Skip to main content
Log in

Extraordinary chromosome diversity in the southernmost populations of the montane grass mouse Akodon montensis (Cricetidae, Sigmodontinae)

  • ORIGINAL PAPER
  • Published:
Mammal Research Aims and scope Submit manuscript

Abstract

Akodon montensis is abundant and widely distributed in the Atlantic Forest, which southern limits extends to northern Argentina, principally in the Misiones province. Chromosomal data from more centrally distributed populations in Brazil showed significant chromosome diversity; however, data from its southern boundaries are scarce. To explore the chromosomal diversity of this species, we conducted conventional chromosome staining, C-banding, CMA3/DAPI fluorochromes, and in situ hybridization with a telomere probe in samples from Argentina. Most specimens had the standard karyotype 2n = 24, although numerical variations due to aneuploidies and supernumerary (B) chromosomes were detected. We registered novel structural polymorphisms for pair 11 and sex chromosomes, and a rearrangement involving pairs 2 and 4, possibly due to a spontaneous chromosomal mutation. Most A. montensis females are homogametic with XX sex chromosomes, although XY and X0 females were observed. Most individuals carrying B chromosomes had 1 B and, to a lesser extent, 2 and 3 B. The chromosomal variability detected at the southern limit of A. montensis distribution is high and similar to other geographically distant populations, despite the fact that it could be a region recently colonized. Some of these variations are unique and could have originated independently in southern populations, while others are shared throughout the species distribution and may have originated earlier.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Beukeboom LW (1994) Bewildering Bs: an impression of the 1 st B-Chromosome Conference. Heredity 73:328–336

    Article  Google Scholar 

  • Bolzán AD, Bianchi MS (2006) Telomeres, interstitial telomeric repeat sequences, and chromosomal aberrations. Mutat Res 612:189–214

    Article  PubMed  Google Scholar 

  • Brandão VM, Percequillo AR, D’Elía G, Paresque R, Carmignotto AP (2021) A new species of Akodon Meyen, 1833 (Rodentia: Cricetidae: Sigmodontinae) endemic from the Brazilian Cerrado. J Mammal 102(1):101–122

    Article  Google Scholar 

  • Braun JK, Coyner BS, Mares MA, Van Den Bussche RA (2008) Phylogenetic relationships of South American grass mice of the Akodon varius group (Rodentia, Cricetidae, Sigmodontinae) in South America. J Mammal 89:768–777

    Article  Google Scholar 

  • Camacho JPM, Sharbel TF, Beukeboom LW (2000) B-chromosome evolution Philos Trans R Soc 355:163–178

    Article  CAS  Google Scholar 

  • Camacho JPM (2005) B chromosomes. In: Gregory TR (ed) The Evolution of the Genome. Elsevier, USA, pp 223–286

    Chapter  Google Scholar 

  • Carnaval AC, Moritz C (2008) Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic forest. J Biogeogr 35:1187–1201

    Article  Google Scholar 

  • Christoff AU, Fagundes V, Sbalqueiro YJ, Mattevi MS, Yonenaga-Yassuda Y (2000) Description of a new species of Akodon (Rodentia: Sigmodontinae) from Southern Brazil. J Mammal 81:838–851

    Article  Google Scholar 

  • Coyner BS, Braun JK, Mares MA, Van Den Bussche RA (2013) Taxonomic validity of species groups in the genus Akodon (Rodentia, Cricetidae). Zool Sc 42:335–350

    Article  Google Scholar 

  • Di Bitetti MS, Placci G, Dietz LA (2003) Una visión de biodiversidad para la Ecorregión del Bosque Atlántico del Alto Paraná: Diseño de un paisaje para la conservación de la biodiversidad y prioridades para las acciones de conservación. World Wildlife Fund, Washington, DC

    Google Scholar 

  • Evans EP, Breckon G, Ford CE (1964) An air-drying method for meiotic preparations from mammalian testes. Cytogenetics 3:289–294

    Article  CAS  PubMed  Google Scholar 

  • Fagundes V, Scalzi-Martin JM, Sims K, Hozier J, Yonenaga-Yassuda Y (1997) ZOO-FISH of a microdissection DNA library and G-banding patterns reveal the homeology between the Brazilian rodents Akodon cursor and A. montensis. Cytogenet Cell Genet 78:224–228

    Article  CAS  PubMed  Google Scholar 

  • Fagundes V, Christoff AU, Yonenaga-Yassuda Y (1998) Extraordinary chromosomal polymorphisms with 28 different karyotypes in the neotropical species Akodon cursor (Muridae, Sigmodontinae), one of the smallest diploid number in rodents (2n = 16, 15 and 14). Hereditas 129:263–274

    Article  CAS  PubMed  Google Scholar 

  • Fagundes V, Christoff A, Scalzi-Martin J, Hozier J, Moreira-Filho C, Yonenaga-Yassuda Y (2000) X;Y translocation revealed by chromosome microdissection and FISH infertile XY females in the Brazilian rodent Akodon montensis. Cytogenet Cell Genet 88:124–129

