Abstract
We examined genealogical relationships among six of seven species of crested-tailed mice (Habromys chinanteco, H. delicatulus, H. ixtlani, H. lepturus, H. lophurus, and H. simulatus) using DNA sequence data from the cytochrome-b gene. Gene trees based on maximum likelihood, Bayesian inference and maximum parsimony were largely congruent in that H. lepturus and H. ixtlani were closely related and formed the sister group to H. lophurus. All analyses also arranged H. chinanteco and H. simulatus as sister taxa. These results are concordant with the phenetic groupings of Carleton et al. (2002) based on morphology. Our unweighted maximum parsimony trees did not resolve placement of H. delicatulus relative to other taxa. However, analyses using weighted maximum parsimony, maximum likelihood and Bayesian inference optimality criteria recovered a sister group relationship between H. delicatulus and the clade comprised of ((H. lepturus H. ixtlani)(H. lophurus)). This relationship differs from the overall phenetic similarity of H. delicatulus with H. simulatus and H. chinanteco, influenced by the small size of these three taxa, but is consistent with some derived features of the phallus (Carleton et al., 2002). Based on our sequence data, a specimen from Michoacán, México, recently assigned to Peromyscus sagax likely was inadvertently misidentified (Tiemann-Boege et al., 2000) and actually represents a new locality record for H. delicatulus. Finally, we comment on the conservation status of species of Habromys.
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Literature cited
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Auto Cont AC-19:716–723
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 37:529–540
Arriaga-Cabrera L, Espinoza JM, Aguilar C, Martínez E, y Loa E (2000) Regiones prioritarias terrestres de México. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, México, D.F.
Atelkar G, Dwarkadas S, Huelsenbeck JP, Ronquist F (2004) Parallel Metropolis-coupled Markov chain Monte Carlo for Bayesian phylogenetic inferences. Bioinformatics 20:407–415
Bailie J (1996a) Habromys lepturus. In: IUCN 2004. 2004 IUCN red list of threatened species
Bailie J (1996b) Habromys simulatus. In: IUCN 2004. 2004 IUCN red list of threatened species
Baker RH (1963) Geographical distribution of terrestrial mammals in Middle America. Am Mid Nat 70:208–249
Barker KF, Lanyon SM (2000) The impact of parsimony weighting schemes on inferred relationships among Toucans and Neotropical Barbets (Aves: Piciformes). Mol Phylogenet Evol 15:215–234
Bibb JJ, Van Etten RA, Wright CT, Walberg MW, Clayton DS (1981) Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–180
Björklund M (1999) Are third positions really that bad? A test using vertebrate cytochrome. B Cladistics 15:191–197
Bradley RD, Baker RJ (2001) A test of the genetic species concept: Cytochrome-b sequences and mammals. J Mammal 82:960–973
Bradley RD, Schmidly DJ, Kilpatrick CW (1996) The relationships of Peromyscus sagax to the P. boylii and P. truei species groups in Mexico based on morphometric, karyotypic, and allozymic data. In: Genoways HH, Baker RJ (eds) Contributions in mammalogy: A memorial volume in honor of J. Knox Jones, Jr. Museum of Texas Tech Univ., Lubbock, pp 95–106
Bradley RD, Carroll DS, Haynie ML, Muñiz Martínez R, Hamilton MJ, Kilpatrick CW (2004) A new species of Peromyscus from western Mexico. J Mammal 85:1184–1193
Carleton MD (1980) Phylogenetic relationships in neotomine-peromyscine rodents (Muroidea) and a reappraisal of the dichotomy with new world Cricetinae. Misc Publ Mus Zool Univ Mich 157:1–146
Carleton MD (1989) Systematics and evolution. In: Kirkland GL Jr, Layne JN (eds) Advances in the Study of Peromyscus (Rodentia). Texas Tech Univ. Press, Lubbock, pp 7–141
Carleton MD, Huckaby DG (1975) A new species of Peromyscus from Guatemala. J Mammal 56:444–451
Carleton MD, Sánchez O, Urbano Vidales G (2002) A new species of Habromys (Muroidea: Neotominae) from México, with generic review of species definitions and remarks on diversity patterns among Mesoamerican small mammals restricted to humid montane forests. Proc Biol Soc Wash 115:488–533
Challenger A (1998) Utilización y conservación de los ecosistemas terrestres de México: Pasado, presente y futuro. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Inst. de Biol., Univ. Nac. Autónom. De México, México, D.F.
