Chromosome evolution in Lophyohylini (Amphibia, Anura, Hylinae)

Pablo Suárez; Juan M. Ferro; Cleusa Y. Nagamachi; Dario E. Cardozo; Ailin Blasco-Zúñiga; Jéssica B. Silva; Euvaldo Marciano; Marco A. Costa; Victor G.D. Orrico; Mirco Solé; Igor J. Roberto; Miryan Rivera; John E. Wiley; Julián Faivovich; Diego Baldo; Julio C. Pieczarka

doi:10.1371/journal.pone.0234331

Chromosome evolution in Lophyohylini (Amphibia, Anura, Hylinae)

Pablo Suárez
, Juan M. Ferro^*
, Cleusa Y. Nagamachi
, Dario E. Cardozo
, Ailin Blasco-Zúñiga
, Jéssica B. Silva
, Euvaldo Marciano
, Marco A. Costa
, Victor G.D. Orrico
, Mirco Solé
, Igor J. Roberto
, Miryan Rivera
, John E. Wiley
, Julián Faivovich
, Diego Baldo^*
, Julio C. Pieczarka

^*Corresponding author for this work

Faculty of Exact and Natural Sciences

Research output: Contribution to journal › Article › peer-review

6 Scopus citations

Abstract

The hyline tribe Lophyohylini includes 87 species of treefrogs, of which cytogenetics aspects have been studied in less than 20% of them. In order to evaluate the evolution of some of its chromosome characters (NOR position, C-bands, and DAPI/CMA₃ bands), we studied the karyotypes of 21 lophyohylines, 16 of them for the first time, and analyzed them in a phylogenetic context. Most species showed similar karyotypes regarding chromosome number (2n = 24) and morphology (FN = 48), excepting Phyllodytes edelmoi and Osteocephalus buckleyi with 2n = 22 (FN = 44) and 2n = 28 (FN = 50), respectively. The NOR location was variable among species and provided valuable phylogenetic information. This marker was located in pair 11 in all species of Trachycephalus, Itapotihyla langsdorffii, and Nyctimantis arapapa, representing the plesiomorphic condition of Lophyohylini. Besides, other apomorphic states were recovered for the clades comprising N. rugiceps and N. siemersi (NOR in pair 5), and Dryaderces pearsoni, Osteocephalus, and Osteopilus (NOR in pair 9). Phyllodytes presented variation for NORs position; they were in pair 2 in P. edelmoi, pair 7 in P. melanomystax, and pair 8 in P. gyrinaethes and P. praeceptor. Polymorphisms in size, number, and activity of this marker were observed for N. siemersi, Osteocephalus fuscifacies, and some species of Trachycephalus. Remarkably, in N. siemersi NORs were detected on a single chromosome in the two specimens studied by this technique, raising the question of how this complex polymorphism is maintained. Interstitial telomeric sequences were found in P. edelmoi,P. melanomystax, and Osteocephalus buckleyi, and their presence seems to be not related to the chromosome reorganization events. Finally, some species showed spontaneous rearrangements, possibly as a consequence of an uncommon phenomenon in anuran cytogenetics: the presence of fragile sites or secondary constrictions not associated with NORs. We propose that this rare feature would have played an important role in the evolution of this group of frogs. From the evidence obtained in this and previous studies, we conclude that Lophyohylini presents a complex chromosome evolution.

Original language	English
Article number	e0234331
Journal	PLoS ONE
Volume	15
Issue number	6 1
DOIs	https://doi.org/10.1371/journal.pone.0234331
State	Published - 11 Jun 2020

Bibliographical note

Publisher Copyright:
© 2020 Suárez et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding

