Inferring a Phylogeny for Hemiptera: Falling Into the 'Autapomorphic Trap'

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Zeitschrift/Journal: Denisia

Jahr/Year: 2002

Band/Volume: 0004

Autor(en)/Author(s): Bourgoin Thierry, Campbell B.C.

Artikel/Article: Inferring a Phylogeny for Hemiptera: Falling into the Â‘Autapomorphic TrapÂ’ 67-82 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

Inferring a Phylogeny for Hemiptera: Falling into the 'Autapomorphic Trap'

TH. BOURGOIN & B.C. CAMPBELL

Abstract groups are clearly established, we suggest inferred intermediate taxonomic units not LlNNE first established Hemiptera and be named. We particularly recommend dis- its main subdivisions as natural groups continuing Auchenorrhyncha and almost 250 years ago. However, he inclu- Homoptera as formal taxonomic terms. ded thrips among his Hemiptera, rende- Resume: L'histoire de la classification ring it paraphyletic at its inception. Aro- des Hemiptera et de la reconnaissance de und 50 years later, DUMERIL and LATREIL- leur principales sous-divisions comme LE established the contrasting taxonomic groupes naturels debute des LlNNE qui, les groups of Auchenorrhyncha versus Stern- regroupant avec les Thrips, en fait un taxon orrhyncha and Heteroptera versus paraphyletique. Quelques 50 ans plus Homoptera based on character-presence tard, Dumeril oppose Auchenorrhyncha et versus character-absence criteria. As Sternorrhyncha, et LATREILLE Homoptera many others, these authors fell into the et Heteroptera. Comme tant d'autres, ces autapomorphic trap'. Indeed, Heteroptera auteurs tomberent dans 'le piege de l'auta- and Sternorrhyncha were defined based on pomorphie'. En effet, si les Heteroptera et obvious autapomorphies. The contrasting Sternorrhyncha etaient definis par des taxa to Heteroptera and Sternorrhyncha autapomorphies evidentes, les taxons qui were grouped based on an absence of leur etaient opposes et qui regroupaient le modification in morphological characters reste des Hemipteres ou des Homopteres, used to establish an opposing group (viz., n'etaient definis que sur des caracteres unmodified tegmina and non-displaced negatifs (non modification des tegmina ou labium). Hence, these 'unmodified' cha- labium non repousse sous le prothorax). racters were, by definition, plesiomor- Par leur definition meme ces carateres phies. In view of how these taxa were defi- sont des plesiomorphies. II est ainsi peu ned, it is not surprising that recognition of surprenant de voir accepter ou rejeter au Auchenorrhyncha and Homoptera as cours du temps la monophylie des Auche- monophyletic groups has been conti- norrhyncha et des Homoptera, dont l'his- nuously debated. We review, here, the toire est ainsi passee en revue. On propo- history of these debates. In conclusion, we se pour terminer une synthese sur la phy- present a synthesis of the phylogeny of logenie des Hemiptera teile qu'elle est Hemiptera according to the latest molecu- actuellement comprise ä la lumiere des lar results and incorporate fossil interpre- derniers resultats moleculaires, et un tations into the evolutionary framework. scenario sur l'histoire evolutive du groupe While some of the very basal affiliations incluant les donnees fossiles. Nous sug- remain indistinct, Sternorrhyncha, Fulgo- gerons de retenir cinq sous-ordres claire- romorpha, Cicadomorpha, Coleorhyncha ment monophyletiques au sein de l'ordre and Heteroptera, are clearly monophyle- des Hemiptera: Sternorrhyncha, Fulgoro- tic. We suggest the names of these five morpha, Cicadomorpha, Coleorhyncha et major groups be formally established as Heteroptera. Nous recommandons de ne suborders for Hemiptera because of histo- plus utiliser ni nommer toute unite taxo- rical precedence and wide recognition. nomique intermediaire, en particulier les Denisia 04, Until basal affiliations between these five zugleich Kataloge des OÖ. Landesmuseums, noms Auchenorrhyncha et Homoptera. Neue Folge Nr. 176 (2002). 67-82

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A prologue phylogeny of the Hemiptera? More specifical- ly, should we continue to use the terms Almost 200 years have passed since Homoptera and Auchenorrhyncha on a for- DUMERIL (1806) and LATREILLE (1810) intro- mal taxonomic basis? duced, respectively, the terms Auchenorrhyn- cha and Homoptera as taxonomic groups wit- Non-monophyly and hin Hemiptera. In 1995, two papers were Hemiptera: an historical legacy puhlished suggesting both these widely recognized taxonomic groups are paraphyletic Since its origin, the task of recognizing and delineating major groups within Hemip- tera has spurred debate. At the outset, when LlNNE (1758: 343) first described Hemiptera he included the eight genera of Cicada, Notonecta, Nepa, Cimex, Aphis, Chermes, Coc- cus and Thrips. From an evolutionary perspec- tive, inclusion of Thrips by LlNNE, currently representing the order Thysanoptera, rende- red Hemiptera paraphyletic at its creation. Indeed, Thysanoptera has more recently been placed in a trifurcated phylogenetic affiliation with the Psocodea (KRISTENSEN 1991, 1995) or even as the sister group to the Psocoptera + Phthiraptera (WHEELER et al. 2001). The fact that thrips were once included in Hemiptera is of historical anecdotal interest, but illustrates non-monophyly beset Hemiptera, or taxonomic groups within it, from the outset. It should he emphasized, however, that current-day Hemiptera is considered a strongly supported monophyletic group.

