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Article
Published: 2022-04-28

Morphological variation and genealogical discordance in Caatinga sand lizards Calyptommatus Rodrigues 1991 (Squamata: Gymnophthalmidae) with the description of a new species

Laboratório de Herpetologia, Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, 05508-090, São Paulo, SP, Brazil.
Laboratório de Herpetologia, Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, 05508-090, São Paulo, SP, Brazil.
Museu de História Natural do Sul do Estado do Espírito Santo, da Universidade Federal do Espírito Santo. Av. Gov. Lindemberg, 316 - Centro, Jerônimo Monteiro, 29550-000, Espírito Santo, Brazil.
Laboratório de Herpetologia, Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, 05508-090, São Paulo, SP, Brazil.
Centro Universitário São Camilo, 29304-910, Cachoeiro de Itapemirim, ES, Brazil.
Laboratório de Herpetologia, Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, 05508-090, São Paulo, SP, Brazil.
Reptilia Caatinga contact zone endemism phylogeny reptiles taxonomy

Abstract

In the last decades, a remarkable fauna of psammophilous and fossorial squamates was discovered in sandy habitats of the semiarid Caatinga of northeast Brazil. Despite the increasing accumulation of genetic data from this unique fauna, an incomplete knowledge of its diversity still hampers a better understanding of its origins and diversification. The fossorial lizard genus Calyptommatus (Gymnophthalmidae) is endemic to sandy habitats of the Caatinga, being currently represented by four allopatric species. In this study, we used morphological and molecular data to assess population-level variation in Calyptommatus. We found a new morphotype of Calyptommatus from the state of Bahia, Brazil, readily distinguished from congeners by the presence of a frontal scale. Morphological, nuDNA and geographic data support the recognition of a new species herein described as Calyptommatus frontalis sp. nov. Nevertheless, genetic data revealed mito-nuclear+morphology discordance, with populations with frontal scales distributed in three distantly related mtDNA clades, suggesting either potential historical and/or current introgressions or incomplete lineage sorting. Further data are needed to clarify the status of the two other mtDNA clades displaying a frontal scale.

 

