Abstract
The Neotropical proconiine sharpshooter genus Abana includes six previously described species, some of which have nearly identical male genitalia but differ in coloration. The taxonomy of the genus is here revised based on comparative morphological study and phylogenetic analysis of partial mitochondrial COI sequences coupled with the following molecular species delimitation methods: ABGD, ASAP, PTP (including bPTP) and GMYC. Phylogenies for the implementation of the tree-based methods for species delimitation were hypothesized based on maximum likelihood and Bayesian inference reconstructions. The results of the molecular species delimitation showed that A. horvathi is a species complex with sexual dimorphism, which is reported for the first time. In addition, two very different color morphotypes were found within A. tissa, recognized as the same species by all delimitation methods. The results of the revision, including photographs of the primary types of all nominal species, support the validity of the six previously known species of Abana. Seven new species are described from Colombia, Panama and Peru: Abana amazonica Sauceda-V & Takiya, sp. nov., A. colombiana Sauceda-V & Takiya, sp. nov., A. confusa Sauceda-V & Takiya, sp. nov., A. inornata Sauceda-V & Takiya, sp. nov., A. minuta Sauceda-V & Takiya, sp. nov., A. ochracea Sauceda-V & Takiya, sp. nov., and A. rufifrons Sauceda-V & Takiya, sp. nov. Abana sonora Melichar, stat. rev. is removed from synonymy with A. horvathi and placed as a valid species outside the genus as Cicadellini incertae sedis. A lectotype is designated for Abana regia Melichar to stabilize the nomenclature. Abana tissa is recorded for the first time in Colombia and the morphology of the last instar nymph of this species is also described and documented for the first time. A key to the species and new geographical records as well as a distribution map are also provided.
References
- Álvarez, D., Pérez, A., Díaz, J. & Beltrán, J. (2011) Transmisión del Virus del mosaico suave del ñame a Dioscorea rotundata (Dioscoreaceae) por Oncometopia sp. (Cicadellidae). Revista Colombiana de Entomología, 37, 77–79. https://doi.org/10.25100/socolen.v37i1.9043
- Bartlett, C.R., Deitz, L.L., Dmitriev, D.A., Sanborn, A.F., Soulier-Perkins, A. & Wallace, M.S. (2018) The diversity of the true hoppers (Hemiptera: Auchenorrhyncha). In: Foottit, R.G. & Adler, P.H. (Eds.), Insect Biodiversity II: Science and Society. Wiley-Blackwell, Chichester, pp. 501–590. https://doi.org/10.1002/9781118945582.ch19
- Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C.-H., Xie, D., Suchard, M.A., Rambaut, A. & Drummond, A.J. (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 10, 1–6. https://doi.org/10.1371/journal.pcbi.1003537
- Carvalho, R.A. & Mejdalani, G. (2014) Remarkable morphological features of taxonomic interest in the female genitalia of five Erythrogonia species (Hemiptera: Cicadomorpha: Cicadellidae). Zootaxa, 3872 (3), 275–290. https://doi.org/10.11646/zootaxa.3872.3.4
- Carvalho, R.A., Mejdalani, G. & Takiya, D.M. (2011) Phylogenetic placement and taxonomy of the Neotropical sharpshooter genus Desamera Young, with description of its sister group, Ciccamera gen. nov. (Hemiptera: Cicadellidae: Cicadellinae). Systematics and Biodiversity, 9, 59–75. https://doi.org/10.1080/14772000.2011.558644
- Cavichioli, R.R. & Sakakibara, A.M. (1989) Novo gênero e espécie de Proconiini (Homoptera, Cicadellidae). Revista Brasileira de Zoologia, 6, 171–174. https://doi.org/10.1590/S0101-81751989000100018
- Ceotto, P.C. & Mejdalani, G. (2005) Phylogenetic analysis of the Abana group of genera (Hemiptera: Cicadellidae: Cicadellinae: Proconiini). Systematic Entomology, 30, 480–496. https://doi.org/10.1111/j.1365-3113.2004.00280.x
