On-line version ISSN 0717-6538
Gayana (Concepc.) vol.71 no.2 Concepción 2007
Gayana 71(2): 187-194, 2007. Comunicación breve
DEFINITION AND DIAGNOSIS OF A NEW TRIBE OF SIGMODONTINE RODENTS (CRICETIDAE: SIGMODONTINAE), AND A REVISED CLASSIFICATION OF THE SUBFAMILY
DEFINICION Y DIAGNOSIS DE UNA TRIBU DE ROEDORES SIGMODONTINOS (CRICETIDAE: SIGMODONTINAE), Y UNA CLASIFICACION REVISADA DE LA SUBFAMILIA
Guillermo D'Elía1, Ulyses F. J. Pardiñas2, Pablo Teta3, & James L. Patton4
1Departamento de Zoología, Universidad de Concepción, casilla 160-C, Concepción, Chile. Email: email@example.com
2Centro Nacional Patagónico, Casilla de Correo 128, Puerto Madryn, Chubut, Argentina.
3Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Avenida Intendente Güiraldes 2160, Pabellón II, 4º Piso (C1428EHA), Ciudad Autónoma de Buenos Aires, Argentina.
4Museum of Vertebrate Zoology, University of California, Berkeley, 3101 Valley Life Sciences Building, Berkeley, CA, 94720 USA.
A new tribe of sigmodontine rodents is formally defined and diagnosed. The tribe contains the extant genera Abrothrix (including Chroeomys), Chelemys, Geoxus, Pearsonomys, and Notiomys, a group of taxa distributed in the central and southern Andes and lowlands both east and west of the cordillera. The new tribe presents a unique combination of characters including nasals and premaxilla usually projected anterior to the incisors, moderately trumpeted; zygomatic plate with upper free border reduced or obsolete; and third upper molar reduced and sub-cylindrical in out-line with an internal ring-like enamel fossette. Molecular phylogenetic analyses indicate that Abrothrix is sister to a clade containing the remaining genera of the new tribe.
Keywords: Abrothrix, Chelemys, Chroeomys, Geoxus, Pearsonomys, Notiomys, South America, classification.
With approximately 84 extant genera, cricetids of the subfamily Sigmodontinae (Reig 1980) are one of the most diverse and complex groups of New World mammals. Notably, new sigmodontine taxa are still being erected on the basis of both newly discovered species (e.g., Pardiñas et al. 2005) and from revisionary museum work (e.g., Weksler et al. 2006). Distributed predominantly in South America, sigmodontines also reach Central and North America, and one extant genus is endemic to the Galapagos Islands (D'Elía 2003a).
Sigmodontine genera have been arranged into different groups, most of which have been given the formal rank of tribes (e.g., Hershkovitz 1966; Reig 1980). In the last 15 years phylogenetic analyses using either or both morphological and molecular data have been used to delimit these groups (e.g., Braun 1993; Smith & Patton 1993, 1999; Steppan 1995; D'Elía 2003b; Pacheco 2003; Weksler, 2003; D'Elía et al. 2003, 2005, 2006a, 2006b), causing several instances of major reconsiderations on their limits and contents. One of the most surprising results of DNA sequences phylogenies was a clade of taxa (Abrothrix, Chelemys, Chroeomys, Geoxus, Notiomys, and Pearsonomys), distributed primarily in the South and Central Andes and traditionally considered to be typical akodontine rodents (and in some cases even considered subgenera of Akodon [e.g., Reig 1987]), which do not form part of the akodont radiation (Smith & Patton 1999; D'Elía 2003b; see also the allozyme based studies of Spotorno et al. 1990 and Barrantes et al. 1993). Smith & Patton (1999:106-107) recommended ranking this group of genera as a tribe, suggesting that an adequate name for it would be Abrotrichini. Although these authors enumerated chromosomal, protein, and parasite features that may be used to diagnose the group, they made no formal definition or diagnosis (e.g., Musser & Carleton, 2005: 1087). Here we provide such a definition and diagnosis. We base our revised classification on the results and conclusions of Carleton (1980), Reig (1980, 1987), Smith & Patton (1993, 1999), Steppan (1995), Engel et al. (1998), D'Elía (2003b), Weksler (2003, 2006), Jansa & Weksler (2004), Percequillo et al. (2004), Steppan et al. (2004), D'Elía et al. (2003, 2005, 2006a, 2006b), Musser & Carleton (2005), and Weksler et al. (2006) and our assessment of qualitative characters. We recognize a new tribe of Sigmodontinae (family Cricetidae) that we describe as follows.