JMF is grateful to the Universidad Nacional de Misiones (16Q001-TI). DB and JF thanks Agencia Nacional de Promoción Científica y Tecnológica (PICTs 2013-404, 2015-820, 2015-2381, PICT 2018-3349). CYN and JCP aknowledge Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), the Fundação Amazônia Paraense de Amparo à Pesquisa (FAPESPA) and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) on projects coordinated by CY Nagamachi (Edital BIONORTE-CNPq, Proc 552032/2010-7; Edital BIONORTE-FAPESPA, ICAAF 007/2011; Edital Pró-Amazônia Proc 047/ 2012); the FAPESPA (Edital Vale - Proc 2010/ 110447) and Banco Nacional de Desenvolvimento Econômico e Social - BNDES (Operação 2.318.697.0001) on a project coordinated by JC Pieczarka. ABZ y MR appreciate the partial financing of this research by Research Directory of the Pontificia Universidad Católica del Ecuador project code QINV0046 - IINV529010100. EMJ thanks Fundação de Amparo à Pesquisa da Bahia - FAPESB (#8952/2014) for the doctoral grant, Fundação de Amparo à Pesquisa e Inovação do Espírito Santo - FAPES (Processo 78252482) for post doctoral Grant and Rede Baiana de Pesquisas sobre Anfíbios for partially funding this project. IJR thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES)-Finance code 001 doctoral fellowship (88882.156872/2016-01). VGDO was supported with a CNPq fellow (#310467/2017-9) PS, JMF, DC, JF, and DB thank the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). PS, JMF, DC, and DB also thank the Universidad Nacional de Misiones (UNaM). CYN and JCP are grateful to the Universidade Federal do Pará. We thank J.M. Boeris for helping in the collection of some specimens from Argentina. CYN, VGDO, and JCP to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). ABZ, MR acknowledge to Santiago Ron (Museo de Zoología QCAZ) and Andrés Merino (Balsa de los Sapos project from PUCE) for providing specimens and for species identification. TNT was provided free by the Willi Hennig Society.

Funders	Funder number
John Merck Fund
Willi Hennig Society
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior	110447, 047/ 2012, 552032/2010-7, ICAAF 007/2011
Consejo Nacional de Investigaciones Científicas y Técnicas
Agencia Nacional de Promoción Científica y Tecnológica	PICTs 2013-404, 2015-820, 2015-2381, PICT 2018-3349
Conselho Nacional de Desenvolvimento Científico e Tecnológico
Fundação Amazônia Paraense de Amparo à Pesquisa
Fundação de Amparo à Pesquisa do Estado da Bahia	8952/2014
Fundação de Amparo à Pesquisa e Inovação do Espírito Santo	78252482, 310467/2017-9, 88882.156872/2016-01
Universidade Federal do Pará
Pontifical Catholic University of Ecuador	QINV0046 - IINV529010100
Universidad Nacional de Misiones	16Q001-TI
Banco Nacional de Desenvolvimento Econômico e Social	2.318.697.0001

Access to Document

10.1371/journal.pone.0234331

Cite this

Suárez, P., Ferro, J. M., Nagamachi, C. Y., Cardozo, D. E., Blasco-Zúñiga, A., Silva, J. B., Marciano, E., Costa, M. A., Orrico, V. G. D., Solé, M., Roberto, I. J., Rivera, M., Wiley, J. E., Faivovich, J., Baldo, D., & Pieczarka, J. C. (2020). Chromosome evolution in Lophyohylini (Amphibia, Anura, Hylinae). PLoS ONE, 15(6 1), Article e0234331. https://doi.org/10.1371/journal.pone.0234331

