Journal of Mammalogy, 85(3):389–395, 2004
PHYLOGENETIC RELATIONSHIPS OF NEOTOMINE– PEROMYSCINE RODENTS: BASED ON DNA SEQUENCES FROM THE MITOCHONDRIAL CYTOCHROME-b GENE ROBERT D. BRADLEY,* CODY W. EDWARDS, DARIN S. CARROLL,
AND
C. WILLIAM KILPATRICK
Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409-3131, USA (RDB, CWE, DSC) Museum of Texas Tech University, Lubbock, TX 79409-3191, USA (RDB) Department of Biology, University of Vermont, Burlington, VT 05405-0086, USA (CWK) Present Address of CWE: Department of Biology, Stephen F. Austin State University, Nacogdoches, TX 75962, USA Present address of DSC: Center for Disease Control, 1600 Clifton Road, Atlanta, GA 30333, USA
DNA sequences obtained from the mitochondrial cytochrome-b gene were used to evaluate phylogenetic relationships among 15 genera of putative neotomine–peromyscine rodents. Tree topologies obtained from maximum likelihood and Bayesian analyses revealed 4 primary clades that, in general, conform to the 4 tribes proposed by Carleton (1980). The Peromyscini (Megadontomys, Ochrotomys, Osgoodomys, Peromyscus, and Reithrodontomys) was sister to the Neotomini (Hodomys, Neotoma, Onychomys, and Xenomys). These 2 clades were then joined by the Baiomyini (Baiomys and Scotinomys) and Tylomyini (Nyctomys, Ototylomys, and Tylomys). The most apparent departure from previously proposed arrangements involved the placement of Onychomys in the Neotomini instead of the Peromyscini. Key words:
Baiomyini, cytochrome-b sequences, Neotomini, Peromyscini, phylogenetics, Tylomyini
Members of the neotomine–peromyscine complex are among the most frequently encountered and studied species of rodents in North America. The diversity within this complex is extensive, ranging from 8 to 18 genera and well over 100 species. In addition, the composition and phylogenetic relationships within this complex has been the source of several investigations (Carleton 1980; Hooper and Musser 1964a, 1964b). At the root of many of these investigations and interpretations has been the questions of what constitutes the Neotomini and Peromyscini and what the phylogenetic relationships are within and between tribes. Most early treatises included the North and South American Cricetines in a single group, albeit at different taxonomic levels ranging from the tribe to family rank (Chaline et al. 1977; Ellerman 1940; Miller and Gridley 1918; Simpson 1945; Thomas 1896; Tullberg 1899). Rinker (1954) appears to have been the 1st to recognize a potential dichotomy within New World cricetines and used as examples the Sigmodon–Oryzomys complex and a Neotoma–Peromyscus complex. Likewise, Hooper and Musser (1964a) hypothesized that a division existed
within New World cricetines and suggested that 2 natural assemblages, South American cricetines and North American cricetines, be recognized. The latter group, containing 12 genera, was further divided into 2 tribes, neotomines (Neotoma, Xenomys, Ototylomys, and Tylomys) and peromyscines (Nelsonia, Baiomys, Scotinomys, Onchyomys, Ochrotomys, Neotomodon, Reithrodontomys, and Peromyscus). Since the classification provided by Hooper and Musser (1964a), several authors have refined or revised this arrangement. Carleton (1980) extensively investigated the morphological relationships of North American cricetines, and his subsequent classification serves as the cornerstone for all following comparisons. Carleton (1980) proposed the elevation of several subgenera of Peromyscus (Habromys, Podomys, Osgoodomys, Isthmomys, and Megadontomys) to generic level and their inclusion within Peromyscini. Likewise, Hodomys, formerly a subgenus within Neotoma, was treated as a separate genus in the Neotomini. In addition, Carleton (1980) removed Baiomys and Scotinomys from the Peromyscini and placed them in a separate tribe (Baiomyini) and removed Tylomys and Ototylomys from the Neotomini and placed them in the tribe Tylomyini. Musser and Carleton (1993) retained the basic composition of Carleton’s classification, with 2 exceptions: Baiomyini was returned to Peromyscini, and Tylomini, along with Nyctomys, Otonyctomys, and Rhagomys, was placed as incertae sedis. McKenna and Bell (1997) retained Carleton’s
* Correspondent:
[email protected]
Ó 2004 American Society of Mammalogists www.mammalogy.org 389
390
Vol. 85, No. 3
JOURNAL OF MAMMALOGY
(1980) Peromyscini and Neotomini but included Nyctomys and Otonyctomys in Tylomini, citing evidence from Reig (1984). In addition, McKenna and Bell (1997) placed Baiomys, Scotinomys, and Rhagomys as incertae sedis. In this paper, we have used DNA sequence data to examine relationships of 15 genera (following Musser and Carleton 1993) that have been proposed by several authors as being affiliated with either Neotomini or Peromyscini. Our goal was to develop a classification scheme reflecting phylogenetic relationships obtained from these DNA sequences.
