Cytogenetics and redescription of Graomys (Rodentia, Sigmodontinae) from Chumbicha, Catamarca, Argentina

Cecilia Lanzone, Agustina Novillo, Natalia S. Suárez, and Ricardo A. Ojeda

GiB (Grupo de Investigaciones de la Biodiversidad), Instituto Argentina de Investigaciones de las Zonas Áridas, CRICYT (CONICET), CC 507, 5500 Mendoza, Argentina

ABSTRACT: The taxonomy, phylogenetic relationships and distribution of the genus Graomys are confusing. In this note we report karyotypic data for specimens of Graomys collected in Chumbicha, Catamarca Province, Argentina. Their karyotypes agree with G. centralis with 2n = 42. The individuals from Chumbicha are similar in morphology to G. griseoflavus but smaller. Our results suggest that Chumbicha's specimens are conspecific with G. medius. Moreover, we propose to synonymize G. medius with G. centralis. Other data of the genus suggest that the name G. chacoensis should be applied to specimens with 2n = 42.

RESUMEN: Citogenética y redescripción de Graomys (Rodentia, Sigmodontinae) de Chumbicha, Catamarca, Argentina. El estado taxonómico, las relaciones filogenéticas y distribución de algunas especies del genero Graomys son confusas. Aquí reportamos datos de cariotipos para especímenes de Graomys colectados en Chumbicha (Catamarca, Argentina). Los cariotipos coinciden con G. centralis con 2n = 42. Los individuos de Chumbicha son similares en morfología a G. griseoflavus, pero mas pequeños. Nuestros resultados sugieren que los ejemplares de Chumbicha son conespecíficos con G. medius. Por lo tanto proponemos sinonimizar G. medius con G. centralis. Otros datos del genero sugieren que el nombre G. chacoensis debería ser aplicado a los especímenes con 2n = 42.

Key words. Chromosomes. Morphometry. Phyllotine. Rodents. Taxonomy.

Palabras clave. Cromosomas. Morfometría. Roedores filotinos. Taxonomía.