- Dellapé, G. (2015) Description of the female terminalia of twenty species of Proconiini (Hemiptera: Cicadellidae) from Argentina. Zootaxa, 3915 (4), 521–539. https://doi.org/10.11646/zootaxa.3915.4.4
- Dietrich, C.H. (2005) Keys to the families of Cicadomorpha and subfamilies and tribes of Cicadellidae (Hemiptera: Auchenorrhyncha). Florida Entomologist, 88, 502–517. https://doi.org/10.1653/0015-4040(2005)88[502:KTTFOC]2.0.CO;2
- Distant, W.L. (1908) VIII.—Rhynchotal notes—XLIV. (concluded from vol. i. p. 531). Annals and Magazine of Natural History, Series 8, 2 (7), 57–84. https://doi.org/10.1080/00222930808692453
- Dmitriev, D.A. (2010) Homologies of the head of Membracoidea based on nymphal morphology with notes on other groups of Auchenorrhyncha (Hemiptera). European Journal of Entomology, 107, 597–613. https://doi.org/10.14411/eje.2010.069
- Dmitriev, D.A., Anufriev, G.A., Bartlett, C.R., Blanco-Rodríguez, E., Borodin, O.I., Cao, Y.-H., Deitz, L.L., Dietrich, C.H., Dmitrieva, M.O., El-Sonbati, S.A., Evangelista de Souza, O., Gjonov, I.V., Gonçalves, A.C., Hendrix, S., McKamey, S., Kohler, M., Kunz, G., Malenovský, I., Morris, B.O., Novoselova, M., Pinedo-Escatel, J.A., Rakitov, R.A., Rothschild, M.J., Sanborn, A.F., Takiya, D.M., Wallace, M.S. & Zahniser, J.N. (2022 onward) World Auchenorrhyncha Database. TaxonPages. Available from: https://hoppers.speciesfile.org/ (accessed 5 June 2024)
- Ezard, T., Fujisawa, T. & Barraclough, T. (2009) splits: Species Limits by Threshold Statistics. R Package Version 1.0-14/r31. Available from: https://rdrr.io/rforge/splits/ (accessed 20 August 2024)
- Feng, L., Takiya, D.M., Krishnankutty, S.M., Dietrich, C.H. & Zhang, Y. (2024) Phylogeny and biogeography of the sharpshooters (Hemiptera: Cicadellidae: Cicadellinae). Systematic Entomology, 49, 314–329. https://doi.org/10.1111/syen.12620
- Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.
- Fowler, W.W. (1898) Order Rhynchota Suborder Hemiptera-Homoptera. Biologia Centrali-Americana, 2, 201–216.
- Freytag, P.H. & Sharkey, M.J. (2002) A preliminary list of the leafhoppers (Homoptera: Cicadellidae) of Colombia. Biota Colombiana, 3, 235–283.
- Fujisawa, T. & Barraclough, T.G. (2013) Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology, 62, 702–724. https://doi.org/10.1093/sysbio/syt033
- Godoy, C. (2005) A new genus of brachypterous leafhoppers (Hemiptera: Cicadellidae: Cicadellinae: Proconiini) from Costa Rica. Proceedings of the Entomological Society of Washington, 107, 259–266. [https://biostor.org/reference/55248]
- Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321. https://doi.org/10.1093/sysbio/syq010
- Hamilton, K.G.A. (1981) Morphology and evolution of the rhynchotan head (Insecta: Hemiptera, Homoptera). Canadian Entomologist, 113, 953–974. https://doi.org/10.4039/Ent113953-11
- Hartert, E. (1898) On a collection of birds from north-western Ecuador collected by Mr. W. F. H. Rosenberg. Novitates Zoologicae, 5, 477–505.
- Hill, B.G. (1970) Comparative morphological study of selected higher categories of leafhoppers (Homoptera: Cicadellidae). PhD Dissertation, North Carolina State University, Raleigh, North Carolina, 186 pp.
- ICZN [International Commission on Zoological Nomenclature] (1999) International Code of Zoological Nomenclature. 4th Edition. The International Trust for Zoological Nomenclature c/o the Natural History Museum, London, 271 pp. https://doi.org/10.5962/bhl.title.50608
- Jacobi, A. (1905) Vorbericht über eine Homopterenfauna der Anden, nebst Diagnosen neuer Arten. Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin, 6, 163–188.
- Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K., Von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. https://doi.org/10.1038/nmeth.4285
- Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35, 1547–1549. https://doi.org/10.1093/molbev/msy096
- Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A. & Lopez, R. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947–2948. https://doi.org/10.1093/bioinformatics/btm404
- Leal, A.H., Mejdalani, G., Cavichioli, R.R. & Carvalho, R.A. (2009) Taxonomy and phylogeny of the leafhopper genus Scoposcartula (Insecta: Hemiptera: Cicadellidae). Systematics and Biodiversity, 7, 215–233. https://doi.org/10.1017/S1477200009002990
- McKamey, S.H. (2007) Taxonomic catalogue of the leafhoppers (Membracoidea). Part 1. Cicadellinae. Memoirs of the American Entomological Institute, 78, 1–394.
- Mejdalani, G. (1998) Morfologia externa dos Cicadellinae (Homoptera, Cicadellidae): comparação entre Versigonalia ruficauda (Walker) (Cicadellini) e Tretogonia cribata Melichar (Proconiini), com notas sobre outras espécies e análise da terminologia. Revista Brasileira de Zoologia, 15, 451–544. https://doi.org/10.1590/S0101-81751998000200015
- Melichar, L. (1926) Monographie der Cicadellinen. III. Annales Historico-Naturales Musei Nationalis Hungarici, 23, 273–1394.
- Metcalf, Z.P. (1965) Cicadelloidea. Part 1. Tettigellidae. General Catalogue of the Homoptera. United States Department of Agriculture, Agricultural Research Service, Washington, D.C., 730 pp.
- Minh, B.Q., Nguyen, M.A.T. & von Haeseler, A. (2013) Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution, 30, 1188–1195. https://doi.org/10.1093/molbev/mst024
- Minh, B.Q., Schmidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D., von Haeseler, A. & Lanfear, R. (2020) IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution, 37, 1530–1534. https://doi.org/10.1093/molbev/msaa015
- Monteiro, A. & Pierce, N.E. (2001) Phylogeny of Bicyclus (Lepidoptera: Nymphalidae) inferred from COI, COII, and EF-1α gene sequences. Molecular Phylogenetics and Evolution, 18, 264–281. https://doi.org/10.1006/mpev.2000.0872
- Nault, L.R. & Ammar, E.D. (1989) Leafhopper and planthopper transmission of plant viruses. Annual Review of Entomology, 34, 503–529. https://doi.org/10.1146/annurev.en.34.010189.002443
- Nielson, M.W. (1965) A revision of the genus Cuerna (Homoptera, Cicadellidae). Technical Bulletin of the United States Department of Agriculture, 1318, 1–48.
- Oman, P. (1949) The Nearctic leafhoppers (Homoptera: Cicadellidae) a generic classification and check list. Memoirs of the Entomological Society of Washington, 3, 1–253.
- Oman, P.W., Knight, W.J. & Nielson, M.W. (1990) Leafhoppers (Cicadellidae): A Bibliography, Generic Checklist and Index to the World Literature 1956–1985. CAB International Institute of Entomology, Wallingford, 368 pp.
- Paradis, E. & Schliep, K. (2019) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics, 35, 526–528. https://doi.org/10.1093/bioinformatics/bty633
- Puillandre, N., Brouillet, S. & Achaz, G. (2020) ASAP: assemble species by automatic partitioning. Molecular Ecology Resources, 21, 609–620. https://doi.org/10.1111/1755-0998.13281
- Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21, 1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x
- R Core Team (2023) R: A language and environment for statistical computing. Version 4.2.3. Available from: https://cran.r-project.org/bin/windows/base/old/4.2.3/ (accessed 31 March 2023)
- Rakitov, R. (1998) On differentiation of cicadellid leg chaetotaxy (Homoptera: Auchenorrhyncha: Membracoidea). Russian Entomology Journal, 6, 7–27.
- Rakitov, R.A. & Godoy, C. (2005) New eggpowdering sharpshooters (Hemiptera: Cicadellidae: Proconiini) from Costa Rica. Annals of the Entomological Society of America, 98, 444–457. https://doi.org/10.1603/0013-8746(2005)098[0444:NESHCP]2.0.CO;2
- Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67, 901–904. https://doi.org/10.1093/sysbio/syy032
- Remes-Lenicov, A.M.M., Virla, E.G. & Manca, M.E. (1998) Difusión de Tapajosa rubromarginata (Homoptera: Cicadellidae) sobre cultivos cerealeros de la Argentina. Revista de la Sociedad Entomológica Argentina, 57, 18.
