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 moderate 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 methods. The aim of this paper describing a new extinct tribe, Netutelini Emeljanov, based on is therefore to test the current classification of Dictyopharidae the tegminal venation, male and female genitalia, and other mor- using a morphology-based phylogenetic hypothesis and to pro- phological characters. These new tribes accommodated a few pose phylogenetic relationships among the tribes. As many of genera originally in Dictyopharini, but many genera remained the recognized genera as possible are studied, covering the full unplaced. Emeljanov (1997) described a new micropterous morphological variation and geographical range of the family. (brachypterous in Emeljanov’s paper) tribe, Cleotychini Emel- New characters and character states are included in the current janov, from Australia, and Szwedo (2008) added the second analysis along with those used in previous studies (Song et al., extinct tribe Worskaitini Szwedo. 2014, 2016b,c).

Fig. 1. Graphical display of the key steps in the evolution of the classification of the Dictyopharidae. [Colour figure can be viewed at wileyonlinelibrary.com].

Materials and methods U.S.A. (LBOB); Museum für Naturkunde der Humboldt Univer- sität, Berlin, Germany (MFNB); Museum and Institute of Zool- Specimens studied ogy, Polish Academy of Sciences, Warsaw, Poland (MIZPAS); Moravian Museum, Brno, Czech Republic (MMBC); Lund The specimens studied are deposited in the following insti- University, Lund, Sweden (MZLU); North Carolina State Uni- tutions, abbreviated as follows: American Museum of Natural versity, Raleigh, NC, U.S.A. (NCSU); Natural History Museum History, New York, U.S.A. (AMNH); Australian National of Denmark, Copenhagen, Denmark (NHMD); National Insect Collection, Canberra, Australia (ANIC); Natural His- Museum, Prague, Czech Republic (NMPC); Swedish Museum tory Museum, London, U.K. (BMNH); Bernice P. Bishop of Natural History, Stockholm, Sweden (NRM); Queensland Museum, Honolulu, HI, U.S.A. (BPBM); California Academy Museum & Sciencentre, South Brisbane BC, Queensland, of Sciences, San Francisco, CA, U.S.A. (CAS); Hungarian Nat- Australia (QM); Senckenberg Deutsches Entomologisches ural History Museum, Budapest, Hungary (HNHM); Institute Institut (SDEI), Müncheberg, Germany; Senckenberg Naturhis- of Zoology, Chinese Academy of Sciences, Beijing, China torische Sammlungen Dresden, Dresden, Germany (SNSD); (IZCAS); Personal Collection of Lois B. O’Brien, Tucson, AZ, University of Delaware, Newark, DE, U.S.A. (UDCC); and

National Museum of Natural History, Washington, DC, U.S.A. representing 104 genera and subgenera in 12 extant tribes of Dic- (USNM). tyopharinae, and nine species representing nine genera in four tribes of Orgeriinae. Incomplete representation of Dictyophar- inae taxa was due to difficulties in obtaining some species Terminology and techniques for dissection: the Australian monogeneric tribe Cleotychini The morphological terminology (Figs 2–7) used in this study and the remaining 21 genera described in different tribes. The follows Song et al. (2016b,c) for most characters, Bourgoin fossil monospecific taxa Netutelini and Worskaitini were also et al. (2015) for the tegminal venation, and Bourgoin (1993) excluded due to incomplete characteristic coding. At least two for the female genitalia. The following abbreviations are used species for each nonmonotypic genus, including the type species where possible, were sampled to capture morphological varia- in the text: a, acutellae; A1, first anal vein; ac, anteclypeus; acCuA, apical cells of CuA; ACL, anterior connective lamina tion within each genus and test its potential monophyly. When of gonapophysis VIII; acMP, apical cells of MP; acRP, apical possible, excluded taxa were discussed in the light of available cells of RP; amp, anterior margin of pronotum; amv, anterior information from the literature. margin of vertex; as, anal style; atht, apical teeth of hind tibiae; Based on the previous analysis of Dictyopharidae relation- athtI, apical teeth of hind tarsomeres I; bc, basal cell; CA, costa ships (Urban & Cryan, 2009; Song et al., 2016b), Zanna anterior; cpe, callus postocularis of eyes; cpl, carina of paran- chinensis (Distant) (Zanninae, Fulgoridae) was used to root all otal lobe of pronotum; cs, common stem of ScP + RandMP; trees. Several representatives of Fulgoridae, originally belong- CuA, cubitus anterior; CuP, cubitus posterior; dll, dorsolateral ing to Dictyopharinae, then considered for a while as a separate lobe of phallotheca; dmp, dorsal margin of pygofer in profile; ep, family related to Fulgoridae and Dictyopharidae (Emeljanov, endosomal processes; fcs, frontoclypeal suture; fl, folding line; 2011a), and now as forming a basal lineage of four tribes within Gp, gonoplacs; gs, gonostyle; Gx VIII, gonocoxae VIII; GxL, Dichopterinae of Fulgoridae (Emeljanov, 2013), were also gonocoxae VIII with endogonocoxal lobe; GxP, gonocoxae VIII added. They included Cladodiptera macrophthalma (Spinola), with endogonocoxal process; hpg, hook-like process of gonos- Diacira varia Walker (Cladyphini), Dichoptera similis Schu- tyle; icf, intermediate carina of frons; icp, intermediate carina macher (Dichopterini), Dorysarthrus sumakowi Oshanin of pronotum; lcf, lateral carina of frons; lcm, lateral carina of (Dorysarthrini), and Protachilus rex Fennah (Protachilini). mesonotum; lcv, lateral carina of vertex; llcp, lower lateral carina of pronotum; ls, lateral spine of hind tibiae; m, mesonotum; mcf, median carina of frons; mcm, median carina of mesonotum; Phylogenetic analysis mcp, median carina of pronotum; mcv, median carina of vertex; MP, media posterior; nl, nodal line; o, ocellus; p, pronotum; pa, The character matrix was created in winclada v.1.00.08 pedicel of antenna; pc, postclypeus; pcc, postcostal cell; PCL, (Nixon, 1999, 2002), comprising 146 morphological characters posterior connective lamina of gonapophysis IX; Pcu, postcubi- of adults from the head (36 characters, 24.7%), thorax including tus; pg, pygofer; pl, platellae; pmp, posterior margin of prono- legs (31 characters, 21.2%), tegmina and hindwings (40 char- tum; pmpg, posterior margin of pygofer; pmv, posterior margin acters, 27.4%), pregenital segment of abdomen (four charac- of vertex; psa, pterostigmal area; pt, phallotheca; R, radius; RA, ters, 2.7%), male genitalia including segment X (10 characters, radius anterior; RP, radius posterior; sa, sensory appendage of 6.8%), and female genitalia including segment X (25 characters, Gp1; ScP, subcosta posterior; ss, subapical spine of fore femora; 17.1%) (File S3). Of 146 characters, 98 are binary and 48 are sx, segment X; t, tegula; tri, trigon; ulcp, upper lateral carina of multistate. All character states were treated as unordered. The pronotum; upg, upper process of gonostyle; v, vertex; vl, ventral character states were scored as dashes (−) if not applicable. lobe of phallotheca; vmp, ventral margin of pygofer in profile. The matrix was analysed using tnt v.1.5 (Goloboff & Cata- The abdomens of specimens used for dissection were cleared lano, 2016) under both equal weighting (EW) and implied in 10% KOH at room temperature for c. 6–12h, rinsed in weighting (IW), respectively. Tree searches were performed distilled water and then transferred to 10% glycerol for exam- using ‘New Technology Search’ with the default algorithms ination. Observations, measurements and photography were (ratchet, sectorial searches, drifting and fusing) with 1000 ran- conducted under a Zeiss Discovery V12 stereomicroscope dom addition sequence replicates. For the larger datasets (i.e. > (Germany) equipped with a Nikon D7000 digital camera 150 taxa), New Technology Search is much more effective than (Japan) in IZCAS or Leica Z16 APO A macroscope (Germany) traditional search (Goloboff et al., 2008b). The EW analysis was equipped with a Leica DFC495 microscope camera and leica also run under heuristic analysis with 1000 replications and ten application suite 3.7.0 (Germany) in MFNB. The final images starting trees per replication in nona v.2.0 (Goloboff, 2000) con- were compiled from multiple photographs using combinezm ducted in winclada. As to IW, the characters are weighted dur- image stacking software and improved with Adobe photoshop ing tree searches and the resultant most parsimonious trees are cs5. compared to determine the maximum total character fit. Char- acter fit can be adjusted using a concavity constantK ( )value, Taxon sampling where K determines how much a character is downweighted based on its level of homoplasy (Legg et al., 2013). In our IW A total of 170 species were explicitly coded for both sexes analysis, a range of K values (3, 5, 7, 10, 15, 20, 25, 30, 35, 40, (File S2). Among them, the ingroup taxa concerned 155 species 50, 75 and 100) were used to investigate the effect of character