@article{1b954b6c91eb48f7bb29b2170247f01d,

title = "Chromosome evolution in Lophyohylini (Amphibia, Anura, Hylinae)",

abstract = "The hyline tribe Lophyohylini includes 87 species of treefrogs, of which cytogenetics aspects have been studied in less than 20\% of them. In order to evaluate the evolution of some of its chromosome characters (NOR position, C-bands, and DAPI/CMA3 bands), we studied the karyotypes of 21 lophyohylines, 16 of them for the first time, and analyzed them in a phylogenetic context. Most species showed similar karyotypes regarding chromosome number (2n = 24) and morphology (FN = 48), excepting Phyllodytes edelmoi and Osteocephalus buckleyi with 2n = 22 (FN = 44) and 2n = 28 (FN = 50), respectively. The NOR location was variable among species and provided valuable phylogenetic information. This marker was located in pair 11 in all species of Trachycephalus, Itapotihyla langsdorffii, and Nyctimantis arapapa, representing the plesiomorphic condition of Lophyohylini. Besides, other apomorphic states were recovered for the clades comprising N. rugiceps and N. siemersi (NOR in pair 5), and Dryaderces pearsoni, Osteocephalus, and Osteopilus (NOR in pair 9). Phyllodytes presented variation for NORs position; they were in pair 2 in P. edelmoi, pair 7 in P. melanomystax, and pair 8 in P. gyrinaethes and P. praeceptor. Polymorphisms in size, number, and activity of this marker were observed for N. siemersi, Osteocephalus fuscifacies, and some species of Trachycephalus. Remarkably, in N. siemersi NORs were detected on a single chromosome in the two specimens studied by this technique, raising the question of how this complex polymorphism is maintained. Interstitial telomeric sequences were found in P. edelmoi,P. melanomystax, and Osteocephalus buckleyi, and their presence seems to be not related to the chromosome reorganization events. Finally, some species showed spontaneous rearrangements, possibly as a consequence of an uncommon phenomenon in anuran cytogenetics: the presence of fragile sites or secondary constrictions not associated with NORs. We propose that this rare feature would have played an important role in the evolution of this group of frogs. From the evidence obtained in this and previous studies, we conclude that Lophyohylini presents a complex chromosome evolution.",

author = "Pablo Su{\'a}rez and Ferro, \{Juan M.\} and Nagamachi, \{Cleusa Y.\} and Cardozo, \{Dario E.\} and Ailin Blasco-Z{\'u}{\~n}iga and Silva, \{J{\'e}ssica B.\} and Euvaldo Marciano and Costa, \{Marco A.\} and Orrico, \{Victor G.D.\} and Mirco Sol{\'e} and Roberto, \{Igor J.\} and Miryan Rivera and Wiley, \{John E.\} and Juli{\'a}n Faivovich and Diego Baldo and Pieczarka, \{Julio C.\}",

note = "Publisher Copyright: {\textcopyright} 2020 Su{\'a}rez et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.",

year = "2020",

month = jun,

day = "11",

doi = "10.1371/journal.pone.0234331",

language = "English",

volume = "15",

journal = "PLoS ONE",

issn = "1932-6203",

publisher = "Public Library of Science",

number = "6 1",

}

TY - JOUR

T1 - Chromosome evolution in Lophyohylini (Amphibia, Anura, Hylinae)

AU - Suárez, Pablo

AU - Ferro, Juan M.

AU - Nagamachi, Cleusa Y.

AU - Cardozo, Dario E.

AU - Blasco-Zúñiga, Ailin

AU - Silva, Jéssica B.

AU - Marciano, Euvaldo

AU - Costa, Marco A.

AU - Orrico, Victor G.D.

AU - Solé, Mirco

AU - Roberto, Igor J.

AU - Rivera, Miryan

AU - Wiley, John E.

AU - Faivovich, Julián

AU - Baldo, Diego

AU - Pieczarka, Julio C.

N1 - Publisher Copyright: © 2020 Suárez et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

