Skip to main content
SpringerLink
Log in

Variability of Minisatellite Loci and mtDNA in Individuals with and without B Chromosomes from Populations of the Grasshopper Dichroplus elongatus

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Dichroplus elongatus is an extensively distributed South American grasshopper considered a pest of major crops. Argentinean populations show a widespread B-chromosome polymorphism which could be maintained as the result trade-offs among opposite selective effects and interactions with their mitotic instability. The main objective of this study was to evaluate the relationships between B chromosomes and mtDNA sequences coupled with minisatellites loci, and verify the genotype/karyotype covariation in 12 populations located at both sides of Paraná River (Eastern and Western Regions). B carrier individuals showed significantly higher genetic diversity (HE and X) respect to standard individuals. AMOVAs based on nuclear loci and mtDNA sequence datasets showed statistically significant levels of differentiation among karyotypes in the Eastern Region. Cluster analysis through Bayesian procedure considering nuclear loci splits B carriers and standard individuals into different genetic clusters in some Eastern populations. The Bayesian phylogenetic analysis showed two divergent mtDNA clades. Haplogroup 1 is composed exclusively of standard individuals, however all B chromosome carriers are included in haplogroup 2. There is an association between some haplotypes and B chromosomes and a strong effect of phylogenetic signal on B chromosome population structure. Genetic differentiation between karyotypes at Eastern Region revealed by AMOVA, Bayesian approaches and clustering analysis based on uniparental and biparental inherited markers may be due to the inherent nature of the B chromosome, to karyotype biased dispersal or to difference tolerance of B chromosomes on different genetic background. The combination of molecular and chromosome analysis performed in this study indicated that B chromosomes in D. elongatus is an important factor in explaining the genetic population structure at minisatellite and mitochondrial DNA levels.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adnadevic, T., Bugarski-Stanojevic, V. Blagojevic J., Stamenkovic, G. Vujosevic M. (2012). Genetic differentiation in populations of the yellow-necked field mouse, Apodemus flavicollis, harbouring B chromosomes in different frequencies. Population Ecology 54, 537–548

    Article  Google Scholar 

  • Avise, J. C. (2000). Phylogeography: The history and formation of species. Cambridge: Harvard University Press.

    Google Scholar 

  • Benito, C., Llorente, F., Henriques-Gil, N., Gallego, F. J., Zaragoza, C., Delibes, A., & Figueiras, A. M. (1994). A map of rye chromosome 4R with cytological and izozyme markers. TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik, 87, 941–946.

    Article  CAS  PubMed  Google Scholar 

  • Benton, T. G., & Bowler, D. E. (2012) Dispersal in invertebrates: Influences on individual decisions. In: J. Clobert, M. Baguette, T. Benton & J. Bullock (Eds.) Dispersal ecology and evolution. (pp 41–49) Oxford: Oxford University Press.

    Chapter  Google Scholar 

  • Beukeboom, L. W. (1994). Bewildering Bs: An impression of the 1st B-chromosome conference. Heredity, 73, 328–336.

    Article  Google Scholar 

  • Blanchet, E., Lecoq, M., Sword, G. A., Pages, C., Blondini, L., Billot, C., Rivallan, R., Foucart, A., Vassal, J. M., Risterucci, A. M., & Chapuis, M. P. (2012). Population structures of three Calliptamus spp. (Orthoptera: Acrididae) across the Western Mediterranean Basin. European Journal of Entomology, 109, 445–455.

    Article  Google Scholar 

  • Bugarski-Stanojevic, V., Stamenkovic, G., Blagojevic, J., Liehr, T., Kosyakova, N., Rajicic, M., & Vujosevic, M. (2016). Exploring supernumeraries -A new marker for screening of B-chromosomes presence in the yellow necked mouse Apodemus flavicollis. PLoS ONE, 11(8), e0160946.

    Article  PubMed  PubMed Central  Google Scholar 

  • Burt, A., & Trivers, R. (1998). Selfish DNA and breeding system in flowering plants. Proceedings of the Royal Society of London. Series B, 265, 141–146.

    Article  PubMed Central  Google Scholar 

  • Cabral-de-Mello, D. C., Moura R. C., Martins C.: (2010) Chromosomal mapping of repetitive DNAs in the beetle Dichotomius geminatus provides the first evidence for an association of 5 S rRNA and histone H3 genes in insects, and repetitive DNA similarity between the B chromosome and A complement. Heredity, 104, 393–400.