MATERIALS AND METHODS Samples.—Twenty-eight species representing 15 genera were examined. Specimens were collected from natural populations or tissues were borrowed from collaborative institutions (Appendix I). All genera but Nelsonia, Habromys, Podomys, and Isthmomys were represented, and with the exception of monotypic genera, multiple individuals or species were examined per genus to verify sequence accuracy and taxon representation. Out-group taxa were selected following the various phylogenetic relationships depicted in Smith and Patton (1999). Specifically, several tribes showing sister-taxon affiliations with North American sigmodontines were included as out-group taxa. Although this, by default, assumes that North American sigmodontines are monophyletic, substantial evidence supports this conclusion (Engel et al. 1998; Smith and Patton 1999). DNA sequences for representative taxa of South American Sigmodontine rodents were obtained from GenBank and were used as outgroup taxa; these included (with GenBank accession numbers) Thomasomys gracilis (AF108674), Microryzomys minutus (AF108698), Abrothrix andinus (AF108671), Eligmodontia morgani (AF108691), Irenomys tarsalis (AFITU03534), Akodon boliviensis (M35691), Delomys sublineatus (AF108687), and Sigmodon hispidus (AF425212). All out-group sequences were reported by Smith and Patton (1999), except S. hispidus, which was reported by Peppers and Bradley (2000). Data collection.—Mitochondrial DNA was extracted from tissue and purified using the Wizard Miniprep kit (Promega, Madison, Wisconsin). The entire cytochrome-b gene was amplified using the polymerase chain reaction (Saiki et al. 1988) with the following parameters: 39 cycles of 928C (15 s) denaturing, 508C annealing (1 min), and 728C (1 min, 10 s) extension, followed by 1 cycle of 728C (4 min). Amplification reactions were performed in 50-ll volumes, 10 mM Tris-HCl pH 8.3, 50 mM KCl, 2 mM MgCl2, 1-lM primer concentration, and 1.25 U of Taq (Fisher Scientific, Pittsburgh, Pennsylvania). PCR primers were those used by Smith and Patton (1993; MVZ05) and Irwin et al. (1991; H15915), respectively. Amplified products were purified with silica gel using QIAquick PCR Purification Kit (Qiagen, Valencia, California). Amplicons were sequenced with dye-labeled terminators (PE Applied Biosystems, Foster City, California) and about 60 to 80 ng of DNA using cycle sequencing conditions of 958C (30 s) denaturing, 508C (20 s) annealing, and 608C (3 min) extension. Eight primers were used in the sequencing protocol: 2 (MVZ05 and H15915) that were used in PCR amplification (Irwin et al., 1991; Smith and Patton 1993), 3 (400R, 700L, and WDRAT 1100) were reported in Peppers and Bradley (2000), and 3 (400F, WDRAT 650, and CWE1) were reported in Edwards et al. (2001). Following 25–29 cycles, reactions were then ethanol precipitated. Sequences for heavy and light strands were analyzed using the ABI-Prism 310 Genetic Analyzer (PE Applied Biosystems, Foster City, California). Sequences were aligned and proofed using Sequencher 5.0 software (Bromberg et al. 1995).
