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ANIMAL SCIENCE • An. Acad. Bras. Ciênc. 97 (suppl 2) • 2025 • https://doi.org/10.1590/0001-3765202520241253 linkcopy

Open-access Geographic variants of Boana crepitans and Boana xerophylla (Anura, Hylidae, Cophomantini) and their chromosomal diversification process

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Abstract

Boana crepitans and Boana xerophylla are species that, until recently, were a synonym of the former Hypsiboas crepitans. They were previously considered two discontinuous and widely distributed population of B. crepitans across different landscapes in Brazil. We analyzed B. crepitans chromosomes from six localities and B. xerophylla from two, using different chromosomal markers. All individuals of both species presented 2n=24 chromosomes and FN=48. The heterochromatin pattern was variable in B. crepitans from different localities, which allowed us to distinguish different geographical variants. The location of nucleolar organizer regions (NORs) was also variable among populations of B. crepitans, with single markings located in the chromosome pairs 7, 10 and 11, suggesting that NOR may be a valuable taxonomic marker for B. crepitans from each locality already cytogenetically studied, since it presented a unique chromosomal organization, likely product of local adaptation that may be associated to other pre-mating mechanisms which can contribute to geographically differentiation. The B. xerophylla individuals on the other hand, presented a conserved chromosomal organization, which may be related to its occurrence in a more homogeneous environment.

Key words
Amazon forest; atlantic forest; biomes; chromosomal rearrangements

INTRODUCTION

Even though the karyotype of some clades of frogs is well known (Schmid et al. 2010, Coelho et al. 2016, Ferro et al. 2018), cytogenetic studies on Cophomantini (i.e. a tribe of frogs in the subfamily Hylinae of the family Hylidae, commonly referenced as “True treefrogs”) is gaining some attention lately, and many species are still poorly studied. The Boana genus (formerly Hypsiboas) comprises 98 recognized Neotropical species clustered in seven clades or species groups (Faivovich et al. 2005, Frost 2024). The Boana faber group (Faivovich et al. 2005), for instance, harbor the species: Boana albomarginatus (Spix 1824), Boana crepitans (Wied 1824), Boana exastis (Caramaschi & Rodrigues 2003), Boana faber (Wied 1821), Boana lundii (Burmeister 1856), Boana pardalis (Spix 1824), Boana pugnax (Schmidt 1857) Boana rosen­bergi (Boulenger 1898), and Boana xerophylla (Dumeril & Bibron 1841). However, the relationship among genera and species are still under debate.

Boana crepitans and B. xerophylla, for instance, were only recently revalidated as a distinct species (Orrico et al. 2017). They were previously considered two discontinuous and widely distributed populations attributed to B. crepitans. Boana xerophylla is restricted to the Northwest of South America, occurring along Panamá, Venezuela, Colombia, Suriname, Guyanas, Brazil (Amazon Forest) (Donoso-Barros & Ochoa 1972, Lutz 1973, Macedo et al. 2011, Señaris et al. 2014, Frost 2024), and Trinidad and Tobago (Lehtinen 2014), whereas Boana crepitans is restricted to Eastern Brazil in the Atlantic Rainforest, Caatinga and Cerrado (Macedo et al. 2011). Although they are similar and closely related species, B. crepitans and B. xerophylla differ from each other in both morphological and molecular characteristics (Orrico et al. 2017). Cytogenetic data have also shown that different populations of Boana crepitans, despite presenting the same diploid number, differ in the macro and micro karyotypic structure (Carvalho et al. 2014). Boana xerophylla in turn, has not yet been studied from a cytogenetic point of view.

Here, considering the wide distribution and the existence of cryptic diversity in B. crepitans (Faivovich et al. 2005, Casal & Juncá 2008, Martins et al. 2009, Carvalho et al. 2014), and the absence of cytogenetic data for B. xerophylla, we performed a cytogenetic characterization of these two species along their distribution towards to contribute to the elucidation of the cryptic diversity evidenced in this neotropical anuran group.