    Article  CAS  PubMed  Google Scholar 

  • Ford CE, Hamerton JL (1956) A colchicine, hypotonic citrate, squash sequence for mammalian chromosomes. Stain Technol 31:247–251

    Article  CAS  PubMed  Google Scholar 

  • Galindo-Leal C, Gusmão Câmara I (2003) The Atlantic Forest of South America: biodiversity status, threats and outlook. Island Press, Washington, USA

    Google Scholar 

  • Galliari C, Pardiñas U (2020) Roedores Cricétidos de la provincia de Misiones (Argentina): síntesis de los datos obtenidos tras una década de muestreos esporádicos. Ecología en Bolivia 56(1):42–64

    Google Scholar 

  • González EM, Langguth A, Oliveira LF (1998) A new species of Akodon from Uruguay and southern Brazil (Mammalia: Rodentia: Sigmodontinae). Comun Zool Mus Hist Nat Montevideo 191:1–8

    Google Scholar 

  • Jayat JP, Ortiz PE, Salazar-Bravo J, Pardiñas UFJ, D'Elía G (2010) The Akodon boliviensis species group (Rodentia: Cricetidae: Sigmodontinae) in Argentina: species limits and distribution, with the description of a new entity. Zootaxa 2409:1–61

    Article  Google Scholar 

  • John B (1988) The biology of heterochromatin. In: Verma RS (ed) Heterochromatin: Molecular and structural aspects. Cambridge University Press, Cambridge, UK, London, New York, pp 1–128

    Google Scholar 

  • Kasahara S, Yonenaga-Yassuda Y (1982) Chromosomal variability in Akodon sp. (Rodentia, Cricetidae). Cytologia 47:317–324

    Article  Google Scholar 

  • Kasahara S (2009) Introdução a Pesquisa em Citogenética de Vertebrados. In: Kassahara S (ed) Sociedade Brasileira de Genética, pp 9–160

    Google Scholar 

  • Labaroni C, Paez Coll Mairhofer VA, Ojeda AA, Novillo A, Teta P, Jayat P, Ojeda RA, Buschiazzo LM, Cálcena EN, Bolzán AD, Lanzone C (In press) Revision and analysis of the chromosome variability in the speciose genus Akodon (Rodentia, Sigmodontinae), including new data from Argentina. An Acad Bras Ciênc

  • Lanzone C, Labaroni CA, Suárez N, Rodríguez D, Herrera ML, Bolzán AD (2015) Distribution of telomeric sequences (TTA GGG) n in rearranged chromosomes of phyllotine rodents (Cricetidae, Sigmodontinae). Cytogenet Genome Res 147:247–252

    Article  PubMed  Google Scholar 

  • Liascovich RC, Reig OA (1989) Low Chromosomal number in Akodon cursor montensis Thomas, and karyologic confirmation of Akodon serrensis Thomas in Misiones Argentina. J Mammal 70:391–395

    Article  Google Scholar 

  • Lisanti JA, Pinna Senn E, Ortiz MI, Dalmasso G, Bella JL (2001) Characterization of the chromosomes of three species of Akodon (Rodentia, Sigmodontinae) by means of fluorochromes highly selective for DNA base composition. Cytologia 66:333–339

    Article  Google Scholar 

  • Malleret MM, Labaroni CA, García GV, Ferro JM, Martí DA, Lanzone C (2016) Chromosomal variation in Argentine populations of Akodon montensis Thomas, 1913 (Rodentia, Cricetidae, Sigmodontinae). Comp Cytogenet 10:129–140

    Article  PubMed  PubMed Central  Google Scholar 

  • Meyne J, Baker RJ, Hobart HH, Hsu TC, Ryder OA, Ward OD, Wiley JE, Wurster-Hill DH, Yates TL, Moyzis RK (1990) Distribution of nontelomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma 99:3–10

    Article  CAS  PubMed  Google Scholar 

  • Ortiz MI, Dalmasso G, Dezi R, Pinna Senn E, Lisanti JA (1998) A C-band polymorphism of the X chromosome in Akodon azarae (Rodentia, Cricetidae). Cytologia 63:365–369

    Article  Google Scholar 

  • Patton JL, Pardiñas UF, D’Elía G (2015) Mammals of South America. Volume 2. Rodents. University of Chicago Press, Chicago, Illinois

    Book  Google Scholar 

  • Rovatsos MT, Marchal JA, Romero-Fernández I, Fernández FJ, Giagia Athanosopoulou EB, Sánchez A (2011) Rapid, independent, and extensive amplification of telomeric repeats in pericentromeric regions in karyotypes of arvicoline rodents. Chromosome Res 19:869–882

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Herrera A, Nergadze SG, Santagostino M, Giulotto E (2008) Telomeric repeats far from the ends: mechanisms of origin and role in evolution. Cytogenet Genome Res 122:219–228

    Article  CAS  PubMed  Google Scholar 

  • Schweizer D (1976) Reverse Fluorescent Chromosome Banding with Chromomycin and DAPI. Chromosoma 58:307–324