Choate JR (1970) Systematics and zoogeography of middle American Shrews of the genus Cryptotis. Univ Kansas Publ Mus Nat Hist 19:195–317
Collins TM, Kraus F, Estabrook G (1994) Compositional effects and weighting of nucleotide sequences for phylogenetic analysis. Syst Biol 43:482–496
Durish ND, Halcomb KE, Kilpatrick CW, Bradley RD (2004) Molecular systematics of the Peromyscus truei species group. J Mammal 85:1160–1169
Edwards CW, Fulhorst CF, Bradley RD (2001) Molecular phylogenetics of the Neotoma albigula species group: Further evidence of a paraphyletic assemblage. J Mammal 39:783–791
Edwards CW, Bradley RD (2002) Molecular systematics of the genus Neotoma. Mol Phylogenet Evol 25:489–500
Engstrom MD, Dowler RC, Rogers DS, Schmidly DJ, Bickham JW (1981) Chromosomal variation within four species of harvest mice (Reithrodontomys). J Mammal 62:129–164
Ericson GP, Johansson US (2003) Phylogeny of Passerida (Aves: Passeriformes) based on nuclear and mitochondrial sequence data. Mol Phylogenet Evol 29:126–138
Farias IP, Ortí G, Sampaio I, Schneider H, Meyer A (2001) The cytochrome b gene as a phylogenetic marker: The limits of resolution for analyzing relationships among cichlid fishes. J Mol Evol 53:89–103
Fetzner JW Jr (1999) Extracting high quality DNA from shed reptile skins: A simplified method. Biotechniques 26:1052–1054
Funk CC (2005) A molecular phylogenetic analysis of the genus Habromys (Rodentia: Muridae). Unpublished Undergraduate Honors Thesis, Brigham Young University, Utah
Garner A, Rachlow JL, Hicks JF (2005) Patterns of genetic diversity and its loss in mammalian populations. Conserv Biol 19:1215–1221
Gene Codes (2000) Sequencher: Version 4.1.2. Gene Codes Corporation, Ann Arbor, Michigan
Geuten K, Smets E, Schols P, Yuan Y-M, Janssens S, Küpfer P, Pyck N (2004) Conflicting phylogenies of balsaminoid families and the polytomy in Ericales: Combining data in a Bayesian framework. Mol Phylogenet Evol 31:711–729
Goodwin GG (1964) A new species and a new subspecies of Peromyscus from Oaxaca, Mexico. Am Mus Novit 2183:1–8
Goldman EA (1951) Biological investigations of México. Smithsonian Misc Coll 115:1–476
Graybeal A (1993) The phylogenetic utility of cytochrome b: Lessons from bufonid frogs. Mol Phylogenet Evol 2:256–269
Gu X, Fu YX, Li WH (1995) Maximum likelihood estimation of the heterogeneity of substitution rate among nucleotide sites. Mol Biol Evol 12:546–557
Guindon S, Gascuel O (2003) PHYML -- A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704 (http://atgc.lirmm.fr/phyml)
Hafner MS, Gannon WL, Salazar-Bravo J, Alvarez-Castaneda ST (1997) Mammal collections in the western hemisphere: A survey and directory of existing collections. Allen Press, Lawrence, Kansas
Harris D, Rogers DS, Sullivan J (2001) Phylogeography of Peromyscus furvus (Rodentia; Muridae) based on cytochrome b sequence data. Mol Ecol 9:2129–2135
Hasegawa M, Kishino H, Yano T-A (1985) Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 2:160–174
Hästad O, Björklund M (1998) Nucleotide substitution models and estimation of phylogeny. Mol Biol Evol 15:1381–1389
Honeycutt RL, Nedhal MA, Adkins RM, Janecek LL (1995) Mammalian mitochondrial DNA evolution: A comparison of the cytochrome b and cytochrome c oxidase II genes. J Mol Evol 40:260–272
Hooper ET (1952) A systematic review of the harvest mice (Genus Reithrodontomys) of Latin America. Misc Publ Mus Zool Univ Mich 77:1–255
Hooper ET, Musser GG (1964) Notes on classification of the rodent genus Peromyscus. Occas. Pap Mus Zool Univ Mich 635:1–13
Huchon D, Madsen O, Sibbald MJJB, Ament K, Stanhope MJ, Catzelflis F, de Jong WW, Douzery EJP (2002) Rodent phylogeny and a timescale for the evolution of Glires: Evidence from an extensive taxon sampling using three nuclear genes. Mol Biol Evol 19:1053–1065
Huelsenbeck J, Ronquist F (2003) MrBayes3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Irwin DM, Kocher TD, Wilson AC (1991) Evolution of the cytochrome b gene of mammals. J Mol Evol 32:128–144
Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge, England
Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA data, and the branching order in Hominoidea. J Mol Evol 29:170–179
