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Morphological Phylogeny of Dictyopharidae (Hemiptera: Fulgoromorpha)

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Morphological Phylogeny of Dictyopharidae (Hemiptera: Fulgoromorpha) Systematic Entomology (2018), 43, 637–658 DOI: 10.1111/syen.12293 Morphological phylogeny of Dictyopharidae (Hemiptera: Fulgoromorpha) ZHI-SHUN SONG1,2, CHARLES R. BARTLETT3, LOIS B. O’BRIEN4, AI-PING LIANG1,5 andTHIERRY BOURGOIN6 1Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China, 2Jiangsu Key Laboratory of Biofunctional Molecule, School of Life Sciences, Chemistry & Chemical Engineering, Jiangsu Second Normal University, Nanjing, China, 3Department of Entomology and Wildlife Ecology, University of Delaware, Newark, Delaware, U.S.A., 4Department of Entomology, University of Arizona, Tucson, AZ, U.S.A., 5College of Life Sciences, University of Chinese Academy of Sciences, Beijing, China and 6Institut Systématique Evolution Biodiversité (ISYEB), UMR 7205 MNHN-CNRS-UPMC-EPHE, Muséum National d’Histoire Naturelle, Sorbonne Universités, Paris, France Abstract. To explore the phylogenetic basis of the current classification of Dic- tyopharidae, especially the relationships among the tribes of Dictyopharinae, we present the first cladistic analysis of this family based on 146 morphological characters of adults. Our analysis includes 104 of 125 recognized genera and subgenera within 12 extant tribes of Dictyopharinae, plus nine genera representing all four tribes of Org- eriinae. The results of this study support Dictyopharidae as a monophyletic group with Aluntiini sister to the remaining Dictyopharidae, but do not support Orgeri- inae as sister to Dictyopharinae. Seven major lineages – Aluntiini, Arjunini, Has- tini, (Taosini + Lappidini) + Nersiini, a Xenochasma+ complex (including ‘Orgeriinae’), Orthopagini, and Dictyopharini – are recovered in Dictyopharidae. The Xenochasma+ complex is proposed here and includes Xenochasma clade + (Scoloptini + ((Fernandea clade + Phylloscelini) + (Rancodini + [Capenini + Orgeriinae]))). Within this complex, some genera are of uncertain tribal placement, and the Orgeriinae are retained as a subfamily until a molecular phylogeny can confirm the results of this paper. The implied weighting analysis supports the monophyly of most tribes of Dictyopharinae (except Taosini), the sister-group relationships of (Taosini + Lappidini) with Nersiini, and Orthopagini + Dictyopharini, and the current tribal classification for Dictyophari- nae. Most Dictyopharinae genera fit their respective tribal affiliation, but some proposed changes are that Pharodictyon, Paramisia, Dictyopharoides s.s., Chondrophana, Sicoris, Chondrodire, and Tupala are provisionally placed in Hastini; Pukuakanga is moved into Nersiini; Sinodictya and Raphiophora are transferred into Orthopagini; and Chiltana, Litocras, and Viridophara are placed in Dictyopharini. Introduction Metcalf, 1946; Bourgoin, 2017). Dictyopharinae have a world- wide distribution and contain 127 genera and subgenera within With more than 720 species in 155 extant and extinct genera, 15 tribes and more than 520 species (updated from Bourgoin, Dictyopharidae Spinola (Hemiptera: Fulgoromorpha), or dic- 2017; File S1). Orgeriinae comprise 52 genera and subgenera tyopharid planthoppers, are currently divided into two subfami- within four tribes restricted to the arid regions of the Holarctic lies: Dictyopharinae Spinola and Orgeriinae Fieber (Muir, 1923; region (Emeljanov, 1980; Emeljanov et al., 2005; updated from Bourgoin, 2017, File S1). Most dictyopharid species are moder- ate to small in size, compared with their asserted sister group Correspondence: Ai-Ping Liang, Institute of Zoology, Chinese Academy of Sciences, No. 1 Beichen West Road, Chaoyang District, Fulgoridae Latreille (e.g. Emeljanov, 1979; Urban & Cryan, Beijing 100101, China. E-mail: [email protected] 2009; Song & Liang, 2013). An elongate and tapering head © 2018 The Royal Entomological Society 637 638 Z.-S. Song et al. is common to both families, but is not unique to them, occur- Several higher taxa were moved from Dictyopharinae into ring widely in the Fulgoromorpha (O’Brien, 2002) and reported Fulgoridae, including Aluntiinae Emeljanov, Cladyphini, to be homoplastic (Urban & Cryan, 2009). The streamlined Dichopterini, Dorysarthrini Emeljanov, and Protachilini Emel- appearance that is characterized by the elongate and tapering janov (Emeljanov, 1979, 2011a, 2013; Song et al., 2011). head can improve jumping performance by reducing drag, lead- After re-evaluating those characters supporting the placement ing to Engela minuta Distant having the fastest take-off velocity of Aluntiinae within Fulgoridae, Emeljanov (2008) moved in all the insects described to date (Burrows, 2014). Members of them back to Dictyopharinae. A few years later, 11 extant