New insights into the molecular phylogeny and taxonomy of the family Issidae (Hemiptera: Auchenorrhyncha: Fulgoroidea)

V.M. Gnezdilov, F.V. Konstantinov and S.Y. Bodrov

Proceedings of the Zoological Institute RAS, 2020, 324(1): 146–161 · https://doi.org/10.31610/trudyzin/2020.324.1.146

Full text

Abstract

The phylogenetic relationships among major lineages of the planthopper family Issidae were explored by analyzing a molecular dataset of nine fragments (COI, CytB, 12S, H3, 16S, 18SII, 18SIII, 28S D3–D5, 28S D6–D7) and 48 terminal taxa. Bayesian and Maximum likelihood analyses yielded similar and mostly well-resolved trees with moderate to high support for most branches. The obtained results suggest subdivision of the family Issidae Spinola into two subfamilies, Issinae Spinola, 1839 (= Thioniinae Melichar, 1906, = Hemisphaeriinae Melichar, 1906) and Hysteropterinae Melichar, 1906. The Issinae was clustered into the tribes Issini Spinola, 1839, with the subtribes Issina Spinola, 1839 and Thioniina Melichar, 1906, Sarimini Wang, Zhang et Bourgoin, 2016, Parahiraciini Cheng et Yang, 1991, Hemisphaeriini Melichar, 1906, and Kodaianellini Wang, Zhang et Bourgoin, 2016. The Hysteropterinae incorporates the rest of Western Palaearctic taxa except Issina. Chimetopini Gnezdilov, 2017, stat. nov. is elevated to tribe from the subtribal level. Most well-supported clades showed clear geographical pattering. Newly obtained data contradicts the scenario of an early split of American Thioniinae from other Issidae and possible origin of the family in the New World, while the combination of Palaearctic Issus Fabricius and Latissus Dlabola with Oriental and American taxa in one well supported clade may serve as an evidence for a common ancestor for extant Oriental, American, and Palaearctic issids.

Key words

Hyteropterinae, Issinae, Issina, Issini, molecular phylogeny, taxonomy, Thioniina

Submitted December 16, 2019 · Accepted January 31, 2020 · Published March 24, 2020

References

Abadi S., Azouri D., Pupko T. and Mayrose I. 2019. Model selection may not be a mandatory step for phylogeny reconstruction. Nature communications, 10(1): 934. https://doi.org/10.1038/s41467-019-08822-w

Arenas M. 2015. Trends of substitution models of molecular evolution. Frontiers in genetics, 6, article 319. https://doi.org/10.3389/fgene.2015.00319

Barringer L.E., Bartlett C.R. and Erwin T.L. 2019. Canopy assemblages and species richness of planthoppers (Hemiptera: Fulgoroidea) in the Ecuadorian Amazon. Insecta Mundi, 726: 1–16.

Belshaw R. and Quicke D.L.J. 2002. Robustness of ancestral state estimates: evolution of life history strategy in ichneumonoid parasitoids. Systematic Biology, 51: 450–477. https://doi.org/10.1080/10635150290069896

Bourgoin T. 2019. FLOW (Fulgoromorpha Lists on The Web): a world knowledge base dedicated to Fulgoromorpha. Available from: http://hemiptera-databases.org/flow/ (accessed 5 September 2019)

Bourgoin T., Guilbert E. and Wang Menglin. 2018. Issidae molecular K-libration. 8th European Hemiptera Congress, 24–29 June, Katowice-Zawiercie, Poland. Abstract book: 36.

Bourgoin T., Steffen-Campbell J.D. and Campbell B.C. 1997. Molecular phylogeny of Fulgoromorpha (Insecta, Hemiptera, Archaeorrhyncha). The enigmatic Tettigometridae: evolutionary affiliations and historical biogeography. Cladistics, 13: 207–224. https://doi.org/10.1111/j.1096-0031.1997.tb00316.x

Chan Mei-Ling, Yeh Hsin-Ting and Gnezdilov V.M. 2013.Thabena brunnifrons (Hemiptera: Issidae), new alien species in Taiwan, with notes on its biology and nymphal morphology. Formosan Entomologist, 33: 149–159.