Fig. 2. (A, D–F, I) Head, pronotum and mesonotum, dorsal view; (B, G, H, J) head and pronotum, lateral view; (C) head and pronotum, ventral view. (A–C) Dictyophara (Euthremma) anatina Puton; (D) Taosa suturalis (Germar); (E) Rancoda rakitovi Emeljanov; (F) Centromeriana jocosa (Gerstaecker); (G) Miasa smaragdilinea (Walker); (H) Pteroplegma sp.; (I, J) Madagascaritia hova (Nast).

B C

F D

HIJK

Fig. 3. (A–D,F–H,J,K)Tegmen;(B,E,I)hindwing.(A)Thanatodictya praeferrata (Distant); (B) Doryphorina stali Melichar; (C) Dendrophora borneensis (Schmidt); (D, E) Arjuna scriba Emeljanov; (F) Dictyopharoides inficita Melichar; (G) Dictyopharina viridissima Melichar; (H, I) Phylloscelis altra Germar; (J) Menenches atropos Fennah; (K) Rancoda rakitovi Emeljanov. weighting on hypotheses of relationship. The bootstrap (Felsen- 2014; Szwedo, 2008; Song et al., 2016b). Like many Fulgoro- stein, 1985) was used as support measure and calculated in tnt morpha groups (e.g. Tropiduchini, Tropiduchidae; Wang et al., v.1.5 for the hypothesized clades with 100 replications, using 2017), the definition of a tribe in Dictyopharidae is generally ‘New Technology Search’ with the default algorithms. Bremer based on a combination of several morphological characters support was calculated in tnt v.1.5 and obtained by TBR swap- (e.g. Emeljanov, 2011b; Song et al., 2016b). The diagnostic ping on the most parsimonious trees and setting ‘suboptimal’ to features to the tribes are not always autamomorphic and may be 100. figtree v.1.4.2 (Rambaut, 2014) and winclada v.1.00.08 present in the other tribes (or absent within the same tribe), and (Nixon, 2002) were used to display the resulting trees. cannot be regarded as a strict synapomorphy. For instance, the trigone on the head is the most important character for Taosini (Emeljanov, 2011b), but also occurs in Cleotychini, Rancodini, Results and even Arjuna Muir of Arjunini (Emeljanov, 1997, 2008, 2014). Similarly, the common stem of ScP + R and MP on the Morphological characters and comments tegmina is a good synapomorphy for Nersiini, but Deltoplana Emeljanov and Plegmatoptera lack it. For more comments on The tribes of Dictyopharide are defined on the basis of the morphological characters see File S4. structures of the head, mesonotum, legs, tegminal venation, and The characters used to diagnose tribes were used in the male and female genitalia, especially the last three structures current analyses. Unfortunately, our analyses show that most (Melichar, 1912; Muir, 1923; Emeljanov, 1983, 2008, 2011b, of the tribal diagnostic features are homoplasious and objective

D E

pl104-1 FG

Fig. 4. (A–C) Fore leg; (D, E) hind leg; (F, G) acutellae of fore tarsomeres I; (H) apical teeth with platellae of hind tarsomeres I; (I) pretarsus of foreleg.(A,C–F,H,I)Orthopagus lunulifer Uhler; (B) Fernandea conradti Melichar; (G) Dictyophara europaea (L.). unique synapomorphies are very rare. This may be because mor- midges (Diptera: Chironomidae: Tanypodinae) (Paladini et al., phologically intermediate forms, such as Litocras Emeljanov 2015; Silva & Ekrem, 2016). and Chiltana Mushtaq & Akbar, tend to obscure distinctions between tribes. In addition, some outgroups (e.g. Dichopteri- nae) used in this study share characters with Dictyopharinae, in which they had historically been placed. However, our results Cladistic analysis show that these same characters support the monophyly and phylogenetic relationships among the Dictyopharinae tribes The EW analysis yielded 147 equally most parsimonious trees and maintain a high retention index. Similar cases also occur in tnt and 10 000 in nona with tree length of 1355 steps, in other insect groups, such as the Neotropical spittlebugs consistency index (CI) of 0.15, and retention index (RI) of 0.73. (Hemiptera: Cercopidae: Ischnorhininae) and the nonbiting A strict consensus of 147 trees in tnt collapsed 39 nodes and