    Article  CAS  PubMed  Google Scholar 

  • Silva MJ, Yonenaga-Yassuda Y (1998) Karyotype and chromosomal polymorphism of an undescribed Akodon from Central Brazil, a species with the lowest known diploid chromosome number in rodents. Cytogenet Cell Genet 81:46–50

    Article  CAS  PubMed  Google Scholar 

  • Silva MJJ, Yonenaga-Yassuda Y (2004) B chromosomes in Brazilian rodents. Cytogenet Genome Res 106:257–263

    Article  CAS  PubMed  Google Scholar 

  • Slijepcevic P (1998) Telomeres and mechanisms of Robertsonian fusion. Chromosoma 107:136–140

    Article  CAS  PubMed  Google Scholar 

  • Soares AA, Castro JP, Balieiro P, Dornelles S, Degrandi TM, Sbalqueiro IJ, Ferreira Artoni R, Hass I (2018) B Chromosome Diversity and Repetitive Sequence Distribution in an Isolated Population of Akodon montensis (Rodentia, Sigmodontinae). Cytogenet Genome Res 154:79–85

    Article  CAS  PubMed  Google Scholar 

  • Steinemann M, Steinemann S (2000) Common mechanisms of Y chromosome evolution. Genetica 109:105–111

    Article  CAS  PubMed  Google Scholar 

  • Sumner AT (1972) A simple technic for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306

    Article  CAS  PubMed  Google Scholar 

  • Tiranti SI (1998) Chromosomal variation in the scrub mouse Akodon molinae (Rodentia: Sigmodontinae) in central Argentina. Texas JSc 50:223–238

    Google Scholar 

  • Valdez L, D'Elía G (2013) Differentiation in the Atlantic Forest: phylogeography of Akodon montensis (Rodentia, Sigmodontinae) and the Carnaval-Moritz model of Pleistocene refugia. J Mammal 94:911–922

    Article  Google Scholar 

  • Ventura K, Silva MJJ, Fagundes V, Christoff UA, YonenagaYassuda Y (2006) Non-telomeric sites as evidence of chromosomal rearrangement and repetitive (TTAGGG)n arrays in heterochromatic and achromatic regions in four species of Akodon (Rodentia, Muridae). Cytogenet Genome Res 115:169–175

    Article  CAS  PubMed  Google Scholar 

  • Ventura K, O'Brien PCM, Yonenaga-Yassuda Y, Ferguson-Smith MA (2009) Chromosome homologies of the highly rearranged karyotypes of four Akodon species (Rodentia, Cricetidae) resolved by reciprocal chromosome painting: the evolution of the lowest diploid number in rodents. Chromosome Res 17:1063–1078

    Article  CAS  PubMed  Google Scholar 

  • Veyrunes F, Watson J, Robinson TJ, Britton-Davidian J (2007) Accumulation of rare sex chromosome rearrangements in the African pygmy mouse, Mus (Nannomys) minutoides: a whole-arm reciprocal translocation (WART) involving an X-autosome fusion. Chromosome Res 15:223–230

    Article  CAS  PubMed  Google Scholar 

  • Vujošević M, Rajičić M, Blagojević J (2018) B Chromosomes in Populations of Mammals Revisited. Genes 9:487

    Article  PubMed  PubMed Central  Google Scholar 

  • Waters PD, Wallis MC, Marshall Graves JA (2007) Mammalian sex Origin and evolution of the Y chromosome and SRY. Semin Cell Dev Biol 18:389–400

    Article  CAS  PubMed  Google Scholar 

  • Yonenaga-Yassuda Y, Kasahara S, Almeida EJC, Peracchi AL (1975) Chromosomal banding patterns in Akodon arviculoides (2n = 14), Akodon sp. (2n = 24 and 25) and two male hybrids with 19 chromosomes. Cytogenet Cell Genet 15:388–399

    Article  Google Scholar 

  • Yonenaga-Yassuda Y, Assis MFL, Kasahara S (1992) Variability of the nucleolus organizes regions and the presence of the rDNA genes in the supernumerary chromosome of Akodon aff. arviculoides (Cricetidae, Rodentia). Caryologia 45:163–174

    Article  Google Scholar 

Download references

Acknowledgements

We thank the anonymous referees for the substantial contribution to this work. The authors thank to the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET).

Funding

This research has been partially funded by Agencia Nacional de Promoción de la Investigación, el Desarrollo Tecnológico y la Innovación (ANPCyT), Préstamo BID 2016 PICT N° 537.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carolina A. Labaroni.

Ethics declarations

The authors have no competing interests to declare that are relevant to the content of this article.

Additional information

Communicated by: Jan M. Wójcik

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Labaroni, C.A., Ferro, J.M., Buschiazzo, L. et al. Extraordinary chromosome diversity in the southernmost populations of the montane grass mouse Akodon montensis (Cricetidae, Sigmodontinae). Mamm Res 68, 355–365 (2023). https://doi.org/10.1007/s13364-023-00687-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13364-023-00687-1

Keywords

Navigation