Homoptera and Auchenorrhyncha: origins

At the beginning of the 19 century, Hemiptera, also known as Ryngota (FABRICIUS 1775: 673 or 'Rhyngota', FABRICIUS 1803: 1) and later modified to Rhynchota by BuR- MEISTER (1835), was divided into a number of

Fig. 1. different main groups. LATREILLE (1802 III: Carl STÄL (1833-1878), Swedish (SORENSEN et al. 1995; CAMPBELL et al. 1995) 256) recognized five divisions including the Hemipterist, is regarded by MUIR as with another study casting doubt on mono- Cicadariae, a group identical to the modern- the 'father of the Hemipterology' phyly of 'Homoptera' alone (VON DOHLEN & day concept of Auchenorrhyncha (see MORAN 1995). The studies questioning the BOULARD 1988). Similarly, a few years later monophyly of these groups used parsimony- DUMERIL (1806: 206) introduced two new- based phylogenetic analyses of nucleotides groups within the Hemiptera: the Aucheno- sequences of 18S rDNA. Seven years have rinques (= Auchenorhtnques, DUMERIL 1816: now passed since publication of these molecu- 303, = Auchenorhynchi AMYOT & SERVILLE lar papers. Yet, despite widely held agreement 1843: 456, = Auchenorrhyncha auctorum) that Auchenorrhyncha and, especially, and the Sternorinques (= Sternorhynchi, Homoptera are not monophyletic, both taxo- AMYOT & SERVILLE 1843: 588, = Stemorrhyn- nomic terms are still commonly used. So, whe- cha auctorum). LATREILLE (1810) later divided re are we now concerning classification and Hemiptera into two main groups, the Heter-

68 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at optera (: 250) and the Homoptera (: 252). Despite numerous morphological studies Thus, the two recognized major divisions of following establishment ot Homoptera and Hemiptera, Homoptera and Auchenorrhyn- Auchenorrhyncha, there are yet to be any cha came to be. It was not until nearly convincing reports of synapomorphies to sup- 80 years later that another somewhat enigma- port their monophyly. Moreover, the absence tic lineage within Hemiptera, the Coleorhyn- of clearly defined synapomorphies has genera- cha (Peloridiidae), was recognized and placed ted numerous conflicting opinions and deba- as a third major division within Homoptera by tes for almost two centuries, prior to and follo- MYERS & CHINA (1929). wing the introduction of cladistics. The 'Autapomorphic Trap'

In early efforts to establish major groups of Hemiptera authors fell into a now familiar and what has been discovered to be a common trap in the field of systematics. Indeed, a common practice in the past was to use two character states, presence of a particular morphological feature versus its absence, as a means to recognize contrasting groups. In many instances, such a 'character-present state' would now be referred to as an obvious auta- pomorphy. If so, the second state of these characters would simply be a plesiomorphy. In naming both groups as valid taxa, authors fell into - what we call here - the 'autapomorphic trap'. This trap is the temptation to give formal taxonomic status to a symplesiomorphic based group as a counteraction to recognizing a valid group based on a synautapomorphy. It has become apparent that use in the past of such 'character-state absent' or 'non- Taxonomic status of Homop- Fig. 2. character' criteria to define a taxon has gene- tera and Auchenorrhyncha: Frederic MUIR (1872-1931) in the year rated many paraphyletic groups in taxonomy. conflicting views 1925 on top of Mount Ka'ala, the The hemipteran taxonomic pairs of Homop- highest mountain of the Waianae- ridge in Oahu/Hawaii. MUIR is with his tera/ Heteroptera and Auchenorrhyncha/ An exhaustive review of the numerous net, sitting. On his left is a man Sternorrhyncha are vivid examples. The apo- phylogenetic schemes proposed for Hemiptera named Taylor, on his right. Otto morphic character rendering the Heteroptera Swezey (1869-1959), another famous is beyond the scope of this chapter. However, Hawaiian Entomologist, then F.X. Wil- was presence of 'hemelytra' ', a transformati- there are certain schemes by prominent liams, a hymenopterist. on of the mesothoracic wings not exhibited by Hemipterists worth noting as pivotal historic Homoptera. The character state used to diffe- events in the classification of Hemiptera, rentiate Sternorrhyncha from Auchenorrhyn- especially with their conceptual focus on cha was the displacement of the labium Homoptera and Auchenorrhyncha. towards the thorax, absent in Auchenorrhyn- cha. The use of present versus absent charac- According to MuiR (1923), STÄL (fig.l) ter states uses plesiomorphies to define both should be considered the 'father of Hemipte- Homoptera and Auchenorrhyncha: the non- rology'. The main reason for this declaration transformation of the mesothoracic wing and stems from work published in STÄL'S fourth the non-displacement of the labial insertion, volume of his Hemiptera Africana (1866). It is respectively. in this work where STAL first proposes a classification for Homoptera, dividing it into three ' In fact this character is a synapomorphy for the Panhe- families, Stridulantia, Jassida and Fulgorida. In teroptera only, while presence of metathoracic scent actuality, however, MUIR (fig. 2) probably- glands represents a reliable synapomoprhy (among others) for the whole of Heteroptera (WHEELER et al. 1993). contributed most to the classification of

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Hemiptera. MuiR maintained the classical, Also, in MuiR's scheme, Cicadoidea were basal Heteroptera-Homoptera and Auchenor- separated from Fulgoroidea. The Fulgoroidea, hynchi-Sternorhynchi divisions (Fig. 3), and in turn, were placed basally, sister to all other argued against separation of Stemorrhyncha Homoptera. This separation was based on a (= Phytophtyriae, BURMEISTER 1835, = Gula- 'peculiar arrangement of the intestine' and rostria, MACGILLIVRAY 1921) from the rest of MuiR divided the Homopera into two groups Hemiptera (MuiR 1923), as proposed by STAL. he called the 'Columata' and the 'Acolumata'. Fig. 3. In MuiR's scheme the Sternorrhyncha were But he has been the first to present an expan- Evolutionary scheme of Hemiptera placed among the Columata distally, as sister according to Mum 1923 ded evolutionary based outline of the group. to a group comprised of Cicadidae, Cercopi- dae and Membracidae. As did his predeces- Auchenorhynhi sors, MuiR fell into the 'autapomorphic trap1 Acolumab Cicadoidea where he proposed contrasting groups, Colu- mata and Acolumata, with one group, the