Fig. 5. (A) Male pygofer and segment X, dorsal view; (B) male genitalia, lateral view; (C) upper process of gonostyle; (D) male pygofer and gonostyles, ventral view; (E) aedeagus, dorsal view; (F, H, I, K) aedeagus, lateral view; (G, J) aedeagus, ventral view; (L) endosomal processes. (A, B, D–G) Orthopagus lunulifer Uhler; (C) Hasta hastata Kirkaldy; (H) Doryphorina stali Melichar; (I) Trigava recurva (Melichar); (J) Toropa ferrifera (Walker); (K) Coronersia sertata (Jacobi); (L) Eudictya grata Melichar. had a length of 1400 steps (Figure S1). The consensus tree of taxa being essentially unaffected by changes in K-values. The nona had the identical topology. consensus trees resulting from the IW analyses under K = 7 The IW analysis in tnt produced 5, 3, 1, 1, 1, 1, 1, 1, 1, and 10, and K = 50–100 were different in part from the for- 1, 3, 3, 3, and 3 most parsimonious trees, corresponding to mer (Figures S3, S4). All consensus trees obtained with IW were K-values of 3, 5, 7, 10, 15, 20, 25, 30, 35, 40, 50, 60, 75, and 100. Among them, the most parsimonious trees found for basally consistent with the EW consensus tree. In most cases, the K = 15–40 seemed to be stable and resulted in an identical strict EW analysis with no potential homoplasy is rare (Legg et al., consensus tree (Figure S2), with the topology for the ingroup 2013), while the IW scheme attempts to lessen the effects of

Fig. 6. (A, D, G) Gonapophysis VIII, dorsolateral view; (B, E, H) gonapophysis IX, ventral view; (F) gonapophysis IX, lateral view; (C, I–M) gonoplacs, ventrolateral view. (A–C) Orthopagus lunulifer Uhler; (D–F, J) Taosa suturalis (Germar); (G–I) Cuernavaca herbida (Walker); (K) Lappida sp.; (L) Niculda sp.; (M) Megadictya multispinosa Melichar.

Fig. 7. (A–D) Thorax and abdomen, dorsal view (A, B), dorsolateral view (C, D); (E–G) male segment X, dorsal view; (H–L) female segment X, dorsal view (H–K), ventral view (L). (A) Menenches atropos Fennah; (B) Ranissus edirneus (Dlabola); (C) Almana longipes (Dufour); (D) Orgerius rhyparus concordus Hartzell & Ball; (E) Aluntia longicephalica Song & Szwedo; (F) Philotheria vinula (Stål); (G) Xenochasma rectirostris (Spinola); (H) Mitrops noctivida (L.); (I) Doryphorina stali Melichar; (J) Phylloscelis altra Germar; (K) Lappida sp.; (L) Hasta hastata Kirkaldy.

© 2018 The Royal Entomological Society, Systematic Entomology, 43, 637–658 Phylogeny of Dictyopharidae 647 homoplasy, improving the phylogenetic analysis of the mor- 68–0) was considered the most important diagnostic character phological datasets (Goloboff et al., 2008a). Certain characters for differentiating Dictyopharidae from Fulgoridae (Emeljanov, will excessively influence those IW trees obtained under low 1979). Accordingly, Emeljanov moved all Dichopterini s.s. with K-values, resulting in clades that are strongly contradicted by one claval vein into Fulgoridae as a subfamily Dichopterinae numerous other characters (Namyatova et al., 2016). We there- (Emeljanov, 1979, 2011a,b, 2013). Despite the external sim- fore chose the consensus tree under K = 30 for the discussion ilarity of the outgroup Dichopterinae, the monophyly of the that follows, with the more robust bootstrap/Bremer support val- Dictyopharidae (node 1–33 in Figures 8–11) is supported in all ues mapped onto the tree (Figs 8–11). parsimony analyses under EW and IW, but the support values are Based on the results of both EW and IW analyses, the not high. Aside from the absence of one claval vein (68–0), five monophyly of Dictyopharidae (as currently accepted) is sup- unambiguous synapomorphies of adults support the monophyly ported. However, neither the EW analysis nor the IW analysis of Dictyopharidae: the elongate clypeus (28–1); the nearly supports partitioning of Dictyopharidae into the subfamilies flat mesonotum (48–1); the relatively short fore coxae (95–1); Dictyopharinae and Orgeriinae. The Dictyopharinae always the developed arolium (106–1); and the separated gonoplacs include a monophyletic ‘Orgeriinae’ lineage, which fall within (135–1). Dictyopharidae are further supported by two contra- a Xenochasma+ complex (named following the categorical dicted changes in characters with the concave posterior margin nomenclature of De Souza Amorin, 1982) in all the analyses, of the pronotum (45–2) and lacking the nodal line on the depicting the nonsister relationship of the two subfamilies. In tegmina (80–0), which are present in most dictyopharid taxa. return, the first dichotomy within the current Dictyopharidae The following morphological characters are generally present strongly supports two monophyletic lineages: Aluntiini on one in Dictyopharidae and also some outgroup taxa: the frons being side and all other Dictyopharidae on the other side. nearly flat (15–0); the MP bifurcating1 MP + 2 and MP3 + 4 poste- In the EW analysis (Figure S1), the relationships among the rior to the middle of the tegmina (74–1); the bifurcated MP3 + 4 New World Hastini, Nersiini and Taosini are not resolved. The in the posterior half of the tegmina (75–1); the hindwings lack- genus Pharodictyon Fennah and the Paramisia+ clade are sister ing numerous transverse veins (90–1); three apical teeth of the to the remaining Dictyopharidae, and are of uncertain tribal inner group on the hind tibiae (102–1); no special chaetotaxy on placement. Hastini not only includes Hastini s.s. defined by the hind tarsomeres I and II (104–0), and the upper process of Emeljanov (2011b), but also adds the Chondrophana+ clade the gonostyles (112–0). These characters in combination allow from Chile (from Nersiini); however, the relationships among us to distinguish Dictyopharidae from the most taxa of Fulgori- them are poorly resolved. A similar situation occurs between dae, although they are not autapomorphies in this analysis as a Nersiini and Taosini. They are divided into three parallel result of different outgroup selection. lineages, Taosini, the Nersia+ clade, and the Digitocrista+ clade, where the latter two clades form Nersiini s.s. In addition, the New World Lappidini fall into the Old World Orthopagini to Xenochasma+ complex and taxonomic status of Orgeriinae form a monophyletic group in the EW analysis. The IW analysis provides better resolution of the phylogeny, In two character-weighting schemes, most submacropter- and groups the taxa in a more coherent way (Figure S2). ous and all micropterous taxa within Dictyopharidae form More precisely, Dictyopharidae genera are grouped into a monophyletic lineage (node 17). The Xenochasma+ com- seven major monophyletic lineages more or less corre- plex is proposed here to describe this putative monophyletic sponding to already recognized tribes and successively group, including the Xenochasma clade (node 18), Scolop- arranged as Figs 8–11: Aluntiini (node 2), Arjunini (node tini (node 19), the Fernandea clade (node 21), Phylloscelini 4), Hastini (node 5), a monophyletic clade of three tribes (node 22), Rancodini (node 24), Capenini (node 25), and [(Taosini + Lappidini) + Nersiini] (nodes 10 and 13), a Orgeriinae (node 26). This large clade is located between the Xenochasma+ clade (node 17), Orthopagini (node 31), and Neotropical Nersiini and the Old World monophyletic group Dictyopharini (node 32). The Xenochasma+ clade is formed Orthopagini + Dictyopharini. They are supported by the follow- by the genera and tribes according to the following schema: ing characters: the connected lateral carinae of the mesonotum [(Xenochasma + Sicorisia) + (Scoloptini + ((Fernandea clade + (50–1); the submacropterous or micropterous tegmina (55–1); Phylloscelini) + (Rancodini + [Capenini + Orgeriinae])))]. and the male and female anal style not reaching beyond the apical ventral margin of the segment X (119–1, 144–1). In the current analysis, the Orgeriinae lineage is recovered, Discussion supported by three synapomorphies of the absence of the tegula (52–1); the absence of basal cell of the tegmina (69–1); and the Monophyly of Dictyopharidae basal portion of the tegmina inserting into the pronotum (70–1). The Orgeriinae, proposed as a subfamily by Muir (1923), were Emeljanov (1979) provided 18 characters distinguishing revised and reclassified by Emeljanov (1969, 1980). Emeljanov Dictyopharidae and Fulgoridae, including 14 morphological (1980) and Emeljanov et al. (2005) proposed that Orgeriinae characters of adults. Most of them were included in the present were derived within the Dictyopharinae and associated with character matrix (File S4). The absence of a claval transverse the formation of the subtropical savannah in Central Asia in vein between CuP and Pcu of the tegmina (character 68, state 0: the Paleocene-Eocene age. He even suggested that Orgeriinae