Abrotrichini, new tribe
Type genus.¾Abrothrix Waterhouse, 1837.
Contents.¾Abrothrix Waterhouse, 1837 (including Chroeomys Thomas, 1916; Habrothrix Wagner, 1843), Chelemys Thomas, 1903, Geoxus Thomas, 1919, Notiomys Thomas, 1890, and Pearsonomys Patterson, 1992.
Definition.¾The clade composed of the last common ancestor of Abrothrix, Chelemys, Geoxus, Notiomys, and Pearsonomys and all of its descendants.
Diagnosis.¾A tribe of the subfamily Sigmodontinae (sensu Reig 1980) grouping mice of small to medium size (from approximately 20 g in Notiomys edwardsii to 75 g in Chelemys macronyx) distinguishable by the following combination of characters: pelage long and soft; tail typically short and well haired; feet large and strongly built, with naked palms; claws equally robust on fore- and hind-feet (Gyldenstolpe 1932; Osgood 1943); skull with long muzzle and rounded braincase, without frontal or lambdoid crests; interorbital region amphora-shaped; nasals and premaxillae slightly projected anterior to the incisors to somewhat trumpeted; nasals longer than frontals; zygomatic plate typically narrow, with the upper free border reduced or absent; infraorbital foramen wide; frontal sinuses moderately developed; palate long; anterior border of mesopterygoid fossa square shaped; mandibular ramus generally gracile and elongated, except in Chelemys (Gyldenstolpe 1932; Osgood 1943; Reig 1987); upper incisors broad and ungrooved; teeth brachyodont to mesodont; upper and lower molars with labial and lingual cusps arranged in opposite or slightly alternate pairs; first upper/lower molars with reduced, fan-shaped, procingulum and shallow or absent anteroflexus(id); first upper molars with a very shallow to obsolete anteromedian flexus; para- and metaflexus strongly oriented backward to transversely oriented; paracone globose and oriented forward, mesoloph(id) poorly to moderately developed, usually fused to the paracone; third upper molars reduced and sub-cylindrical in outline, except in Chelemys, with an internal ring-like enamel fossette (Gyldenstolpe 1932; Reig 1987; D'Elía et al. 2006a). Axial skeleton includes 13 ribs, 13 thoracic vertebrae, 6 lumbar vertebrae, and 18-29 caudal vertebrae (Steppan 1995). Stomach unilocular-hemiglandular (Carleton 1973; D'Elía et al. 2006a).
Etymology.¾Waterhouse (1837: 21, footnote) coined Abrothrix, the type genus of the new tribe, from the Greek words "abros" (soft or delicate) and "thrix" (hair), which capture a key trait of these rodents that he had noted ("fur long and soft"). The tribal name is constructed by dropping the case ending from the genitive singular form of Abrothrix (ICZN, Article 29.3), or abro-trichos, to create the stem abrotrich. Thus, the family-group name becomes abrotrich + ini = Abrotrichini, not Abrothricini.
Known distribution.¾Argentina (Pliocene-Recent), Bolivia (Recent), Chile (Pleistocene-Recent), Ecuador (Recent), Peru (Recent). Species of this tribe are known from the altiplano in west-central Peru and western mountain ranges in Argentina and Bolivia to southernmost Argentina and Chile, including several austral off-shore islands and the Patagonian steppes to the Atlantic Coast (Osgood 1943; Patterson et al. 1984; Teta et al. 2006; Fig. 2).