4> Acolumata, retaining a plesiomorphic charac- 2 1 € ter state in the intestines. This trap also led I 8 him to conjecture a sister relationship bet- ä ween Sternorrhyncha and a Cicadomorpha that lacked the Cicadellidae. The next notable effort of inferring a phylogenetic scenario for Hemiptera was performed by HESLOP-HARRISON (1956). In his Stemorhynchi scenario he used a metaphorical concept of a Columata 'tree' to present his phylogeny (Fig. 4) and took into account known fossil groups. Alt- Hoittopteia Hemiptera | hough he did not include Cercopidae in his tree, HESLOP-HARRISON stated that 'clear lines of affinity lie between the Cicadomorpha and ALSUROOIDOMORPHA the Jassidomorpha via the Cercopoidae'. This APHIOIOOMORPHA glf ADtOOMORPHA view on the cercopid-jassidomorphic link was JASSIOOMOHPHA a slight modification of SPOONER's proposition i FULGORIOOMORPHA

EXTINCT Of* (1938) that all Homoptera were derived from UNRECOGNISED CONNLCriNC ancestral cercopids. HESLOP-HARRISON'S sche- otviiinOMORPMA me was very similar to that of MuiR (1923), COCCIOOMORPM* but included Coleorhyncha placed in a trichotomy with Homoptera and Heteroptera.

EXTINCT OR UNRECOGNISED While CHINA (1962) transferred CONNECTING LINKS BETWEEN THE MODERN Coleorhyncha into the Auchenorrhyncha, HOMOPTEP.A PALAEOBRMYNCHA AND THE EVANS (1963) was the first to make any major HETEP.OPTERA PERMIAN HOMOPTEROVS changes in the classification of Hemiptera MAIN - TRUNK from that proposed by MuiR. EVANS recognized the Auchenorrhyncha as a monophyletic FIG.4- group deserving taxonomic status. However, THE he surmised its phylogenetic position was ARBONIFERCUS AND HEMIPTEROID RE-CARBONIFEROUS unclear and placed it in a trichotomy with OOTO-HEMIPTEROID PHYLOGENETIC NCESTRAL PLCXUS Coleorhyncha and Sternorrhyncha within the TREE Homoptera. The monophyletically based clas- Fig. 4. sification scheme of EVANS, an Auchenorr- Evolutionary scheme of hyncha and a Sternorrhyncha housed within Hemiptera as Homoptera sister to Heteroptera, was widely proposed by DCV'ONIAN/AND SILURI/ . PSOCOCO-OBTHOPTEROIO-MEMIPTEOOIO acknowledged, even recently (BLOCKER 1996). HESLOP- HARRISON / ANCESTRAL PLEXUS \ 1956 Perhaps the best synthesis of taxonomic

70 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at groups for Hemiptera based on EVANS' scena- were not directly affiliated with other stern- rio was that of BOULARD (1988) (fig. 5). orrhynchans but were sister to Fulgoroidea, Within the suborder Homoptera, sister to both groups belonging to the Fulgoromorpha Heteroptera, BOULARD recognized 10 superfa- (fig- 6). milies distributed among Coleorhyncha (Pelo- In 1981, HENNIG proposed a phylogenetic ridoidea), sister to Sternorrhyncha (Psyl- scenario for Hemiptera similar to that of loidea, Aleyrodoidea, Aphidoidea, Coc- EVANS, with monophyltic Heteroptera and coidea) and Auchenorhyncha (Fulgoroidea, Fig. 5. Homoptera in a basal hemipteran dichotomy. Evolutionary scheme of Hemiptera Cercopoidea, Cicadoidea, Cicadelloidea, However, he questioned the monophyly of according to BOULARD 1988 Membracoidea).

2. The Hennigian period: a search for synapomorphies •8 a o 8 o S _i Shortly after EVANS presented his classifi- s cation scheme for Homoptera, based on his morphological interpretations, a number of other morphologically based studies came to Psyltomorpha Aphidornorpha different conclusions. These other studies suggested Auchenorrhyncha and Homoptera Fulgoromorpha Cicadomorpha were not monophyletic. Based on morphologi- Phytophtiriae Cicadariae = Stemorhyncha cal and histological studies of the hemipteran = Auchenorhyncha digestive tract, GOODCHILD (1966) recognized Homoptera three main lineages within Hemiptera (Heter- Hemiptera = Hemipteroidea optera + Fulgoromorpha), (Cicadomorpha + = Rhynchota Sternorrhyncha), and Coleorhyncha. This scheme, portraying both Homoptera and Auchenorrhyncha as paraphyletic, was also inferred later by COBBEN (1978), based on his study of hemipteran mouthparts.

•§ •8 HAMILTON (1981), based on head capsule 2. characters, also concluded Auchenorrhyncha S. was paraphyletic. However, his inferred asso- ciations within Hemiptera, (Fulgoromorpha + (Sternorrhyncha + Cicadomorpha)), were somewhat different than those proposed by GOODCHILD (1966) and COBBEN (1978). HAMILTON provided several synapomorphic characters to support each branch of his phylogenetic scenario. His conclusions were later suppported by Ross et al. 1982. HAMILTON Psyllamorpha Cicadamarpha (1996), based on cladistic analysis of venation in fossilized wings, derived nearly the same phylogenetic scheme as in his earlier studies. However, based on his study of what was per- ceived to be a fossil whitefly, Megakurodes megocellatcfl, he concluded the Aleyrodoidea Auchenorrhyncha based on conclusions simi- Fig. 6. lar to those of HAMILTON (1981), discussed Phylogeny of the Homoptera accor- 2 HAMILTON'S views were recently discussed by SHCHER- ding to HAMILTON 1996. t denotes a BAKOV (2000) who excluded Megaleurodes megocellata above. Both studies inferred a paraphyletic fossil group. HAMILTON 1990, from Aleyrodoidea. According to Auchenorrhyncha with Cicadomorpha being SHCHERBAKOV, this taxon has nothing in common with boreoscytids (a group of fossil sternorrhynchans) but is more closely affiliated with Sternorrhyncha probably a poorly preserved planthopper. than with Fulgoromorpha.