Fig. 8. Phylogenetic hypothesis for Dictyopharidae, resulting from strict consensus tree under implied weighting analysis (K = 30), with clade number (on nodes) and bootstrap (values < 50% not shown)/Bremer support (> 1) values. Part I, nodes 1–9. [Colour figure can be viewed at wileyonlinelibrary.com]. were evolved within the Dictyopharini or Orthopagini, de facto However, our sampling of Orgeriinae remains limited, and rendering one of these two lineages paraphyletic and setting up there may be autapomorphies that might be added to our data a classification issue of a subfamily placed into a tribe. matrix in the future, especially nymphal features, which might The Orgeriinae lineage, however, is not supported as sister to deserve, again, a subfamilial rank to orgeriines. Indeed, the com- Dictyopharinae, but instead is nested within Dictyopharinae in binations of submacropterous or micropterous dictyopharines this study. This group falls within the Xenochasma+ complex, and orgeriines may result from parallel or convergent evolution implying that our results confirm recent Emeljanov views of due to the reduction of the tegmina and body habitus, a scenario orgeriine taxa derived from some dictyopharine lineage, and that we cannot exclude based on evidence available at present. confirm the need to reject a basal separation of the family into Accordingly, we do not suggest altering the taxonomic status Orgeriinae and Dictyopharinae. Alternatively, the Dictyophar- of Orgeriinae taxa until it is investigated with additional data, idae (as currently recognized) are segregated into seven major especially molecular, with the explicit goal of establishing the lineages with the first division occurring between Aluntiini and phylogenetic placement of the Orgeriinae. the rest of the Dictyopharidae, and the Orgeriinae can no longer be supported as a subfamily, if all Dictyopharinae and other Monophyly and phylogenetic relationships among tribes are maintained. Accordingly, the results of the present Dictyopharinae tribes analysis suggest that Orgeriinae might be downgraded ad minima to a tribal status in Dictyopharinae, and the tribes within Discounting the placement of Orgeriinae, the topology of Orgeriinae should be considered as subtribes of Orgeriini. phylogenetic relationships within Dictyopharinae obtained

Fig. 9. Phylogenetic hypothesis for Dictyopharidae. Part II, nodes 10–16. [Colour figure can be viewed at wileyonlinelibrary.com].

Fig. 10. Phylogenetic hypothesis for Dictyopharidae. Part III, nodes 17–29. [Colour figure can be viewed at wileyonlinelibrary.com]. from IW analysis under K = 30 (Figure S5) approximates to are posited at the base of Dictyopharidae. The following synapo- Figs 8–11. The monophyly and phylogenetic relationships morphic characters strongly support the monophyly of Aluntiini: among the currently defined tribes of Dictyopharinae are the extended vertex (14–1); the elongate oval eyes (33–1); the resolved in our tree (Figs 8–11). This subfamily, if we exclude elongate pedicel (35–1); the overlapped distally tegmina Orgeriinae, tentatively comprises 12 extant tribes: Aluntiini, (59–0); and the location of the ACL teeth (121–0). The tribe is Arjunini, Capenini, Dictyopharini, Hastini, Lappidini, Ner- further characterized by the tegmina with suboblique veinlets in siini, Orthopagini, Phylloscelini, Rancodini, Scoloptini and the costal cell (85–0); the open clavus (87–1); the small teeth of Taosini. Two fossil tribes, Netutelini and Worskaitini, may the ACL (122–0); only one GxP (130–0); the gonapophysis IX belong to Dictyopharinae, although coding for Netutelini only with posterior fibula extending to the gonospiculum (133–0); contains characteristics of the tegminal venation. Based on an additional Gp3 (134–1); and tiny setae of the Gp1 (140–1). the previous study of the phylogeny of Aluntiini, Worskaitini In addition, two unique characters of the fifth-instar nymphs, were placed between the Australian Hastini and the Old World the large wax-secreting plates and the longitudinal linear areas Orthopagini + Dictyopharini, and sister to the combination separating wax gland pores on the wax-secreting plates, are two of Orthopagini and Dictyopharini (Song et al., 2016b). The autapomorphies, also supporting the monophyly of Aluntiini micropterous Cleotychini are provisionally excluded in this (Liang & Song, 2012; Song et al., 2016b). study because of a lack of available specimens and numerous unique features (see discussion in the following). Node 4: Arjunini

Arjunini are sister to the remaining tribes, similar to that Node 2: Aluntiini proposed by Song et al. (2016b). Eight characters support this grouping: the vertical posterior margin being not ridged (13–0); Recent phylogenetic analysis (Song et al., 2016b) supported the elongate clypeus (28–2); the longer rostrum (30–2); the the placement of Aluntiini s.l. in Dictyopharidae, and their divi- submacropterous tegmina (55–1); the pointed apically tegmina sion into two different taxa, Aluntiini s.s. and Arjunini. These (58–2); the tegmina with long setae (60–2); and the simple results are confirmed here and the monophyletic Aluntiini s.s. hindwings (91–1, 92–1).