Dictyopharidae are found in every part of the world, excluding tribes, including micropterous Capenini and Cleotychini, were Arctic and Antarctic regions, with the highest diversity in the assigned to Dictyopharinae, and an updated key to the tribes tropical and subtropical zones (Metcalf, 1946; Bourgoin, 2017). was given with most genera placed into tribes to improve the Most dictyopharids are predominantly dicot feeders, and a few generic and tribal classification of Dictyopharinae (Emeljanov, species are economically important agricultural pests on grasses 2011b). In 2014, Emeljanov described the third micropterous (Wilson & O’Brien, 1987; Wilson et al., 1994). Polyphagous tribe, Rancodini Emeljanov from Chile, and Song et al. (2016b) Dictyophara europaea (Linné) in Europe is a potentially mul- separated a new tribe, Arjunini Song & Szwedo, from Aluntiini tilateral vector in the transmission of diverse phytoplasma dis- based on a phylogeny inferred from morphological data. eases, e.g. Flavescence dorée, and may acquire phytoplasmas Dictyopharinae currently comprise 13 extant tribes and two from a variety of plant sources (Krstic´ et al., 2016). Another dic- extinct tribes (Melichar, 1912; Muir, 1923; Metcalf, 1946; tyopharid planthopper, Cuernavaca longula (Remes Lenicov), Emeljanov, 1983, 1997, 2011b, 2014; Szwedo, 2008; Song endemic to South America, is an effective agent for the bio- et al., 2016b). Species in most tribes are hyperpterous, i.e. logical control of water hyacinth, Eichhornia crassipes (Mart.) the tegmina have various degrees of hyper-development with (Sacco et al., 2013). addition of the supranumerous forkings of the main veins (more The higher classification of Dictyopharidae has changed little than two), leading to the recognition of at least a second rank since Spinola (1839) first recognized dictyopharids as a sub- of postnodal closed cell(s) after the nodal cells (Bourgoin et al., family (as ‘Dictiophoroïdes’) of Fulgoridae (as ‘Fulgorites’) 2015). In the hyperpterous tribes, the tegmina generally extend based on Dictyophara Germar, Plegmatoptera Spinola, and far beyond the abdomen (macropterous in Emeljanov, 2011b), three other non-dictyopharid genera (Fig. 1). Fieber (1872) and either cover all but the last segment or barely extend beyond first recognized Orgeriae as a distinct unit before Melichar the tip of the abdomen (submacropterous), while Capenini, (1912) separated Dictyopharinae (i.e. Dictyopharidae) into Cleotychini and Rancodini are micropterous, with the tegmina five groups: Cladyphini Melichar, Dichopterini Melichar, Dic- strongly shortened and terminating above the abdominal tergite tyopharini Spinola, Bursini Melichar, and Orgerini [sic] Fieber. III, similar to Orgeriinae. Muir (1923) further divided this family into two subfamilies, Little research has been done on the phylogenetic relation- Dictyopharinae and Orgeriinae, with five tribes. Emeljanov ships within Dictyopharinae, although recently morphologi- (1969) reclassified the subfamily Orgeriinae and restricted them cal phylogenies have been completed on Miasa Distant, Cen- to the Holarctic region. The groups Capenini Emeljanov, Lyn- tromeria Stål (both of Orthopagini), Aluntiini, and Orthopagini cidini Schmidt, Risiina Fennah and Strongylodematina Fen- (Song et al., 2014, 2016b,c). Song et al. (2016b) confirmed nah, distributed in South Africa and Madagascar, were pro- the placement of Aluntiini back to Dictyopharidae from Ful- visionally treated as members of the subfamily Lyncidinae goridae, but this group was distinctly paraphyletic. Moreover, Schmidt and were later moved into Fulgoridae (Emeljanov, although the length, thickness and curvature of the cephalic pro- 1979). In 1980, Emeljanov recognized four tribes within Org- cess varied dramatically in Orthopagini, most Oriental genera of eriinae – Almanini Kusnezov, Colobocini Emeljanov, Orgeri- Orthopagini formed a monophyletic group (Song et al., 2016c). ini, and Ranissini Emeljanov – and proposed an evolutionary The monophyly of Aluntiini, Arjunini and most Orthopagini hypothesis of the group where Orgeriinae were derived within genera appeared reliable (e.g. Song & Liang, 2006, 2008, 2011, Dictyopharinae (Emeljanov et al., 2005). 2012; Song et al., 2014, 2016b,c). Later, Emeljanov (1983) proposed that Dictyopharini (sensu To date, the phylogenetic relationships and monophyly of Metcalf, 1946) was not a natural group, defining seven new most tribes of Dictyopharidae have not been tested cladistically. tribes for them (Orthopagini Emeljanov, Lappidini Emeljanov, The current tribal classification suggested mainly by Emeljanov Nersiini Emeljanov, Hastini Emeljanov, Taosini Emeljanov, (1969, 1980, 1983, 2011b) is a basic hypothesis that can now Scoloptini Emeljanov, and Phylloscelini Emeljanov) and be evaluated using phylogenetic
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