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Intra-generic and interspecific karyotype patterns of Leptodactylus and Adenomera (Anura, Leptodactylidae) with inclusion of five species from Central Amazonia

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Abstract

The genera Leptodactylus and Adenomera comprise 92 species distributed throughout the Neotropical region. These species have a modal diploid chromosome number 2n = 22. However, chromosome rearrangements are evident in the differentiation of five intra-generic groups in the genus Leptodactylus (L. fuscus, L. latrans, L. marmoratus (formally composed by the species of the genus Adenomera), L. melanonotus, L. pentadactylus), yet it is not clear if there is a karyotype pattern for each group. Aiming to understand the intra-generic and interspecific karyotype patterns of Leptodactylus and Adenomera, cytogenetic analyses were performed in A. andreae, L. macrosternum, L. pentadactylus, L. petersii, and L. riveroi using conventional staining, C-banding, nucleolus organizer region (NOR) and hybridization in situ fluorescent (FISH). The karyotype of Leptodactylus riveroi was described for the first time. Adenomera andreae had 2n = 26, while the remaining species 2n = 22. The NOR was found on pair No. 8 of A. andreae, L. macrosternum, L. pentadactylus, and L. riveroi, whereas L. petersii had it on pairs Nos. 6 and 10. These locations were confirmed by the FISH with 18S rDNA probe, except for pair No. 10 of L. petersii. The C-banding pattern was evident at the centromeres of chromosomes of all species and some interspecific variations were also observed. 2n = 22 was observed in the species of the L. latrans group, as well as in the intra-generic groups L. fuscus and L. pentadactylus; in the L. melanonotus group there were three diploid chromosome numbers 2n = 20, 22 and 24; and a larger variation in 2n was also evident in the L. marmoratus group.

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References

  • Amaro-Ghilardi RC, Rodrigues MT, Yonenaga-Yassuda Y (2004) Chromosomal studies after differential staining and fluorescence in situ hybridization using telomeric probe in three Leptodactylus species (Leptodactylidae, Anura). Caryologia 57:53–65

    Article  Google Scholar 

  • Amaro-Ghilardi RC, Skuk G, de Sá RO, Rodrigues MT, Yonenaga-Yassuda Y (2006) Karyotypes of eight species of Leptodactylus (Anura, Leptodactylidae) with a description of a new karyotype for the genus. Phyllomedusa 5:119–133

    Article  Google Scholar 

  • Andrades-Miranda J, Zanchin NIT, Oliveira LFB, Langguth AR, Mattevi MS (2002) (TTAGGG) n telomeric sequence hybridization indicating centric fusion rearrangements in karyotype of the rodent Oryzomys subflavus. Genetica 144:11–16

    Article  Google Scholar 

  • Angulo A, Icochea J (2010) Cryptic species complexes, widespread species and conservation: lessons from Amazonian frogs of the Leptodactylus marmoratus group (Anura: Leptodactylidae). Syst Biodivers 8:357–370

    Article  Google Scholar 

  • Angulo A, Cocroft RB, Reichle S (2003) Species identity in the genus Adenomera (Anura: Leptodactylidae) in southeastern Peru. Herpetologica 59:490–504

    Article  Google Scholar 

  • Arruda MP, Morielle-Versute E (2008) Cytogenetic and random amplified polymorphic DNA analysis of Leptodactylus species from rural and urban environments (Anura, Amphibia). Genet Mol Res 7:161–176

    Article  CAS  PubMed  Google Scholar 

  • Baldissera FA Jr, Oliveira PSL, Kasahara S (1993) Cytogenetics of four Brazilian Hyla species (Amphibia-Anura) and description of a case with a supernumerary chromosome. Rev Bras Genet 16:335–345

    Google Scholar 

  • Beçak ML (1968) Chromosomal analysis of eighteen species of Anura. Caryologia 21:191–208

    Article  Google Scholar 

  • Bogart JP (1973) Evolution of anuran karyotypes. In: Vial JL (ed) Evolutionary biology of the anurans: contemporary research on major problems. University of Missouri Press, Columbia, pp 337–349