MATERIALS AND METHODS

We analyzed 56 individuals of B. crepitans from six localities covering more than 1000 km along eastern Brazil and 29 individuals from two localities of B. xerophylla (Figure 1). The animal ethical committee of National Institute of Amazonian Research under protocol number 005/2016 approved the present study (SISBIO: 52426-2). The information of the coordinates of the collection sites, and the number of the individuals and sex are presented in Table I.

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Table I
List of the individuals used in the cytogenetic analyses.
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Figure 1
Collecting localities of Boana crepitans (1-6) and Boana xerophylla (7 and 8). Illustrations by Fabian Costa.

The chromosome preparations followed King & Rofe (1976), with slight modifications. The animals were treated with 1% colchicine solution for 24h and then euthanized through the administration of 5% lidocaine on the ventral skin to minimize suffering. Then, the intestinal epithelium was removed, washed and treated with distilled water for hypotonization for 60 minutes. After hypotonization step, we properly scraped the intestine epithelium and fixed in Carnoy’s solution. The specimens were deposited at the Herpetological Collections of Universidade Estadual do Sudoeste da Bahia - UESB, Universidade de São Paulo - USP and Instituto Nacional de Pesquisas da Amazônia - INPA.

The C-banding pattern was obtained according to Sumner (1972) and the detection of the Nucleolar Organizer Regions (NORs) was performed by silver nitrate impregnation following Howell & Black (1980). The chromosome spreads were stained with 5% Giemsa and the images were captured using an Olympus BX51 microscope (Olympus Corporation). The chromosomes were measured using the software ImageJ, 1.54g (Schneider et al. 2012) and the classification of the chromosomes followed Levan et al. (1964), according to their arm ratios.

The fluorescence in situ hybridization (FISH) procedures followed Viana et al. (2022), using 18S rDNA probes as described in Gross et al. (2010) labelled with Dig-Nick, Bio-Nick Translation Mix kit, Roche. Briefly, the chromosome slides were denatured in 70% formamide/2xSSC at 70°C for 4 minutes; spreads were dehydrated in ethanol (100%). Then, 20 µL of the hybridization mixture (100 ng of 18S rDNA probe, 50% deionized formamide, and 10% dextran sulfate) was dropped on the slides, and the hybridization was carried out for 24 h at 37°C in a moist chamber containing distilled water. The post-hybridization washes were performed once in 2× SSC (44°C, 5 min) and a final wash in 4× SSC/0.1% Tween (5 min, room temperature). The chromosomes were counterstained with DAPI (1.2 µg/mL) and mounted in antifade solution (Vector, Burlingame, CA, USA). We analyzed at least 20 metaphases per individual to confirm the karyotype structure, NOR sites, C-banding pattern and FISH results.

RESULTS

Almost all individuals of both analyzed species presented 2n = 24 chromosomes composed by metacentrics, submetacentrics and subtelocentrics, with a FN = 48. Individuals from different localities presented distinct karyotypic formulas (see Table II, Figure 2). Additionally, a single individual of B. crepitans from Capela-SE presented a 2n=25 chromosomes, due to the presence of an additional chromosome similar in size and shape to the eighth chromosome pair (Figure 2, 6 - Capela-SE).

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Table II
Karyotype formulas, NOR location and C-banding pattern of Boana crepitans and Boana xerophylla analyzed in the present study. We also included the chromosomal data of Boana crepitans from Wenceslau Guimarães - Bahia (Carvalho et al. 2014) and Piranhas - Alagoas (Gruber et al. 2007) for comparative purposes.
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Figure 2
Chromosomes of Boana crepitans and Boana xerophylla in Giemsa Staining and their respective sampling sites: (1) Florestal - BA, (2) Jequié - BA, (3) Maracás - BA, (4) Itapetinga - BA, (5) São Roque do Canaã - ES, (6) Capela - SE, (7) Caracarai - RR, (8) Pacaraima – RR. Illustrations by Fabian Costa.

In all populations, the chromosome morphology of the pairs 1, 2, 3, 5, 11, 12 remained conserved in all individuals/species, however, the morphology of the other chromosome pairs was variable (Table II, Figure 2).