Data analysis.—Maximum parsimony analyses were conducted using PAUP software (version 4.0b10—Swofford 2002). Variable nucleotide positions were treated as unordered, discrete characters with 4 possible character states: A, C, G, and T. Uninformative characters were excluded from all parsimony analyses. Four nucleotide weighting schemes were employed in the parsimony analyses. These included equal weighting for all characters and downweighting of transitions by a factor of 2.1 (calculated from the average transition:transversion ratio of in-group taxa), and to offset potential saturation affects, transitions were eliminated in 1 analysis (transversions only) and 3rd positions removed in another. Nucleotide sequences were weighted using MacClade software (version 3.04— Maddison and Maddison 1992) and subsequently analyzed using the maximum parsimony option of PAUP. Optimal trees were estimated using the heuristic search method with tree bisection-reconnection branch swapping and stepwise addition sequence options. Robustness and nodal support for individual clades were evaluated using 1,000 heuristic bootstrap iterations (Felsenstein 1985), and Bremer decay indices (Bremer 1994) were calculated using PAUP and the Autodecay program (Eriksson 1997). The GTRþIþc model of evolution was identified by the MODELTEST software (version 3.06—Posada and Crandall 1998) as significantly better than alternative models in best fitting the data. The GTRþIþc model subsequently was used in a maximum likelihood analysis (heuristic search option in PAUP). Parameters for this model included the proportion of invariable sites (I ¼ 0.4178), gamma distribution shape (c ¼ 0.5786), and base compositions estimated from the data (A ¼ 0.3804, C ¼ 0.3355, G ¼ 0.0692, and T ¼ 0.2149). The software program MrBayes (Huelsenbeck and Ronquist 2001), based on a GTR model of evolution with no prior assumptions, was used to construct a topology and posterior clade probabilities. In this analysis, the following parameters were employed: 4 Markov chains, 2 106 generations, and sampled every 100th generation. Following an inspection of likelihood scores, the first 300 trees were discarded, and the program was rerun using the remaining stable likelihood values. A consensus tree (50% majority rule) was constructed from remaining trees. The Shimodaira and Hasegawa (1999) test was used to test for significance among tree topologies generated in this study and that depicted in Carleton (1980). In these tests, the likelihood tree generated herein was constrained to match that of Carleton (1980).
RESULTS Four weighting schemes (equal weights, transitions downweighted by factors of 2.1, transversions only, and 1st and 2nd positions only) were evaluated under a parsimony framework. The equal weighting scheme is discussed in detail in the following, and the resulting topology is presented in Figure 1; topologies resulting from the other weighting schemes are not shown but are compared relative to the topology presented in Figure 1. For ease of comparison, in most instances taxa are referred to by their generic names. Two trees (3,938 steps, consistency index [CI ] ¼ 0.238, retention index [ RI ] 0.375) were obtained from the analysis in which characters were weighted equally. A strict consensus tree (Fig. 1) was generated, and 4 major clades (I–IV) were identified. Clade I contained samples representing 6 genera (Hodomys, Xenomys, Neotoma, Onychomys, Ochrotomys, and Reithrodontomys) and formed a sister relationship to clade II, which contained samples from 4 genera (Megadontomys, Peromyscus,
June 2004
BRADLEY ET AL.—PHYLOGENETICS OF RODENTS
391
FIG. 1.—Strict consensus tree of the 2 most parsimonious trees generated from the analysis using equal weighting of characters. Roman numerals refer to major clades as identified in the text. Bootstrap values are shown above branches, and Bremer support indices are shown below.
