Abstract
Tuco-tucos (small subterranean rodents of the genus Ctenomys) that inhabit sandy soils of the area under the influence of the second largest wetland of South America, in Northeastern Argentina (Corrientes province), are a complex of species and forms whose taxonomic status were not defined, nor are the evolutionary relationships among them. The tuco-tuco populations of this area exhibit one of the most ample grades of chromosomal variability within the genus. In order to analyze evolutionary relationships within the Corrientes group and its chromosomal variability, we completed the missing karyotypic information and performed a phylogenetic analysis. We obtained partial sequences of three mitochondrial markers: D-loop, cytochrome b and cytochrome oxidase I. The Corrientes group was monophyletic and split into three main clades that grouped related karyomorphs. The phylogeny suggested an ancestral condition of the karyomorph with diploid number (2n) 70 and fundamental number (FN) 84 that has evolved mainly via reductions of the FN although amplifications occurred in certain lineages. We discuss the relationship between patterns of chromosomal variability and species and groups boundaries. From the three main clades the one named iberá exhibited a remarkable karyotypic homogeneity, and could be considered as an independent and cohesive evolutionary lineage. On the contrary, the former recognized species C. dorbignyi is a polyphyletic lineage and hence its systematic classification should be reviewed.


References
Argüelles CF, Suárez P, Giménez MD, Bidau CJ (2001) Intraspecific chromosome variation between different populations of Ctenomys dorbignyi (Rodentia, Ctenomyidae) from Argentina. Acta Theriol 46(4):363–373
Avise JC (2004) Molecular markers, natural history and evolution. Sinauer Associates, Sunderland
Baker RJ, Bickham JW (1986) Speciation by monobrachial centric fusions. Proc Natl Acad Sci USA 83:8245–8248
Bohn VY, Campo AM (2010) Estimación de escurrimientos superficiales para cuencas no aforadas en Corrientes, Argentina. Investigaciones Geográficas 71:31–42
Bryja J, Granjon L, Dobigny G et al (2010) Plio-Pleistocene history of West African Sudanian savanna and the phylogeography of the Praomys daltoni complex (Rodentia): the environment/geography/genetic interplay. Mol Ecol 19:4783–4799
Castillo AH, Cortinas MN, Lessa EP (2005) Rapid diversification of South American tuco-tucos (Ctenomys; Rodentia, Ctenomyidae): contrasting mitochondrial and nuclear intron sequences. J Mammal 86:170–179
Contreras JR (1989) Ctenomys roigi, una nueva especie de ‘anguya tutu’ de la Provincia de Corrientes, Argentina (Rodentia: Ctenomyidae). Bol Inst Estud Almerienses 1988 (extra)(1989): 51–67
Contreras JR, Contreras ANCH (1984) Diagnosis preliminar de una nueva especie de ‘anguyá tutú’ (género Ctenomys) para la provincia de Corrientes, Argentina (Mammalia, Rodentia). Hist Nat 4:131–132
Cook JA, Anderson S, Yates TL (1990) Notes on Bolivian mammals. 6, The genus Ctenomys (Rodentia, Ctenomyidae) in the highlands. Am Mus Novit 2980:1–27
Cutrera AP, Antinuchi CD, Mora MS, Vassallo AI (2006) Home-range and activity patterns of the South American subterranean rodent Ctenomys talarum. J Mammal 87:1183–1191
Cutrera AP, Mora MS, Antenucci CD, Vassallo AI (2010) Intra- and interspecific variation in home-range size in sympatric tuco-tucos, Ctenomys australis and C. talarum. J Mammal 91:1425–1434
D’Elía G, Lessa EP, Cook JA (1999) Molecular phylogeny of tuco-tucos, genus Ctenomys (Rodentia: Octodontidae): evaluation of the mendocinus species group and the evolution of asymmetric sperm. J Mamm Evol 6:19–38
Fernández-Stolz GP, Stolz JFB, De Freitas TRO (2007) Bottlenecks and dispersal in the tuco-tuco das Dunas, Ctenomys flamarioni (Rodentia: Ctenomyidae), in Southern Brazil. J Mammal 88:935–945
Ford CE, Hamerton JL (1956) A colchicine, hypotonic citrate, squash sequence for mammalian chromosomes. Stain Technol 31:247–251
Francescoli G (2010) Tuco-tucos’ vocalization output varies seasonally (Ctenomys pearsoni; Rodentia, Ctenomyidae): implications for reproductive signaling. Acta Ethol 14:1–6
Freitas TRO (1994) Geographical variation of heterochromatin in Ctenomys flamarioni (Rodentia-Octodontidae) and its cytogenetic relationships with other species of the genus. Cytogenet Cell Genet 67:193–198