References

  1. Arnold, M.L. (1992) Natural hybridization as an evolutionary process. Annual review of Ecology and Systematics, 23 (1), 237–261. https://doi.org/10.1146/annurev.es.23.110192.001321
    Barreto, A.M.F., Suguio K., Oliveira, P.E. & Tatumi, S.H. (2002) Campo de Dunas Inativas do Meìdio Rio SaÞo Francisco, BA—Marcante registro de ambiente deseìrtico do Quaternaìrio brasileiro. In: Schobbenhaus, C., Campos, D.A. & Queiroz, E.T. (Eds.), Siìtios Geoloìgicos e Paleontoloìgicos do Brasil. ComissaÞo Brasileira de Siìtios Geoloìgicos e Paleobioloìgicos (SIGEP), Brasiìlia, pp. 223–231.
    Camacho, A., Pavão, R., Moreira, C.N., Pinto, A.C.B.F., Navas, C.A. & Rodrigues, M.T. (2015) Interaction of morphology, thermal physiology and burrowing performance during the evolution of fossoriality in Gymnophthalmini lizards. Functional Ecology, 29 (4), 515–521. https://doi.org/10.1111/1365-2435.12355
    Camacho, A., Recoder, R., Teixeira Jr, M., Kohlsdorf, T., Rodrigues, M.T. & Lee, M.S. (2017) Overcoming phylogenetic and geographic uncertainties to test for correlates of range size evolution in gymnophthalmid lizards. Ecography, 40 (6), 764–773. https://doi.org/10.1111/ecog.02282
    Cavalcanti, L., Costa, T., Colli, G., Costa, G., França, F., Mesquita, D., Palmeira, C., Pelegrin, N., Soares, A., Tucker, D. & Garda, A.A. (2014) Herpetofauna of protected areas in the Caatinga II: Serra da Capivara National Park, Piauí, Brazil. Check list, 10 (1), 18–27. https://doi.org/10.15560/10.1.18
    Clement, M., Snell, Q., Walker, P., Posada, D. & Crandall, K. (2002) TCS: Estimating gene genealogies. Proceedings 16th International Parallel and Distributed Processing Symposium, Fort Lauderdale, 2022, 1–184. https://doi.org/10.1109/IPDPS.2002.1016585
    Dal Vechio, F., Teixeira Jr., M., Recoder, R.S., Rodrigues, M.T. & Zaher, H. (2016) The herpetofauna of Parque Nacional da Serra das Confusões, state of Piauí, Brazil, with a regional species list from an ecotonal area of Cerrado and Caatinga. Biota Neotropica, 16 (3), e20150105. https://doi.org/10.1590/1676-0611-BN-2015-0105
    Damasceno, R., Strangas, M.L., Carnaval, A.C., Rodrigues, M.T. & Moritz, C. (2014) Revisiting the vanishing refuge model of diversification. Frontiers in Genetics, 5 (353), 1–12. https://doi.org/10.3389/fgene.2014.00353
    Dowling, T.E. & Secor, C.L. (1997) The role of hybridization and introgression in the diversification of animals. Annual review of Ecology and Systematics, 28 (1), 593–619. https://doi.org/10.1146/annurev.ecolsys.28.1.593
    Dayrat, B. (2005) Towards integrative taxonomy. Biological Jornal of the Linnean Society, 85 (3), 407–417. https://doi.org/10.1111/j.1095-8312.2005.00503.x
    Fetzner Jr., J.W. (1999) Extracting High-Quality DNA from Shed Reptile Skins: A Simplified Method. BioTechniques, 26, 1052–1054. https://doi.org/10.2144/99266bm09
    Gehara, M., Garda, A.A., Werneck, F.P., Oliveira, E.F., da Fonseca, E.M., Camurugi, F., Magalhães, F.M., Lanna, F.M., Sites, J.W. Jr., Marques, R., Silveira-Filho, R., São Pedro, V.A., Colli, G.R., Costa, G.C. & Burbrink, F.T. (2017) Estimating synchronous demographic changes across populations using hABC and its application for a herpetological community from northeastern Brazil. Molecular Ecology, 26 (18), 4756–4771. https://doi.org/10.1111/mec.14239
    Guedes, T.B., Nogueira, C. & Marques, O.A. (2014) Diversity, natural history, and geographic distribution of snakes in the Caatinga, Northeastern Brazil. Zootaxa, 3863 (1), 1–93. https://doi.org/10.11646/zootaxa.3863.1.1
    Hewitt, G.M. (1988) Hybrid zones-natural laboratories for evolutionary studies. Trends in ecology & evolution, 3 (7), 158–167. https://doi.org/10.1016/0169-5347(88)90033-X
    Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30, 772–80. https://doi.org/10.1093/molbev/mst010
    Kearse, M., Moir, R., Wilson, A., Stones–Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Mentjies, P. & Drummond, A. (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649. https://doi.org/10.1093/bioinformatics/bts199
    Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874. https://doi.org/10.1093/molbev/msw054
    Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2016) PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34, 772–773. https://doi.org/10.1093/molbev/msw260
