論 壇

(ᖪ 22: 297-305 (2002ٿέ៉ Formosan Entomol. 22: 297-305 (2002)

Preliminary Thoughts on the Phylogeny of Coleorrhyncha- Heteroptera (Hemiptera)

Chung-Tu Yang Professor Emeritus, Department of Entomology, National Chung Hsing University, No.250 Kuo-Kuang Road, Taichung 402, Taiwan R.O.C.

ABSTRACT

The Psylloidea is selected as the sister group of Coleorrhyncha- Heteroptera. The Dipsocoromorpha, Gerromorpha, and Nepomorpha are determined to be a monophyletic taxon by the possession of a synapomorphy, i.e., the hypopleurites of abdominal segment VIII that evolved to an appendage-like structure. A new formal relationship hypothesis in the Coleorrhyncha-Heteroptera is proposed with the Psylloidea as the sister group: (Coleorrhyncha + Enicocephalomorpha + (Leptopodomorpha + Cimicomorpha + Pentatomomorpha)) + (Dipsocoromorpha + (Gerromorpha + Nepomorpha)).

Key words: Coleorrhyncha, Heteroptera, cladistic analysis, phylogeny

Introduction with their importance. 1) The Coleorrhyncha, Enicocephalomorpha, The author finds it hard to resist the Leptopodomorpha, Cimicomorpha, and temptation to study the amazing Pentatomomoprha form a monophyletic diversity of external male genitalia taxon. This monophyletic taxon is among the Heteroptera. After examin- determined by the possession of a ation of 40 families and 300 species, the synapomorphy, i.e., abdominal hypo- evolutionary trends of characters pleurite VIII is prominent; or the seemingly have emerged. At this time, epipleurites are fused with the tergite, the phylogenetic tree is much needed for the hypopleurites are fused with the consultation. Unfortunately the current sternite, and the tergite-sternite is view of phylogenetic relationships of separated; or the tergite-sternite is fused infraorders (Wheeler et al., 1993) appears and ring-like. 2) The Disocoromorpha, difficult to use to interpret evolutionary Gerromorpha, and Nepomorpha form a trends. In view of this, the present data monophyletic taxon. This monophyletic were carefully evaluated. taxon is determined by the possession of An evaluation was made based only a synapomorphy, i.e., abdominal hypo- upon the data of the present investing- pleurite VIII evolved to appendage-like ation, and several points impressed me structure, and a parallel derived

! Preliminary Thoughts on the Phylogeny of Coleorrhyncha-Heteroptera 297 character, abdominal tergite is separated If the characters of the external from the remainder. 3) As for the male genitalia actually have high weight outgroup, in the prevailing view, the as in Wygodznsky’s words, the above Auchenorrhyncha is the sister group of information can offer a different view of Coelorrhyncha-Heteroptera. However, the the phylogenetic relationships in the data here indicated that (a) the general Heteroptera from the prevailing one. features in the external male genitalia of the Psylloidea, Coleorrhyncha, and Outgroup selection Ochteroidea are similar in every respect: the phallobase is tube-shaped, extremely According to the prevailing view, long, and situated at the base of the Coleorrhyncha is unquestionably the aedeagus. (b) abdominal tergite IX is sister group of Heteroptera, but the separated from the remainder in the Psylloidea is not. Why is it selected? The Psylloidea, Dipsocoromorpha, Gerro- reasons were mentioned in the morpha, and Nepomorpha. (c) the Introduction. Furthermore, abdominal ejaculatory duct is expanded before the sternite XI in the Auchenorrhyncha is anterior opening of abdominal segment differentiated into the so-called anal style, IX (foramen sensu Singh-Pruthi, 1925), while it is undifferentiated in Coleorr- in the Psylloidea, it is the sperm pump; hyncha and Heteroptera. This seemingly in the Miridae and Corixoidea it appears excludes Heteroptera from having after the opening, but it has not been common ancestor with a later line of carefully examined and termed yet; in Auchenorrhyncha. the Pentatomomorpha, it protrudes in the apical half of the aedeagus as the Character analyses, codes, and ejaculatory reservoir (defined differently state definitions from that of Singh-Pruthi). The relationships of these three forms are 1. Sperm pump difficult to understand. Are these worthy Sperm pump differentiation is judged of further exploration? Why did the to be the advanced character state. evolutionary events so frequently in these (1) 0 Sperm pump is undifferentiated taxa, as compared to the Auchenorr- 1 Sperm pump is already different- hyncha? tiated Furthermore, Wygodzinsky (1966: 31) 2. Connective (basal plates sensu commented “The male genitalia of most Singh-Pruthi, 1925; articulatory ap- of the Emesinae do not differ in any paratus sensu Dupuis, 1970) significant way from those of other Yang and Chang (2000: 7) stated reduviids. The structure of the pygophore “The lower bulb-like growth of the and parameres has been used by many segmental membrane, variable in form, authors for taxonomic purposes, but the connecting the phallobase, aedeagus or phallus has not been given the necessary sheath with genital styles.” On pape 713, attention and has not been analyzed “The connective exposing in genital carefully as to its taxonomic significance. chamber distributes in Aphidoidea, As shown in the following discussion and Coccoidea, Aleyrodoidea, Psylloidea, Coca- in the systematic part of this paper, the doidea, Cercopoidea and Membracoidea. study of the phallus provides characters The connective evaginating into body useful on the specific, generic, and often cavity distributes in Membracoidea (part), tribal levels. Its amazing diversity Fulgoroidea, Coleorrhyncha and Heterop- frequently surpasses that of the external tera.” “The connective situating below visible features of the bug.” phallobase distritubes in Aphidoidea,