- Sauceda-V., J. & Takiya, D.M. (2023) On the sharpshooter genus Yunga Melichar, 1924 (Hemiptera: Cicadellidae: Cicadellinae): descriptions of a new species from Panama and of the internal female terminalia of Y. cartwrighti Young, 1968 and Y. coriacea Stål, 1864. Zootaxa, 5389 (4), 434–444. https://doi.org/10.11646/zootaxa.5389.4.2
- Schmidt, E. (1928) Die Cicadellinen des Stettiner Museums. I. Stettiner entomologische Zeitung, 89, 31–62.
- Silva, R.D.S., Cavichioli, R.R., Takiya, D.M. & Mejdalani, G. (2018) Descriptions of seven new Acrogonia species from South America (Hemiptera: Cicadellidae: Cicadellinae: Proconiini). Zootaxa, 4374 (3), 375–394. https://doi.org/10.11646/zootaxa.4374.3.3
- Silva, R.D.S.D., Cavichioli, R.R., Takiya, D.M. & Mejdalani, G. (2017) Descriptions of eight new Acrogonia species from the Amazon region, including peculiar features of the female genitalia (Hemiptera: Cicadellidae: Cicadellinae: Proconiini). Zootaxa, 4244 (4), 515–534. https://doi.org/10.11646/zootaxa.4244.4.4
- Sorensen, J.T. & Gill, R.J. (1996) A range extension of Homalodisca coagulata (Say) (Hemiptera: Clypeorrhyncha: Cicadellidae) to southern California. Pan-Pacific Entomologist, 72, 160–161.
- Takiya, D.M. & Cavichioli, R.R. (2004) A review of the Neotropical sharpshooter genus Onega Distant, 1908 (Hemiptera: Cicadellidae: Cicadellini). Zootaxa, 718 (1), 1–19. https://doi.org/10.11646/zootaxa.718.1.1
- Takiya, D.M. & Mejdalani, G. (2004) Taxonomic revision and phylogenetic analysis of the sharpshooter genus Balacha Melichar (Hemiptera: Cicadellidae: Cicadellini). Systematic Entomology, 29, 69–99. https://doi.org/10.1111/j.1365-3113.2004.00231.x
- Wilson, M.R. & Takiya, D.M. (2007) Cicadellinae (Hemiptera, Auchenorrhyncha: Cicadellidae) described by Leopold Melichar in the Hungarian Natural History Museum. Annales historico-naturales Musei nationalis hungarici, 99, 29–48.
- Young, D.A. (1965) Cicadelline types in the British Museum (Natural History) (Homoptera: Cicadellidae). Bulletin of the British Museum (Natural History) Entomology, 17, 163–199. https://doi.org/10.5962/bhl.part.14810
- Young, D.A. (1968) Taxonomic study of the Cicadellinae (Homoptera: Cicadellidae), Part 1, Proconiini. Bulletin of the United States National Museum, 261, 1–287. https://doi.org/10.5962/bhl.part.20869
- Young, D.A. (1977) Taxonomic study of the Cicadellinae (Homoptera: Cicadellidae). Part 2, New World Cicadellini and the genus Cicadella. Bulletin of the North Carolina Agricultural Experiment Station, 239, 1–1135.
- Young, D.A. & Lauterer, P. (1964) Cicadelline lectotypes from A. Jacobi collection (Homoptera, Cicadellidae). Reichenbachia, 2, 293–296.
- Young, D.A. & Lauterer, P. (1966) Types of Cicadellinae (Homoptera, Cicadellidae) in the Moravian Museum. Acta Musei Moraviae, Scientiae naturales, 51, 261–270.
- Young, D.A. & Nast, J. (1963) Cicadelline types of species described by Edmund Schmidt (Homoptera, Cicadellidae). Annales Zoologici, 21, 265–271.
- Young, D.A. & Soos, A. (1964) Types of Cicadellinae (Homoptera, Cicadellidae) in the Hungarian Natural History Museum. Annales historico-naturales Musei nationalis hungarici, 56, 465–467.
- Zanol, K.M.R. (1988) Morfologia de Neophlepsius gracilis (Osborn, 1923). Revista Brasileira de Entomologia, 32, 69–93.
- Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29, 2869–2876. https://doi.org/10.1093/bioinformatics/btt499