PY - 2020/6/11

Y1 - 2020/6/11

N2 - The hyline tribe Lophyohylini includes 87 species of treefrogs, of which cytogenetics aspects have been studied in less than 20% of them. In order to evaluate the evolution of some of its chromosome characters (NOR position, C-bands, and DAPI/CMA3 bands), we studied the karyotypes of 21 lophyohylines, 16 of them for the first time, and analyzed them in a phylogenetic context. Most species showed similar karyotypes regarding chromosome number (2n = 24) and morphology (FN = 48), excepting Phyllodytes edelmoi and Osteocephalus buckleyi with 2n = 22 (FN = 44) and 2n = 28 (FN = 50), respectively. The NOR location was variable among species and provided valuable phylogenetic information. This marker was located in pair 11 in all species of Trachycephalus, Itapotihyla langsdorffii, and Nyctimantis arapapa, representing the plesiomorphic condition of Lophyohylini. Besides, other apomorphic states were recovered for the clades comprising N. rugiceps and N. siemersi (NOR in pair 5), and Dryaderces pearsoni, Osteocephalus, and Osteopilus (NOR in pair 9). Phyllodytes presented variation for NORs position; they were in pair 2 in P. edelmoi, pair 7 in P. melanomystax, and pair 8 in P. gyrinaethes and P. praeceptor. Polymorphisms in size, number, and activity of this marker were observed for N. siemersi, Osteocephalus fuscifacies, and some species of Trachycephalus. Remarkably, in N. siemersi NORs were detected on a single chromosome in the two specimens studied by this technique, raising the question of how this complex polymorphism is maintained. Interstitial telomeric sequences were found in P. edelmoi,P. melanomystax, and Osteocephalus buckleyi, and their presence seems to be not related to the chromosome reorganization events. Finally, some species showed spontaneous rearrangements, possibly as a consequence of an uncommon phenomenon in anuran cytogenetics: the presence of fragile sites or secondary constrictions not associated with NORs. We propose that this rare feature would have played an important role in the evolution of this group of frogs. From the evidence obtained in this and previous studies, we conclude that Lophyohylini presents a complex chromosome evolution.

AB - The hyline tribe Lophyohylini includes 87 species of treefrogs, of which cytogenetics aspects have been studied in less than 20% of them. In order to evaluate the evolution of some of its chromosome characters (NOR position, C-bands, and DAPI/CMA3 bands), we studied the karyotypes of 21 lophyohylines, 16 of them for the first time, and analyzed them in a phylogenetic context. Most species showed similar karyotypes regarding chromosome number (2n = 24) and morphology (FN = 48), excepting Phyllodytes edelmoi and Osteocephalus buckleyi with 2n = 22 (FN = 44) and 2n = 28 (FN = 50), respectively. The NOR location was variable among species and provided valuable phylogenetic information. This marker was located in pair 11 in all species of Trachycephalus, Itapotihyla langsdorffii, and Nyctimantis arapapa, representing the plesiomorphic condition of Lophyohylini. Besides, other apomorphic states were recovered for the clades comprising N. rugiceps and N. siemersi (NOR in pair 5), and Dryaderces pearsoni, Osteocephalus, and Osteopilus (NOR in pair 9). Phyllodytes presented variation for NORs position; they were in pair 2 in P. edelmoi, pair 7 in P. melanomystax, and pair 8 in P. gyrinaethes and P. praeceptor. Polymorphisms in size, number, and activity of this marker were observed for N. siemersi, Osteocephalus fuscifacies, and some species of Trachycephalus. Remarkably, in N. siemersi NORs were detected on a single chromosome in the two specimens studied by this technique, raising the question of how this complex polymorphism is maintained. Interstitial telomeric sequences were found in P. edelmoi,P. melanomystax, and Osteocephalus buckleyi, and their presence seems to be not related to the chromosome reorganization events. Finally, some species showed spontaneous rearrangements, possibly as a consequence of an uncommon phenomenon in anuran cytogenetics: the presence of fragile sites or secondary constrictions not associated with NORs. We propose that this rare feature would have played an important role in the evolution of this group of frogs. From the evidence obtained in this and previous studies, we conclude that Lophyohylini presents a complex chromosome evolution.

UR - https://www.scopus.com/pages/publications/85086424411

U2 - 10.1371/journal.pone.0234331

DO - 10.1371/journal.pone.0234331

M3 - Article

C2 - 32525943

AN - SCOPUS:85086424411

SN - 1932-6203

VL - 15

JO - PLoS ONE

JF - PLoS ONE

IS - 6 1

M1 - e0234331

ER -

Chromosome evolution in Lophyohylini (Amphibia, Anura, Hylinae)

Abstract

Bibliographical note

Funding

Access to Document

Other files and links

Cite this