Figura 1. Vistas de distintas características morfológicas de Abrotrichini. A) Rostro alargado y acuminado (A. sanborni). B) Región interorbitaria en forma de ánfora con senos frontales bien desarrollados (A. sanborni). C). Orientación de la placa zigomática y gran desarrollo del foramen infraorbitario (N. edwardsii). D) Nasales largos y acuminados en su extremo posterior (A. longipilis). E) Nasales y premaxilares proyectados anteriormente a los incisivos (A. sanborni). F) Placa zigomática estrecha con borde libre reducido (flecha) (A. andinus). G) Incisivos superiores robustos y ortodontes (C. macronyx). H) Típica morfología oclusal de los molares superiores desplegada por los abrotrichinos, con un procíngulo con forma de abanico, mesolofos reducidos y una foseta interna de esmalte en forma de anillo en el M3 (A. sanborni). I) Paladar largo (A. jelskii). J) Proceso coronal robusto y alto (C. macronyx). K) Mandíbula alargada con una proyección capsular inconspicua (A. lanosus). L) Topografía coronal en dos niveles (A. longipilis). Abreviaturas: ca = proyección capsular, co = cóndilo, cp = proceso coronoides, fs = seno frontal, if = foramen infraorbitario, n = nasal/es, pa = paladar, pm = premaxilar, zp = placa zigomática.
Phylogenetic relationships.¾Phylogenetic relationships among abrotrichine genera have been studied by Smith & Patton (1999), D'Elía (2003b), and D'Elía et al. (2006a) based on both mitochondrial and nuclear DNA sequences. Data are available for all currently recognized genera, although not for all species. These studies delineate a basal dichotomy separating Abrothrix from a clade composed by the remaining abrotrichines. The distinction of both clades is marked, with both strongly supported and corroborated by patterns of morphological variation. Within the latter clade, the three predominantly fossorial abrotrichine genera (Geoxus, Notiomys, and Pearsonomys) form a clade to which Chelemys is sister. Relationships among species of Abrothrix have not been thoroughly explored as some species have not been included in any phylogenetic analysis (we are aware of on-going studies that include A. illuteus, A. lanosus, A. markhami, and A. sanborni). Available phylogenetic studies, together with some unpublished phylogenetic analyses, indicate that current generic classification of abrotrichines may require adjustment since some genera as currently delimited are not monophyletic (D'Elía, Pardiñas, and Lessa unpublished data; see also D'Elía et al. 2006a).
Remarks.¾Based on information summarized by Reig (1987) for several abrotrichine taxa (Abrothrix spp., Chelemys macronyx, Geoxus valdivianus) and data provided by Liascovich et al. (1989) for A. illuteus, and Spotorno et al. (1990) for additional species of Abrothrix, Smith & Patton (1999) suggested that a diploid number of 2n = 52 could be a synapomorphy for the abrotrichine group. While no study has tested that hypothesis, new data indicates that the 2n = 52 is not a diagnostic character of the tribe. Pearsonomys annectens has a 2n = 56 (D'Elía et al. 2006a), unpublished results of M. Gallardo indicate that some abrotrichine taxa also depart from a 2n = 52, and a population of Abrothrix olivaceus with a 2n = 44 was recently documented by Rodríguez & Theiler (2007). The karyotype of Notiomys edwardsii and some other forms remain unknown. Further studies are needed to assess abrotrichine chromosomal evolution. What is important here is to acknowledge that a 2n = 52 is not a diagnostic feature of Abrotrichini, new tribe.
The pelage of the abrotrichinos is generally slate gray or brownish, although there are some blackish (A. sanborni, Chelemys, Geoxus) and brightly colored (A. jelskii) forms. Species of Abrothrix have elongated phalli with a much reduced or no distal baculum; the genera Chelemys, Geoxus, Notiomys and Pearsonomys have a tridigitate distal baculum; the phalli of Pearsonomys and Geoxus have a prominent dorsal hood that extends beyond the terminal crater (Hooper & Musser 1964; Spotorno 1986; D'Elía et al. 2006a). Abrothrix longipilis, A. jelskii, A. olivaceus, and Geoxus valdivianus have two pairs of preputial glands (Voss & Linzey 1981). The number of preputial glands in other genera is unknown.