   The taxonomy and systematics of South American rodents are a matter of continuous revision and debate (e.g., Hershkovitz, 1962; Reig, 1981; Musser and Carleton, 1993; Steppan, 1995, 1998; Smith and Patton, 1999; D' Elía, 2003). Within sigmodontines, those of the Phyllotini tribe are primarily distributed throughout the arid and semiarid biomes. Among these, the genus Graomys Thomas, 1916, is distributed from Paraguay and Bolivia to southern Argentina (Musser and Carleton, 2005). Several species have been described in this genus; however their taxonomic status, phylogenetic relationships and overall distribution are confusing (Braun 1993; Steppan, 1995; Steppan and Sullivan, 2000).
   After its original description (Thomas, 1916), some earlier reviews of phyllotines included the genus Graomys within the genus Phyllotis (Hershkovitz, 1962). Later research recognized Graomys as an independent genus, but the identity of species it contains has not been completely clarified (Pearson and Patton, 1976; Braun, 1993; Steppan, 1993, 1995). Recently, Musser and Carleton (2005) and Díaz et al. (2006) recognized it as a polytypic genus with four species: G. domorum (Thomas, 1902a) distributed on the east of the Andes in Bolivia and northwestern Argentina; G. edithae (Thomas, 1919) confined to Catamarca Province in Argentina; G. centralis (Thomas, 1902b) distributed in central Argentina; and G. griseoflavus (Waterhouse, 1837) as the most widely distributed species in Bolivia, Paraguay, Argentina and probably in southern Brazil. In addition, the taxonomic status of G. cachinus (Allen, 1901), G. chacoensis (Allen, 1901), G. lockwoodi (Thomas, 1918) and G. medius (Thomas, 1919) is uncertain and they are considered synonymous with G. griseoflavus (Musser and Carleton, 2005; Díaz et al., 2006).
   Karyotypic data for several phyllotine rodents have significantly contributed to the taxonomic delimitation of some of their species (Pearson 1972; Pearson and Patton, 1976; Zambelli et al., 1994; Tiranti, 1998; Spotorno et al., 2001; Bonvicino et al., 2003; Lanzone and Ojeda, 2005; Lanzone et al., 2007). In Graomys, three basically different chromosome complements were reported: G. domorum with 2n = 28 (Pearson and Patton, 1976), G. griseoflavus with diploid numbers ranging from 2n = 34 to 2n = 38 and G. centralis with 2n = 42 (Zambelli et al., 1994; Tiranti, 1998). The latter two are considered sister species and both karyotypes can be derived from successive Robertsonian translocations (Zambelli et al., 1994; 2003). This chromosomal diversity has been achieved without major phenotypic changes in the group (Theiler and Blanco, 1996a; Tiranti, 1998; Theiler et al., 1999; Catanesi et al., 2002; Rodríguez, 2005). The existence of a marked genetic differentiation and reproductive barriers between G. centralis and G. griseoflavus has been demonstrated, supporting that they are true biological species (Theiler and Blanco, 1996a and b; Catanesi et al., 2006).
   In his pioneering works, Thomas (1919) recognized three species of Graomys coexisting in sympatry at the locality of Chumbicha, Catamarca Province, Argentina: G. cachinus Allen 1901 corresponding to the largest species, G. medius Thomas 1919, having an intermediate size; and G. edithae Thomas 1919, the smallest species in the genus. However, these species are considered as of doubtful taxonomic assignment or as synonymous with G. griseoflavus (Williams and Mares, 1978; Musser and Carleton, 2005; Díaz et al., 2006).
   During a field expedition to the locality of Chumbicha (28° 53' 23" S/66° 17' 05.1" W; 390 m) in March 2006, we collected three specimens of Graomys. This region corresponds to the transition area between the Chaco and Monte desert biomes (Cabrera, 1976). It is a semiarid woodland dominated by Acacia, Prosopis sp., Larrea sp., Opuntia sp., Aspidosperma quebrachoblanco and Suaeda divaricata, among others. The specimens were collected using Sherman traps baited with oatmeal and peanut butter. Two of the three individuals were adults (one female and one male) and one was a juvenile (female). The specimens (skin, skull, cellular suspensions and tissues) are housed at the Colección Mastozoológica - IADIZA (CMI-07254, CMI-07253, CMI-07252). External and cranial features were measured using a digital caliper (Martin et al., 2001). Qualitative morphological data were compared with G. griseoflavus (N = 5; 3 males and 2 females) from Ñacuñán, Mendoza Province, Argentina. G. griseoflavus was selected for the comparison for being the best characterized species in the genus, and to include in its synonymy the possible species present at the studied locality. Chromosome preparations were obtained from bone-marrow using standard techniques (Ford and Hamerton, 1956), with minimal modifications, and chromosomes were stained with Giemsa. Ten metaphase spreads were counted for each specimen. The nomenclature for chromosome morphology and fundamental number (FN) follows Patton (1967).
   The karyotypes of the three specimens from Chumbicha are similar, with 2n = 42 (Fig. 1), although some differences are observed in the biarmed autosomal pairs that produce variations in the FN. In one of the specimens, pairs 1 to 18 are acrocentrics decreasing in size. Pair 19 is composed of medium size submetacentric chromosomes and pair 20 is a small submetacentric. This karyotype has an FN = 44. The other two specimens have one small extra pair of biarmed chromosomes, which increases their FN to 46. The X chromosome is a large submetacentric, and the Y a small acrocentric in all thee specimens (Fig. 1). These karyotypes agree with the chromosome complement described and assigned to G. centralis by proximity (30 Km NW) to the type locality in Cruz del Eje, Córdoba Province (Zambelli et al., 1994; Tiranti, 1998).

Fig. 1. Standard Giemsa stained bone marrow karyotype of one male of Graomys from Chumbicha with 2n = 42, FN = 46.

   On the other hand, specimens from Chumbicha are similar in general morphology to G. griseoflavus but smaller in size (Fig. 2). Externally they present a white undersurface, with wholly white hair up to the base. The dorsal and lateral coloration is similar to that of G. griseoflavus, but the lateral band is less marked, the tail is less tufted and bicoloured. Compared to G. griseoflavus, the skull is smaller; nasals are narrower and shorter at the distal portion. The rostrum of the Chumbicha specimens is smaller and has greater downward curvature at the anterior end. The maximum breadth of the braincase is smaller and in dorsal view the tympanic bullae do not present a lateral expansion as in G. griseoflavus. In lateral view, the zygomatic plate in the Chumbicha specimens is more robust, slightly wider and more concave at its anterior insertion. The zygomatic notch is less expanded in the anterior-posterior axis. In ventral view, the tympanic bullae are less inflated, with slightly larger and cylindrical bullar tubes; the external auditory meatus is more prominent in ventral view. The petrotympanic fossa is more expanded in its lateral portion, possibly due to the smaller size of the bullae compared to G. griseoflavus. In this latter species, the petrotympanic fossa is covered by the tympanic bullae in the internal portion. The foramen ovale is smaller in the individuals from Chumbicha. The posterolateral palatal pits are located posteriorly to M 3. In the upper molar toothrow, M 3 possesses a more rounded shape and the labial and lingual folds are not in contact. It differs from that observed in G. griseoflavus. In this last species, the labial fold is deeper than in specimens from Chumbicha.