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There were yet other scenarios based on amino acid sequences) could provide a large cladistic studies that countered that of EVANS. number of homologous characters for cladistic SCHUH (1979) was probably the first since analysis of morphologically disparate groups. STÄL (1866) to suggest Stemorrhyncha was The belief was molecular characters would be the sister group to all other Hemiptera, thus less vulnerable to human subjective interpre- rendering Homoptera paraphyletic. POPOV tations than morphological characters, either (1981), based on palaeontological results, of extant species or fossils. Use of molecular EMELJANOV (1987) and ZRZAVY (1990, 1992a, techniques began to yield a number of revolu- b), based on different interpretations of mor- tionary findings in evolutionary biology star- phological characters, came to the same infe- ting in the mid-1980s. The molecule that was rence as SCHUH (1979). In all these studies the main source of information in early ende- the authors recognized a Euhemiptera clade avors was the gene encoding 18S ribosomal [Auchenorrhyncha + (Coleorhyncha + Heter- RNA (18S rDNA). This gene had a number optera)] sister to Stemorrhyncha, thus presen- of attributes making it a favorable source of ting profoundly new phylogenetic affiliations information for phylogenetic work. It was for major lineages of Hemiptera than those relatively conserved, fundamental to the presented by EVANS. Within the Cicadina molecular biological processing of all orga- (= Auchenorrhyncha), EMELJANOV (1987) nisms since the origin of life and, because of recognized two main branches, (Cercopoidea high copy number, was relatively easy to sequence. WHEELER et al. (1993) were the first + Cicadoidea) and (Cicadelloidea + Fulgoro- to employ 18S rDNA to infer a phylogeny for idea). However, all these studies clearly indi- Hemiptera, with chief emphasis on Heterop- cated Homoptera was paraphyletic. tera. Their results strongly supported the exi- Finally BOURGOIN, using morphological stence of a monophyletic Heteropterodea interpretations of the head capsule (tentorium group (Coleorhyncha + Heteroptera), but and laminae) (1986a,1986b) and male (1988, hinted at a non-monophyletic Homoptera. BOURCOIN & HUANG 1990) and female geni- The potential for paraphyly of Auchenorrhyn- talia (1993), concluded that neither Homop- cha was not tested in that a fulgoromorphan tera nor Auchenorrhyncha were monophyle- was not included in their analysis. tic. He further surmised that Fulgoromorpha should be more closely affiliated to Heterop- One year later, CAMPBELL et al. (1994) tera than to Cicadomorpha, similar to the published a phylogenetic analysis of 18S view of GOODCHILD (1966). To rectify taxono- rDNA nucleotide sequences of various stern- mic confusion resulting from inferences for so orrhynchan taxa, focusing on the Aleyro- many different hemipteran phytogenies, doidea. In this analysis, single exemplary taxa MlNET & BOURGOIN (1986) suggested an inte- of a fulgoromorphan and a cicadomorphan rim system of classification. They proposed were used. Although the paper's intent was that only five main groups within Hemiptera not to address paraphyly and included few should be recognized taxonomically, Stemorr- taxa, the results hinted at a paraphyletic Homoptera again showing Stemorrhyncha as hyncha, Fulgoromorpha, Cicadomorpha, the sister taxon of all other Hemiptera (Euhe- Coleorhyncha and Heteroptera. Furthermore, miptera). Among Stemorrhyncha, the authors they suggested suspending use of Homoptera inferred that the traditional sister relationship and Auchenorrhyncha until future results, if between Psylliforma-Aphidiforma of SCHLEE any, could support monophyly of these groups. (1969) needed to be reconsidered. Indeed, the Psylliforma appeared to be paraphyletic and a Molecules and fossils: new stemorhynchan phylogenetic sequence the new message was proposed: (Psylloidea + (Aleyrodoidea + (Aphidoidea + Coccoidea))). Recent efforts employing molecular phylogenetic analyses have rekindled interest in The following year, 1995, will probably be higher group relationships within Hemiptera. remembered as a key year in fueling the que- This interest was stimulated by the potential stion of monophyly of Homoptera and Auche- promise that molecules (mainly nucleotide or norrhyncha and reassessing their taxonomic

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Status within Hemiptera. The titles of several (= Heteropteroidea sensu SCHUH 1979). papers published that year included the sub- Coleorhyncha, sister to Heteroptera, was ject of paraphyly of Homoptera and/ or given rank of infraorder along with the seven Auchenorrhyncha (SORENSEN et al. 1995; other main clades of Heteroptera. VON DOHLEN & MORAN 1995; CAMPBELL et al. Though SORENSEN et al.'s phylogeny 1995). All these papers employed molecular (1995) did not completely agree with paleon- phylogenetic analyses using nucleotide tological interpretations, they argued the sequences of 18S rDNA. As with WHEELER et nucleotide-based topology was "superior to al. (1993), these papers used only varying very nebulous indications of origin ... revealed amounts of partial sequences of the molecule. VON DOHLEN & MORAN analyzed portions 2 corresponding to helices 1-19 (approximately 2 CL O the first 600 nucleotides out of approximately 2 2000). CAMPBELL et al. and SORENSEN et al. CL analyzed helices 20-48 (about the middle 1200 e nucleotides) of the 50 helices generally reco- Ö gnized in the secondary structure of its synonymous RNA. All papers found Sternorrhyn- cha sister to Euhemiptera, indicating a paraphyletic Homoptera. VON DOHLEN & MORAN indicated some of their shortest trees hinted at a paraphyletic Auchenorrhyncha. The other Panheteroptera two papers signaled a stronger indication of Neoheteroptera paraphyly of Homoptera and Auchenorrhyn- Euheteroptera cha. Both showed that Fulgoromorpha came Heteroptera as the sister group to Coleorhyncha + Heter- Prosorrhyncha optera (Heteropterodea). However, the Fulgo- Neohemiptera romorpha + Heteropterodea node was only Euhemiptera supported by one molecular synapomorphy. SORENSEN et al. dubbed this clade 'Neohemip- Hemiptexa tera'. SORENSEN et al. (1995) argued that not by fossils". Indeed, although the fossil eviden- Fig. 7. ce did not support a classical auchenorrhyn- Evolution of Hemiptera according to only did molecular evidence not support SORENSEN et al. 1995. monophyly for Homoptera and Auchenorr- chan clade, they did not appear to support the Underlined taxa were given rank of hyncha, but that recent morphological and newly proposed neohemipteran clade, either. suborder within order Hemiptera, The fossil interpretations at the time mostly other names are infraorders. Clypeorr- paleontological evidence did not support their hyncha = extant Cicadomorpha; monophyly, either. In view of a non-mono- supported the phylogenetic sequence: (Fulgo- Archaeorrhyncha = Fulgoromorpha phyletic Auchenorrhyncha and different uses romorpha + (Cicadomorpha + Heteroptero- of taxonomic terms of major hemipteran dea)) (SHCHERBAKOV 1984, 1988). However, groups by systematists in different regions of one year after SORENSEN et al.'s results, the world, SORENSEN et al. proposed new taxo- SHCHERBAKOV (1996) and POPOV & SHCHER- nomic names for 'suborders' of Hemiptera. BAKOV (1996) reiterated their previously They also recommended discontinuing use of published interpretations stating Heteroptero- Auchenorrhyncha. The suborder names pro- dea descended from an ingruid ancestral group posed were coordinated to use a standardized which itself emerged from the Prosbolopsei- '-rrhyncha' suffix to distinguish them from dae' as well as the Prosbolidae', an ancestral other clade names and informal names having group for the Cicadomorpha. Hence, based on the '-morpha' suffix within the Hemiptera their paleontological appraisals, the suborders (Fig. 7). The four suborders named were Coleorhyncha and Heteroptera are more clo- Sternorrhyncha (no change), Clypeorrhyncha sely related to Cicadomorpha than to Fulgoro- (= extant Cicadomorpha), Archaeorrhyncha morpha, and thus could be considered as des- (= Fulgoromorpha) and Prosorrhyncha cendants of an auchenorrhynchan (in a wider