    Article  CAS  PubMed  Google Scholar 

  • Camacho, J. P. M., Sharbel, T. F., & Beukeboon, L. W. (2000). B-chromosome evolution. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 355, 163–178.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clemente, M., Garma, C., De Sola, B. G., & Henriques-Gil, N. (2001). Steep variation in mitochondrial DNA and B chromosomes among natural populations of Eyprepocnemis plorans (Acrididae). Hereditas, 134(2), 135–140.

    Article  CAS  PubMed  Google Scholar 

  • Clemente, M., Remis, M. I., Vilardi, J. C., & Alberti, A. (1994). Supernumerary heterochromatin, chiasma conditions and abnormal sperm formation in Dichroplus elongatus (Orthoptera): intra and interpopulation analysis. Caryologia, 46, 321–335.

    Google Scholar 

  • Collinge, J. E., Hoffmann, A. A., & McKechnie, S. W. (2006). Altitudinal patterns for latitudinally varying traits and polymorphic markers in Drosophila melanogaster from eastern Australia. Journal of Evolutionary Biology, 19, 473–482.

    Article  CAS  PubMed  Google Scholar 

  • Coluzzi, M., Sabatini, A., Petrarca, V., & Di Deco, M. A. (1979). Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Transactions of the Royal Society of Tropical Medicine and Hygiene, 3(5), 483–497.

    Article  Google Scholar 

  • De Wysiecki, M.L., Cigliano M. M., Lange C. E. (1997). Fertility and longevity of Dichroplus elongatus adults (Orthoptera: Acrididae) under controlled conditions. Revista de la Sociedad Entomológica Argentina, 56 (1–4), 101–104.

    Google Scholar 

  • De Wysiecki, M. L., Torrusio S., Cigliano M. M. (2004). Caracterización de las comunidades de acridios (Orthoptera: Acridoidea) del partido de Benito Juárez, sudeste de la provincia de Buenos Aires, Argentina. Revista de la Sociedad Entomológica Argentina 63, 87–96.

    Google Scholar 

  • Excoffier, L., Lava, I., & Schneider, S. (2009). Arlequin version 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47–50.

    Google Scholar 

  • Excoffier, L., Smouse, P. E., & Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics, 131, 479–491.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hall, T.A. (1999). Bioedit: A user friendly biological sequence alignment editing and analysis program for Windows 95–98 NT. Nucleic Acid Symposium Series 41, 95–98.

    CAS  Google Scholar 

  • Harpending, H. C. (1994). Signature of ancient population-growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology, 66, 591–600.

    CAS  PubMed  Google Scholar 

  • Henriques-Gil, N., Santos, J. L., & Arana, P. (1984). Evolution of a complex polymorphism in the grasshopper Eyprepocnemis plorans. Chromosoma, 89, 290–293.

    Article  Google Scholar 

  • Hoffmann, A. A., Sgro, C. M., & Weeks, A. R. (2004). Chromosomal inversion polymorphisms and adaptation. Trends in Ecology and Evolution, 19(9), 482–488.

    Article  PubMed  Google Scholar 

  • Holsinger, K. E., Lewis, P. O., & Dipak, K. D. (2002). A Bayesian approach to inferring population structure from dominant markers. Molecular Ecology, 11, 1157–1164.

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck, J. P., & Ronquist, F. (2001). MrBayes: Bayesian inference of phylogeny. Bioinformatics (Oxford, England), 17, 754–755.

    Article  CAS  Google Scholar 

  • Jeanmougin, F., Thompson, J. D., Gouy, M., Higgins, D. G., & Gibson, T. J. (1998). Multiple sequence alignment with Clustal X. Trends in Biochemical Sciences, 23, 403–405.

    Article  CAS  PubMed  Google Scholar 

  • Jones, R. N., & Rees, H. (1982). B chromosomes. London: Academic Press.

    Google Scholar 

  • Kennington, W. J., & Hoffmann, A. A. (2013). Patterns of genetic variation across inversions: geographic variation in the ln(2L)t inversion in populations of Drosophila melanogaster in eastern Australia. BMC Evolutionary biology, 13, 100. doi:10.1186/1471-2148-13-100.

    Article  PubMed  PubMed Central  Google Scholar 

  • Krimbas, C. B. (1967). The genetics of Drosophila subobscura populations. 111. Inversion polymorphism and climatic factors. Molecular and General Genetics, 99, 133–150.

    Article  CAS  PubMed  Google Scholar 

  • Krimbas, C. B., & Powel, J. R. (1992). Drosophila inversion polymorphism. Boca Raton: CRC Press.