The mapping of rDNA 18S confirmed the number and location of NORs observed by silver nitrate impregnation. These regions were located interstitially on the q arms of the pair 7 for the individuals of B. crepitans from Jequié – Bahia and on pair 11 for B. crepitans from Capela - Sergipe, B. crepitans from Florestal – Bahia, Maracás – Bahia, Itapetinga – Bahia, São Roque do Canaá - Espírito Santo and B. xerophylla from Caracaraí – Roraima and Pacaraima - Roraima (Table II, Figure 3 boxes).

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Figure 3
C-banding pattern, Ag-NOR sites detected by silver nitrate impregnation (white boxes) and 18S rDNA sites (dark boxes) in chromosomes of Boana crepitans and Boana xerophylla and theirs respective localities: (1) Florestal - BA, (2) Jequié - BA, (3) Maracás - BA, (4) Itapetinga - BA, (5) São Roque do Canaã - ES, (6) Capela - SE, (7) Caracarai - RR, (8) Pacaraima – RR. Illustrations by Fabian Costa.

All chromosomes in all individuals/species showed conspicuous heterochromatic blocks. B. xerophylla presented pericentromeric heterochromatic blocks in all chromosomes of the complement without variation, whereas B. crepitans presented particular heterochromatic pattern for each locality analyzed (Figure 3). The likely supernumerary chromosome of B. crepitans from Sergipe, presented the same heterochromatin pattern seen in pair 8 (Image not shown).

DISCUSSION

The chromosomal analysis of B. crepitans and B. xerophylla populations reinforce the proposition of a huge conservadorism of the macrostructure of the karyotype (2n = 24 and FN = 48) in most Boana species. This trait follows the general pattern found for Hylidae family as a whole, with few exceptions presenting reduction in the chromosome number (Gruber et al. 2007, Mattos et al. 2014, Ferro et al. 2018) or occurrence of supernumerary chromosomes (Gruber et al. 2007, 2014, Ferro et al. 2012, 2018, present study).

It is currently inferred that for Hylidae family, the most common 2n = 22 and 2n = 24 (Bogart 1973) derived from a 2n = 26 ancestral karyotype based on the phylogenetic framework provided by Faivovich et al. (2005) and Duellman et al. (2016). Analyzing the morphology of the chromosomes of the individuals from different localities of B. crepitans and B. xerophylla, six pairs (1, 2, 3, 5, 11 and 12) retained an evident conservatism in chromosome morphology. The other pairs slightly vary in relation to the centromere position between submetacentric and subtelocentrics (pairs 4 and 6) or between metacentric and submetacentric (pairs 7, 8, 9 and 10). Some of the small differences can represent only different condensation levels of the chromosomes, as a result of the technique. However, some differences in chromosomal morphology among populations surely could have a phylogenetic signal, so could indicate preliminary stages of genetic differentiation (Busin et al. 2006).

In the scenario where changes in chromosomal morphology occurs together with conservation of the diploid number and of the size of the chromosomes, one mechanism accepted for amphibian karyotypes is the pericentric inversion (Sumner 1990, Oliveira 2013, Carvalho et al. 2014). Speciation events have already been attributed to pericentric inversions for some Hylidae species, such as already reported for the genus Scinax (Oliveira 2013), where such rearrangements may prevent gene flow among populations (Schmid et al. 1991, Guerra 2004, Faria & Navarro 2010).

Chromosomal data, such as variations in number and chromosome morphology, have been used to distinguish morphologically similar species, as for instance Colostethus (Veiga-Menoncello et al. 2003) and Boana species (Giaretta & Aguiar Jr 1998). However, B. xerophylla and B. crepitans analyzed in the present study showed great chromosomal similarity in relation to morphology and chromosome number, with only the pair number 9 as the main difference between them. In this sense, we assume that despite chromosomes may have an active role in the genetic isolation processes, they are not the unique determinant factors.

For both species, we found the NOR sites located in a single chromosome pair (pair 7 or 11), which is a general feature for anurans (Schmid 1978). Ferro et al. (2018) stated that single NORs located on pair 11 would be a synapomorphy for Hylinae, and that NORs in other chromosome pairs (e.g., pair 7) would be a derived state for few species. Here we found that single and interstitial NORs located in the pair 11 is the most probable plesiomorphic feature for both species, as found for Boana faber group (Ferro et al. 2018).