Fig. 11. Phylogenetic hypothesis for Dictyopharidae. Part IV, nodes 30–33. [Colour figure can be viewed at wileyonlinelibrary.com].

Arjunini are monophyletic in most analyses. However, EW analysis, Taosini appear directly monophyletic and sister Arjunini fall into Hastini s.l. to form a monophylum in the IW to Nersiini, while Lappidini fall into Old World Orthopagini under K = 7 and 10 (Figure S3), or form a series of successive (Figure S1). Emeljanov (2008) proposed that the taxonomic sister taxa to the remaining dictyopharines under K = 50–100 position of Taosini and Lappidini was overestimated, and down- (Figure S4). Morphologically, the common stem of ScP + R graded them as the subtribes of Nersiini based on the common and MP veins on the tegmina and the consistency of the female stem of ScRM and more longitudinal folds on the forewing genitalia support the close relationship between Arjunini and membrane (Emeljanov, 2008), but they were still regarded as Hastini (Song et al., 2016b). The common characters of the the tribes in his subsequent paper without further explanation female genitalia include the arrangement and size of the ACL’s (Emeljanov, 2011b). Our IW analysis confirms Emeljanov’s pre- apical teeth (124–0, 125–0); the bifurcated PCL (132–1); the vious statement placing the two tribes together, and as sister to gonoplacs lacking sensory appendage (138–0); and spinous Nersiini in which they should be included as subtribes in the setae of the Gp1 (141–1). These features have been consid- future. Support for Taosini and Lappidini monophyly is based on ered as tribal diagnoses within Dictyopharinae (Emeljanov, the following characters: the frons surpassing the vertex (19–0); 1983, 2011b; Song et al., 2016b,c); however, they are not the incomplete intermediate carinae of the pronotum (39–1); the autapomorphies because they are sparsely present among posterior margin of the pronotum not being notched (46–0); and other dictyopharine taxa. The relationships among these clades the wider pygofer (111–1). deserve a detailed and full revision and phylogenetic analysis (Z–S. Song, unpublished data). Node 11: Taosini s.s.

Node 5: Hastini Taosini s.l. were established for Taosa Distant, Rhynchomi- tra Fennah, Protachilus and Mitrops Fennah for the similar- Hastini were first considered a tribe based on Hasta Melichar ity in female genitalia (Emeljanov, 1983). The latter three and Thanatodictya Kirkaldy, both from the Australian region genera were subsequently excluded from Taosini because of (Emeljanov, 1983). Two Neotropical genera, Dorimargus the absence of the trigones (Emeljanov, 2011b, 2013), and Melichar and Eudictya Melichar, were added, leading this small six genera were added to this tribe (Emeljanov, 2011b). In taxon to show an ‘Australian–South American’ distributional the IW analysis, Taosini are paraphyletic with Netaosa Emel- disjunction (Emeljanov, 2008). Emeljanov (2008, 2011b) pro- janov sister to the combination of Cuernavaca Kirkaldy, Taosa posed that Hastini share two common characters: the outer (node 11) and Lappidini (node 12); also Sicorisia Melichar lobes of the gonoplacs with a filmy margin (137–1) and the is excluded from Taosini due to absence of the trigones and female anal tube with ventral setae sitting on high papilliform other distinctive characters (see later). The trigones are the digitate socles (145–1). In our analysis, Hastini not only include main character for Taosini (Emeljanov, 2011b), but this char- Hastini s.s. as defined by Emeljanov (2011b), but also several acter is simultaneously present in Cleotychini and Rancodini, other Neotropical taxa: the Paramisia+ clade, Pharodictyon and and is even a generic-level diagnostic feature for Arjuna (Emel- the Chondrophana+ clade that belonged to Nersiini. Several janov, 1997, 2008, 2014; Song et al., 2016b). Taosini s.s., morphological characters support them as a monophyletic lin- including Cuernavaca and Taosa in this study, are supported eage, including one folding line on the tegmina (62–1) and the by five characters: two to four folding lines on the tegmina large and stout spines on the phallobase (114–1). In addition, (62–2); five to seven apical teeth on the hind tarsomeres II the papilliform digitate socles (145–1) are present in most (105–0); the large and stout spines on the phallobasal lobes Hastini taxa. (114–1); and the rounded female segment X (143–0). Two Hastini are further divided into four lineages, the Paramisia+ submacropterous genera, Brachytaosa Muir and Phormotegus clade (node 6), the Pharodictyon clade (node 7), the Dorimar- Emeljanov, belong to this tribe based on Emeljanov’s comments gus+ clade (node 8) and the Hasta+ clade (node 9). The Mada- (2011b), although they were not analysed because of the lack of gascan genus Tupala is similar to Sicoris gayi (Spinola) in specimens. appearance and male genitalia, obviously belonging to the Dori- margus clade. This genus is different from all the dictyopharid genera in the Old World by the common stem of tegminal Node 12: Lappidini ScP + R and MP and the structures of female genitalia. The type material of Tupala occulta Stroinski´ & Szwedo might be mis- Lappidini were erected by Emeljanov (1983) based upon labeled or incidentally introduced in Madagascar from South Lappida Amyot & Serville, including five genera. The venation America (Stroinski´ & Szwedo, 2015). of the forewings and the basal ovipositor plates bearing a separated appendage, both apparent synapomorphies, were used to support this tribe (Emeljanov, 2011b). Our analysis shows Node 10: Monophyly of Taosini + Lappidini that the tegminal venation provides a series of synapomorphies shared by combination of Cuernavaca, Taosa and Lappidini. Taosini and Lappidini together are monophyletic, and form The monophyletic Lappidini are supported by contradicted the sister group to Nersiini in the IW analysis. However, in the characters as follows: the laterally compressed head (2–0); the

© 2018 The Royal Entomological Society, Systematic Entomology, 43, 637–658 Phylogeny of Dictyopharidae 653 elevated vertex (7–1); the angularly concave posterior margin of Nersiini, but not an autapomorphic one. This character shows of the vertex (12–1); the frons lacking median carina (20–4); a high degree of homoplasy, with independent origin of the the bifurcation of MP anterior to CuA on the tegmina (76–0); carinate tegulae in the African Dictyopharini and Orthopagini seven apical teeth on the hind tibiae (101–1); the elongate male (Fennah, 1958; Synave, 1965; Emeljanov, 2011b; Z–S. Song, segment X (118–2); an additional Gp3 (134–1); the Gp1 with unpublished data). sensory appendage (138–1); and the Gp1 lacking spinous setae (141–0). Node 18: Xenochasma+ clade