    Google Scholar 

  • Lange, C. E., Cigliano, M. M., & De Wysiecki, M. L. (2005). Los acridoideos (Orthoptera: Acridoidea) de importancia económica en la Argentina. En: Barrientos Lozano. In L. &amp & P. Almaguer Sierra (Eds.), Manejo integrado de la langosta centroamericana (Schistocerca piceifrons piceifrons Walker) y acridoideos plaga en América Latina. Instituto Tecnológico de Ciudad Victoria, Tamaulipas, México, pp. 93–135.

  • Lynch, M., & Milligan, B. G. (1994). Analysis of population genetic structure with RAPD markers. Molecular Ecology, 3, 91–99.

    Article  CAS  PubMed  Google Scholar 

  • Manel, S., Schwartz, M. K., Luikart, G., & Taberlet, P. (2003). Landscape genetics: combining landscape ecology and population genetics. Trends in Ecology & Evolution (Personal edition), 18, 189–197.

    Article  Google Scholar 

  • Manrique-Poyato, M. I., Lopez-Leon, M. D., Gomez, R., Camacho, J. P. M. (2013). Population Genetic Structure of the Grasshopper Eyprepocnemis plorans in the South and East of the Iberian Peninsula. PLoS ONE, 8 (3), e59041. doi:10.1371/journal.pone.0059041.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nei, M. (1987). Molecular evolutionary genetics. New York: Columbia University Press.

    Google Scholar 

  • Nei, M., & Jin, L. (1989). Variance of the average numbers of nucleotide substitutions within and between populations. Molecular Biology and Evolution, 6, 290–300.

    CAS  PubMed  Google Scholar 

  • Orengo, D. J., & Prevosti, A. (2002). Relationship between chromosomal polymorphism and wing size in a natural population of Drosophila subobscura. Genetica, 115, 311–318.

    Article  PubMed  Google Scholar 

  • Ortego, J., Bonal, R., Cordero, P. J., & Aparicio, J. M. (2009). Phylogeography of the Iberian populations of Mioscirtus wagneri (Orthoptera: Acrididae), a specialized grasshopper inhabiting highly fragmented hypersaline environments. Biological Journal of the Linnean Society, 97, 623–633.

    Article  Google Scholar 

  • Palestis, B.G., Trivers R., Burt A., Jones R.N. (2004). The distribution of B chromosomes across species. Cytogenetic and Genome Research. 106, 151–158.

    Article  CAS  PubMed  Google Scholar 

  • Parker, J. S., Jones, G. H., Edgar, L., & Whitehouse, C. (1991). The population cytogenetics of Crepis capillaris IV. The distribution of B chromosomes in British populations. Heredity, 66, 211–218.

    Article  Google Scholar 

  • Peakall, R. & Smouse P. E. (2001). GenAlEx V5: Genetic Analysis in Excel. Population genetic software for teaching and research. Australian National University, Canberra, Australia. (Online) Available with updates at http://www.anu.edu.au/BoZo/GenAlEx/.

  • Pimper, L.; Goodall N.; Olavarria C.; Baker S.; Remis M. I. (2010). Mitochondrial DNA variation and population structure of Commerson’s dolphins (Cephalorhynchus commersonii) in their southernmost distribution. Conservation Genetics, 11: 2157–2168.

    Article  Google Scholar 

  • Pritchard, J. K., Stephens, M., & Donnelly, P. J. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qi-luncc, Y., Ke-cheng Y., Guang-tang P., Ting-zhao R. (2007). A Comparative analysis of B chromosomes and genetic diversity in maize (Zea mays L.) landraces from Southwest China. Agricultural Sciences in China 10, 1166–1172.

    Google Scholar 

  • Ramos, E., Cardoso, A. L., Brown, J., Marques, D. F., Fanatinatti, B.E.A., Cabral de Mello, D. C., Oliveira, R. A., O’Neill, R. J., & Martins, C. (2016). The repetitive DNA element BncDNA, enriched in the B chromosome of the cichlid fish, Astatotilapia latifasciata, transcribes a potentially noncoding RNA. Chromosoma. doi:10.1007/s00412-016-0601-x.

    PubMed  Google Scholar 

  • Remis, M. I., & Vilardi, J. C. (1986). Meiotic behaviour and dosage effect of B chromosomes on recombination in Dichroplus elongatus (Orthoptera: Acrididae). Caryologia, 39, 287–308.