Since Patton & Smith (1999) first identified the abrotrichine clade, the names Abrotrichini, Abrothrichini, and their informal derivatives (including the Spanish abrotrichinos and abrotriquinos) have repeatedly appeared in the literature (e.g., D'Elía 2003; Weksler 2003; Jansa & Weksler 2004; Geise et al. 2004; Ojeda et al. 2005; Palma et al. 2005; Jayat et al. 2006). However, none of these usages can be considered as the formal designation of the tribe since no diagnosis was provided, nor did any such appearance explicitly identify the creation of a new taxon (ICZN, 1999: Articles 13 and 16). Similarly, the usage of Abrotrichini by Smith and Patton (1999: 106) cannot be considered a formal designation of the tribe because their statement -"An appropriate name for the new tribe would be Abrotrichini " [emphasis ours]- clearly indicates only a conditional proposal, and as such, it is not available (ICZN, 1999: Articles 15.1, which corresponds to Article 15 of the edition of the Code in usage when the paper was published). Musser & Carleton (2005: 1087) also considered the earlier usages of Abrotrichini to be unavailable and recommended that a "full and proper diagnosis" was needed.
The informal term "Andean clade" has also been used to refer to the abrotrichine group. We note that even though several abrotrichines have exclusively Andean distributions (e.g., A. jelskii), several others are distributed in the lowlands west and east of the Andes (e.g., A. olivaceus), while still others are not found in the Andes at all (e.g., P. annectens).
Figura 2. Distribución geográfica de Abrotrichini, nueva tribu.
Currently (Carleton & Musser 2005 with the present modification), nine tribes are recognized within Sigmodontinae; these are: Abrotrichini new tribe, Akodontini, Ichthyomyini, Oryzomyini, Phyllotini, Reithrodontini, Sigmodontini, Thomasoyini, and Wiedomyini. In addition, several genera (e.g., Abrawayaomys, Phaenomys, Wilfredomys) are considered as Sigmodontinae incertae sedis (Smith & Patton 1999; D'Elía 2003; Jorge Salazar-Bravo, personal communi-cation). We are aware of four additional genera that are to be proposed in the near future, two in the Akodontini and two in Oryzomyini. We close this contribution by offering the following revised classification of the extant Sigmodontinae.
We thank Alvaro Mones, Michael D. Carleton, and Scott J. Steppan for critically reviewing an earlier version of this paper. Jorge Salazar-Bravo shared unpublished results with us.
Barrantes, G.E., M.O. Ortells & O.A. Reig. 1993. New studies on allozyme genetic distance and variability in akodontine rodents (Cricetidae) and their systematic implications. Biological Journal of the Linnean Society 48:283-298. [ Links ]
Braun J.K. 1993. Systematic relationships of the tribe Phyllotini (Muridae: Sigmodontinae) of South America. Special Publication. Oklahoma Museum of Natural History, Norman. [ Links ]
Carleton, M.D. 1973. A survey of gross stomach morphology in New World Cricetine (Rodentia, Muroidea) with comments on functional interpretations. Miscellaneous Publications Museum of Zoology, University of Michigan 146:1-43. [ Links ]
Carleton, M.D. 1980. Phylogenetic relationships of neotomine-peromyscine rodents (Muroidea) and a reappraisal of the dichotomy within New World Cricetinae. Miscellaneous Publications Museum of Zoology, University of Michigan 157:1-146. [ Links ]
D'Elía, G. 2003a. Rats, mice, and relatives IV. South American rats and mice (Sigmodontinae). In: Grzimek's Animal Life Encyclopedia, 2nd edition. Volumes 12-16, Mammals I-V (Eds. Hutchins, M., D.G. Kleiman, V. Geist, & M.C. McDade), pp. 263-279. Gale Group. Farmington Hills. [ Links ]
D'Elía, G. 2003b. Phylogenetics of Sigmodontinae (Rodentia, Muroidea, Cricetidae), with special reference to the akodont group, and with additional comments on historical biogeography. Cladistics 19:307-323. [ Links ]
