Skip to main content

Advertisement

SpringerLink
Log in

Population genetic structure and historical dispersal patterns in the subterranean rodent Ctenomys “chasiquensis” from the southeastern Pampas region, Argentina

  • Original investigation
  • Published:
Mammalian Biology Aims and scope Submit manuscript

Abstract

Gene flow plays an essential role in the evolutionary history of the organisms and helps to identify those historical landscape features that most likely had affected the dispersal patterns. In this work, we assess, using mitochondrial control region DNA sequences, the historical migration patterns and population structure in Ctenomys “chasiquensis”, a highly, vulnerable and endemic subterranean rodent distributed in a very small area from the central part of Argentina. We used Bayesian and maximum likelihood approaches to evaluate the effects of historical gene flow among populations. Moreover, we used Bayesian skyline plots, tests of neutrality and mismatch distributions to assess the potential changes in population size through time. Our analyses show that populations of C. “chasiquensis” are moderate structured at regional level and this population pattern is probably the result of an asymmetric historical gene flow essentially from the South-West to the North-West, further of a recent demographic population expansion in the North-West, in conjunction with an important degree of isolation in some populations over its eastern geographical range. Evidently, historical gene flow seems to have been more frequently on the West. Finally, a close relationship appears to exist between the major climatic episodes occurred during the Late Quaternary in the central region of Argentina and the main historical demographic changes inferred for C. “chasiquensis”. The current distribution of C. “chasiquensis” appear to be a relicts of a more extended historical distribution in the Argentinean Pampas in the Late Pleistocene, with a perceptible population decline at the beginning of the Holocene. In this context, Bayesian demographic inferences showed a small but constant increment of population expansion of this species from approximately 90,000 to 11,000 years BP, after which a period of decrease in population size (that started in the early Holocene and continues nowadays) was observed.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Beerli, P., Felsenstein,J., 2001. Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach, Proc. Natl. Acad. Sci. U. S. A. 98, 4563–4568.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brandelt, H.J., Forster, P., Röhl, A., 1999. Median-joining networks for inferring intraspecific phylogenies, Mol. Biol. Evol 16, 37–48.

    Article  Google Scholar 

  • Contreras, J.R., 1973. El tuco-tuco ysus relaciones con los problemas del suelo en la Argentina, Idia 29, 14–36.

    Google Scholar 

  • Contreras, J.R., Maceiras, A.J., 1970. Relaciones entre tucu-tucusy los procesos del suelo en la región semiárida del sudoeste bonaerense, Agro 12, 1–26.

    Google Scholar 

  • D’Elía, G., Lessa, E.P., Cook, J., 1999. Molecular phylogeny of tuco-tucos, genus Ctenomys (Rodentia: Octodontidae): evaluation of the mendocinus species group and the evolution of asymmetric sperm, J. Mammal. Evol. 6, 19–38.

    Article  Google Scholar 

  • Drummond, A.J., Rambaut, A., 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214.

    Google Scholar 

  • Drummond, A.J., Rambaut, A., Shapiro, B., Pybus, O.G., 2005. Bayesian coalescent inference of past population dynamics from molecular sequences, Mol. Biol. Evol. 22, 1185–1192.

    Article  CAS  PubMed  Google Scholar 

  • Excoffier, L, Laval, G., Schneider, S., 2005. Arlequin ver, 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. 1, 47–50, Online.

    CAS  Google Scholar 

  • Fasanella, M., Bruno, C, Cardoso, Y., Lizarralde, M., 2013. Historical demography and spatial genetic structure of the subterranean rodent Ctenomys magellanicus inTierradel Fuego (Argentina), Zool. J. Linn. Soc. 169, 697–710.

    Article  Google Scholar 

  • Fernández-Stolz, G.P., Stolz, J.F.B., Thales, R.O.F., 2007. Bottlenecks and dispersal in the tuco-tuco das dunas, Ctenomys flamarioni (Rodentia: Ctenomyidae): in Southern Brazil, J. Mammal. 88, 935–945.