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sense) ancestor, the sister group to Sternorr- goromorpha + (Cicadomorpha + Heteroptero- hyncha. SHCHERBAKOV (2000) intoned, "mor- idea)). Finally, unpublished recent molecular phological and fossil evidence should not be results (BOURGOIN et al. 1999, 2001) inclu- discredited simply in favor of novel molecular ding more taxa, secondary structure recon- techniques!" structions and complete 18S rDNA sequences, One year after presentation of the paleon- still show a closer relationship of Heteroptero- tological arguments, BOURGOIN et al. (1997) dea to Cicadomorpha than to Fulgoromorpha. confirmed monophyly of the Fulgoromorpha, with inclusion of the phylogenetically enigma- Hemiptera classification tic Tettigometridae, contrary to the views of and phytogeny, a tentative YANG & FANG (1993). BOURGOIN et al's ana- synthesis lysis continued from that of CAMPBELL et al. (1995) by adding further molecular data from Figure 8 presents a proposed evolutionary framework for Hemiptera based on recent newly sequenced taxa. In this study, most par- molecular analysis of full 18S rRNA sequences simonious trees supported a Neohemiptera cla- aligned using inferred secondary structures de (as opposed to Auchenorrhyncha), but did (red branches). The framework is based on not support a monophyletic Cicadomorpha past analyses (SORENSEN et al. 1995; CAMPBELL probably because of taxa sampling bias (the et al. 1995) with recent modifications (OUVR- study focused on the Fulgoromorpha). Howe- ARD et al. 2000; BOURGOIN et al. 1999, 2001). ver, analyses excluding the psyllid (the only It also includes tentative placement of reco- sternorrhynchan taxon included) resulted in a gnized major hemipteran fossil taxa. The monophyletic Cicadomorpha but then Neohe- paleontological interpretations chiefly follow miptera and Auchenorrhyncha were equally those of SHCHERBAKOV expressed in his 1984 supported. paper, and which has been updated regularly OUVRARD et al. (2000) reached similar (1988, 1990, 1992, 1996), completed by KLI- ambiguous results. In this study, a more rigo- MASZEWSKI (1995), KLIMASZEWSKI & WOJCIE- rous effort was made to assure alignment of CHOWSKI (1992) and POPOV & SHCHERBAKOV homologous nucleotides in the data matrix. (1996). A conservative view (basal polytomy) This was performed by creating a secondary has been maintained for Fulgoroidea based on structural model of the synonymous 18S BOURGOIN et al. (1997), LEFEBVRE (1997) and rRNA wherein alignment could be based on HOLZINGER et al. (2001); this clade will be position of bases in various substructures of the treated in more detail elsewhere. For Membra- molecule. Also, in this study they used full coidea we have followed the framework propo- nucleotide sequences of 18S rRNA and added sed by DIETRICH & DEITZ (1993). Some yet new coleorhynchan taxa to the previous data unpublished data provided by P. Stys and of CAMPBELL et al. 1995. Analysis using all J. Szwedo (pers. com.) are also incorporated nucleotides (a 'full data set') recognized mono- into the inference of this phylogeny. phyly of the four major hemipteran lineages. Using this framework, we recognize five However, support for Neohemiptera and affi- suborders within Hemiptera (bold text). They liations between Fulgoromorpha, Prosorrhyn- are Sternorrhyncha, Fulgoromorpha, Cicado- cha and Clypeorrhyncha remained unclear morpha, Coleorhyncha and Heteroptera. For and Auchenorrhyncha was still not supported. major lineages within Sternorrhyncha it follows To improve the phylogenetic signal (viz., redu- molecular results of CAMPBELL et al., (1994) ce homoplasious noise) they attempted an- which concur with earlier cladistic analysis other analysis of the data after removing many of morphological characters (SCHLEE 1969) of the homoplasious sites from the data set and paleontological interpretations of through outgroup polarization. Again, a SHCHERBAKOV (2000). The paleontological monophyletic Auchenorrhyncha clade was and morphological interpretations separate not supported in any of the most parsimonious the Sternorrhyncha into two main groups, trees but also Neohemiptera was not supported Aphidinea (Aphidoidea, Coccoidea and rela- any more favorably than the phytogenetic ted fossils groups) and Psyllinea (Psylloidea, sequence suggested by the fossil studies: (Ful- Aleyrodoidea and related fossil taxa).