Node 13: Nersiini The Chilean genera Xenochasma and Sicorisia, initially placed in Nersiini, occupy a basal position in the Xenochasma+ Nersiini are the second largest tribe in Dictyopharinae, com- complex. The characters supporting this clade are the tuber- prising 26 genera mostly distributed in the Neotropical region culate frons (18–1); the longer basal segment of the rostrum and few in the Nearctic region (Emeljanov, 2011b; Bartlett (31–0); the bifurcation of MP anterior to CuA on the tegmina et al., 2014; Bartlett, 2017). This tribe is polyphyletic in our (76–0); the basally fused gonoplacs (135–0); and the Gp1 with- phylogenetic hypothesis because the genera Dictyopharoides out long setae (139–0). s.s. Fowler, Paramisia Melichar, Pharodictyon, Sicoris and Xenochasma Emeljanov should be excluded from Nersiini. Three clades, the Digitocrista+ clade (node 14), the Trigava+ Node 19: Scoloptini clade (node 15) and the Nersia+ clade (node 16), form Nersiini in the tree, supported by three characters: more tegminal folding The monotypic Scoloptini were established by Emeljanov lines (62–2); the number of acutellae (99–2); and the bifur- (1983) based on the polytypic genus Scolops Schaum from cated endosomal processes (115–1). Unfortunately, these char- North America, comprising two subgenera and 32 species acters are not synapomorphic and are often present in the other (Breakey, 1928; Bartlett et al., 2014). The monophyly of taxa. Nersiini display the greatest disparity within Dictyophar- Scoloptini is supported by the following characters: the cephalic inae, such as the massive size, carinate tegulae, complicated process being compressed dorsoventrally and laterally, and dis- venation, piercing-cutting ovipositor and bifurcated endosomal tinctly curved upwardly (1–0, 2–0, 3–1); the smooth vertical processes. posterior margin (13–0); the intermediate carinae of the frons In the Trigava+ clade, Mitrops and Rhynchomitra have a (24–3); the callus postocularis of the eyes (32–0); the dimorphic piercing-cutting ovipositor, which is characterized by the unique tegmina (54–1); the pointed tegmina (58–2); the compressed features, the ACL with more than 12 teeth (123–2); the basal upper process of the gonostyles (112–1); and the slender Gp2 teeth of ACL paralleling double columns (127–1); and the (142–0). Emeljanov (2011b) considered lacking median carina extremely elongate PCL and gonoplacs (131–1, 136–1). Emel- on the frons as a tribal diagnostic feature of Scoloptini. In fact, janov (2011b) proposed that the piercing-cutting ovipositor the median carina is present in the basal part of the frons, and may allow the Mitrops clade to be a subtribe of Nersiini. this character shows homoplasy and is of independent origin in However, this feature simultaneously occurs in Cuernavaca of many dictyopharine taxa. Taosini and is considered as a secondarily elongate type from the raking-kneading ovipositor. The raking-kneading ovipositor, which is generally present within Dictyopharidae, might origi- Node 20: Fernandea + Phylloscelini nate from the common ancestor of the families Achilidae, Dic- tyopharidae and Fulgoridae (Emeljanov, 2011b). Fernandea and Phylloscelini form a monophyletic group, The Nersia+ clade is a monophyletic lineage, including diverse supported by five characters: the frons surpassing the vertex species varying dramatically in morphology. The genera Delto- (19–0); the median carina of the pronotum being weakly ridged plana and Megadictya Melichar are large, exceeding 25 mm in (38–0); the pronotum lacking intermediate carinae (39–0); the length, similar to fulgorids. Although the body size is considered strongly flattened and foliaceous fore coxae (94–0); and the homoplastic (Emeljanov, 2013), the overwhelming majority of Gp1 with sensory appendage (138–1). Two groups show an dictyopharids are moderate to small in size, implying that Dic- odd ‘Afrotropical-Nearctic’ geographical distribution, and their tyopharidae were likely to have originated from a small-sized relationship may be convergently evolved due to adapting to ancestor that was probably a grass feeder and more widely dis- similar habitats. tributed than ancestral Fulgoridae. The tegmina of Deltoplana Fernandea (node 21) was revised recently by Song et al. and Plegmatoptera lack the common stem of ScP + RandMP (2016a), and includes two species in western Africa. This genus (71–1), in contrast to other Nersiini, because they are strongly was traditionally placed in Dictyopharini (Melichar, 1912; Met- broadened from base to the truncate apex, with the basal cell calf, 1946) and assigned to Orthopagini by Emeljanov (2011b). large and wide, leading to ScP + R and MP separately originat- The African genera Macronaso Synave and Nesolyncides Fen- ing from this cell (Emeljanov, 2011b). Lacking a common stem nah belong to this clade. appears to be a derived condition within Nersiini. Similarly, the Phylloscelini (node 22), including Phylloscelis Germar carinate tegulae (53–1) is the most important diagnostic feature and four species from North America, were recognized as a

© 2018 The Royal Entomological Society, Systematic Entomology, 43, 637–658 654 Z.-S. Song et al. monobasic tribe (Emeljanov, 1983). The tribe is defined by a (7–1); the smooth posterior margin of the vertex (13–0); the noncontradicted synapomorphy of the transversely elongate tuberculate frons (18–1); the incomplete lateral carinae of eyes (33–2), and seven contradicted characters: the absence of the pronotum (40–1); the fore femora with numerous spines cephalic process (0–0); the wider vertex (5–0); the tuberculate (98–2); and more than 20 apical teeth on the hind tarsomeres frons (18–1); lacking callus postocularis (32–2); the tubercu- II (105–3). late pronotum (37–1); the dimorphic tegmina (54–1); and the open clavus (87–1). Node 26: Relationships among Orgeriinae tribes