Neotomodon, and Osgoodomys). Clade III contained samples of Baiomys and Scotinomys and was sister to the larger clade formed by clades I and II. Clade IV contained members of 3 genera (Nyctomys, Ototylomys, and Tylomys) and was the most basal clade. Bootstrap and Bremer support values (Fig. 1) for the sister relationship within and between clades I and II were very low; however, strong support was apparent for the association and placement of clades III and IV relative to the other clades. When transitions were downweighted by a factor of 2.1 (estimated from the data), 2 trees were obtained (CI ¼ 0.240, RI ¼ 0.423). A strict consensus tree revealed 4 clades similar in composition to those obtained previously, except that clades II and III formed a sister relationship. Analyses where only transversions were considered (2 trees, CI ¼ 0.230, RI ¼
0.531) produced similar results to those in the 2.1 weighting scheme. The exceptions were that Onychomys, Ochrotomys, and Reithrodontomys were removed from clade I and were placed basally in clade II. In each of these analyses, bootstrap and Bremer support values were very low within and between clades II and III but showed similar or stronger support for the placement of clades I and IV compared to those presented in Figure 1. The analyses in which 3rd positions were removed (8 trees, CI ¼ 0.312, RI ¼ 0.497) produced a similar topology to that obtained in the unweighted analysis. However, in these analyses, members of clades I and II were combined into a single clade whose internal topology was mostly unresolved. Support values were very low, except for clades III and IV.
392
JOURNAL OF MAMMALOGY
The maximum likelihood and Bayesian inference methods produced nearly identical results. Only the tree and associated clade probability values generated from the Bayesian inference analysis are presented (Fig. 2). In these analyses, 4 clades were obtained. The 1st clade (I) contained samples of Hodomys, Xenomys, Neotoma, and Onychomys. Clade II contained samples representing 6 genera (Megadontomys, Osgoodomys, Peromyscus, Neotomodon, Reithrodontomys, and Ochrotomys). Clade III contained samples of Baiomys and Scotinomys, whereas clade IV included samples of Nyctomys, Tylomys, and Ototylomys. Clade probability values (Fig. 2) were high (.95) in most cases. The only difference between maximum likelihood and Bayesian analyses involved the relationship between the 2 species of Onychomys. In the likelihood analysis, the 2 taxa were added to clade I in a stepwise fashion. However, in the Bayesian inference analysis, the 2 taxa formed a sister relationship prior to joining clade I.
DISCUSSION Parsimony methods (including a variety of weighting schemes) generated topologies that were poorly supported when examined with bootstrap and Bremer support tests. In most cases, clades collapsed, producing unresolved relationships among taxa. This was most apparent for nodes near the middle of the tree, especially at the base of clades containing the peromyscines and neotomines. The only strongly supported clades in the parsimony analyses were the Baiomyine clade and the clade containing the Peromyscines, Neotomines, and Baiomyines. Therefore, parsimony failed to recover strongly supported phylogenetic patterns critical to resolving questions concerning relationships among the 4 tribes. In addition, given the potential for weighted parsimony analyses to overestimate bootstrap support (Sullivan et al. 1997; Yang et al. 1995), few constructive inferences (strongly supported) can be drawn from the results generated by the parsimony analyses. Therefore, the discussion will emphasize results obtained from the likelihood and Bayesian methods. Maximum likelihood and Bayesian analyses each produced 4 clades (I–IV; Fig. 2) that were identical in content. These clades appear to represent natural groupings and are similar in content to the tribes described by Carleton (1980). Therefore, the tribal nomenclature proposed by Carleton (1980) is used to discuss phylogenetic relationships within and between the 4 clades generated in this study. The suggested classification is presented in Appendix I. Neotomini.—Clade I contained Neotoma, Hodomys, Xenomys, and Onychomys. With the exception of Onychomys, this arrangement corresponds to Carleton’s (1980) vision of the Neotomini. In our study, Onychomys was placed as the basal member of the Neotomini clade and, although surprising, may be explained by at least 2 scenarios. First, the phylogenetic affiliation of Onychomys may be difficult to determine. Carleton (1980) realized a similar problem in placing Onychomys in that, depending on the type of characters or analyses, it was placed with either the Peromyscini or the Baiomyini. Similarly, the study of the mitochondrial ND3/4 region by Engel et al. (1998) placed Onychomys inside the clade containing several species of