Fig. 2. Lateral and ventral views of the skull of: a) Graomys from Chumbicha and b) G. griseoflavus from Ñacuñán. Note the differences in the petrotympanic fossa and the foramen ovale (arrows).

   In morphology, the general description and the range of variation observed in most (11/14) external and cranial measurements of the specimens from Chumbicha studied here are concordant with, or very close to, those recorded for the type of G. medius from this locality (Table 1). But, the same measurements are smaller when compared with specimens of G. cachinus (Allen, 1901; Thomas, 1919). Some measurements (8/14) are also concordant with those of the type of G. edithae, but the others are larger. Considering that specimens from Chumbicha assigned by Thomas to the last species are of doubtful assignment (Williams and Mares, 1978), the morphological results seem to indicate that the specimens analyzed here are conspecific with that described as G. medius.

   If the karyotype is a good indicator of species in this genus, our results suggest that G. medius must be synonymous with G. centralis and not with G. griseoflavus as was proposed by some authors (Musser and Carleton, 2005; Díaz et al., 2006). Nevertheless, several external and cranial measurements for the type of G. centralis are not concordant with those of the specimens studied here (Table 1), but nothing is known about the range of morphological variation in specimens with 2n = 42.
   Furthermore, specimens from the Paraguayan Chaco, 460 km NW of Villa Hayes, Department of Boquerón, have the same 2n and FN as our specimens from Chumbicha (Patton, pers. comm. and unpubl. data), which shows a previously unsuspected wide geographic range for this karyomorph. Moreover, in a recent phylogenetic analysis, a specimen assigned to G. griseoflavus from Bolivia was found to group closely with specimens from Argentina assigned to G. centralis on the basis of karyotypic data (Steppan et al., 2007). Altogether, these data suggest that the specimens from the northern part of the distributional range of the genus could belong to the same species. If this were true and only one Graomys species inhabits the Chaco biome, the name chacoensis Allen (1901) should be applied to those specimens, with medius and centralis as junior synonyms. However, no information is available about specimens of G. chacoensis from the type locality in Waikthlatingwayalwa, Paraguay, to sustain this hypothesis.
   This proposition is also supported by the geographical distribution of Graomys species in different biomes. Whereas G. chacoensis (2n = 42) is distributed over the Gran Chaco and Espinal, from central Argentina (Theiler and Blanco, 1996a; Tiranti, 1998) and Paraguay, G. domorum occurs in the Yungas and transitional forests, and G. griseoflavus in the Monte Desert and marginally in the Patagonian steppe (Theiler and Blanco, 1996a; Tiranti, 1998; Rodríguez, 2005).
   Our records from Chumbicha help to partially clarify the group's taxonomy and to define more precisely the geographic ranges of the species of Graomys. On the other hand, the names G. edithae and G. cachinus assigned by Thomas (1916) to specimens from Chumbicha are still in an uncertain state, and our small sample size leaves doubts as to how many species inhabit this locality. Future analysis of specimens from type localities as well as of type specimens and broad sampling across the geographic range of the genus, are needed to solve the taxonomy of the group.

ACKNOWLEDGEMENTS

   We thank Jim Patton who kindly provided us the karyotypes of Graomys from Paraguay prepared by Oliver Pearson. We thank Solana Tabeni for her critical comments and suggestions to a preliminary version of this manuscript. We thank Maria Ana Dacar for field help and Marisa Rosi and Agustina Ojeda for assistance with cranial photographs. Nelly Horak assisted in the English version. This work was partially financed by CONICET (PIP 5944 and PIP 6179), SECYT-AGENCIA (PICT 11768).