Node 23: (Rancodini + Capenini) + Orgeriinae The relationships among the orgeriine tribes are similar to that proposed by Emeljanov (1980). This group is divided into three The micropterous Rancodini, Capenini, and Orgeriinae clades, Ranissini, Colobocini and the Orgeriini clade. Ranissini comprise a monophylum, which is sister to Fernan- (node 27) are sister to the remaining orgeriines, supported by dea + Phylloscelini, and is supported by six noncontradicted the much wider vertex (8–2); the bifurcated PCL (132–1); the synapomorphies: the absence of the ocelli (34–0); the Gp1 without filmy edging (137–0); the sensory appendage on micropterous tegmina (55–2); the incurved postcostal cell the Gp1 (138–1); and the spinous setae of the Gp1 (141–1). on the tegmina (66–1); the unbranched ScP + R on the tegmina Colobocini (node 28) include one monotypic genus and species (72–1); the absence of the claval suture (86–1); and the Colobocus conspersus (Puton), which might be the transitional hindwing pads (89–1). form between Ranissini and Orgeriini. The Orgeriini clade (node 29) includes Almanini and Orgeriini, supported by a synapomorphy of the intermediate carinae on the pregenital Node 24: Rancodini segments (109–1), and the following contradicted characters: the sensory pits on the frons, pronotum and pregenital segments Rancodini, a recent monotypic tribe of Dictyopharinae, were (17–1, 36–1, 110–1), and the longer rostrum (30–2). This erected by Emeljanov (2014) based on Rancoda rakitovi Emel- study does not support the respective monophyly of Almanini janov from Chile. The adults of R. rakitovi are strongly and Orgeriini. micropterous and have sensory pits on the body, very similar to the representatives of Almanini and Orgeriini of Orgeriinae. However, the tegulae, the simple median carina on the abdomi- Node 30: Monophyly of Orthopagini + Dictyopharini nal tergites, and the arrangement of the sensory pits on tergites VI–VIII supported the tribe being placed in Dictyopharinae Orthopagini are the closest phylogenetically to Dictyopharini (Emeljanov, 2014). This taxon is highly autapomorphic, sup- in our previous studies, both distributed in the Old World (Song ported by the distinctive synapomorphic characters of the sen- et al., 2016b,c). Two tribes have the similar tegmina and female sory pits on the frons, pronotum and pregenital segments (17–1, genitalia, which are regarded as important features differentiat- 36–1, and 110–1). The following characters further support its ing tribes of Dictyopharinae (Emeljanov, 1983, 2011b). Charac- monophyly: the short and wide vertex (5–0, 8–2); the trigones ters in support of the monophyly of two tribes are: the tegmina

(6–1); two teeth of the inner group on the hind tibiae (102–0); having one folding line between MP3 and MP4 (62–1); the sen- the large and stout spines on the phallobasal lobes (114–1); sory appendage of the Gp1 (138–1); and the gonoplacs lacking the fused gonoplacs (135–0); and the Gp1 without long setae spinous setae on the Gp1 (141–0). In addition, their common (139–0). node is supported by the following characters: the separated lateral carinae of the mesonotum (50–0); the gonocoxae VIII with two GxPs (130–1); and the Gp1 without filmy edging (137–0). Node 25: Capenini

Fennah (1962) included three genera, Capena Stål, Diasphax Node 31: Orthopagini Fennah, and Menenches Fennah, from South Africa into the subtribe Orgeriina of Orgeriini. Emeljanov (1969) excluded Most Orthopagini genera in the Oriental region formed a good them from Orgeriinae, defined them as the tribe Capenini, and monophylum (Song et al., 2016c). In this study, Afrotropical later moved them to Fulgoridae without further explanation taxa were added to test the phylogeny of Orthopagini. The (Emeljanov, 1979). More recently, this taxon was considered phylogenetic results support the monophyly of the tribe well , but a tribe of Dictyopharinae (Emeljanov, 2011b). Although only show a slightly different topology. Orthopagini are supported by Menenches was in our analysis, there is no doubt that three a synapomorphic character of one spine on the ventral margin of Capenini genera make up a monophyletic group based on the the fore femora (98–1). The Afrotropical genera Centromeriana Fennah’s detailed descriptions and illustrations. Capenini are Melichar, Phaenodictyon Fennah and Raphiophora Schaum supported by an unambiguous synapomorphy of the concave belong to Orthopagini. Australian Ellipoma Emeljanov was not mesonotum (48–2). The characters further support it as follows: examined in this study but is provisionally placed in the tribe in the dorsoventrally compressed head (1–0); the elevated vertex light of Emeljanov’s view (2008, 2011b).

Node 32: Dictyopharini history of Dictyopharidae facilitating future revisionary work of the family. Our results show a monophyletic Dictyopharidae as Dictyopharini include the type genus of Dictyopharidae and they are currently considered, with Aluntiini sister to the remain- another 28 genera, representing the typical dictyopharid group. ing Dictyopharidae, but do not support the basal splitting of the Dictyopharini are supported by a synapomorphy of the fore and family into Orgeriinae and Dictyopharinae. middle tarsomeres I and II, having more than four acutellae However, our analysis does not provide support for a dic- (99–2). Some changes in characters are present in most Dic- tyopharid clade sister to Fulgoridae, but rather suggests that tyopharini, including one carina on the paranotal lobes (42–1); Fulgoridae is paraphyletic with respect to Dictyopharidae. This the straight and parallel lateral carinae of the mesonotum (49–1, hypothesis needs to be tested further: which taxa should be 51–0); seven apical teeth on the hind tibiae (101–1); and the included in Dictyopharidae and how can paraphyletic Fulgori- long and slender spines on the phallobasal lobes (113–1). These characters were used as tribal diagnoses to define Orthopagini dae be turned into monophyletic groups recognized in the classi- and Dictyopharini (Emeljanov, 2011b; Song et al., 2016c), and fication? All this suggests further research, especially at thebase support well their monophyly in our EW analysis (Figure S1). of the family tree and within an additional molecular framework, However, the genera Litocras and Chiltana (node 33) are will allow us to formally review Dictyopharidae classification excluded from Orthopagini and Dictyopharini to form a mono- that we maintain at the moment with two subfamilies: Orgeri- phyletic clade, sister to Orthopagini and Dictyopharini in the inae and Dictyopharinae. EW analysis, mainly based on the absence of the cephalic pro- Although most current tribes are recovered, most tribal and cess and frontal median and intermediate carinae (0–0, 20–4, generic concepts lack solid autapomorphic support. In connec- 22–1). Absence of these important characters could be either a tion with molecular approaches yet to be undertaken, future derived condition or a reversal within the Dictyopharini. This investigations for the morphological side should combine a new feature may affect the synapomorphies supporting the mono- set of characters. Female internal genitalia (Bourgoin, 1993; phyly of Orthopagini and Dictyopharini in the IW analysis. Soulier-Perkins, 2001; Gnezdilov, 2003; Weirauch, 2008), nymphs, fossil and even outgroup selection to lessen the impact of homoplasy need to be taken properly into consideration. Taxonomic position of Cleotychini Female accessory genitalic glands, in particular (Song & Bourgoin, in preparation), but also nymphal morphological The monotypic Cleotychini were considered the most peculiar characters, especially pattern and structure of the sensory and tribe in Dictyopharinae, the habitus of which is between Orgeri- glandular units (wax-plate areas) on the tergites, may also inae and Caliscelidae types, unlike dictyopharines (Emeljanov, 1997). The tribe does not have any synapomorphic charac- display important new sets of characters (Emeljanov, 1980, ters with Orgeriinae, excluding similar micropterous tegmina 2009; Liang & Song, 2012). (Emeljanov, 1997). Cleotychini were considered related to Our results offer a framework for further explorations into the Nersiini and Taosini based on the presence of the trigones and systematics of the family. We are confident that future systematic the phallobasal lobes with a pair of large and stout spines (Emel- investigation will soon lead to an updated classification (includ- janov, 1997, 2011b). The Cleotychini species, unfortunately, ing identification keys). Well-tested phylogenetic hypotheses was not available for the present analysis. However, according will also allow investigations into the biogeographic history and to the descriptions and comments of Emeljanov (1997), numer- the evolution of multitrophic ecological interactions in this con- ous autapomorphic features fall beyond familial definition of spicuous group of herbivores. Dictyopharidae: (i) the calisceloid habitus; (ii) the very short apical segment of the rostrum; (iii) two lateral spines on the hind tibiae; (iv) two apical teeth of the inner group of the hind Supporting Information tibiae; (v) the patellae replacing apical teeth of hind tarsomeres I and II; (vi) the male abdominal sternite VIII fused with the Additional supporting information may be found online in pygofer; (vii) the endoconnective fused with the ventral wall the Supporting Information section at the end of the article. of the pygofer; and (viii) the gonostyles without upper process, File S1. List of the subfamily, tribes, genera and subgenera fused basally, and not connected with the endoconnective. of Dictyopharidае. Therefore, we prefer to exclude Cleotychini from Dic- tyopharidae, as a taxon of uncertain familial placement within File S2. Materials for the phylogenetic analysis. Fulgoroidea. File S3. Morphological character matrix in nexus format for the phylogenetic analysis. Conclusions File S4. List and comments of morphological characters used in the phylogenetic analysis. This analysis represents the phylogenetic analysis of the Dic- tyopharidae, based on 146 morphological characters of adults Figure S1. Strict consensus tree for Dictyopharidae, result- and provides an initial outline for understanding the evolutionary ing from the equal weighting analysis.