Vol. 85, No. 3
Peromyscus. Given these inconsistencies in the placement of Onychomys, it may be that Onychomys represents an early and separate offshoot from the neotomine–peromyscine lineage. If a rapid radiation of neotomines and peromyscines occurred, then Onychomys may share few synapomorphies with either group and consequently can be placed basal to either lineage. Second, our study did not include Nelsonia, which may represent the basal branch of the Neotomini clade, and this omission may have forced Onychomys from a basal position in the Peromyscini clade into the basal position of the Neotomini clade. However, when Onychomys was constrained into the peromyscine clade (II), sensu Carleton (1980), a significantly worse tree (P ¼ 0.004, SH test—Shimodaira and Hasegawa 1999) was obtained when compared to the tree generated from the raw data (Fig. 2), thus allowing the rejection of the hypothesis of Onychomys placement within the Peromyscines. Unfortunately, we were unable to successfully generate sequence data for Nelsonia and thus were unable to evaluate Carleton’s (1980) placement of Nelsonia in the Neotomini. However, sufficient data exist to support the inclusion of Nelsonia in the Neotomini (Carleton 1980; Goldman 1910). Additionally, data generated herein and by Edwards and Bradley (2002) support Carleton’s (1980) recognition of Hodomys as a valid genus with a sister-taxon relationship to Xenomys instead of being placed as a subgenus in Neotoma. Peromyscini.— Clade II contained 6 genera (Megadontomys, Osgoodomys, Peromyscus, Neotomodon, Reithrodontomys, and Ochrotomys). However, the placement of Reithrodontomys and Ochrotomys should be viewed cautiously, as they were not supported by Bayesian posterior probability values. Peromyscus, Megadontomys, Osgoodomys, and Neotomodon formed a monophyletic clade that was sister to Reithrodontomys, consistent with the phylogenetic relationships proposed by Hooper and Musser (1964b). This arrangement contradicts that of Carleton (1980), which placed Reithrodontomys as sister to Peromyscus (sensu stricto) followed by the addition of the remaining genera (formerly subgenera of Peromyscus). Although these relationships differ substantially, the assessment of the phylogenetic relationships among Peromyscus (sensu stricto—Carleton 1980, 1989) and genera formerly considered as subgenera within Peromyscus is beyond the scope of this study. To properly investigate this question, a more holistic approach and broader taxonomic coverage will be necessary than was available herein. This Peromyscus (and allies)–Reithrodontomys clade was joined, basally, by Ochrotomys. This basal position of Ochrotomys supports the observations of Carleton (1989) and Engstrom and Bickham (1982) that it is quite divergent from the other peromyscines. Carleton (1989) further postulated that Ochrotomys eventually may merit recognition as a separate tribe. The DNA sequence data are compatible with the idea that Ochrotomys represents an early offshoot of the peromyscine lineage but suggests that it be aligned with the peromyscines, although the Bayesian support value (80) was nonsupportive. Of the 4 clades recognized in this study, the peromyscine clade received the least amount of support, probably reflecting the association of Ochrotomys with the remaining members of the
June 2004
BRADLEY ET AL.—PHYLOGENETICS OF RODENTS
393
FIG. 2.—Maximum likelihood tree calculated using Bayesian inference methods. Roman numerals refer to major clades as identified in the text. Clade probability values are shown above branches.