D'Elía, G., E.M. González & U.F.J. Pardiñas. 2003. Phylogenetic analysis of sigmodontine rodents (Muroidea), with special reference to the akodont genus Deltamys. Mammalian Biology 68:351-364. [ Links ]
D'Elía G., U.F.J. Pardiñas & P. Myers. 2005. An introduction to the genus Bibimys (Rodentia: Sigmodontinae): phylogenetic position and alpha taxonomy. In: Mammalian Diversification: From Chromosomes to Phylogeography (Eds. Lacey E. & P. Myers), pp. 211-246. University of California Publications in Zoology,) Berkeley. [ Links ]
D'Elía G., A.A. Ojeda, F. Mondaca & M.H. Gallardo. 2006a. New data of the long-clawed mouse Pearsonomys annectens (Cricetidae, Sigmodontinae) and additional comments on the distinctiveness of Pearsonomys. Mammalian Biology 71:39-51. [ Links ]
D'Elía G., L. Luna, E.M. González & B.D. Patterson. 2006b. On the Sigmodontinae radiation (Rodentia, Cricetidae): An appraisal of the phylogenetic position of Rhagomys. Molecular Phylogenetics and Evolution 38:558-564. [ Links ]
Engel, S.R., K.M. Hogan, J.F. Taylor & S.K. Davis. 1998. Molecular systematics and paleobio-geography of the South American sigmodontine rodents. Molecular Biology and Evolution 15:35-49. [ Links ]
Geise, L., M. Weksler & C.R. Bonvicino. 2004. Presence or absence of gall bladder in some Akodontini rodents (Muridae, Sigmodontinae). Mammalian Biology 69:210-214. [ Links ]
Gyldenstolpe, N. 1932. A manual of Neotropical sigmodont rodents. Kunglia Svenska Vetenskapsakademiens Handlingar, Stockholm (ser. 3) 11:1-164. [ Links ]
Hershkovitz, P. 1966. South American swamp and fossorial rats of the scapteromyine group (Cricetinae, Muridae), with comments on the glans penis in murid taxonomy. Zeitschrift für Säugetierkunde 31:81-149. [ Links ]
Hooper, E.T. 1959. The glans penis in five genera of cricetid rodents. Occasional Papers of the Museum of Zoology, University of Michigan 613:1-11. [ Links ]
Hooper, E.T. & G.G. Musser. 1964. The glans penis in Neotropical cricetines (family Muridae) with comments on classification of muroid rodents. Miscellaneous Publications Museum of Zoology, University of Michigan 123:1-57. [ Links ]
International Commission on Zoological Nomenclature. 1999. International Code of Zoological Nomenclature (ICZN), 4th Edition. The International Trust for Zoological Nomenclature c/o The Natural History Museum. London. Fourth Edition. 306 pp. [ Links ]
Jansa, S.A. & M. Weksler. 2004. Phylogeny of muroid rodents: relationships within and among major lineages as determined by IRBP gene sequences. Molecular Phylogenetics and Evolution 31:256-276. [ Links ]
Jayat, J.P., P.E. Ortiz, P. Teta, U.F.J. Pardiñas & G. D'Elía. 2006. Nuevas localidades argentinas para algunos roedores sigmodontinos (Rodentia: Cricetidae). Mastozoología Neotropical 13:51-67. [ Links ]
Liascovich, R.C., R.M. Barquez & O.A. Reig. 1989. A karyological and morphological reassessment of Akodon (Abrothrix) illuteus Thomas. Journal of Mammalogy 70:386-391. [ Links ]
Musser, G.M. & M.D. Carleton. 2005. Superfamily Muroidea. In: Mammal species of the world: A taxonomic and geographic reference Third ed. (Eds. Wilson, D.E. & D.M. Reeder),. pp 894-1531. Johns Hopkins University Press, Baltimore. [ Links ]
Ojeda, A.A., G. D'Elía & R.A. Ojeda. 2005. Taxonomía alfa de Chelemys y Euneomys (Cricetidae, Sigmodontinae): el número diploide de ejemplares topotípicos de C. macronyx y E. mordax. Mastozoología Neotropical 12:79-82. [ Links ]
Osgood, W.H. 1943. The mammals of Chile. Field Museum of Natural History (Zoology) 30:1-268. [ Links ]
Pacheco, V. 2003. Phylogenetic analyses of the Thomasomyini (Muroidea: Sigmodontinae) based on morphological data. Ph.D. Dissertation, The City University of New York, New York, USA. [ Links ]