Cryan J.R., Wiegmann B.M., Deitz L.L. and Dietrich C.H. 2000. Phylogeny of the treehoppers (Insecta: Hemiptera: Membracidae): evidence from two nuclear genes. Molecular Phylogenetics and Evolution, 17: 317–334. https://doi.org/10.1006/mpev.2000.0832

Dlabola J. 1980. Tribus-Einteilung, neue Gattungen und Arten der Subf. Issinae in der eremischen Zone (Homoptera, Auchenorrhyncha). Acta Musei Nationalis Pragae, 36B(4): 173–248.

Dlabola J. 1987. Zur Tribus-Einteilung der Issinae und Beschreibung von drei neuen Taxa (Homoptera, Issidae). Acta Entomologica Musei Nationalis Pragae, 42: 61–71.

Edgar R.C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32: 1792–1797. https://doi.org/10.1093/nar/gkh340

Emeljanov A.F. 1969. Auchenorrhyncha (Homoptera). In: L.V. Arnoldi and A.A. Yunatov (Eds). Plant and animal communities of the Central Kazakhstan steppe and deserts. Part 1. Biocomplex investigation in Kazakhstan. Nauka, Leningrad: 358–381. [In Russian].

Emeljanov A.F. 1978. New genera and species of leafhoppers (Homoptera, Auchenorrhyncha) from the USSR and Mongolia. Entomologicheskoe obozrenie, 57(2): 316–332. [In Russian]. (English translation published in Entomological Review, 57(2): 220–233).

Fennah R.G. 1954. The higher classification of the family Issidae (Homoptera: Fulgoroidea) with descriptions of new species. Transactions of the Royal Entomological Society of London, 105(19): 455–474. https://doi.org/10.1111/j.1365-2311.1954.tb00772.x

Giribet G., Carranza S., Baguna J., Riutort M. and Ribera C. 1996. First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Molecular Biology and Evolution, 13(1): 76–84. https://doi.org/10.1093/oxfordjournals.molbev.a025573

Gnezdilov V.M. 2002. Morphology of the ovipositor in members of the subfamily Issinae (Homoptera, Cicadina, Issidae). Entomologicheskoe obozrenie, 81(3): 605–626. [In Russian]. (English translation published in Entomological Review (2004), 82(8): 957–974).

Gnezdilov V.M. 2003. Review of the family Issidae (Homoptera, Cicadina) of the European fauna, with notes on the structure of ovipositor in planthoppers. Meetings in memory of N.A. Cholodkovsky, St. Petersburg, 56(1): 1–145. [In Russian with English summary].

Gnezdilov V.M. 2007. On the systematic positions of the Bladinini Kirkaldy, Tonginae Kirkaldy, and Trienopinae Fennah (Homoptera, Fulgoroidea). Zoosystematica Rossica, 15(2): 293–297.

Gnezdilov V.M. 2009. Revisionary notes on some tropical Issidae and Nogodinidae (Hemiptera: Fulgoroidea). Acta Entomologica Musei Nationalis Pragae, 49(1): 75–92.