Kluge AG (1989) A concern for evidence and a phylogenetic hypothesis of relationships among Epicrates (Boidae, Serpentes). Syst Biol 8:7–25
Kumar S, Tamura K, Nei N (1993) MEGA: Molecular evolutionary genetics analysis, version 2. The Pennsylvania State University, University Park
Larget B, Simon DL (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16:750–759
Léon-Paniagua L, Romo-Vázquez E (1993) Mastofauna de la Sierra de Taxco, Guerrero. In: Medelín RA, Ceballos G (eds) Avances en el Estudio de los Mamíferos de México. Asoc Mex Mast, A.C. México, D.F., pp 45–64, Publ. Esp. No. 1
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 5:249–261
Merriam CH (1898) Descriptions of twenty new species and a new subgenus of Peromyscus from Mexico and Guatemala. Proc Biol Soc Wash 12:115–125
Metropolis NA, Rosenbluth A, Rosenbluth M, Teller A, Teller E (1953) Equations of state calculations by fast computing machines. J Chem Phys 21:1087–1092
Meyer A (1994) Shortcomings of the cytochrome b gene as a molecular marker. Trends Ecol Evol 9:278–280
Musser GG (1969) Notes on Peromyscus (Muridae) of Mexico and Central America. Am Mus Novit 2357:1–23
Osgood WH (1904) Thirty new mice of the genus Peromyscus from Mexico and Guatemala. Proc Biol Soc Wash 17:55–77
Osgood WH (1909) Revision of the mice of the American genus Peromyscus. North Am Fauna 28:1–285
Palumbi SR (1996) Nucleic acids I: The polymerase chain reaction. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics, 2nd edn. Sinauer, Sunderland, Massachusetts, pp 205–247
Peppers LL, Bradley RD (2000) Molecular systematics of the genus Sigmodon. J Mammal 81:332–343
Periera SL, Baker AJ, Wajntal A (2002) Combined nuclear and mitochondrial DNA sequences resolve generic relationships within the Cracidae (Galliformes, Aves). Syst Biol 51:946–958
Posada D (2003) Selecting models of evolution. In: Vandemme AM, Salemi M (eds) The phylogenetic handbook. Cambridge University Press, pp 256–282
Posada D, Crandall KA (1998) MODELTEST: Testing the model Of DNA substitution. Bioinformatics 14:817–818
Poux C, Douzery EJP (2004) Primate phylogeny, evolutionary rate variations, and divergence times: A contribution from the nuclear gene IRBP. Am J Phys Anthropol 124:1–16
Reeder SA, Carroll DS, Edwards CW, Kilpatrick CW, Bradley RD (2006) Neotomine-peromyscine rodent systematics based on combined analysis of nuclear and mitochondrial DNA sequences. Mol Phylogenet Evol 40:251–258
Robertson PB, Musser GG (1976) A new species of Peromyscus (Rodentia: Cricetidae), and a new specimen of P. simulatus from southern Mexico, with comments on their ecology. Occas Pap Mus Nat Hist Univ Kansas 47:1–8
Rodriquez FJ, Oliver F, Marin A, Medina JR (1990) The general stochastic model of nucleotide substitutions. J Theor Biol 142:485–501
Romo-Vázquez E, León-Paniagua L, Sánchez O (2005) A new species of Habromys (Rodentia: Neotominae) from México. Proc Biol Soc Wash 118:606–618
Snchez-Cordero V, Illoldi-Rangel P, Linaje M, Sarkar S, Peterson AT (2005) Deforestation and extant distributions of Mexican endemic mammals. Biol Conserv 126:465–473
Sanderson MJ, Shaffer HB (2002) Troubleshooting in molecular phylogenetic analysis. Annu Rev Ecol Syst 33:49–72
Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116
Smith MF, Patton JL (1993) The diversification of South American murid rodents: Evidence form mitochondrial DNA sequence data for the akodontine tribe. Biol J Linn Soc 50:149–177
Soltis PS, Soltis DE (2003) Applying the bootstrap in phylogeny reconstruction. Statistical Sci 18:256–267
Sullivan J, Arellano E, Rogers DS (2000) Comparative phylogeography of Mesoamerican highland rodents: concerted versus independent response to past climatic fluctuations. Amer Nat 155:755–768
Suzuki Y, Glazko GV, Nei M (2002) Overcredibility of molecular phylogenies obtained by Bayesian phylogenetics. Proc Natl Acad Sci USA 99:16138–16143
Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4.0b10, Sinauer Assoc., Sunderland, MA