clade. Taxonomically, 2 choices are available: either remove Ochrotomys from the peromyscines and treat it as a distinct tribe or, alternatively, recognize Ochrotomys as a divergent, basal member that is loosely affiliated with this clade. Until additional data are available, we recommend the latter. Baiomyini.—The 3rd clade (III) contained only Baiomys and Scotinomys. Although this relationship supports the contention of Hooper (1960), Hooper and Musser (1964a), Carleton (1980), and Carleton et al. (1975) that Baiomys and Scotinomys are sister taxa instead of being related to other South American genera (Packard 1960), the assumption of monophyly of the North American sigmodontine rodents prevents objective testing of Packard’s (1960) hypothesis. Additionally, the monophyletic nature of this clade supports Carleton’s (1980) view of the Baiomyini as a separate tribe but contradicts the more recent view of Musser and Carleton (1993) that these taxa be placed within the Peromyscini. If Baiomys and Scotinomys
are constrained into the peromyscine clade (II), a significantly worse tree (P ¼ 0.006, SH test—Shimodaira and Hasegawa 1999) was obtained compared to the tree generated from the raw data (Fig. 2), suggesting that the Baiomyini should be considered a separate tribe. Tylomyini.— The 4th clade (IV) contained only Tylomys, Ototylomys, and Nyctomys. The relationship of Tylomys and Ototylomys as sister taxa separate from the neotomines contradicts Hooper’s (1960) and Hooper and Musser’s (1964a) hypothesis but supports Carleton’s (1980) assessment that they diverged prior to the origin of the neotomines and peromyscines. The addition of Nyctomys to this group confirms Carleton’s (1980) suspicion that these 3 genera represent a basal group to the other Neotomini–Peromyscini rodents. Additionally, our data tentatively support the conclusions of Haiduk et al. (1988) and Voss and Linzey (1981) in refuting the association of Nyctomys with the South American sigmodon-
394
JOURNAL OF MAMMALOGY
tines as proposed by Engel et al. (1998) and Hershkovitz (1962). However, additional representatives of South American tribes are needed to verify the placement of Nyctomys given that we have treated Nyctomys as an in-group taxon. Based on the data from the mitochondrial cytochromeb gene, it seems appropriate to classify the North American Sigmodontines into the 4 tribes sensu Carleton (1980). In addition, we propose that Nyctomys be added to the Tylomyini. Future studies should include Nelsonia to determine if it is a member of the Neotomini as suggested by Carleton (1980). Additionally, as Otonyctomys has been proposed as the sisterspecies relationship to Nyctomys (Carleton 1980), it should be investigated to determine if it is a member of the Tylomyini.
RESUMEN Secuencias de ADN obtenidas del gen cytochrome b fueron usadas para evaluar las relaciones filogene´ticas entre 15 ge´neros de roedores pertenecientes a los grupos neotomine–peromyscine. Tres topologı´as obtenidas a trave´s de probabilidad ma´xima y ana´lisis de Bayesian revelaron 4 grupos primarios que, en general, se conforman a las 4 tribus propuestas por Carleton (1980). La tribu Peromyscini (Megadontomys, Ochrotomys, Osgoodomys, Peromyscus, y Reithrodontomys) resulto´ hermana a la tribu Neotomini (Hodomys, Neotoma, Onychomys, y Xenomys). Estos 2 grupos se adhieren a las tribus Baiomyini (Baiomys y Scotinomys) y Tylomyini (Nyctomys, Ototylomys, y Tylomys). La diferencia ma´s grande a los arreglos propuestos previamente fue la posicio´n de Onychomys en la tribu Neotomini en vez de en la tribu Peromyscini.
ACKNOWLEDGMENTS We thank B. Amman and N. Durish for providing some of the DNA sequences. M. D. Engstrom (Royal Ontario Museum) and R. J. Baker (Museum, Texas Tech University) kindly provided tissue loans. B. R. Amman, M. L. Haynie, S. A. Reeder, J. Hanson, J. R. Suchecki, and F. Mendez-Harclerode provided helpful comments on previous revisions of this manuscript. Animal care and use procedures followed guidelines approved by the American Society of Mammalogists (Animal Care and Use Committee 1998). This research was supported by a grant from the National Institutes of Health (DHHS A141435-01 to R. D. Bradley).
LITERATURE CITED ANIMAL CARE AND USE COMMITTEE. 1998. Guidelines for the capture, handling, and care of mammals as approved by the American Society of Mammalogists. Journal of Mammalogy 79:1416–1431. BREMER, K. 1994. Branch support and tree stability. Cladistics 10:295–304. BROMBERG, C. H., ET AL. 1995. Sequencher. Gene Codes Corporation, Ann Arbor, Michigan. CARLETON, M. D. 1980. Phylogentic relationships in neotomineperomyscine rodents (Muridae) and a reappraisal of the dichotomy within New World cricetinae. Miscellaneous Publications, Museum of Zoology, University of Michigan 157:1–146. CARLETON, M. D. 1989. Systematics and evolution. Pp. 7–142 in Advances in the study of Peromyscus. (G. L. Kirkland, Jr., and J. N. Layne, eds.). Texas Tech University Press, Lubbock.