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Hypoperhda f

Archescytinoideat Protopsylloideat Sternorrhyncha P3yl loidea ' Aleyrodoidea • Boreoscytidaet Pincombeidaet 1 Aphidoidea Henuptcn Coccoidea Coleoscytidaet Fulgoramorpha Surijokocixi idaet Del phac idae Fulgoridi idaet • Cixiidae si Meenoplidae - Kinnaridae La lacidaet Achilidae Achilixndae Derbidae Dictyopharidae Fulgoridae • Other Fulgoroidea Curvicubitidaet Euhemiptera Ignolatidaet Cicadomorpha J Pe re bori idaet Prosbolopseidaet Palaeontinidaet Mesogereon idaet Dunstani idaet Dysmorphoptilidaet Pros bo I idaet Myerslopi idaet Cicadoidea Procercopoideat Cercopoidea Chiliocyclidaet Hylicellidae Karajassidaet Cicadellidae Membracoidea I Mel izoder idae Mem brae idae Ingruidaet Cicadocorinaet Progonocimicinaet Hoploridiinaet Karabasiinaet Heteropterodea Peloridiidae Scytinopteridaet Ipsviciidaet Stenovici idaet Serpentiven idaet Paraknighti idaet Enicocephalomorpha Dipsocoromorpha Gerromorpha Euheteropte Nepornorpha Neoheteroptera| Leptopodomorpha Panheteroptera | Cimicomorpha Pentatomomorpha

Fig. 8. Proposed evolutionary framework for Hemiptera based on a composite of current inferences including fossil, molecular, and morphological interpretations. Based on this framework the order Hemiptera is divided into five suborders (in bold). Red branches of the tree indicate extant terminal taxa and follow most recent molecular results, grey boxes represent paraphyletic taxa (grades). Several monophyletic groups (clades) are named according to the text indication. Fossil groups are denoted by t. Taxa which monophyly is in doubt are presented in doted lines or in italics.

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With regard to our framework, within the gy of fossil characters rendering nodes for a Fulgoromorpha, there are three major ance- cladogram remains untested. Translation of stral lineages placed as a trichotomy, paleontological interpretations into clado- Coleoscytoidea (Coleoscytidae*), Surijokoci- grams is an uncertain process because most xioidea (Surijokocixiidae') and Fulgoroidea. basal fossil groups are considered grades (steps According to LEFEBVRE (1997) based on a cla- in evolution) and not as clades, per se. Most of distic analysis of wing characters, Surijokoci- these fossil groups are instead considered as xiidae* should be more closely affiliated to ancestral taxa to more recent ones, than as Coleoscytidae' than to Fulgoroidea. Until terminal taxa. For example, the Prosbolopsei- there is a clearer consensus of paleontological dae' is described as a fossil group from which information, we have removed Surijokocixi- arose the three Prosboloidea groups idae' from the Fulgoroidea, as proposed by (Pereboroidea, Prosboloidea, Palaeonti- SHCHERBAKOV (1996), and placed it as a third noidea) and the Prosbolidae , within Cicado- major lineage within Fulgoromorpha. Also, morpha. However, it is also described to have two fossil taxa, Fulgorodiidae' and Lalaci- theoretically given rise to Ingruidae*, a linea- dae', have been proposed as subfamilies wit- ge within the Heteropterodea (SHCHERBAKOV hin Cixiidae (SHCHERBAKOV 1996). The evi- 1996). dence for this placement is not clear and Heteropteroidea was the clade name first monophyly of Cixiidae, itself, is questionable proposed by SCHLEE (1969) to include the (HOLZINGER et al. 2001). We, therefore, adop- Coleorhyncha and Heteroptera, each indivi- ted a conventional view in placing these two dually considered here as hemipteran subor- extinct taxa as individually valid families. Fol- ders. To eliminate confusion for interpretating lowing cladistic analysis of LEFEBVRE (1997), Heteropteroidea as a superfamily, ZRZAVY Fulgoridiidae' are considered as sister to the (1992a) changed the -oidea suffix and rena- Cixiidae (sensu lato), and Lalacidae' is consi- med it to Heteropterodea, as adopted in the dered a monophyletic group sister to the present study. SCHLEE's morphologically based Achilidae-Derbidae clade. A yet more basal inference has since been supported by both lineage within Fulgoromorpha, represented by paleontological interpretations (POPOV & a yet to be described fossil family from the ear- SHCHERBAKOV 1996) and molecular phyloge- ly Permian, has been suggested by SHCHER- netic analyses (WHEELER et al. 1993, OUVR- BAKOV (1996). ARD et al. 2000). As discussed for basal fossil Unlike Fulgoromorpha, the Cicadomor- groups of Cicadomorpha, the fossil group Scy- pha appear to have diversified considerably in tinopteroidea (Fig. 8, grey box) should be con- the late Permian. SHCHERBAKOV (1996) reco- sidered a grade rather than manifesting a cla- gnizes three major ancestral groups of Cicado- de within the Heteropterodea. According to morpha. The first are the Prosboloidea, a para- Stys (pers. com.) infra-order Dipsocoromor- phyletic group (Fig. 8, grey box) that serves as pha within Heteroptera probably represents a an ancestor of a number of other fossil linea- paraphyletic taxon. ges within Cicadomorpha. Two other groups recognized by SHCHERBAKOV are the early Per- In conclusion mian Pereboroidea and the interesting Meso- zoic cicadas, grouped into Palaeontinoidea. Efforts on the part by those performing Within Prosboloidea, Prosbolidae' is consi- molecular and paleontological analyses reveal dered the sister group to Clypeata, which there are still ambiguities in inferring affilia- includes the extant Cicadomorpha. Diversifi- tions among certain hemipteran lineages. On cation of the extant cicadomorphan lineages one hand, room for debate remains on several appears to have begun during the Jurassic. important questions, as follows: 1) Does The phylogenetic framework proposed Sternorrhyncha have a diphyletic (or even here for Cicadomorpha must be considered paraphyletic) origin, favored by palaeontolo- provisional, especially among the basal linea- gical studies but never observed in any of the ges. A cladistic analysis of cicadomorphan fos- molecular studies? 2) Should tettigometrids be sils has not been performed. As such, homolo- considered recent taxa? If so, basal affiliations