Swofford DL, Olsen GJ, Waddell PJ, Hillis DM (1996) Phylogenetic inference. In: Hills DM, Moritz C, Mable BK (eds) Molecular systematics , 2nd edn. Sinauer Associates, Inc. Publishers, Sunderland, Massachusetts, pp 407–514
Tajima F (1993) Simple methods for testing molecular clock hypothesis. Genetics 135:599–607
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Teimann-Boege I, Kilpatrick CW, Schmidly DJ, Bradley RD (2000) Molecular phylogenetics of the Peromyscus boylii species group (Rodentia: Muridae) based on mitochondrial cytochrome b sequences. Mol Phylogenet Evol 16:366–378
Whiting AS, Bauer AS, Sites JW Jr (2003) Phylogenetic relationships and limb loss in sub-Saharan African Scincine lizards (Squamata: Scincidae). Mol Phylogenet Evol 29:583–598
Woodman N, Timm RM (1999) Geographic variation and evolutionary relationships among broad-clawed shrews of the Cryptotis goldmani group (Mammalia: Insectivora: Soricidae). Field Zool New Ser 9:1–35
Xia X (2000) Data analysis in molecular biology and evolution. Kluwer Academic Publishers, Boston
Xia X, Xie Z (2001) DAMBE: Data analysis in molecular biology and evolution. J Heredity 92:371–373
Yang Z (1994) Estimating the pattern of nucleotide substitution. J Mol Evol 39:105–111
Yang Z (1996a) Among-site rate variation and its impact on phylogenetic analysis. Trends Ecol Evol 11:367–372
Yang Z (1996b) Maximum-likelihood models for combined analyses of multiple sequence data. J Mol Evol 42:587–596
Yang ZH, Rannala B (1997) Bayesian phylogenetic inference using DNA sequences: A Markov Chain Monte Carlo method. Mol Biol Evol 14:717–724
Yang Z, Roberts D (1995) On the use of nucleic acid sequences to infer early branchings in the tree of life. Mol Biol Evol 12:451–458
Yoder AD, Yang Z (2000) Estimation of primate speciation dates using local molecular clocks. Mol Biol Evol 17:1081–1090
Yoder AD, Vilgalys R, Ruvulo M (1996) Molecular evolutionary dynamics of cytochrome b in strepsirrhine Primates: The phylogenetic significance of third-position transversions. Mol Biol Evol 13:1339–1350
Acknowledgments
We thank the following persons for their help in obtaining specimens or tissue loans that formed the basis of this report: E. Arellano, F.A. Cervantes, J. Dines, F.X. González-Cózatl, D.J. Harris, J. Martínez and T. Maxwell. Permits for field work in Mexico were issued by the Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT). R.M. Timm and T. Holmes kindly allowed us to sequence DNA from the skin of a Habromys chinanteco housed in the University of Kansas, Museum of Natural History. F.A. Cervantes generously allowed us to sequence a skin sample of a specimen from the type series of Habromys delicatulus housed in the Colección Nacional de Mamíferos, Universidad Nacional Autónoma de México. Financial support was provided by Professional Development Grants, Department of Integrative Biology and the M.L. Bean Life Science Museum, Brigham Young University (to DSR), the Honors Office and Office of Undergraduate Research, Brigham Young University (to CCF), the Ontario Graduate Student Scholarship program (to JRM), and the Royal Ontario Museum Foundation (to MDE). E. Arellano and F.X. González-Cózatl provided comments on an earlier version of this paper.
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Appendix
Appendix
Specimens examined are listed by taxon, collecting locality, museum acronym and voucher number and GenBank accession number. Museum acronyms (Hafner et al., 1997) are as follows: BYU=Monte L. Bean Life Science Museum, Brigham Young University; CMC=Colección de Mamíferos, del CEAMISH (Centro de Educación Ambiental e Investigación Sierra de Huautla), Universidad Autónoma del Estado de Morelos; CNMA=Colección Nacional de Mamíferos, Universidad Nacional Autónoma de México; LAF=Los Angeles County Museum; ROM=Royal Ontario Museum.
Habromys chinanteco: MEXICO; Oaxaca, N slope of Cerro Pelon, 31.6 km S Vista Hermosa, 2,650 m (KU 124131 – DQ861380).
Habromys delicatulus: MEXICO; México, Municipio Jilotepec, Dexcaní Alto, 2 km E and 3.5 km S Jilotepec, Cañada de la Ermita, 2,570 m (19°56′ N, 99°30′ W)(LAF 1801 – DQ861399, CNMA 22442–EF043236); Michoacn, Puerto Garnacia, 9,200 ft (AF155404*).