Vol. 85, No. 3
CARLETON, M. D., E. T. HOOPER, AND J. HONACKI. 1975. Karyotypes and accessory reproductive glands in the rodent genus Scotinomys. Journal of Mammalogy 56:916–921. CHALINE, J. P. Mein, AND F. PETTER. 1977. Les grandes lignes d’une classification e´volutive des Muroidea. Mammalia 41:245–252. EDWARDS, C. W., AND R. D. BRADLEY. 2002. Molecular systematics of the genus Neotoma. Molecular Phylogenetics and Evolution 25: 489–500. EDWARDS, C. W., C. F. FULHORST, AND R. D. BRADLEY. 2001. Molecular phylogenetics of the Neotoma albigula species group: further evidence of a paraphyletic assemblage. Journal of Mammalogy 82:267–279. ELLERMAN, J. R. 1940. The families and genera of living rodents. Vol. 1. Rodents other than Muridae. British Museum of Natural History, London, United Kingdom. ENGEL, S. R., K. M. HOGAN, J. F. TAYLOR, AND S. K. DAVIS. 1998. Molecular systematics and paleobiogeography of the South American sigmodontine rodents. Molecular Biology and Evolution 15:35–49. ENGSTROM, M. D., AND J. W. BICKHAM. 1982. Chromosome banding and phylogenetics of the golden mouse, Ochrotomys nuttalli. Genetica 59:119–126. ERIKSSON, T. 1997. Autodecay 3.03. Botaniska Institution, Stockholm University, Stockholm, Sweden. FELSENSTEIN, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. GOLDMAN, E. A. 1910. Revision of the wood rats of the genus Neotoma. North American Fauna 31:1–124. HAIDUK, M. W., C. SANCHEZ-HERNANDEZ, AND R. J. BAKER. 1988. Phylogenetic relationships of Nyctomys and Xenomys to other cricetine genera based on data from G-banded chromosomes. Southwestern Naturalist 33:397–403. HERSHKOVITZ, P. 1962. Evolution of neotropical cricetine rodents (Muridae), with special reference to the phyllotine group. Fieldiana Zoologica 46:1–524. HOOPER, E. T. 1960. The glans penis in Neotoma (Rodentia) and allied genera. Occasional Papers of the Museum of Zoology, University Michigan 618:1–20. HOOPER, E. T., AND G. G. MUSSER. 1964a. The glans penis in neotropical cricitines (family Muridae) with comments on classification of muroid rodents. Miscellaneous Publications, Museum of Zoology, University of Michigan 123:1–57. HOOPER, E. T., AND G. G. MUSSER. 1964b. Notes on classification of the rodent genus Peromyscus. Occasional Publications of the Museum of Zoology, University of Michigan 635:1–13. HUELSENBECK, J. P., AND F. R. RONQUIST. 2001. MrBayes: Bayesian inference for phylogeny. Biometrics 17:754–756. IRWIN, D. M., T. D. KOCHER, AND A. C. WILSON. 1991. Evolution of the cytochrome b gene in mammals. Journal of Molecular Evolution 2:37–55. MADDISON, W. P., AND D. R. MADDISON. 1992. MacClade 3.04. Sinauer Associates, Inc., Publishers, Sunderland, Massachusetts. MCKENNA, M. C., AND S. K. BELL. 1997. Classification of mammals above the species level. Columbia University Press, New York. MILLER, G. S., AND J. W. GRIDLEY. 1918. Synopsis of the supergeneric groups of rodents. Journal of the Washington Academy of Sciences 8:431–448. MUSSER, G. G., AND M. D. CARLETON. 1993. Family Muridae. Pp. 501–755 in Mammal species of the world: a taxonomic and geographic reference. 2nd ed. (D. E. Wilson and D. M. Reeder, eds.). Smithsonian Institution Press, Washington, D.C.