Gnezdilov V.M. 2013a. Modern classification and the distribution of the family Issidae Spinola (Homoptera, Auchenorrhyncha: Fulgoroidea). Entomologicheskoe Obozrenie, 92(4): 724–738. [In Russian]. (English translation in Entomological Review (2014), 94(5): 687–697). https://doi.org/10.1134/S0013873814050054

Gnezdilov V.M. 2013b. Issidisation of fulgoroid planthoppers (Homoptera, Fulgoroidea) as an evidence of parallel adaptive radiation. Entomologicheskoe obozrenie, 92(1): 62–69. [In Russian]. (English translation published in Entomological Review (2013), 93(7): 825–830). https://doi.org/10.1134/S001387381307004X

Gnezdilov V.M. 2013c. Notes on planthoppers of the tribe Hemisphaeriini (Homoptera, Fulgoroidea, Issidae) from Vietnam with description of a new genus and new species. Zoologichesky Zhurnal, 92(6): 659–663. [In Russian]. (English translation published in Entomological Review (2013), 93(8): 1024–1028). https://doi.org/10.1134/S0013873813080095

Gnezdilov V.M. 2015. Description of a new genus and species of Hemisphaeriini from Brunei with an identification key to the Bornean species of the tribe (Hemiptera: Fulgoroidea: Issidae). Acta Entomologica Musei Nationalis Pragae, 55(1): 9–18.

Gnezdilov V.M. 2016a. Planthoppers of the family Issidae (Hemiptera, Fulgoroidea) of Western Palaearctic. Thesis of Doctoral Dissertation (Dr. Sci. habilitation), St.-Petersburg, 44 p. [In Russian].

Gnezdilov V.M. 2016b. A review of the genus Ikonza Hesse with notes on evolution of the family Issidae (Hemiptera: Auchenorrhyncha: Fulgoroidea). Entomologicheskoe Obozrenie, 95(1): 185–195. [In Russian]. (English translation published in Entomological Review (2016), 96(2): 225–234). https://doi.org/10.1134/S0013873816020093

Gnezdilov V.M. 2016c. Notes on phylogenetic relationships of planthoppers of the family Issidae (Hemiptera, Fulgoroidea) of the Western Palaearctic fauna, with description of two new genera. Entomologicheskoe Obozrenie, 95(2): 362–382. [In Russian]. (English translation published in Entomological Review (2016), 96(3): 332–347). https://doi.org/10.1134/S0013873816030106

Gnezdilov V.M. 2016d. A new species of the genus Eusarima Yang (Hemiptera: Fulgoroidea: Issidae) from Pakistan. Entomologicheskoe Obozrenie, 95(1): 176–184. [In Russian]. (English translation published in Entomological Review (2016), 96(2): 218–224). https://doi.org/10.1134/S0013873816020081

Gnezdilov V.M. 2017a. To the knowledge of the African fauna of the family Issidae (Hemiptera, Auchenorrhyncha: Fulgoroidea) with descriptions of new genera and new species. Entomological Review, 96(9): 1234–1260. https://doi.org/10.1134/S0013873816090074

Gnezdilov V.M. 2017b. New genus and species of the tribe Parahiraciini (Hemiptera, Fulgoroidea, Issidae) from the Philippines and Vietnam. Acta Zoologica Academiae Scientiarum Hungaricae, 63(4): 429–442. https://doi.org/10.17109/AZH.63.4.429.2017

Gnezdilov V.M. 2018a. To the revision of the genus Thionia Stål (Hemiptera, Fulgoroidea, Issidae), with description of new genera and new subtribe. Zootaxa, 4434(1): 158–170. https://doi.org/10.11646/zootaxa.4434.1.10

Gnezdilov V.M. 2018b. A new genus representing a new tribe of the family Issidae (Hemiptera: Auchenorrhyncha: Fulgoroidea) from the forest canopy of French Guiana. Zoosystematica Rossica, 27(1): 122–129. https://doi.org/10.31610/zsr/2018.27.1.122

Gnezdilov V.M. 2019a. A new genus and a new species, representing a new tribe of the family Issidae (Hemiptera: Auchenorrhyncha: Fulgoroidea), from Costa Rica. Zoosystematica Rossica, 28(1): 108–115. https://doi.org/10.31610/zsr/2019.28.1.108