    Lanna, F.M., Gehara, M., Werneck, F.P., Fonseca, E.M., Colli, G.R., Sites Jr., J.W., Rodrigues, M.T. & Garda, A.A. (2020) Dwarf geckos and giant rivers: the role of the São Francisco River in the evolution of Lygodactylus klugei (Squamata: Gekkonidae) in the semi-arid Caatinga of north-eastern Brazil. Biological Journal of the Linnean Society, 129 (1), 88–98.
    Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25 (11), 1451–1452. https://doi.org/10.1093/bioinformatics/btp187
    Leal, I.R., Tabarelli, M. & Da Silva, J.M.C. (2003) Ecologia e conservação da Caatinga. Editora Universitária UFPE, Recife, 822 pp.
    Leigh, J.W. & Bryant D. (2015) PopART: Full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6 (9), 1110–1116. https://doi.org/10.1111/2041-210X.12410
    Mallet, J. (2005) Hybridization as an invasion of the genome. Trends in ecology & evolution, 20 (5), 229–237. https://doi.org/10.1016/j.tree.2005.02.010
    Mares, M.A., Willig, M.R., Streilein, K.E. & Lacher, T.E. (1981) The mammals of northeastern Brazil: a preliminary assessment. Annals of the Carnegie Museum of Natural History, 50 (4), 81–137.
    McGuire, G. & Wright, F. (2000) TOPAL 2.0: Improved Detection of Mosaic Sequences within Multiple Alignments. Bioinformatics, 16, 130–134. https://doi.org/10.1093/bioinformatics/16.2.130
    Mesquita, D.O., Costa, G.C., Garda, A.A. & Delfim, F.R. (2017) Species composition, biogeography, and conservation of the Caatinga lizards. In: da Silva, J.M.C., Leal, I.R. & Tabarelli, M. (Eds.), Caatinga: the largest tropical dry forest region in South America. Springer, Cham, pp. 151–180. https://doi.org/10.1007/978-3-319-68339-3_6
    Milne, I., Lindner, D., Bayer, M., Husmeier, D., McGuire, G., Marshall, D.F. & Wright, F. (2009) TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi–core desktops. Bioinformatics, 25, 126–127. https://doi.org/10.1093/bioinformatics/btn575
    Moritz, C., Wright, J.W. & Brown, W.M. (1992) Mitochondrial DNA analyses and the origin and relative age of parthenogenetic Cnemidophorus: phylogenetic constraints on hybrid origins. Evolution, 46 (1), 184–192. https://doi.org/10.2307/2409813
    de Oliveira, P.E., Barreto, A.M.F. & Suguio, K. (1999) Late Pleistocene/Holocene climatic and vegetational history of the Brazilian caatinga: the fossil dunes of the middle São Francisco River. Palaeogeography, palaeoclimatology, palaeoecology, 152 (3-4), 319–337. https://doi.org/10.1016/S0031-0182(99)00061-9
    Oliveira, E.F., Martinez, P.A., São-Pedro, V.A., Gehara, M., Burbrink, F.T., Mesquita, D.O., Garda, A.A., Colli, G.R. & Costa, G.C. (2018) Climatic suitability, isolation by distance and river resistance explain genetic variation in a Brazilian whiptail lizard. Heredity, 120 (3), 251–265. https://doi.org/10.1038/s41437-017-0017-2
    Padial, J.M., Miralles, A., de la Riva, I. & Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology, 7 (1), 16. https://doi.org/10.1186/1742-9994-7-16
    Passoni, J.C., Benozzati, M.L. & Rodrigues, M.T. (2008) Phylogeny, species limits, and biogeography of the Brazilian lizards of the genus Eurolophosaurus (Squamata: Tropiduridae) as inferred from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 46 (2), 403–414. https://doi.org/10.1016/j.ympev.2007.10.022
    Pedrosa, I.M.M.C., Costa, T.B., Faria, R.G., França, F.G.R., Laranjeiras, D.O., Oliveira, T.C.S.P.D., Palmeira, C.N.S., Torquato, S., Mott, T., Calazans, G.H.V & Garda, A.A. (2014) Herpetofauna of protected areas in the Caatinga III: The Catimbau National Park, Pernambuco, Brazil. Biota Neotropica, 14 (4), e20140046. https://doi.org/10.1590/1676-06032014004614
    R Core Team. (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: http://www.R-project.org/ (accessed 1 April 2020)
    Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67, 901–904. https://doi.org/10.1093/sysbio/syy032
    Ramiro, C.N., Junior, M.T. & Rodrigues, M.T. (2017) Reproductive biology of three sympatric species of gymnophthalmid lizards from the sand dunes of the middle Sao Francisco river, Bahia, Brazil. South American Journal of Herpetology, 12 (1), 76–88. https://doi.org/10.2994/SAJH-D-16-00044.1