Figure S2. Strict consensus tree for Dictyopharidae, result- Bourgoin, T. (2017) FLOW (Fulgoromorpha Lists On the Web), a world ing from the implied weighting analysis (K = 30). knowledge base dedicated to Fulgoromorpha. Version 8. [WWW document]. URL http://hemiptera–databases.org/flow/ [access ed on Figure S3. Phylogenetic hypothesis for Dictyopharidae, 10 May 2017] resulting from the strict consensus tree under implied weight- Bourgoin, T., Wang, R.-R., Asche, M. et al. (2015) From micropter- ing analysis (K = 7, 10). ism to hyperpterism: recognition strategy and standardized homology-driven terminology of the forewing venation patterns Figure S4. Phylogenetic hypothesis for Dictyopharidae, in planthoppers (Hemiptera: Fulgoromorpha). Zoomorphology, 134, 63–77. resulting from the strict consensus tree under implied weight- Burrows, M. (2014) Jumping mechanisms in dictyopharid planthoppers ing analysis (K = 50–100). (Hemiptera, Dictyopharidae). Journal of Experimental Biology, 217, 402–413. Figure S5. Phylogenetic hypothesis for Dictyopharinae De Souza Amorin, D. (1982) Classificação por seqüenciação: uma excluding Orgeriinae, resulting from the strict consensus tree proposta para a denominação dos ramos retardados. Revista Brasileira under implied weighting analysis (K = 30). de Zoologia, 1,1–9. Emeljanov, A.F. (1969) Reclassification of Palearctic planthoppers of the subfamily Orgeriinae (Homoptera, Dictyopharidae). Entomologi- Acknowledgements cal Review, 48, 189–198. Emeljanov, A.F. (1979) Problema razgranichenhiya semeïstv Fulgoridae We extend our appreciation to the following individuals and i Dictyopharidae (Homoptera, Auchenorrhyncha). Trudy Zoologich- eskogo Instituta Akademii Nauk SSSR, 82, 3–22. institutions for loans of specimens or access to collections: Emeljanov, A.F. (1980) Filogeniya i evolyutsiya podsemseïstva Org- Jürgen Deckert (MFNB), Igor Malenovsky´ (MMBC), Tomasz eriinae (Homoptera, Dictyopharidae). Chteniya pamyati Kholod- Huflejt (MIZPAS), Petr Kment andríˇ Ji Hájek (NMPC), Chris- kovskovo, 32, 3–96. tian Schmidt (SNSD), Stephan Blank (SDEI), Gunvi Lind- Emeljanov, A.F. (1983) Dictyopharidae from the Cretaceous deposits berg (NHRS), Rune Bygebjerg (MZLU), Christine Lambkin on the Taymyr Peninsula (Insecta, Homoptera). Paleontologicheskii and Susan Wright (QM), Federica Turco and Andreas Zwick Zhurnal, 3, 79–85. (ANIC), Keith Arakaki and David Preston (BPBM), Yvonne D. Emeljanov, A.F. (1997) A new genus and species of the Dictyopharidae van Nierop (NCB Naturalis), Andras Orosz, David Redei and from Australia belonging to a new tribe (Homoptera, Cicadina). Tamás Vásárhelyi (HNHM), Norman D. Penny (CAS), Randall Zoosystematica Rossica, 6, 77–82. T. Schuh (AMNH), Richard C. Froeschner and Thomas J. Henry Emeljanov, A.F. (2008) New genera and species of the family Dic- tyopharidae (Homoptera), with notes on the systematics of the sub- (USNM), Robert L. Blinn and Lewis L. Deitz (NCSU), Niels family Dictyopharinae. Entomological Review, 88, 296–328. Peder Kristensen (NHMD), and Masaaki Suwa and Masahiro Emeljanov, A.F. (2009) Evolutionary transformations of abdominal Ohara (HU). We also wish to thank Dr Christiane Weirauch for wax-plates in the larvae of the Fulgoroidea (Homoptera, Cicadina). her very kind editorial help and comments on the article. Four Entomological Review, 89, 1035–1054. anonymous reviewers are greatly appreciated for their efforts in Emeljanov, A.F. (2011a) A new genus and species of lanternflies of improving this paper. the subfamily Cladyphinae (Homoptera, Fulgoridae). Entomological The work on which this paper is based was supported by grants Review, 91, 484–489. from the National Natural Science Foundation of China (no. Emeljanov, A.F. (2011b) Improved tribal delimitation of the subfamily 31572297, to ZSS) and Southeast Asia Biodiversity Research Dictyopharinae and description of new genera and new species Institute, Chinese Academy of Sciences (no. Y4ZK111B01), (Homoptera, Fulgoroidea, Dictyopharidae). Entomological Review, 91, 1122–1145. and partially by grants from the National Natural Science Emeljanov, A.F. (2013) A new species of the genus Pibrocha Kirkaldy Foundation of China (nos 31561163003 and 31572298, to APL). (Homoptera, Fulgoridae) with notes on the systematics of the subfam- Conflict of interest: All authors certify that they have no ily Dichopterinae and with description of a new tribe. Entomological affiliation with or involvement in any organization or entity with Review, 93, 775–780. any financial or nonfinancial interest in the subject matter or Emeljanov, A.F. 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