Habromys ixtlani: MEXICO; Oaxaca, Atepec, Llano de las Flores, Km 132 Carretera Tuxtepec-Oaxaca, 2,750 m (CNMA 29842 – DQ861391, CNMA 29845 – DQ861390); Distrito de Ixtlani, 28 km SW (by road) La Esperanza, 2,950 m (BYU 15271 – DQ861395, 15272 – DQ861394 and 15273 – DQ861393); Distrito de Ixtlani, 28 km SW (by road) La Esperanza, 17°35′08′′ N, 96°30′41′′ W, 2,950 m (CMC 56 – DQ861392).
Habromys lepturus: MEXICO; Oaxaca, Municipio Tlahuitoltepec, 16 km E Tlahuitoltepec, 2,750 (CNMA 29893 – DQ861386); Municipio Tlahuitoltepec, Santa María Yacochi, 3 km N Cerro Zempoaltepec, 2,450 m (CNMA 34867 – DQ861382 and 34869 – DQ861381); Municipio Tlahuitoltepec, Santa María Yacochi, 4.5 km N Cerro Zempoaltepec, 2,450 m (CNMA 33629 – DQ861384 and 33631 – DQ861383); Municipio Tlahuitoltepec, Santa María Yacochi, 3.5 km N Cerro Zempoaltepec, 2,750 m (CNMA 29972 – DQ861385); Municipio Tlahuitoltepec, vicinity Santa María Yacochi, 17°15′00′′ N, 96°00′45′′ W, 2,400 m (CMC 38 – DQ861387 and 85 – DQ861388); Municipio Tlahuitoltepec, vincinty Santa María Yacochi, 17°09′30′′ N, 96°01′00′′ W, 2,300 m (CMC 73 – DQ861389).
Habromys lophurus: GUATEMALA; Huehuetenango, 12 km NW of Santa Eulalia (ROM 98321 – DQ861396 and 98379 – DQ861398); Zacapa, 2 km. N of San Lorenzo (ROM 99834 – DQ861397).
Habromys simulatus: MEXICO; Oaxaca, Municipio Teotitlán, 1.5 km S Puerto de la Soledad, 18°09.742′ N, 96°59.852′ W, 2,600 m (BYU 15052 – DQ861404, 15053 – DQ861401, 16060 – DQ861403, 16061 – DQ861402 and 16063 – DQ861400).
Outgroup taxa
Megadontomys cryophilus: MEXICO; Oaxaca, Municipio Teotitlán, 1.5 km S Puerto de la Soledad, 18°09.742′ N, 96°59.852′ W, 2,600 m (BYU 16076 – DQ861373).
Neotomodon alstoni: MEXICO; Morelos, Huitzilac, Lagunas de Zempoala, 3 km W Huitzilac, 19°02.020′ N, 99°17.626′ W (BYU 15513 – DQ861374).
Peromyscus boylii: USA; Utah, Kane Co., Smoky Hollow, 37°09.41′ N, 111°32.10′ W, 1,270 m (BYU 19433 – DQ861379).
Peromyscus crinitus: USA; Utah, Kane Co., 59 km E, 25 km N Kanab, 1,450 m (BYU 18029 – DQ861378).
Peromyscus leucopus: MEXICO; San Luis Potosí, Municipio Xilitla, Ejido Aguayo, 6.2 km N Xilitla, 1,000 m (BYU 15919 – DQ861376).
Peromyscus megalops: MEXICO; Guerrero, 6.1 km N (by road) Omiltemi, 17°32.950′ N, 99°43.260′ W, 2,490 m (BYU 20755 – DQ861377).
Peromyscus truei: USA; Utah, Kane Co., Wolverine Petrified Forest, 37°48.0902′ N, 111°12.3641′ W, 1,840 m (BYU 20324 – DQ861375).
Reithrodontomys creper: COSTA RICA; Cartago, Rio Birris, 12 km N of Porter (ROM 97321 – DQ861372).
Scotinomys xerampelinus: COSTA RICA; Cartago, Parque Nacional Volcán Irazu (ROM 116812 – DQ861371).
*Listed as Peromyscus sagax in GenBank.
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Rogers, D.S., Funk, C.C., Miller, J.R. et al. Molecular Phylogenetic Relationships Among Crested-tailed Mice (Genus Habromys). J Mammal Evol 14, 37–55 (2007). https://doi.org/10.1007/s10914-006-9034-2
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DOI: https://doi.org/10.1007/s10914-006-9034-2