The occurrence of the NORs in the pair 7 of B. crepitans from Wenceslau Guimarães, BA (Carvalho et al. 2014) and of B. crepitans from Jequié, BA (present study), as apomorphies, might indicate that the plesiomorphic state could vary more often than expected, even in different populations of the same species. Although some chromosomal features might indeed represent a phylogenetic signal, NOR variations in most cases are subproduct of chromosomal rearrangements that result in repositioning and location, therefore not necessarily correlate to phylogenetic distance among species and populations, especially given the polymorphic nature of NOR sites even in closely related species (Tymowska 1991, Viana et al. 2019, Karakus et al. 2024), being difficult to trace an evolutionary pathway for NOR pattern.

Both of our analyzed species presented pericentromeric heterochromatic blocks in almost all chromosomes of the complement, with some populations of B. crepitans showing interstitial and terminal blocks varying in position. Most of the Boana karyotypes described so far present heterochromatic blocks distributed mainly on pericentromeric regions of the chromosomes (Carvalho et al. 2014, Ferro et al. 2018) feature that is frequent for amphibians (Green & Sessions 2007). Although no clear pattern is observed among the populations of B. crepitans, this variation in the amount and distribution of heterochromatin can contribute to the chromosomal isolation mechanism, since this character rapidly changes during evolution, so that in some morphologically very similar anurans, hidden diversity may be evidenced by the karyotype differences, in the heterochromatin pattern or in the NORs position (John 1988, Siqueira et al. 2009, Oliveira 2013).

For a long time, herpetologists informally admitted cryptic diversity of B. crepitans group. In 2014, Carvalho et al. (2014) based on chromosomal data, reinforced this argument that was further supported by Orrico et al. (2017), with mitochondrial genes, showing that B. crepitans had at least two distinct evolutionary lineages. Based on the chromosomal differences found here, it is hard to propose the existence of independent evolutionary units, since the organization of the chromosomal macrostructure does not have any conspicuous pattern that clearly group the populations, and therefore appears to maintain a greater phylogeographic than phylogenetic pattern based on the phylogeny of Orrico et al. (2017). The evolution of macrostructural chromosomal characters can occur with a certain frequency and in a practically stochastic way, without necessarily directly affect the phylogenetic structure or reproductive success of a species (Damas et al. 2020). In this sense, we could not discard the existence of cryptic diversity on B. crepitans, as found on the recently described B. xerophylla (Escalona et al. 2021), but we assume that all variations found in the chromosome structure of this species are only populational variations.

This speciation scenario is plausible both for the absence of gene flow among the allopatric populations (Orr & Turelli 2001), as well as in populations occurring in sympatry or parapatry, provided that divergent natural selection exists or has existed or any other mechanism able of neutralizing gene flow (Faria & Navarro 2010).

As every locality exhibited a different pattern in their karyotype structure, it is possible to interpret such karyotypes particularities in two ways, (1) local adaptation with natural selection or (2) neutral divergence. If these adaptations were favored by the occurrence of alternative chromosomal rearrangements in each locality, as shown by Kirkpatrick & Barton (2006), natural selection may favor rearrangements that reduce the recombination of alleles involved in local adaptation, and they could be fixed and become genetic barriers, capable of leading to speciation. Or the variations encountered may be merely occasional, and if not leading to any disadvantage, could be fixed through the generations.

We can infer that the populations of B. xerophylla have the most conserved karyotype in comparison to its sister clade, as it presented only one macrostructural synapomorphy (pair 9 as submetacentric). Some authors believe that the dispersion of Boana spp. must have occurred from the Amazon region to the other biomes (Orrico et al. 2017). Analyzing the karyotype differences and similarities among the individuals of B. crepitans and B. xerophylla, their geographic distribution and the direction of the ancestral dispersion proposed in the literature (Costa 2003, Ledo & Colli 2017), it makes sense to believe that B. crepitans ancestor came from Amazon through the North and Northeastern Brazil, and that the occupation of the new areas favored the characters variation to emerge.