    Recoder, R.S. & Rodrigues, M.T. (2020) Diversification Processes in Lizards and Snakes from the Middle São Francisco River Dune Region, Brazil. In: Rull, V. & Carnaval, A.C. (Eds.), Neotropical Diversification: Patterns and Processes, Fascinating Life Sciences. Springer, Cham and New York, pp. 713–740. https://doi.org/10.1007/978-3-030-31167-4_26.
    Rivera, D., Prates, I., Rodrigues, M.T. & Carnaval, A.C. (2020) Effects of climate and geography on spatial patterns of genetic structure in tropical skinks. Molecular Phylogenetics and Evolution, 143, 106661.
    Rodrigues, M.T. (1986) Um novo Tropidurus com crista dorsal do Brasil, com comentários sobre suas relações, distribuição e origem (Sauria, Iguanidae). Papéis Avulsos de Zoologia, 36 (17), 171–179.
    Rodrigues, M.T. (1991) Herpetofauna das dunas interiores do rio São Francisco: Bahia: Brasil. I. Introdução aÌ área e descrição de um novo gênero de microteiídeos (Calyptommatus) com notas sobre sua ecologia, distribuição e especiação (Sauria, Teiidae). Papéis Avulsos de Zoologia, São Paulo, 37, 285–320.
    Rodrigues, M.T. (1996) Lizards, Snakes, and Amphisbaenians from the Quaternary Sand Dunes of the Middle Rio São Francisco, Bahia, Brazil. Journal of Herpetology, 30 (4), 513–523.
    Rodrigues, MT. (2003) Herpetofauna da caatinga. In: Leal, I.R., Tabarelli, M. & Da Silva, J.M.C. (Eds.), Ecologia e Conservação da Caatinga. Universidade Federal de Pernambuco, Recife, pp. 181–236.
    Rodrigues, M.T., Zaher, H. & Curcio, F. (2001) A new species of lizard, genus Calyptommatus, from the caatingas of the state of Piauí, northeastern Brazil (Squamata, Gymnophthalmidae). Papéis Avulsos de Zoologia, São Paulo, 41 (28), 529–546.
    Rodrigues, M.T., Carvalho, C.M., Borges-Nojosa, D.M., Freire, E.M.X., Curcio, F.F., Oliveira, F.F., Silva, H.R. & Dixo, M.B.D.O. (2004) Anfíbios e répteis: áreas e ações prioritárias para a conservação da Caatinga. In: Silva, J.M.C., Tabarelli, M., Fonseca, M.T. & Lins, L.V. (Eds.), Biodiversidade da Caatinga: áreas e ações prioritárias para a conservação. Ministério do Meio Ambiente, Brasília, pp. 181–188.
    Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B. Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542. https://doi.org/10.1093/sysbio/sys029
    Siedchlag, A.C., Benozzati, M.L., Passoni, J.C. & Rodrigues, M.T. (2010) Genetic structure, phylogeny, and biogeography of Brazilian eyelid-less lizards of genera Calyptommatus and Nothobachia (Squamata, Gymnophthalmidae) as inferred from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 56 (2), 622–630. https://doi.org/10.1016/j.ympev.2010.04.027
    da Silva, J.M.C., Leal, I.R. & Tabarelli, M. (2017) Caatinga: the largest tropical dry forest region in South America. Springer, Cham, 482 pp.
    Stephens, M. & Donnelly, P.A. (2003) Comparison of Bayesian methods for haplotype reconstruction from population genotype data. The American Journal of Human Genetics, 73, 1162–1169. https://doi.org/10.1086/379378
    Sullivan, J. & Joyce, P. (2005) Model selection in phylogenetics. Annual Review of Ecology, Evolution, and Systematics, 36, 445–466. https://doi.org/10.1146/annurev.ecolsys.36.102003.152633
    Vaidya, G., Lohman, D.J. & Meier, R. (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics, 27, 171–180. https://doi.org/10.1111/j.1096-0031.2010.00329.x
    Vanzolini, P.E. (1976) On the lizards of a Cerrado-Caatinga contact: evolutionary and zoogeographical implications (Sauria). Papéis Avulsos de Zoologia, São Paulo, 29, 111–119.
    Vanzolini, P.E. (1988) Distributional patterns of south american lizards. In: Heyer, W.R. & Vanzolini, P.E. (Eds.), Proceedings of a workshop on neotropical distribution patterns. Academia Brasileira de Ciências, Rio de Janeiro, pp. 317–342
    Werneck, F.P., Gamble, T., Colli, G.R., Rodrigues, M.T. & Sites Jr., J.W. (2012) Deep diversification and long-term persistence in the South American ‘dry diagonal’: integrating continent-wide phylogeography and distribution modeling of geckos. Evolution: International Journal of Organic Evolution, 66 (10), 3014–3034. https://doi.org/10.1111/j.1558-5646.2012.01682.x
    Werneck, F.P., Leite, R.N., Geurgas, S.R. & Rodrigues, M.T. (2015) Biogeographic history and cryptic diversity of saxicolous Tropiduridae lizards endemic to the semiarid Caatinga. BMC Evolutionary Biology, 15 (1), 94. https://doi.org/10.1186/s12862-015-0368

  2.