Gnezdilov V.M. 2019b. On the taxonomic position of Thabenoides smedleyi Baker, 1927 (Hemiptera, Auchenorrhyncha, Fulgoroidea: Issidae). Entomological Review, 98(9): 1175–1176. https://doi.org/10.1134/S0013873818090038

Gnezdilov V.M. and Aguin-Pombo D. 2014. A new species of the planthopper genus Conosimus associated with an endemic shrub in southern Spain. Journal of Insect Science, 14(1), article 92. https://doi.org/10.1093/jis/14.1.92

Gnezdilov V.M. and Bartlett C.R. 2018. A new genus and two new species of the family Issidae (Hemiptera, Auchenorrhyncha: Fulgoroidea) from Amazonian Ecuador. Proceedings of the Entomological Society of Washington, 120(1): 62–75. https://doi.org/10.4289/0013-8797.120.1.62

Gnezdilov V.M., Bonfils J., Aberlenc H.-P. and Basset Y. 2010. Review of the Neotropical genus Oronoqua Fennah, 1947 (Insecta, Hemiptera, Issidae). Zoosystema, 32(2): 247–257. https://doi.org/10.5252/z2010n2a3

Gnezdilov V.M., Bouhachem S. and Konstantinov F.V. 2019. New records for the genus Issus Fabricius (Hemiptera: Auchenorrhyncha: Fulgoroidea: Issidae) from northern Africa and Spain. Zootaxa, 4613(3): 546–556. https://doi.org/10.11646/zootaxa.4613.3.7

Gnezdilov V.M. and Bourgoin T. 2016. On the taxonomic position of Issus reticulatus Bervoets, 1910 (Hemiptera: Fulgoroidea: Issidae) from Baltic amber. Entomological Review, 96(5): 631–633. https://doi.org/10.1134/S0013873816050092

Gnezdilov V.M., Bourgoin T., Mozaffarian F. and Manzari S. 2015. Difficulties in building a molecular phylogeny of the issidoid planthopper lineages (Insecta: Hemiptera: Fulgoroidea). Proceedings of the 1st Iranian International Congress of Entomology, Part II: 218–227.

Gnezdilov V.M. and Fletcher M. J. 2010. A review of the Australian genera of the planthopper family Issidae (Hemiptera: Fulgoromorpha) with description of an unusual new species of Chlamydopteryx Kirkaldy. Zootaxa, 2366: 35–45. https://doi.org/10.11646/zootaxa.2366.1.2

Gnezdilov V.M., Holzinger W.E. and Wilson M.R. 2014. The Western Palaearctic Issidae (Hemiptera, Fulgoroidea): an illustrated checklist and key to genera and subgenera. Proceedings of the Zoological Institute RAS, 318, Supplement 1: 1–124.

Gnezdilov V.M. and O’Brien L.B. 2006. Hysteropterum severini Caldwell & DeLong, 1948, a synonym of Agalmatium bilobum (Fieber, 1877) (Hemiptera: Fulgoroidea: Issidae). The Pan-Pacific Entomologist, 82(1): 50–53.

Kusnezova V. and Aguin-Pombo D. 2015. Comparative cytogenetics of Auchenorrhyncha (Hemiptera, Homoptera): a review. ZooKeys, 583: 63–93. https://doi.org/10.3897/zookeys.538.6724

Lunt D.H., Zhand D.X., Szymura J.M. and Hewitt G.M. 1996. The insect cytochrome oxidase I gene evolutionary patterns and conserved primers for phylogenetic studies. Insect Molecular Biology, 5: 153–165. https://doi.org/10.1111/j.1365-2583.1996.tb00049.x

Melichar L. 1906. Monographie der Issiden (Homoptera). Abhandlungen der K. K. Zoologisch-botanischen Gesellschaft in Wien, 3(4): 1–327.