    Google Scholar 

  • Bogart JP (1974) A karyosystematic study of frogs in the genus Leptodactylus (Anura: Leptodactylidae). Copeia 3:728–737

    Article  Google Scholar 

  • Bohne A, Brunet F, Galiana-Arnoux D, Schulthesis C, Volff JN (2008) Transposable elements as drivers of genomic and biological diversity in vertebrates. Chromosome Res 16:203–215

    Article  PubMed  Google Scholar 

  • Busin CS, Vinciprova G, Recco-Pimentel SM (2001) Chromosomal rearrangements as the source of variation in the number of chromosomes in Pseudis (Amphibia, Anura). Genetica 110:131–141

    Article  Google Scholar 

  • Campos JRC (2010) Constituição cariotípica em leptodactilídeos do gênero Leptodactylus e em espécies de famílias relacionadas à Leptodactylidae (Amphibia: Anura). Thesis, Universidade Estadual Paulista “Júlio de Mesquita Filho”

  • Campos JRC, Ananias F, Brasileiro CA, Yamamoto M, Haddad CFB, Kasahara S (2009) Chromosome evolution in three Brazilian Leptodactylus species (Anura, Leptodactylidae), with phylogenetic considerations. Hereditas 146:104–111

    Article  Google Scholar 

  • Coelho AC (2013) Citogenética comparativa de seis espécies de anuros do gênero Leptodactylus (Leptodactylidae) coletadas no estado do Amazonas, Brasil. Dissertation, Instituto Nacional de Pesquisas da Amazônia

  • Cole CJ, Leavens CR (1971) Chromosome preparations of amphibians and reptiles: improved technique. Herpetol Rev 3:102

    Google Scholar 

  • De Lucca E, Jim J (1974) Os cromossomos de alguns Leptodactylidae (Amphibia, Anura). Rev Bras Biol 34:407–410

    Google Scholar 

  • de Sá RO, Grant T, Camargo A, Heyer WR, Ponssa ML, Stanley E (2014) Systematics of the Neotropical genus Leptodactylus Fitzinger, 1826 (Anura: Leptodactylidae): phylogeny, the relevance of non-molecular evidence, and species accounts. S Am J Herpetol 9:S1–S128

    Article  Google Scholar 

  • Denaro L (1972) Karyotypes of Leptodactylidae anurans. J Herpetol 6:71–74

    Article  Google Scholar 

  • Ford C, Hamerton J (1956) A colchicine hypothonic citrate squash sequence for mammalian chromosomes. Stain Technol 31:247–251

    CAS  PubMed  Google Scholar 

  • Frost DR (2015) Amphibian species of the world: an online reference. Version 6.0. American Museum of Natural History, New York. http://research.amnh.org/vz/herpetology/amphibia/index.html. Accessed 24 April 2015

  • Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad CFB, de Sá RO, Channing A, Wilkinson M, Donnellan SC et al (2006) The amphibian tree of life. Bull Am Mus Nat Hist 297:1–370

    Article  Google Scholar 

  • Gazoni T, Gruber SL, Silva APZ, Araújo OGS, Narimatsu H, Strüssmann C, Haddad CFB, Kasahara S (2012) Cytogenetic analyses of eight species in the genus Leptodactylus Fitzinger, 1843 (Amphibia, Anura, Leptodactylidae), including a new diploid number and a karyotype with multiple translocations. BMC Genet 13:109

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Grant T, Frost DR, Caldwell JP, Gagliardo R, Haddad CFB, Kok PJR, Means DB, Noonan BP, Schargel WE, Wheeler WC (2006) Phylogenetic systematic of dart-poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae). Bull Am Mus Nat Hist 269:1–262

    Article  Google Scholar 

  • Green DM, Sessions SK (1991) Nomenclature for chromosomes. In: Green DM, Sessions SK (eds) Amphibian cytogenetics and evolution. Academic Press, New York, pp 431–432