Palma, R.E., P.A. Marquet & D. Boric-Bargetto. 2005. Inter- and intraspecific phylogeography of small mammals in the Atacama Desert and adjacent areas of northern Chile. Journal of Biogeography 32:1931-1941. [ Links ]
Pardiñas, U.F.J., G. D'Elía, S. Cirignoli & P. Suárez. 2005. A new species of Akodon (Rodentia, Cricetidae) from the Northern Campos grasslands of Argentina. Journal of Mammalogy 86:462-474. [ Links ]
Patterson, B.D., M.H. Gallardo & K.E. Freas. 1984. Systematics of mice of the subgenus Akodon (Rodentia: Cricetidae) in southern South America, with the description of a new species, Fieldiana: Zoology (new series) 23:1-16. [ Links ]
Percequillo, A.R., P.R. Gonçalves & J.A. Oliveira. 2004. The rediscovery of Rhagomys rufescens (Thomas, 1886), with a morphological redescription and comments on its systematic relationships based on morphological and molecular (cytochrome b) characters. Mammalian Biology 69:238-257. [ Links ]
Reig, O.A. 1980. A new fossil genus of South American cricetid rodents allied to Wiedomys, with an assessment of the Sigmodontinae. Journal of Zoology 192:257-281. [ Links ]
Reig, O.A. 1987. An assessment of the systematics and evolution of the Akodontini with the description of new fossil species of Akodon (Cricetidae: Sigmodontinae). Fieldiana: Zoology (new series) 39:347-399. [ Links ]
Rodríguez, V.A. & G.R. Theiler. 2007. Micromamíferos de la región de Comodoro Rivadavia (Chubut, Argentina). Mastozoología Neotropical 14:97-100. [ Links ]
Smith, M.F. & J.L. Patton. 1993. The diversification of South American murid rodents: evidence from mitochondrial DNA sequence data for the akodontine tribe. Biological Journal of the Linnean Society 50:149-177. [ Links ]
Smith, M.F. & 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. [ Links ]
Spotorno, A.O. 1986. Systematics and evolutionary relationships of Andean phyllotine and akodontine rodents. Ph.D. Dissertation. University of California. Berkeley, USA. [ Links ]
Spotorno, A.E., C.A. Zuleta & A. Cortés. 1990. Evolutionary systematics and heterochrony in Abrothrix species (Rodentia, Cricetidae). Evolución Biológica 4:37-62. [ Links ]
Steppan, S.J. 1995. Revision of the tribe Phyllotini (Rodentia: Sigmodontinae), with a phylogenetic hypothesis for the Sigmodontinae. Fieldiana: Zoology (new series) 80:1-112. [ Links ]
Steppan, S.J., R.M. Adkins & J. Anderson. 2004. Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Systematic Biology 53:533-554. [ Links ]
Teta, P., U.F.J. Pardiñas & G. D'Elía. 2006. "Abrotrichinos". In: Mamíferos de Argentina: taxonomía y distribución (Eds. Barquez, R.M., M.M. Díaz, & R.A. Ojeda), pp. 192-197. Sociedad Argentina para el Estudio de los Mamíferos, Mendoza. [ Links ]
Voss, R.S. 1988. Systematics and ecology of ichthyomyine rodents (Muroidea): patterns of morphological evolution in a small adaptative radiation. Bulletin of the American Museum of Natural History 188:259-493. [ Links ]
Voss, R.S. & 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. [ Links ]
Waterhouse, G.R. 1837. Characters of new species of the genus Mus, from the collection of Mr. Darwin. Proceedings of the Zoological Society of London 1837:15-21, 27-29. [ Links ]
Weksler, M. 2003. Phylogeny of Neotropical oryzomyine rodents (Muridae: Sigmodontinae) based on the nuclear IRBP exon. Molecular Phylogenetics and Evolution 29:331-349. [ Links ]
Weksler, M. 2006. Phylogenetic relationships of oryzomine rodents (Muroidea: Sigmodontinae): separate and combined analyses of morpho-logical and molecular data. Bulletin of the American Museum of Natural History 296:1-149. [ Links ]
Weksler, M., A.R. Percequillo & R.S. Voss. 2006. Ten new genera of oryzomyine rodents (Cricetidae: Sigmodontinae). American Museum Novitates 3537:1-29. [ Links ]