June 2004
BRADLEY ET AL.—PHYLOGENETICS OF RODENTS
PACKARD, R. L. 1960. Speciation and evolution of the pygmy mice, genus Baiomys. University of Kansas Publication, Museum of Natural History 9:579–670. PEPPERS, L. L., AND R. D. BRADLEY. 2000. Cryptic speciation in Sigmodon hispidus: evidence from DNA sequences. Journal of Mammalogy 81:332–343. POSADA, D., AND K. A. CRANDALL. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818. REIG, O. A. 1984. Distribuc¸a˜o geogra´phica e histo´ria evolutiva dos reodores muroides sulamericanos (Cricetidae: Sigmodontidae). Revista Brasileira de Genetica 7:333–365. RINKER, G. C. 1954. The comparative myology of the mammalian genera Sigmodon, Oryzomys, Neotoma, and Peromyscus (Cricetinae), with remarks on their intergeneric relationships. Miscellaneous Publications, Museum of Zoology, University of Michigan 83:1–124. SAIKI, R. K., ET AL. 1988. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487–491. SHIMODAIRA, H., AND M. HASEGAWA. 1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16:114–116. SIMPSON, G. G. 1945. The principles of classification and a classification of mammals. Bulletin of the American Museum of Natural History 85:1–350. SMITH, M. F., AND J. L. PATTON. 1993. The diversification of South American rodents: evidence from mitochondrial sequence data for the akodontine tribe. Biological Journal of the Linnean Society 50:149–177. SMITH, M. F., AND J. L. PATTON. 1999. Phylogenetic relationships and the radiation of sigmodontine rodents in South America: evidence from cytochrome b. Journal of Mammalian Evolution 6: 89–128. SULLIVAN, J., J. A. MARKERT, AND C. W. KILPATRICK. 1997. Phylogeography and molecular systematics of the Peromyscus aztecus species group (Rodentia: Muridae) inferred using parsimony and likelihood. Systematic Biology 46:426–440. SWOFFORD, D. L. 2002. PAUP*: phylogenetic analysis using parsimony (*and other methods), Version 4.0b10. Sinauer Associates, Inc., Publishers, Sunderland, Massachusetts. THOMAS, O. 1896. On the genera of rodents: an attempt to bring up to date the current arrangement of the order. Proceedings of the Zoological Society of London 1896:1012–1028. TULLBERG, T. 1899. Ueber das System der Nagethiere, eine phylogenetische Studie. Acta Societatis Medicorum. Upsaliensis 3:1–514. VOSS, R. S., AND A. V. LINZEY. 1981. Comparative gross morphology of male accessory glands among neotropical Muridae (Mammalia: Rodentia) with comments on systematic implications. Miscellaneous Publications, Museum of Zoology, University of Michigan 159:1–41.
395
YANG, Z., N. GOLDMAN, AND A. FRIDAY. 1995. Maximum likelihood trees from DNA sequences: a peculiar statistical estimation problem. Systematic Biology 44:384–399.
Submitted 25 April 2003. Accepted 13 May 2003. Associate Editor was Eric A. Rickart.
APPENDIX I Taxa examined in this study are listed here and arranged by tribes in the form of a suggested classification based on the results presented herein. GenBank accession numbers also are provided. Classification
Taxon
GenBank number
Neotomini Hodomys Neotoma
Onychomys Xenomys
Hodomys alleni Neotoma cinerea N. leucodon N. mexicana Onychomys arenicola O. leucogaster Xenomys nelsoni
AF186801 AF186799 AF186828 AF294345 AY195793 AY195794 AF307838
Megadontomys thomasi Neotomodon alstoni Neotomodon alstoni Ochrotomys nuttalli Osgoodomys banderanus Peromyscus attwateri P. beatae P. californicus P. eremicus P. leucopus P. maniculatus P. winkelmanni P. zarhynchus Reithrodontomys fulvescens R. raviventris R. sumichrasti
AY195795 AY195796 AY195797 AY195798 AF155383 AF155384 AF131921 AF155393 AY195799 AF131926 AF119261 AF131930 AY195800 AF176257 AF176255 AF176256
Baiomys taylori B. musculus Scotinomys xerampelinus
AF548469 AF548487 AF108706
Nyctomys sumichrasti Ototylomys phyllotis O. phyllotis Tylomys nudicaudus
AY195801 AY009788 AY009789 AF307839
Peromyscini Megadontomys Neotomodon Ochrotomys Osgoodomys Peromyscus
Reithrodontomys
Baiomyini Baiomys Scotinomys Tylomini Nyctomys Ototylomys Tylomys