    Google Scholar 

  • Green DM, Sessions SK (2007) Karyology and cytogenetics. In: Heatwole H, Tyler M (eds) Amphibian biology, vol 7. Surrey Beatty and Sons, Chipping Norton, pp 2756–2841

    Google Scholar 

  • Gross MC, Schneider CH, Valente GT, Martins C, Feldberg E (2010) Variability of 18S rDNA locus among Symphysodon fishes: chromosomal rearrangements. J Fish Biol 76:1117–1127

    Article  CAS  PubMed  Google Scholar 

  • Haddad CFB, Prado CPA (2005) Reproductive modes in frogs and their unexpected diversity in the Atlantic forest of Brazil. Bioscience 55:207–217

    Article  Google Scholar 

  • Heyer WR (1969) The adaptive ecology of the species groups of the frog genus Leptodactylus (Amphibia, Leptodactylidae). Evolution 23:421–428

    Article  Google Scholar 

  • Heyer WR (1974) Relationships of the marmoratus species group (Amphibia, Leptodactylidae) within the subfamily Leptodactylinae. Nat Hist Mus Los Angeles Co Contr Sci 256:1–46

    Google Scholar 

  • Howell WM, Black DA (1980) Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method. Experientia 36:1014–1015

    Article  CAS  PubMed  Google Scholar 

  • King M (1991) The evolution of heterochromatin in the Amphibian genome. In: Green DM, Session SK (eds) Amphibian cytogenetics and evolution. Academic Press, San Diego, pp 359–391

    Google Scholar 

  • Kuramoto M, Allison A (1989) Karyotypes of michrohylid frogs of Papua New Guinea and their systematic implication. Herpetologica 45:250–259

    Google Scholar 

  • Lima AP, Magnusson WE, Menin M, Erdtmann LK, Rodrigues DJ, Keller C, Hödl W (2012) Guia de Sapos da Reserva Adolpho Ducke, Amazônia Central = Guide to the Frogs to Reserva Adolpho Ducke, Central Amazonia, 2nd edn. Instituto Nacional de Pesquisas da Amazônia, Manaus

    Google Scholar 

  • López-Flores I, Garrido-Ramos MA (2012) The repetitive DNA content of eukaryotic genomes. In: Garrido-Ramos MA (ed) Repetitive DNA, vol 7. Karger, Basel, pp 1–28

    Chapter  Google Scholar 

  • Mattos TL, Coelho AC, Schneider CH, Telles OC, Menin M, Gross MC (2014) Karyotypic diversity in seven Amazonian anurans in the genus Hypsiboas (family Hylidae). BMC Genet 15:43

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Miura I, Niishioka M, Bordikin LJ, Wu Z (1995) The origin of the brown frogs with 2n = 24 chromosomes. Experientia 51:79–188

    Article  Google Scholar 

  • Morescalchi A (1973) Amphibia. In: Chiarelli AB, Capana E (eds) Cytotaxonomy and vertebrate evolution. Academic Press, New York, pp 233–348

    Google Scholar 

  • Oliveira HHP, Souza CCN, Ribeiro CL, da Cruz AD, Bastos RP, Melo e Silva D (2010) Citogenética comparativa das famílias Leptodactylidae e Hylidae do cerrado Goiano. Estudos 37:725–735

    Google Scholar 

  • Pinkel D, Straume T, Gray JW (1986) Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proc Natl Acad Sci USA 83:2934–2938

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ponssa ML (2008) Cladistic analysis and osteological descriptions of the frog species in the Leptodactylus fuscus species group (Anura, Leptodactylidae). J Zool Syst Evol Res 46:249–266

    Article  Google Scholar 

  • Pyron A, Wiens JJ (2011) A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol Phylogenet Evol 61:543–583

    Article  PubMed  Google Scholar 

  • Rocchi M, Archidiacono N, Schempp W, Capozzi O, Stanyon R (2012) Centromere repositioning in mammals. Heredity 108:59–67