Gallardo M (1979) Las especies Chilenas de Ctenomys (Rodentia, Octodontidae). I. Estabilidad Cariotípica. Archivos de Biología y Medicina experimental 12:71–82
García L, Ponsa M, Egozcue J, García M (2000a) Comparative chromosomal analysis and phylogeny in four Ctenomys species (Rodentia, Octodontidae). Biol J Linn Soc 69:103–120
García L, Ponsa M, Egozcue J, García M (2000b) Cytogenetic variation in Ctenomys perrensi (Rodentia, Octodontidae). Biol J Linn Soc 71:615–624
Giménez MD, Mirol PM, Bidau CJ, Searle JB (2002) Molecular analysis of populations of Ctenomys (Caviomorpha, Rodentia) with high karyotypic variability. Cytogenet Genome Res 96:130–136
Godinho R, Crespo EG, Ferrand N (2008) The limits of mtDNA phylogeography: complex patterns of population history in a highly structured Iberian lizard are only revealed by the use of nuclear markers. Mol Ecol 17:4670–4683
Kiblisky P, Brum-Zorrilla N, Perez G, Saez F (1977) Variabilidad cromosómica entre diversas poblaciones uruguayas del roedor cavador del genero Ctenomys (Rodentia-Octodontidae). Mendeliana 2:85–93
Lanzone C, Giménez MD, Santos JL, Bidau CJ (2007) Meiotic effects of Robertsonian translocations in tuco-tucos of the Ctenomys perrensi superspecies (Rodentia: Ctenomyidae). Caryologia 60:233–244
Lara MC, Patton JL, Da Silva MNF (1996) The simultaneous diversification of South American echimyid rodents (Hystricognathi) based on complete cytochrome b sequences. Mol Phylogenet Evol 5:403–413
Larkin MA et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Larmuseau MHD, Raeymaekers JAM, Hellemans B et al (2010) Mito-nuclear discordance in the degree of population differentiation in a marine goby. Heredity 105:532–542
Lessa EP, Cook JA (1998) The molecular phylogenetics of tuco-tucos (genus Ctenomys, Rodentia: Octodontidae) suggests an early burst of speciation. Mol Phylogenet Evol 9:88–99
Levan A, Fredga K, Sandberg AA (1964) Nomenclature for centromeric position on chromosomes. Hereditas 52:1–22
Mascheretti S, Mirol PM, Giménez MD, Bidau CJ, Contreras JR, Searle JB (2000) Phylogenetics of the speciose and chromosomally variable rodent genus Ctenomys (Ctenomyidae, Octodontoidea), based on mitochondrial cytochrome b sequences. Biol J Linn Soc 70:361–376
Massarini A, Freitas TRO (2005) Morphological and cytogenetics comparison in species of the mendocinus-group (genus Ctenomys) with emphasis in C. australis and C. flamarioni (Rodentia-Ctenomyidae). Caryologia 58:21–27
Massarini A, Barros MA, Ortells MO, Reig OA (1991) Evolutionary biology of fossorial Ctenomyine rodents (Caviomorph: Octodontidae). I. Chromosomal polymorphism and small karyotypic differentiation in Central Argentinian populations of tuco-tucos. Genetica 83:131–144
Mirol PM, Mascheretti S, Searle JB (2000) Multiple nuclear pseudogenes of mitochondrial cytochrome b in Ctenomys (Caviomorpha, rodentia) with either great similarity to or high divergence from the true mitochondrial sequence. Heredity 84(Pt 5):538–547
Mirol P, Giménez MD, Searle JB, Bidau CJ, Faulkes CG (2010) Population and species boundaries in the South American subterranean rodent Ctenomys in a dynamic environment. Biol J Linn Soc 100:368–383
Mora MS, Mapelli FJ, Gaggiotti OE et al (2010) Dispersal and population structure at different spatial scales in the subterranean rodent Ctenomys australis. BMC Genet 11:9
Nyakaana S, Arctander P (1999) Population genetic structure of the African elephant in Uganda based on variation at mitochondrial and nuclear loci: evidence for male-biased gene flow. Mol Ecol 8:1105–1115
Ortells MO, Barrantes GE (1994) Genetic distances and variability study in several species of the genus Ctenomys (Rodentia: Octodontidae), with special reference to a probable causal role of chromosomes in speciation. Biol J Linn Soc 53:189–208
Ortells MO, Contreras JR, Reig OA (1990) New Ctenomys karyotypes (Rodentia, Octodontidae) from north-eastern Argentina and from Paraguay confirm the extreme chromosomal multiformity of the genus. Genetica 82:189–201
Parada A, D’Elía G, Bidau CJ, Lessa EP (2011) Species groups and the evolutionary diversification of tuco-tucos, genus Ctenomys (Rodentia: Ctenomyidae). J Mammal 92:671–682
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14(9):817–818
Quintana CA (1994) Ctenominos primitivos (Rodentia, Octodontidae) del Mioceno de la Provincia de Buenos Aires, Argentina. Bol R Soc Esp Hist Nat (Sec Geol) 89:19–23