Looking for the almost inexistent structure of the cytogenetic data between the population, and between the two species B. xerophylla and B. crepitans, our data indicate the existence of the remaining cryptic diversity within B. crepitans. The macrostructural features of the karyotype of B. crepitans seems to be highly changeable through time, with every population or groups of population presenting unique particularities that does not resemble to any phylogenetic pattern. More studies, with an integrative approach focusing on cytogenomics and molecular markers will certainly fill in this gap and reveal the hidden diversity within B. crepitans group, potentially cryptic species or populational structure related to speciation processes.

Acknowledgements

We thank to Alexander Mônico, Anderson Rocha, “Guigó” for the collection of specimens; the directors of Parque Nacional do Viruá (Caracarai-RR), Museu de Biologia Professor Mello Leitão (Santa Tereza- ES) and Refúgio de Vida Silvestre Mata do Junco (Capela-SE) for his assistance during field trips. Financial support to this work was provided by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES - AUXPE – Pró Amazônia 3297/2013/Process 23038.009446/2013-09), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), (POSGRAD/ Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Centro de Estudos de Adaptação às Mudanças Ambientais na Amazônia (INCT ADAPTA II, FAPEAM/CNPq 573976/2008-2), MA received a study grant from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

References

  • BOGART JP. 1973. Evolution of anuran karyotypes. In: Vial JL (Ed), Evolutionary Biology of the Anurans: contemporary research on major problems. UM Press USA, p. 337-349
  • BUSIN CS, LIMA AP, DE ALMEIDA PRADO CP, STRUSSMANN C, JUNIOR SS & RECCO-PPIMENTEL SM. 2006. Chromosomal differentiation of populations of Lysapsus limellus limellus, L. l. bolivianus, and of Lysapsus caraya (Hylinae, Hylidae). Micron 37: 355-362.
  • CARVALHO MA, RODRIGUES MT, GARCIA C & SIQUEIRA S. 2014. Dynamics of chromosomal evolution in the genus Hypsiboas (Anura: Hylidae). Genet Mol Res 13: 7826-7838.
  • CASAL FC & JUNCÁ FA. 2008. Tadpole and advertisement call of Hypsiboas crepitans (Amphibia: Anura: Hylidae) from Bahia State, Brazil, and taxonomic regards. Bol Mus Para Emílio Goeldi 3: 217-224.
  • COELHO AC ET AL. 2016. Intra-generic and interspecific karyotype patterns of Leptodactylus and Adenomera (Anura, Leptodactylidae) with inclusion of five species from Central Amazonia. Genetica 144(1): 37-46.
  • COSTA LP. 2003. The historical bridge between the Amazon and the Atlantic Forest of Brazil: a study of molecular phylogeography with small mammals. J Biogeogr 30: 71-86.
  • DAMAS J, CORBO M & LEWIN HA. 2020. Vertebrate Chromosome Evolution. Annu Rev Anim Biosci 16(9): 1-27.
  • DONOSO-BARROS R & OCHOA JL. 1972. Desarrollo y evolucion larval de Hyla crepitans (Amphibia – Salientia). Bol Soc Biol Concepcion 44: 117-127.
  • DUELLMAN WE, MARION AB & HEDGES SB. 2016. Phylogenetics, classification, and biogeography of the treefrogs (Amphibia: Anura: Arboranae). Zootaxa 4104(01): 1-109.
  • ESCALONA M, LA MARCA E, CASTELLANOS M, FOUQUET A, CRAWFORD A, FERNANDO JM, ROJAS-RUNJAIC FJM, GIARETTA A, SEÑARIS JC & CASTROVIEJO-FISHER S. 2021. Integrative taxonomy reveals a new but common Neotropical treefrog, hidden under the name Boana xerophylla Zootaxa 4981(3): 401448.