    Article  Google Scholar 

  • Fu, Y.X., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection, Genetics 147, 915–925.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guindon, S., Gascuel, O., 2003. A simple fast, and accurate algorithm to estimate large phylogenies by maximum likelihood, Syst. Biol. 52, 696–704.

    PubMed  Google Scholar 

  • Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W., Gascuel, O., 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML3.0. Syst. Biol. 59, 307–321.

  • Harpending, H.C., Batzer, M.A., Gurven, M., Jorde, LB., Rogers, A.R., Sherry, S.T., 1998. Genetic traces of ancient demography, Proc. Natl. Acad. Sci. U. S. A. 95, 1961–1967.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hudson, R.R., Slatkin, M., Maddison, W.P., 1992. Estimation of levels of gene flow from DNA sequence data, Genetics 132, 583–589.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Iriondo, M., 1999. Climatic changes in the South American plains: records of a continent-scale oscillation. Quatern. Int. 57/58, 93–112.

    Google Scholar 

  • Kittlein, M.J., Gaggiotti, O., 2008. Interactions between environmental factors can preclude the detection of isolation by distance patterns: a case study of Ctenomys rionegrensis in Uruguay, Proc. R. Soc. Lon. B 275, 2633–2638.

    Article  Google Scholar 

  • Kocher, T.D., Thomas, W.K., Meyer, A., Edwards, S.V., Paabo, S., Villablanca, F., Wilson, A.C., 1989. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc. Natl. Acad. Sci. U S. A. 86, 6196–6200.

    Google Scholar 

  • Lessa, E.P., 2000. The evolution of subterranean rodents: a synthesis. In: Lacey, E.A., Patton, J.L., Cameron, G.N. (Eds.), Life Underground: The Biology of Subterranean Rodents. University of Chicago Press, Chicago and London, pp. 389–420.

    Google Scholar 

  • Librado, P., Rozas,J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data, Bioinformatics 25, 1451–1452.

    Article  CAS  PubMed  Google Scholar 

  • Manel, S., Gaggiotti, O.E., Waples, R.S., 2005. Assignment methods: matching biological questions with appropriate techniques, Trends Ecol. Evol. 20, 136–142.

    Article  PubMed  Google Scholar 

  • Mantel, N., 1967. The detection of disease clustering and a generalized regression approach, Cancer Res. 27, 209–220.

    CAS  PubMed  Google Scholar 

  • Mapelli, F.J., Kittlein, M.J., 2009. Influence of patch and landscape characteristics on the distribution of the subterranean rodent Ctenomys porteousi, Landscape Ecol. 24, 726–733.

    Article  Google Scholar 

  • Mapelli, F.J., Mora, M.S., Mirol, P.M., Kittlein, M.J., 2012a. Effects of quaternary climatic changes on the phylogeography and historical demography of the subterranean rodent Ctenomys porteousi. J. Zool. 286, 48–57.

    Article  Google Scholar 

  • Mapelli, F.J., Mora, M.S., Mirol, P.M., Kittlein, M.J., 2012b. Population structure and landscape genetics in the endangered subterranean rodent Ctenomys porteousi. Conserv. Genet. 13, 165–181.

    Article  Google Scholar 

  • Massarini, A.I., Barros, M.A., Ortells, M.O., Reig, O.A., 1991. Chromosomal polymorphism and small karyotypic differentiation in a group of Ctenomys species from central Argentina (Rodentia: Octodontidae), Genetica 83, 131–144.

    Article  Google Scholar 

  • Massarini, A.I., de Freitas, T.R.O., 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.

    Article  Google Scholar 

  • Miller, S.A., Dikes, D.D., Polesky, H.H., 1988. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 16, 215.

    Book  Google Scholar 

  • Mirol, P., Giménez, M.D., Searle,J.B., Bidau, C.J., Faulkes, C.G., 2010. Population and species boundaries in the South American subterranean rodent Ctenomys in a dynamic environment, Biol. J. Linn. Soc. 100, 368–383.

