  59. Morrone JJ (2005) Hacia una síntesis biogeográfica de México. Rev Mex Biodiv 76:207–252Google Scholar
  60. Morrone JJ (2006) Biogeographic areas and transition zones of Latin American and Caribbean Islands, based on panbiogeographic and cladistic analyses of the entomofauna. Annu Rev Entomol 51:467–494PubMedCrossRefGoogle Scholar
  61. Musser GG, Carleton MD (2005) Family Cridetidae. In: Wilson DE, Reeder DM (eds) Mammal species of the world: a taxonomic and geographic reference, 3rd edn. Smithsonian Institution Press, Washington, pp 955–1189Google Scholar
  62. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858PubMedCrossRefGoogle Scholar
  63. Nachman NW (2005) The genetic basis of adaptation: lessons from concealing coloration in pocket mice. Genetica 123:125–136PubMedCrossRefGoogle Scholar
  64. Nachman MW, Hoekstra HE, D’Agostino SL (2003) The genetic basis of adaptive melanism in pocket mice. Proc Nat Acad Sci USA 100:5268–5273PubMedCrossRefGoogle Scholar
  65. Nylander JAA (2004) MrModeltest version 2Google Scholar
  66. Ortega-Huerta MA, Peterson AT (2004) Modelling spatial patterns of biodiversity for conservation prioritization in North-eastern Mexico. Divers Distrib 10:39–54CrossRefGoogle Scholar
  67. Patton JL, Smith MF (1994) Paraphyly, polyphyly, and the nature of species boundaries in pocket gophers (genus Thomomys). Syst Biol 43:11–26Google Scholar
  68. Patton JL, Huckaby DG, Álvarez-Castañada ST (2008) The evolutionary history and a systematic revision of woodrats of the Neotoma lepida group. University of California Press, BerkeleyGoogle Scholar
  69. Peppers LL, Bradley RD (2000) Cryptic species in Sigmodon hispidus: Evidence from DNA sequences. J Mammal 81:332–343CrossRefGoogle Scholar
  70. Pergams ORW, Lacy RC (2008) Rapid morphological and genetic change in Chicago-area Peromyscus. Mol Ecol 17:450–463Google Scholar
  71. Pergams ORW, Lawler JJ (2009) Recent and widespread rapid morphological change in rodents. PLoS ONE 4:e6452 Google Scholar
  72. Posada D, Crandall KA (1998) Model test: testing the model of DNA substitution. Bioinforatics 14:817–818CrossRefGoogle Scholar
  73. Prusak B, Grzybowski T, Bednarek J (2005) Cytochrome b gene (cytb) in analysis of anonymous biological traces and its application in veterinary diagnostics and animal conservation. Anim Sci Pap Rep 23:229–236Google Scholar
  74. Rambaut A, Drummond AJ (2003) Tracer version 1.4 [computer program]. Available via http://tree.bio.ed.ac.uk/software/tracer/. Accessed 24 September 2009
  75. Rogers DS, Schmidly DJ (1981) Geographic variation in the white-throated woodrat (Neotoma albigula) from New Mexico, Texas and northern Mexico. Southwestern Nat 26:167–181CrossRefGoogle Scholar
  76. Ronquist F, Huelsenbeck JP (2003) MrBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  77. Rzedowski J (1978) Vegetación de México. Editorial Limusa, MéxicoGoogle Scholar
  78. Sánchez-Cordero V, Illoldi-Rangel P, Linaje M, Sarkar S, Peterson AT (2005) Deforestation and extant distributions of Mexican endemic mammals. Biol Conserv 126:465–473CrossRefGoogle Scholar
  79. Sayer JA, Whitmore TC (1991) Tropical moist forests destruction and species extinction. Biol Conserv 55:199–213CrossRefGoogle Scholar
  80. Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116Google Scholar
  81. Smith MF, Patton JL (1999) Phylogenetic relationships and the radiation of sigmodontine rodents in South America: evidence from cytochrome b. J Mammal Evol 6:89–128CrossRefGoogle Scholar
  82. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. 3rd ed. W.H. Freeman, New YorkGoogle Scholar
  83. Stangl FB, Rodgers BE, Haiduk MW (1999) Ecological observations on the melanistic woodrats (Neotoma albigula) of black gap wildlife management area Brewster County of Trans-Pecos Texas. Texas J Sci 51:25–30Google Scholar
  84. Swofford DL (2003) PAUP*, Phylogenetic Analysis Using Parsimony (*and other methods), version 4.0b10Google Scholar
  85. Toledo VM (1988) La diversidad biológica de México. Ciencia y Desarrollo 14:17–30 Google Scholar
  86. Tsai LC, Huang MT, Hsiao CT, Lin ACY, Chen SJ, Lee JC, Hsieh HM (2007) Species identification of animal specimens by cytochrome b gene. Forensic Sci J 6:63–65Google Scholar
  87. Vargas-Contreras JA, Hernández-Huerta A (2001) Distribución actitudinal de la mastofauna en la Reserva “El Cielo”, Tamaulipas, Mexico. Acta Zool Mex 82:83–109Google Scholar
  88. Wiley EO, Mayden R (2000) The evolutionary species concept. In: Wheeler QD, Meier R (eds) Species concepts and phylogenetic theory: a debate. Columbia University Press, New York, pp 70–89Google Scholar
  89. Workman MS, Leamy LJ, Routman EJ, Cheverud JM (2002) Analysis of quantitative trait locus effects on the size and shape of mandibular molars in mice. Genetics 160:1573–1586PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Duke S. Rogers
    • 1
  • Rafael N. Leite
    • 2
  • Rustin J. Reed
    • 2
  1. 1.Department of Biology and Monte L. Bean LifeScience Museum, Brigham Young UniversityProvoUSA
  2. 2.Department of BiologyBrigham Young UniversityProvoUSA

Personalised recommendations