LITERATURE CITED

ALLEN JA. 1901. New South American Muridae and a new Metachirus. Bulletin American Museum of Natural History 14:408-409.         [ Links ]

BONVICINO CB, JFS LIMA, and FC ALMEIDA. 2003. A new species of Calomys Waterhouse (Rodentia, Sigmodontinae) from the Cerrado of Central Brazil. Revista Brasileira de Zoologia 20:301-307.         [ Links ]

BRAUN JK. 1993. Systematic relationships of the tribe Phyllotini (Muridae: Sigmodontinae) of South America. Special Publication. Oklahoma Museum of Natural History.         [ Links ]

CABRERA AL. 1976. Regiones fitogeográficas de la Argentina. Enciciclopedia Argentina de Agricultura y Jardinería 1:1-85.         [ Links ]

CATANESI CI, L VIDAL-RIOJA, JV CRISCI, and A ZAMBELLI. 2002. Phylogenetic relationships among Robertsonian karyomorphs of Graomys griseoflavus (Rodentia, Muridae) by mitochondrial cytochrome b DNA sequencing. Hereditas 136:130-136.         [ Links ]

CATANESI CI, L VIDAL-RIOJA, and A ZAMBELLI. 2006. Molecular and phylogenetic analysis of mitochondrial control region in Robertsonian karyomorphs of Graomys griseoflavus (Rodentia, Sigmodontinae). Mastozoología Neotropical 13:21-30.         [ Links ]

D´ELÍA G. 2003. 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 ]

DÍAZ MM, P TETA, UFJ PARDIÑAS, and RM BARQUEZ. 2006. Tribu Phyllotini, Pp. 175-189, in: Mamíferos de Argentina. Sistemática y distribución (RM Barquez, MM Díaz, and RA Ojeda, eds.). Publicación de la Sociedad Argentina para el Estudio de los Mamíferos.         [ Links ]

FORD CE and JL HAMERTON. 1956. A colchicine, hypotonic citrate, squash sequence for mammalian chromosomes. Stain Technology 31:247-251.         [ Links ]

HERSHKOVITZ P. 1962. Evolution of Neotropical Cricetine Rodents (Muridae) with special reference to the Phyllotine group. Fieldiana, Zoology 46:1-524.         [ Links ]

LANZONE C and RA OJEDA. 2005. Citotaxonomía y distribución del género Eligmodontia (Rodentia, Cricetidae, Sigmodontinae). Mastozoología Neotropical 12:73-7         [ Links ]

LANZONE C, RA OJEDA, and MH GALLARDO. 2007. Integrative taxonomy, systematics and distribution of the genus Eligmodontia (Rodentia, Cricetidae, Sigmodontinae) in the temperate Monte Desert of Argentina. Mammalian Biology 72:299-312.         [ Links ]

MARTIN RE, RH PINE, and AF DEBLASE. 2001. A Manual of Mammalogy with Keys to Families of the World. New York: McGraw-Hill.         [ Links ]

MUSSER GG and MD CARLETON. 1993. Subfamily Sigmodontinae. Pp. 687-752, in: Mammal species of the world. A taxonomic and geographic reference. Second edition. (DE Wilson and DM Reeder, eds.). Washington DC and London: Smithsonian Institution Press.         [ Links ]

MUSSER GG and MD CARLETON. 2005. Superfamily Muroidea. Pp. 894-1531, in: Mammal species of the world. A taxonomic and geographic reference. Third edition. (DE Wilson and DM Reeder, eds.). Baltimore: The Johns Hopkins University Press.         [ Links ]

PATTON JL. 1967. Chromosome studies of certain pocket mice, genus Perognathus (Rodentia, Heteromyidae). Journal of Mammalogy 48:27-37.         [ Links ]

PEARSON OP. 1972. New information on ranges and relationships within the rodent genus Phyllotis in Peru and Ecuador. Journal of Mammalogy 53:677-686.         [ Links ]

PEARSON OP and JL PATTON. 1976. Relationship among South American phyllotine rodents based on chromosomal analysis. Journal of Mammalogy 57:339-350.         [ Links ]

REIG OA. 1981. Teoría y desarrollo de la fauna de mamíferos de América del Sur. Monographiae Naturae. Museo Municipal de Ciencias Naturales «Lorenzo Scaglia», Mar del Plata, 162 pp.         [ Links ]

RODRÍGUEZ VA. 2005. Determinación específica y niveles de polimorfismo alozímico de Graomys (Rodentia, Muridae) de los alrededores de Comodoro Rivadavia. Mastozoología Neotropical 12:105-107.         [ Links ]

SMITH MF and JL 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 AE, LI WALKER, SV FLORES, M YEVENES, JC MARÍN, and C ZULETA. 2001. Evolución de los filotinos (Rodentia, Muridae) en los Andes del Sur. Revista Chilena de Historia Natural 74:151-166.         [ Links ]