    Article  Google Scholar 

  • Mora, M.S., Lessa, E.P., Kittlein, M.J., Vassallo, A.I., 2006. Phylogeography of the subterranean rodent Ctenomys australis in sand-dune habitats: evidence of population expansion, J. Mammal. 87, 1192–1203.

    Article  Google Scholar 

  • Mora, M.S., Lessa, E.P., Cutrera, A.P., Kittlein, M.J., Vassallo, A.I., 2007. Phylogeographical structure in the subterranean tuco-tuco Ctenomys talarum (Rodentia: Ctenomyidae): contrasting the demographic consequences of regional and habitat-specific histories, Mol. Ecol. 16, 3453–3465.

    Article  CAS  PubMed  Google Scholar 

  • Mora, M.S., Cutrera, A.P., Lessa, E.P., Vassallo, A.I., D’Anatro, A., Mapelli, F.J., 2013. Phylogeography and population genetic structure of the Talas tuco-tuco (Ctenomys talarum): integrating demographic and habitat histories, J. Mammal. 94, 459–476.

    Article  Google Scholar 

  • Parada, A., D’Elía, G., Bidau, C.J., Lessa, E.P., 2011. Species groups and the evolutionary diversification of tuco-tucos, genus Ctenomys (Rodentia: Ctenomyidae), J. Mammal. 92, 671–682.

    Article  Google Scholar 

  • Posada, D., 2008. jModelTest: phylogenetic model averaging, Mol. Biol. Evol. 25, 1253–1256.

    CAS  PubMed  Google Scholar 

  • Prieto, A.R., 2000. Vegetational history of the late glacial-Holocene transition in the grassland of eastern Argentina, Palaeogeogr. Palaeocl. 157, 167–188.

    Article  Google Scholar 

  • Quattrocchio, M.E., Borromei, A.B., Deschamps, CM., Grill, S.C., Zavala, C.A., 2008. Landscape evolution and climate changes in the Late Pleistocene-Holocene, southern Pampa (Argentina): evidence from palynology, mammals and sedimentology, Quatern. Int. 181, 123–138.

    Article  Google Scholar 

  • Rambaut, A., 2012. FigTree v1.4 Program Distributed by the Authors (accesed 08.02.13.) https://doi.org/tree.bio.ed.ac.uk/software/figtree/last

  • Rambaut, A., Suchard, M.A., Xie, D., Drummond, A.J., 2014. Tracer v1.6, https://doi.org/beast.bio.ed.ac.uk/Tracer.

  • Ramos-Onsins, S.E., Rozas,J., 2002. Statistical properties of new neutrality test against population growth, Mol. Biol. Evol. 19, 2092–2100.

    Article  CAS  PubMed  Google Scholar 

  • Raymond, M., Rousset, F., 1995. Genepop (version 1.2): population genetics software for exact tests and ecumenicism, J. Heredity 86, 248–249.

    Article  Google Scholar 

  • Reig, O.A., Busch, C, Contreras, J., Ortells, M., 1990. An overview of evolution, systematic, population biology and molecular biology in Ctenomys. In: Nevo, E., Reig, O.A. (Eds.), Biology of Subterranean Mammals. Allan Liss, New York, pp. 71–96.

    Google Scholar 

  • Rosenberg, M.S., Anderson, CD., 2011. PASSaGE pattern analysis, spatial statistics and geographic exegesi, Version 2. Methods Ecol. Evol. 2, 229–232.

    Article  Google Scholar 

  • Schneider, S., Excoffier, L, 1999. Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA, Genetics 152, 1079–1089.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shikano, T., Shimada, T., Herzeg, G., Merilä, J., 2010. History vs: habitat type: explaining the genetic structure of European nine-spined stickleback (Pungitius pungitius) populations, Mol. Ecol. 19, 1147–1161.