  • FAIVOVICH J, HADDAD CFB, GARCIA PCA, FROST DR, CAMPBELL JA & WHEELER WC. 2005. Systematic review of the frog family Hylidae, with special reference to Hylinae: phylogenetic analysis and taxonomic revision. Bull Am Mus Nat Hist 294: 1-240.
  • FARIA R & NAVARRO A. 2010. Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol Evol 25: 660-669.
  • FERRO JM ET AL. 2018. Chromosome evolution in Cophomantini (Amphibia, Anura, Hylinae). PLoS ONE 13: e0192861.
  • FERRO JM, MARTI D, BIDAU C, SUAREZ P, NAGAMACHI CY & PIECZARKA JC. 2012. B chromosomes in the tree frog Hypsiboas albopunctatus (Anura: Hylidae). Herpetol 68(4): 482-490.
  • FROST DR. 2024. Amphibian species of the world: an online reference. Archived by WebCite. Available at: http://research.amnh.org/herpetology/amphibia/index.html Accessed on June 20, 2024.
    » http://research.amnh.org/herpetology/amphibia/index.html
  • GIARETTA AA & AGUIAR JR O. 1998. A new species of Megaelosia from the Mantiqueira Range, Southeastern Brazil. J Herpetol 32: 80-83.
  • GREEN DM & SESSIONS SK. 2007. Karyology and Cytogenetics. In: Heatwole H & Tyler M (Eds), Amphib Biol Surrey Beatty and Sons, Chipping Norton, p. 2756-2841.
  • 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.
  • GRUBER SL, DINIZ D, SOBRINHO-SCUDELER PE, FORESTI F, HADDAD CFB & KASAHARA S. 2014. Possible interspecific origin of the B chromosome of Hypsiboas albopunctatus (Spix 1824) (Anura, Hylidae), revealed by microdissection, chromosome painting, and reverse hybridization. Comp Cytogenet 8: 185-197.
  • GRUBER SL, HADDAD CFB & KASAHARA S. 2007. Chromosome banding in three species of Hypsiboas (Hylidae, Hylinae), with special reference to a new case of B-chromosome in anuran frogs and to the reduction of the diploid number of 2n = 24 to 2n = 22 in the genus. Genetica 130(3): 281-291.
  • GUERRA M. 2004. FISH: Conceitos e Aplicações na Citogenética. Sociedade Brasileira de Genética. Ribeirão Preto, 126 p.
  • HOWELL WM & BLACK DA. 1980. Controlled silver staining of nucleolar organizer regions with a protective colloidal developer: a 1-step method. Experientia 36: 1014-1015.
  • JOHN B. 1988. The biology of heterochromatin. In: Verma RS (Ed), Heterochromatin Molecular and Structural Aspects Cambridge Univ Press, UK, p. 1-47.
  • KARAKUS SU, GAFFAROĞLU M, AYATA MK & KNYTL M. 2024. A Detailed Karyological Investigation of three Endemic Cobitis Linnaeus, 1758 Species (Teleostei, Cobitidae) in Anatolia, Türkiye. Cytogenet and Genome Res 164(5-6): 243.
  • KING M & ROFE R. 1976. Karyotype variation in the Australian gekko Phyllodactylus marmoratus (Gray) (Gekkonidae: Reptilia). Chromosoma 54: 75-87.
  • KIRKPATRICK M & BARTON N. 2006. Chromosome inversions, local adaptation and speciation. Genetics 173: 419-434.
  • LEDO RMD & COLLI GR. 2017. The historical connections between the Amazon and the Atlantic Forest revisited. J Biogeogr 44: 2551-2563.
  • LEHTINEN RM. 2014. Confirmation of nest building in a population of the gladiator frog Hypsiboas crepitans (Anura, Hylidae) from the island of Tobago (West Indies). Herpetol Notes 7: 227-229.
  • LEVAN A, FREDGA K & SANDBERG AA. 1964. Nomenclature for Centromeric position on chromosomes. Hereditas 52: 201-220.
  • LUTZ B. 1973. Brazilian species of Hyla. UT Press Austin & London, 283 p.
  • MACEDO RG, ANDRADE EB & LEITE JRS. 2011. New record and distribution extension of Hypsiboas crepitans (Wied-Neuwied, 1824) (Anura, Hylidae) to the northern part of the state of Piauí, Brazil. Revista CEPSUL - Biodiv Con Mar 2: 30-33.