76 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at of fulgoromorphan families are still unclear. 3) in Hemiptera almost indisputably monophyle- Is there a Neohemiptera clade or is (Fulgoro- tic (the placement of certain fossil taxa aside). morpha + (Cicadomorpha + Heteroptero- Although our current phylogenetic framework idea)) the valid clade? differs somewhat from that of SORENSEN et al. Alternatively, some important points (1995) with regard to the existence of Neohe- seem to have been gained. 1) A consensus has miptera, the four to five main lineages are the been reached by both molecular and fossil stu- same. In view of the non-monophyly of dies. There is not much support for a mono- Homoptera and Auchenorrhyncha, SORENSEN phyletic Homoptera or Auchenorrhyncha. et al. proposed new suborder names, Sternorr- 2) The molecular work has shown the impor- hyncha, Clypeorrhyncha, Archaeorrhyncha, and Prosorrhyncha, having a coordinated suf- tance of nucleotide alignments and the results fix for four of the main lineages of Hemiptera. of an analysis can swing one way or the other The Clypeorrhyncha was to include only depending on mechanisms used to make align- extant groups of Cicadomorpha. ments. It is concluded that alignments based on secondary structure are now fundamental While we acknowledge the worthy intent to a rigorous analysis of nucleotide data using of renaming hemipteran suborders by SOREN- rRNA of hemipterans. SEN et al., do we really need these new names? As stated in SORENSEN et al. (1995), the One fundamental problem that can creep into main lineages of Hemiptera seem to have biological nomenclature is changing names as radiated quite rapidly, leaving few unambi- taxonomic studies advance. At lower taxono- guous synapomorphies to be discovered in mic levels such problems are generally mitiga- morphological, molecular or paleontological ted and the number of potentially confusing quests. Perhaps Neohemiptera as opposed to synonymies reduced by rules of accepted inter- (Fulgoromorpha + (Cicadomorpha + Heter- national codes. However, at the suborder level opteroidea)) will be the next area of debate of classification there are no actual rules, among the 'pre-Heteropterodea-Euhemiptera' except the acceptance of their use. So, should workers (auchenorrhynchologists)? Another we adopt Archaeorrhyncha, or Prosorrhyncha, course to follow should be to examine other etc? Moreover, is it necessary to create a new molecules that might provide additional infor- clade name at each bifurcation of the hemip- mation in answering the question of relation- teran tree? Instead of creating new names, we ships between major hemipteran groups. propose that the already designated nomen- Moreover, new groups of morphological cha- clature for monophyletic groups in Hemiptera racters still need to be tested. One example is be retained. Some of these names have been the recent study of YOSHIZAWA & SAIGUSA in use for over a decade and are readily asso- (2001). These authors inferred that Auche- ciated with recognized groups, though these norrhyncha was monophyletic based on a names were never formally introduced as sub- newly discovered morphological character. order names. They point to an apparent autapomorphic Despite the logic behind SORENSEN et al.'s reduction of the proximal median plate in the nomenclature proposed in 1995, it has been wing articulation of 'auchenorrhynchans' not variously accepted. Of the four new suborder found in other hemipterans. However, they names they proposed three are synonyms of acknowledge that such a character reduction already previously published names and one, may not have much weight. Neohemiptera, is a name for a clade whose monophyly is still under debate. Prosorrhyn- About naming higher rank cha is a strict synonym of Heteropterodea groups in Hemiptera ... ZRZAVY (1992a), itself a variant proposed because of the seemingly suprafamilial suffix of It appears, based on the consensus of cur- the initial spelling Heteropteroidea by SCHLEE rent paleontological, morphological and (1969). Archaeorrhyncha is a strict synonym molecular knowledge the taxa Homoptera and of Fulgoromorpha. The fourth name, Cly- Auchenorrhyncha are not monophyletic. In peorrhyncha, is a synonym of 'Clypeata' of the contrast, there are four to five major lineages Russian authors, which moreover leaves alone

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numerous basal cicadomorphan lineages (see historical precedence at this rank. Such a SORENSEN et al. 1995, fig. 4). SORENSEN et al. system, as noted previously (MlNET & BOUR- argued that Clypeorrhyncha should replace GO1N 1986), does not presume affiliations nor Cicadomorpha in view of how it had different names groups at higher levels that might be meanings depending upon whether Cicado- invalidated in the future. As long as these morpha included (e.g. SHCHERBAKOV 1984) or names refer to monophyletic groups and the excluded (e.g., CARVER et al. 1991) fossil taxa. names are already universally recognized we However, this argument is unconvincing: we assert their use will provide stability to the do not change names of groups each time a nomenclature within Hemiptera. Moreover, as new taxon (fossil or not) is added or removed. well as we recommend discontinuing Auche- SORENSEN et al. offered the "-rrhyncha" suffix norrhyncha and Homoptera as formal taxono- to denote a suborder rank in Hemiptera. This mic terms, we also recommend not naming was done as a means to remove confusion over intermediate taxonomic units between them the -morpha suffices and the -oidea and -odea (e.g., Neohemiptera). As such, we have not suffices of Heteroptero(i)dea. Also the named the phylogenetic sequence of (Fulgoro- -rrhyncha suffix was chosen because Sternorr- morpha + (Cicadomorpha + Heteroptero- hyncha, already having the -rrhyncha suffix, dea)) proposed here. Creating taxonomic was a recognized suborder and remained terms for every node of a newly proposed phy- monophyletic. While this effort to coordinate logeny may be just the modern counterpart of suborder nomenclature within Hemiptera can "failling into the autamorphic trap" of our old be appreciated, is the need important enough masters. to adopt and disband use of already recognized synonymous names? There is no rule manda- Acknowledgements ting that suffices of names of higher rank taxonomic groups must be coordinated. For exam- We would like to thank M. Asche for ple, the "-ptera" suffix of Neoptera, Paraneop- providing the photos of C. Stil and F. Muir for tera, etc. is not mandated to signify order rank this paper, and P. Stys and J.Szwedo for useful and it is missing in the names of other orders discussions during the preparation of the such as Odonata or Phasmida, etc. manuscript. In conclusion, the now widely recognized paraphyly of Homoptera and Auchenorrhyn-. Zusammenfassung cha calls for rejecting them as formal taxonomic groups within Hemiptera. It is recommen- Die „Hemiptera" (Schnabelkerfe) und ded to discontinue their formal use as taxono- ihre wichtigsten Vertreter wurden bereits vor mic terms in systematic papers. They can be fast 250 Jahren als natürliche Gruppen durch used in the lower case, 'auchenorrhyncha' and LlNNE etabliert. Allerdings integrierte er die 'homoptera', to convey their historical con- Fransenflügler in „seine" Hemiptera und schuf cepts. In contrast, formal recognition of the damit bereits ein paraphyletisches Taxon. five major lineages, Sternorrhyncha, Cicado- Etwa 50 Jahre später etablierten DUMERIL und morpha, Fulgoromorpha, Coleorhyncha and LATREILLE mit Auchenorrhyncha versus Heteroptera, each a valid clade, as suborders Sternorrhyncha und Heteroptera versus of Hemiptera appears appropriate. In agree- Homoptera zwei mal zwei jeweils durch Prä- ment with the same philosophy expressed in senz-Absenz-Merkmale definierte Gruppen SORENSEN et al. (1995), this categorization innerhalb der Hemiptera. Wie viele andere would still be a conventional treatment that Autoren, fielen sie damit in die „Autapomor- preserves both morphological and eco-evolu- phie-Falle". Tatsächlich wurden Heteroptera tionary delineation of these groups. Moreover und Sternorrhyncha mit Hilfe mehreren recognizing Coleorhyncha as an independent Autapomorphien definiert. Die beiden damit suborder (versus SORENSEN et al. 1995) preser- „ausgegrenzten" Gruppen, Homoptera und ves the particular taxonomic history of this Auchenorrhyncha, wurden hingegen nur group and retains a suborder ranking of Heter- durch den Erhalt der ursprünglichen Merk- optera, already having high recognition and malsausprägung (nicht modifizierte Vorderflü-