    Article  PubMed  Google Scholar 

  • Slatkin, M., 1993. Isolation by distance in equilibrium and non-equilibrium populations, Evolution 47, 264–279.

    Article  PubMed  Google Scholar 

  • Slamovits, C.H., Cook, J.A., Lessa, E.P., Rossi, M.S., 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.

    Article  CAS  PubMed  Google Scholar 

  • Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism, Genetics 123, 585–595.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. MEGA6: molecular evolutionary genetics analysis version 6.0, Mol. Biol. Evol. 30, 2725–2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teta, P., Formoso, A., Tammone, M., De Tommaso, D., Fernández, F., Torres, J., Pardin˜as, U.F.J., 2014. Micromamíferos, cambio climático e impacto antrópico: ¿Cuánto han cambiado las comunidades del sur de América del Sur en los últimos 500 años? Therya 5, 7–38.

  • Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., Higgins, D.G., 1997. The CLUSTALX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools, Nucleic Acids Res. 25, 4876–4882.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tomasco, I.H., Lessa, E.P., 2007. Phylogeography of the tuco-tuco Ctenomys pearsoni: mtDNA variation and its implication for chromosomal differentiation. In: Kelt, D., Lessa, E.P., Salazar-Bravo,J., Patton, J.L. (Eds.), The Quintessential Naturalist: Honoring the Life and Legacy of Oliver P. Pearson. University of California Publications in Zoology, pp. 859–882.

    Google Scholar 

  • Tonni, E.P., Cione, A.L., Figini, A.J., 1999. Predominance of arid climates indicated by mammals in the pampas of Argentina during the Late Pleistocene and Holocene, Palaeogeogr. Palaeocl. 147, 257–281.

    Article  Google Scholar 

  • Weir, B.S., Cockerham, CC, 1984. Estimating F-statistics for the analysis of population structure, Evolution 38, 1358–1370.

    CAS  PubMed  Google Scholar 

  • Wlasiuk, G., Garza, J.C, Lessa, E.P., 2003. Genetic and geographic differentiation in the Río Negro tuco-tuco (Ctenomys rionegrensis): inferring the roles of migration and drift from multiple genetic markers, Evolution 57, 913–926.

    Article  PubMed  Google Scholar 

  • Zárate, M.A., Tripaldi, A., 2012. The aeolian system of central Argentina, Earth 3, 401–417.

    Google Scholar 

  • Zech, W., Zech, M., Zech, R., Peinemann, N., Morrás, H.J.M., Moretti, L., Oglef, N., Kalim, R.M., Fuchs, M., Schad, P., Glasera, B., 2009. Late Quaternary palaeosol records from subtropical (38°S) to tropical (16°S) South America and palaeoclimatic implications, Quatern. Int. 196, 107–120.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Instituto de Investigaciones Marinas y Costeras, (IIMyC, CONICET), Departamento de Biología, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, CP7600 Mar del Plata, Provincia de Buenos Aires, Argentina

    Matías Sebastián Mora, Fernando Javier Mapelli & Marcelo Javier Kittlein

  2. Área de Recursos Naturales, CONICET INTA EEA Bariloche, Provincia de Río Negro, CC277 8400, Bariloche, Argentina

    Aldana López

  3. Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Ángel Gallardo 470, Ciudad Autónoma de Buenos Aires, Argentina

    María Jimena Gómez Fernández & Patricia Mónica Mirol

Authors
  1. Matías Sebastián Mora
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fernando Javier Mapelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aldana López
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. María Jimena Gómez Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Patricia Mónica Mirol
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marcelo Javier Kittlein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matías Sebastián Mora.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mora, M.S., Mapelli, F.J., López, A. et al. Population genetic structure and historical dispersal patterns in the subterranean rodent Ctenomys “chasiquensis” from the southeastern Pampas region, Argentina. Mamm Biol 81, 314–325 (2016). https://doi.org/10.1016/j.mambio.2016.02.008

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.mambio.2016.02.008

Keywords

Search

Navigation