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487–491

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, vol 1. Cold Spring Harbor Press, New York

    Google Scholar 

  • Silva APZ, Haddad CFB, Kasahara S (2000) Chromosomal studies on five species of the genus Leptodactylus Fitzinger, 1826 (Amphibia, Anura) using differential staining. Cytobios 103:25–38

    CAS  PubMed  Google Scholar 

  • Silva APZ, Garcia PCA, Martins VG, Bacci M, Kasahara S (2004) Chromosomal and molecular analyses of Leptodactylus gracilis gracilis, L. gracilis delattini, and L. plaumanni (Anura, Leptodactylidae): taxonomic implications. Amphib-Reptil 25:185–196

    Article  Google Scholar 

  • Silva APZ, Haddad CFB, Galassi G, Kasahara S (2006) Multiple nucleolus organizer regions in Leptodactylus mystacinus (Amphibia, Anura) and comments on its systematic position in the L. fuscus group based on cytogenetic and molecular analyses. Genetica 127:35–44

    Article  CAS  PubMed  Google Scholar 

  • Suárez P (2010) Estudos cromossômicos em anuros das famílias Hylidae Rafinesque, 1815 e Leptodactylidae Werner, 1896 (Amphibia: Anura). Thesis, Museu Paraense Emílio Goeldi/Universidade Federal do Pará

  • Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 74:304–306

    Article  Google Scholar 

  • Sumner AT (1990) Chromosome banding. Unwin Hyman Ltd., London

    Google Scholar 

  • Vittorazzi SE, Lourenço LB, Recco-Pimentel SM (2014) Long-time evolution and highly dynamic satellite DNA in leptodactylid and hylodid frogs. BMC Genet 15:111

    Article  PubMed Central  PubMed  Google Scholar 

  • Wiley JE, Meyne J, Little MN, Stout JC (1992) Interstitial hybridization sites of the (TTAGGG)ntelomeric sequence on the chromosomes of some North American hylid frogs. Cytogenet Cell Genet 51:55–57

    Article  Google Scholar 

  • Zaracho VH, Hernando AB (2011) The karyotype of Adenomera diptyx (Boettger 1885) (Anura, Leptodactylidae) from northeastern Argentina. Genet Mol Biol 34:84–87

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank Anne Baldisseri for the English review; Alexandre Almeida and Karla da Silva for granting use of facilities at the INPA and UFAM Zoological Collection; the Herpetology group from the SISBIOTA project for collection and identification of some specimens. Financial support was provided by Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (CNPq # 573976/2008-2, 558318/2009-6, 563348/2010-0; FAPEAM # 062.00383/2013; FAPEAM # 20/2013; FAPEAM/CNPq 062.02317/2011). The current study was supported by graduate fellowships from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) to ACC and TLM and a Research Productivity grant from CNPq to MM and FAPEAM to MCG.

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  1. Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo, 2936, Manaus, AM, 69080-971, Brazil

    Ana Carolina Coelho, Thais Lemos de Mattos & Patrik Viana

  2. Universidade Federal da Integração Latino-Americana, Av. Silvio Américo Sasdelli, 1842 - Vila A, Foz do Iguaçu, PR, CEP 85866-000, Brazil

    Maria Leandra Terencio

  3. Laboratório de Citogenômica, Departamento de Biologia, Instituto de Ciências Biológicas, Universidade Federal do Amazonas, Av. General Rodrigo Octávio Jordão Ramos, 3000, Manaus, AM, 69077-000, Brazil

    Ana Carolina Coelho, Carlos Henrique Schneider, Marcelo Menin & Maria Claudia Gross

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  1. Ana Carolina Coelho
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Coelho, A.C., de Mattos, T.L., Viana, P. et al. Intra-generic and interspecific karyotype patterns of Leptodactylus and Adenomera (Anura, Leptodactylidae) with inclusion of five species from Central Amazonia. Genetica 144, 37–46 (2016). https://doi.org/10.1007/s10709-015-9876-8

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