STEPPAN SJ. 1993. Phylogenetic Relationships among the Phyllotini (Rodentia: Sigmodontinae) using morphological characters. Journal of Mammalian Evolution 1:187-213.         [ Links ]

STEPPAN SJ. 1995. Revision of the tribe Phyllotini (Rodentia: Sigmodontinae), with a phylogenetic hypothesis for the Sigmodontinae. Fieldiana: Zoology 80:1-112.         [ Links ]

STEPPAN SJ. 1998. Phylogenetic relationships and species limits within Phyllotis (Rodentia: Sigmodontinae): concordance between mtDNA sequence and morphology. Journal of Mammalogy 79:573-593.         [ Links ]

STEPPAN SJ and J SULLIVAN. 2000. The emerging statistical perspective in systematics: a comment on Mares and Braun. Journal of Mammalogy 81:260-270.         [ Links ]

STEPPAN SJ, O RAMIREZ, J BANBURY, D HUCHON, V PACHECO, LI WALKER, and AE SPOTORNO. 2007. A molecular reappraisal of the systematics of the leaf-eared mice Phyllotis and their relatives. Pp. 799-826, en: The quintessential naturalist: honoring the life and legacy of Oliver P. Pearson (DA Kelt, EP Lessa, J Salazar-Bravo, and JL Patton, eds.). University of California Publications in Zoology 134:1-981.         [ Links ]

THEILER GR and A BLANCO. 1996a. Patterns of evolution in Graomys griseoflavus (Rodentia: Muridae): II. Reproductive isolation between cytotypes. Journal of Mammalogy 77:776-784.         [ Links ]

THEILER GR and A BLANCO. 1996b. Patterns of evolution in Graomys griseoflavus (Rodentia: Muridae): III. Olfactory discrimination as a premating isolation mechanism between cytotypes. The Journal of Experimental Zoology 274:346-350.         [ Links ]

THEILER GR, CN GARDENAL and A BLANCO. 1999. Patterns of evolution in Graomys griseoflavus (Rodentia: Muridae). IV. A case of rapid speciation. Journal of Evolutionary Biology 12:970-979.         [ Links ]

THOMAS O. 1902a. On mammals from Cochabamba, Bolivia, and the region north of that place. Annals and Magazine of Natural History 7:125-143.         [ Links ]

THOMAS O. 1902b. On mammals collected at Cruz del Eje, central Cordoba, by Mr P.O. Simmons. Annals and Magazine of Natural History 7:237-245.         [ Links ]

THOMAS O. 1916. On the grouping of the South American Muridae that have been referred to Phyllotis, Euneomy s and Eligmodontia. Annals and Magazine of Natural History 8:139-143.         [ Links ]

THOMAS O. 1918. On small mammals from Salta and Jujuy collected by Mr. E. Budin. Annals and Magazine of Natural History 9:187.         [ Links ]

THOMAS O. 1919. On small mammals from «Otro Cerro,» North-eastern Rioja, collected by Sr. E. Budin. Annals and Magazine of Natural History 9:489-500.         [ Links ]

TIRANTI SI. 1998. Cytogenetics of Graomys griseoflavus (Rodentia: Sigmodontinae) in central Argentina. Zeitschrift für Säugetierkunde 63:32-36.         [ Links ]

WILLIAMS DF and MA MARES. 1978. A new Genus and species of phyllotine rodent (Mammalia: Muridae) from Northwestern Argentina. Annals of Carnegie Museum. Carnegie Museum of Natural History 47:193-220.         [ Links ]

WATERHOUSE GR. 1837. Characters of new species of Mus, from the collection of Mr. Darwin. Proceedings of the Zoological Society of London 27-29.         [ Links ]

ZAMBELLI A, L VIDAL-RIOJA, and R WAINBERG. 1994. Cytogenetic analysis of autosomal polymorphism in Graomys griseoflavus (Rodentia, Cricetidae). Zeitschrift für Säugetierkunde 59:14-20.         [ Links ]

ZAMBELLI A, CI CATANESI, and L VIDAL-RIOJA. 2003. Autosomal rearrangements in Graomys griseoflavus (Rodentia): a model of non-random Robertsonian divergence. Hereditas 139:167-173.         [ Links ]

Recibido 25 agosto 2006.
Aceptación final 3 mayo 2007.