Meng Rui, Wang Yinglun and Qin Daozheng. 2013. A new genus of the tribe Hemisphaeriini (Hemiptera: Fulgoromorpha: Issidae) from China. Zootaxa, 3691: 283–290. https://doi.org/10.11646/zootaxa.3691.2.7

Miller M.A., Pfeiffer W. and Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA, USA: 1–8. https://doi.org/10.1109/gce.2010.5676129

Mitjaev I.D. 2002. Fauna, biology, and zoogeography of Cicadinea (Homoptera) of Kazakhstan. Tethys Entomological Research, 5: 1–171. [In Russian].

Ogden T.H. and Whiting M. 2003. The problem with “the Paleoptera problem”: sense and sensitivity. Cladistics, 19: 432–442. https://doi.org/10.1111/j.1096-0031.2003.tb00313.x

Ronquist F., Huelsenbeck J. and Teslenko M. 2011. MrBayes version 3.2 Manual: Tutorials and Model Summaries. Available at: http://mrbayes.sourceforge.net/mb3.2_manual.pdf

Simon C., Frati F., Beckenbach A., Crespi B., Liu H. and Flook P. 1994. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America, 87: 651–701. https://doi.org/10.1093/aesa/87.6.651

Song Nan and Liang Ai-Ping. 2013. A Preliminary Molecular Phylogeny of Planthoppers (Hemiptera: Fulgoroidea) Based on Nuclear and Mitochondrial DNA Sequences. PLoS ONE, 8(3), e58400: 1–11. https://doi.org/10.1371/journal.pone.0058400

Spinola M. 1839. Sur les Fulgorelles, sous-tribu de la tribu des Cicadaires, ordre des Rhyngotes. Suite. Annales de la Société Entomologique de France, 8: 339–454.

Stamatakis A. 2016. The RAxML v8.2.X manual. Heidleberg Institute for Theoretical Studies. Available at: https://cme.h-its.org/exelixis/resource/download/NewManual.pdf

Sun Yanchun, Meng Rui and Wang Yinglun. 2015. Molecular systematics of the Issidae (Hemiptera: Fulgoroidea) from China based on wingless and 18S rDNA sequence data. Entomotaxonomia, 37(1): 15–26. https://doi.org/10.11680/entomotax.2015003

Urban J. M. and Cryan J. R. 2007. Evolution of the planthoppers (Insecta: Hemiptera: Fulgoroidea). Molecular Phylogenetics and Evolution, 42: 556–572. https://doi.org/10.1016/j.ympev.2006.08.009

Vaidya G., Lohman D.J. and Meier R. 2011. SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics, 27(2): 171–180. https://doi.org/10.1111/j.1096-0031.2010.00329.x

Wang Menglin, Zhang Yalin and Bourgoin T. 2016. Planthopper family Issidae (Insecta: Hemiptera: Fulgoromorpha): linking molecular phylogeny with classification. Molecular Phylogenetics and Evolution, 105: 224–234. https://doi.org/10.1016/j.ympev.2016.08.012

Yeh Wen-Bin and Yang Chung-Tu. 1999. Fulgoromorpha phylogeny based on 28S rDNA nucleotide sequence. Chinese Journal of Entomology. Special publication, 11: 87–111.

Yeh Wen-Bin, Yang Chung-Tu and Hui Cho-Fat. 1998. Phylogenetic relationships of the Tropiduchidae-group (Homoptera: Fulgoroidea) of planthoppers inferred through nucleotide sequences. Zoological Studies, 37(1): 45–55.

Yeh Wen-Bin, Yang Chung-Tu and Hui Cho-Fat. 2005. A molecular phylogeny of planthoppers (Hemiptera: Fulgoroidea) inferred from mitochondrial 16S rDNA sequences. Zoological Studies, 44(4): 519–535.

Zhao Songping, Bourgoin T. and Wang Menglin. 2019. The impact of a new genus on the molecular phylogeny of Hemisphaeriini (Hemiptera, Fulgoromorpha, Issidae). ZooKeys, 880: 61–74. https://doi.org/10.3897/zookeys.880.36828