  • MARTINS FM, TEMPLETON AR, PAVAN ACO, KOHLBACH BC & MORGANTE JS. 2009. Phylogeography of the common vampire bat (Desmodus rotundus): Marked population structure, Neotropical Pleistocene vicariance and incongruence between nuclear and mtDNA markers. BMC Evol Biol 9: 1-13.
  • MATTOS DE TL, COELHO AC, SCHNEIDER CH, TELLES DOC, MENIN M & GROSS MC. 2014. Karyotypic diversity in seven Amazonian anurans in the genus Hypsiboas (family Hylidae). BMC Genetics 15(43): 1-13.
  • OLIVEIRA MPC. 2013. Cytogenetic variation in populations of Scinax tripui Lourenço Nascimento and Pires, 2009 (Anura, Hylidae): first detection of sexual chromosomes in the genus. Dissertação (Mestrado em Biologia e Manejo animal) - Universidade Federal de Viçosa 50p. Available at: http://locus.ufv.br/handle/123456789/2272. (Unpublished).
  • ORR HA & TURELLI M. 2001. The evolution of postzygotic isolation: accumulating Dobzhansky-Muller incompatibilities. Evolution 55: 1085-1094.
  • ORRICO VGD ET AL. 2017. Integrative taxonomy supports the existence of two distinct species within Hypsiboas crepitans (Anura: Hylidae). Salamandra 53: 99-113.
  • SCHMID G, LEHNERT A, MALM JO & BOVIN JO. 1991. Ligand-Stabilized Bimetallic Colloids Identified by Hrtem and Edx. Angew Chem Int 30: 874-876.
  • SCHMID M. 1978. Chromosome banding in Amphibia I. Constitutive heterochromatin and nucleolus organizer regions in Bufo and Hyla Chromosoma 66: 361-388.
  • SCHMID M, BOGART JP & HEDGES SB. 2010. The Chromosomes of Terraranan Frogs Insights into Vertebrate Cytogenetics. Cytogenet Genome Res 130-131: 1-568.
  • SCHNEIDER CA, RASBAND WS & ELICEIRI KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675.
  • SEÑARIS JC, MARGARITA L, ROJAS-RUNJAIC F & BARRIO-AMOROS CL. 2014. Guia ilustrada de los anfibios del Parque Nacional Canaima. Venezuela. Caracas.
  • SIQUEIRA S, AGUIAR JRO, PANSONATO A, GIARETTA AA, STRÜSS MANN C, MARTINS I & RECCO-PIMENTEL SM. 2009. The karyotype of three Brazilian Terrarana frogs (Amphibia, Anura) with evidence of a new Barycholos species. Gen Mol Biol 32: 470-476.
  • SUMNER AT. 1972. A simple technique for demonstrating centromeric heterochromatin. Cell Res 75: 304-306.
  • SUMNER AT. 1990. C-banding and related methods. In: Hyman U (Ed), Chromosome Banding, London, UK.
  • TYMOWSKA J. 1991. Polyploidy and cytogenetic variation in frogs of the genus Xenopus. In: Green DM & Sessions SK (Eds), Amphibian Cytogenetics and Evolution, San Diego: Academic Press, p. 259-297.
  • VEIGA-MENONCELLO ACP, LIMA AP & RECCO-PIMENTEL SM. 2003. Cytogenetic analysis of four central Amazonian species of Colostethus (Anura - Dendrobatidae) with a diploid complement of 22 chromosomes. Hereditas 139: 189-198.
  • VIANA PF, EZAZ T, DE BELLO CIOFFI M, JACKSON ALMEIDA B & FELDBERG E. 2019. Evolutionary insights of the ZW sex chromosomes in snakes: A new chapter added by the Amazonian puffing snakes of the genus Spilotes. Genes 10(4): 288.
  • VIANA PF, FELDBERG E, TAKAGUI FH, MENEZES S, VOGT RC & EZAZ T. 2022. Matamatas Chelus spp. (Testudines, Chelidae) have a remarkable evolutionary history of sex chromosomes with a long-term stable XY microchromosome system. Sci Rep 12(1): 6676.

Publication Dates

  • Publication in this collection
    20 Oct 2025
  • Date of issue
    2025

History

  • Received
    06 Nov 2025
  • Accepted
    04 May 2025
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