Reig OA (1989) Karyotypic repatterning as one triggering factor in cases of explosive speciation. In: Fontdevila A (ed) Evolutionary biology of transient unstable populations. Springer, Berlin, pp 246–289
Reig OA, Kiblisky P (1969) Chromosome multiformity in the genus Ctenomys (Rodentia, Octodontidae), a progress report. Chromosoma 28:211–244
Reig OA, Quintana CA (1992) Fossil ctenomyine rodents of the genus Eucelophorus (Caviomorpha: Octodontidae) from the Pliocene and early Pleistocene of Argentina. Ameghiniana 29:363–380
Reig OA, Busch C, Ortells MO, Contreras JR (1990) An overview of evolution, systematics, population biology, cytogenetics, molecular biology and speciation in Ctenomys. Prog Clin Biol Res 335:71–96
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Slade RW, Moritz C, Heideman A (1994) Multiple nuclear-gene phylogenies: application to pinnipeds and comparison with a mitochondrial DNA gene phylogeny. Mol Biol Evol 11:341–356
Slamovits CH (2002) Filogenia molecular y dinámica del ADN satélite: su relación con la evolución de los roedores tuco-tucos (Ctenomys, Octodontidae) PhD thesis. Universidad de Buenos Aires, Buenos Aires, Argentina
Slamovits CH, Cook JA, Lessa EP, Rossi MS (2001) Recurrent amplifications and deletions of satellite DNA accompanied chromosomal diversification in South American tuco-tucos (genus Ctenomys, Rodentia: Octodontidae): a phylogenetic approach. Mol Biol Evol 18:1708–1719
Swofford DL (2003) PAUP: phylogenetic analysis using parsimony (and other methods), version 4. Sinauer Associates, Sunderland, MA
Tomasco IH, Lessa EP (2007) Phylogeography of the tuco-tuco: mtDNA variation and its implication for chromosomal differentiation. In: Kelt DA, Lessa EP, Salazar-Bravo JA, Patton JL (eds) The quintessential naturalist: honoring the life and legacy of Oliver P. Pearson. University of California Publications in Zoology, San Diego, pp 859–882
Verzi DH, Montalvo CI, Vucetich MG (1991) Nuevos restos de Xenodontomys simpsoni Kraglievich y la sistemática de los más antiguos Ctenomyinae (Rodentia, Octodontidae). Ameghiniana 28:325–331
Woods C, Kilpatrick C (2005) Infraorder Hystricognathi Brandt, 1855. In: Wilson DE, Reeder DM (eds) Mammal species of the world: a taxonomic and geographic reference, 3rd edn. John Hopkins University Press, Baltimore, MD, pp 1538–1600
Xia X, Xie Z (2001) DAMBE: data analysis in molecular biology and evolution. J Hered 92:371–373
Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7
Zenuto RR, Busch C (1998) Population biology of the subterranean rodent Ctenomys australis (tuco-tuco) in a coastal dune-field in Argentina. Zeitschrift für Säugetierkunde 63:357–367
Zenuto RR, Lacey EA, Busch C (1999a) DNA fingerprinting reveals polygyny in the subterranean rodent Ctenomys talarum. Mol Ecol 8:1529–1532
Zenuto RR, Malizia AI, Busch C (1999b) Sexual size dimorphism, testes size and mating system in two populations of Ctenomys talarum (Rodentia: Octodontidae). J Nat History 33:305–314
Zenuto RR, Vasallo AI, Busch C (2002) Comportamiento social y reproductivo del roedor subterráneo solitario Ctenomys talarum (Rodentia: Ctenomyidae) en condiciones de semicautiverio. Rev Chil Hist Nat 75:165–177
Acknowledgments
This work was supported by grants from the Agencia Nacional de Investigaciones Científicas y Técnicas (PICT 3836/1) and Consejo Nacional de Investigaciones Científicas y Técnicas (PIP 5776) from Argentina. D.A.C. is supported by a doctoral fellowship awarded by CONICET. M. S. R. is career investigator of the CONICET. We would like to thank Diana Avedikian, Pablo Belluscio, Paola Jablonski and Pablo Rebagliati. We also would like to thank Rodrigo Álvarez, Thales R. de Freitas, María Jimena Gómez Fernández, Marcelo Kittlein, Fernando Mapelli, Patricia Mirol, Matías Mora, Vanina Raimondi, Verónica Trucco Cano, and Laura Wolfenson for assistance at the fieldwork. Finally we thank two anonymous reviewers whose comments have improved the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Caraballo, D.A., Abruzzese, G.A. & Rossi, M.S. Diversity of tuco-tucos (Ctenomys, Rodentia) in the Northeastern wetlands from Argentina: mitochondrial phylogeny and chromosomal evolution. Genetica 140, 125–136 (2012). https://doi.org/10.1007/s10709-012-9664-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-012-9664-7