78 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at gel und nicht caudad verschobenes Labium) BOURGOIN Th. (1988): A new interpretation of the und damit durch klare Plesiomorphien defi- homologies in the Hemiptera male genitalia, illustrated by the Tettigometridae (Hemiptera niert. Daher ist es auch nicht verwunderlich, Fulgoromorpha). — 6th Auchenorrhyncha Mee- daß die Mono- oder Paraphylie der Auche- ting, Turin (Italie), 1987. Proceedings: 113-120. norrhyncha und der Homoptera immer wieder BOURGOIN Th. & J. HUANG (1990): Morphologie com- kontrovers diskutiert wurde und noch immer paree des genitalia males des Trypetimorphini diskutiert wird. In dieser Arbeit geben wir et remarques phylogenetiques (Hemiptera: Ful- goromorpha: Tropiduchidae). — Annales de la einen Überblick über die historische Entwick- Societe Entomologique de France (N.S.) 26(4): lung dieses Diskussionsprozesses und präsen- 555-564.- tieren abschließend eine Synthese der Phylo- BOURGOIN Th. (1993): Female genitalia in Hemiptera genie der Hemiptera auf Basis der jüngsten Fulgoromorpha, morphological and phylogene- Ergebnisse molekularer Forschung und neuer tical data. — Annales de la Societe Entomologi- aus Fossilfunden gewonnener Erkenntnisse. que de France (N.S.) 29(3): 225-244. Während einige sehr basale Verwandtschafts- BOURGOIN Th., STEFFEN-CAMPBELL J.D. S B.C. CAMPBELL beziehungen unklar bleiben, ist die Monophy- (1997): Molecular phylogeny of Fulgoromorpha (Insecta, Hemiptera, Archaeorrhyncha). The lie der Sternorrhyncha, Fulgoromorpha, Cica- enigmatic Tettigometridae: evolutionary affilia- domorpha, Coleorhyncha und Heteroptera tions and historical biogeography. — Cladistics sehr gut belegt. Wir schlagen vor, die Namen 13: 207-224. dieser fünf Hauptgruppen aus historischen BOURGOIN Th., CHAN K., OUVRARD D. & B.C. CAMPBELL Gründen und aufgrund des hohen Bekannt- (1999): Character analysis using ribosomal RNA heitsgrads beizubehalten und sie formell als secondary structure and its application to Hemiptera and Fulgoromorpha phylogeny. — Unterordnungen der Hemiptera zu klassifizie- 10"1 International Auchenorrhyncha Congress, ren. Weiters schlagen wir vor, bis zur hinrei- Cardiff, Wales, UK, 6-10 Sept. 1999. chenden Klärung der verwandtschaftlichen BOURGOIN Th., CAMPBELL B.C., OUVRARD D. & K. CHAN Beziehungen innerhalb dieser fünf Gruppen (2001): 18S Ribosomal RNA patterns in Hemip- nd keine Namen für Gruppen auf einem Niveau tera with emphasis on Fulgoromorpha. — 2 European Hemiptera Congress, 20-24 June zwischen den Hemiptera und den fünf Unter- 2001, Fiesa, Slovenie: 18. ordnungen zu verwenden; insbesondere soll- BURMEISTER H.C. (1835): Rhynchota. — Handb. Ent. ten „Auchenorrhyncha" und „Homoptera" als 2(1): 1-396. formale taxonomische Begriffe nicht weiter CAMPBELL B.C., STEFFEN-CAMPBELL J.D. & R.J. GILL 1994): verwendet werden. Evolutionary origin of whiteflies (Hemiptera: Sternorrhyncha: Aleyrodidae) inferred from 18S rDNA sequences. — Insect Molecular Biology 3: References 73-88.

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Address of the authors:

Th. BOURGOIN Museum national d'Histoire naturelle, Laboratoire d' Entomologie and ESA 8043 CNRS, 45 rue Buffon, F-75OO5, Paris, France

B.C. CAMPBELL WRRC, USDA-ARS, 800 Buchanan St., Albany, California 94710-1100, USA.