    Article  Google Scholar 

  • Rosetti, N., & Remis, M. I. (2012). Spatial genetic structure and mitochondrial DNA phylogeography of Argentinean populations of the grasshopper Dichroplus elongatus. PLoS ONE, 7(7), e40807. doi:10.1371/journal.pone.0040807.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosetti, N., & Remis, M. I. (2013). Latitudinal cline in the grasshopper Dichroplus elongatus: Coevolution of the A genome and B chromosomes? Journal of Evolutionary Biology, 26(4), 719–732.

    Article  CAS  PubMed  Google Scholar 

  • Rosetti, N., Vilardi, J. C., & Remis, M. I. (2007). Effects of B chromosome and supernumerary segments on morphometric traits and adult fitness components in the grasshopper, Dichroplus elongatus (Acrididae). Journal of Evolutionary Biology, 20, 249–259.

    Article  CAS  PubMed  Google Scholar 

  • Rosetti, N., Vilardi, J. C., & Remis, M. I. (2008). Effects of phenotype and B chromosomes on adult survival in the grasshopper Dichroplus elongatus (Orthoptera: Acrididae). Annals of the Entomological Society of America, 101, 922–929.

    Article  Google Scholar 

  • Ruiz-Ruano, F. J., Cuadrado, A., Montiel, E. E., Camacho J.P.M., & Lopez-León, M. D. (2015). Next generation sequencing and FISH reveal uneven and nonrandom microsatellite distribution in two grasshopper genomes. Chromosoma, 124, 221–234. doi:10.1007/s00412-014-0492-7.

    Article  CAS  PubMed  Google Scholar 

  • Selkoe, K. A., & Toonen, R. J. (2006). Microsatellites for Ecologist: A practical guide to using and evaluating microsatellite markers. Ecology Letters, 9, 615–629.

    Article  PubMed  Google Scholar 

  • Shaw, M. W. (1984). The Population genetics of the B-chromosome of Myrmeleotettix maculatus (Thunb.). (Orthoptera: Acrididae). Biological Journal of the Linnean Society, 23, 77–100.

    Article  Google Scholar 

  • Simard, F., Ayala, D., Kamdem, G., Pombi, M., Etouna, J., Ose, K., Fotsing, J. M., Fontenille, D., Besansky, N., & Costantini, C. (2009). Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: The ecological side of speciation. BMC Ecology, 9, 17–18.

    Article  PubMed  PubMed Central  Google Scholar 

  • Slatkin, M., & Hudson, R. R. (1991). Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics, 129, 555–562.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Statistica Statsoft Inc. (1996). Statistica 5 for Windows (Computer Program Manual). Statistica, Tulsa, OK.

  • Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 23, 585–595.

    Google Scholar 

  • Timmermans, M. J. T. N., Ellers, J., Marien, J., Verhoef, S. C., Ferwerda, E. B., & Van Straalen, N. M. (2005). Genetic structure in Orchesella cincta (Collembola): strong subdivision of European populations inferred from mtDNA and AFLP markers. Molecular Ecology, 14, 2017–2024.

    Article  CAS  PubMed  Google Scholar 

  • Tokarskaia, O. N., Efremova, D. A., Kan, N. G., Danilkin, A. A., Sempere, A., Petrosian, V. G.,. Semenova, S. K., & Ryskov, A. P. (2000). Variability of multilocus DNA markers in populations of the Siberian (Capreolus pygargus Pall.) and European (C. capreolus L.) roe deer. Genetika, 36(11), 1520–1530.

    CAS  PubMed  Google Scholar 

  • Vekemans, X., Beauwens, T., Lemaire, M., & Roldan-Ruiz, I. (2002). Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Molecular Ecology, 11, 139–151.

    Article  CAS  PubMed  Google Scholar 

  • Zhivotovsky, L. A. (1999). Estimating population structure in diploids with multilocus dominant DNA markers. Molecular Ecology, 8, 907–913.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Funding provided by CONICET (11220130100492CO) and Universidad de Buenos Aires (20020130100358BA) through grants to Dr. M.I. Remis is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, C1428EHA, Buenos Aires, Argentina

    N. Rosetti & M. I. Remis

Authors
  1. N. Rosetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. I. Remis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. I. Remis.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rosetti, N., Remis, M.I. Variability of Minisatellite Loci and mtDNA in Individuals with and without B Chromosomes from Populations of the Grasshopper Dichroplus elongatus . Evol Biol 44, 273–283 (2017). https://doi.org/10.1007/s11692-016-9406-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-016-9406-3

Keywords

Search

Navigation