ௐαഇס˟˩˟ᖪௐٿέ៉ 298 Coccoidea, Aleyrodoidea, Psylloidea, tera. Cicadoidea, Membracoidea and Fulgo- (5) 0 The support tube is undifferentiated roidea. The connective situating before 1 The support tube is already phallobase distributes in Coleorrhyncha differentiated and Heteroptera.” According to the 5. Genital plates (subgenital plates phylogenetic tree, evagination into the sensu Singh-Pruthi, 1925) body cavity and being situated before the Yang and Chang (2000: 7) stated: phallobase are advaced character states. “The pair of plates at posterior margin of (2) 0 The connective is exposed in the abdominal sternite nine.” On page 707, genital chamber “Genital plates present only in 1 The connective is evaginated into Cercopoidea and Membracoidea.” The the body cavity above distribution record is wrong. In (3) 0 The connective is situated below the Pantinia darwini China (Coleorrhyncha), base of the phallobase the so-called longitudinal ridge should be 1 The connective is situated at the the modified genital plates; in most base of the phallobase Heteroptera they are recognizable, except 3. Support bridge (struts sensu in a few cases in which they are difficult Singh-Pruthi, 1925; ligamentary to recognize. They are not found in the processes sensu Dupuis, 1970) Psylloidea, so it is judged to be Yang and Chang (2000: 7) stated: undifferentiated. “The differentiated structure of dorsoan- (6) 0 The genital plates are undifferen- terior upper portion of the phallobase, tiated highy variable in form.” On page 709, 1 The genital plates already are “The structure is unrecognizable in differentiated Stenorrhyncha, Cicadoidea, Cercopoidea 6. Abdominal segment eight (VIII) and Membracoidea. It is recognizable in Sweet (1996: 120) in comparing the Fulgoroidea, Coleorrhyncha and Heterop- external morphology of the pregenital tera.” On page 17, “the structure abdomen of the Hemiptera stated: “The unrecongizable are judged based on pregenital abdomen includes secondary phylogenetic tree undifferentiation.” segments 1-8.” On page 133, “Psyllo- (4) 0 The support bridge is undiffer- morpha ….. there is a single series of entiated spiracle-bearing lateral pleurites on 1 The support bridge is already segments 1-8.” On page 139, “Coleorr- differentiated hyncha ….. There is a single series of 4. Support tube (basal plates bridge large ventral hypopleurites bearing sensu Singh-Pruthi, 1925; ductifer spiracles 3-8.” In the Heteroptera, Sweet sensu Dupuis, 1970) judged that there are a double set of Yang and Chang (2000: 9) stated: pleurites: the dorsal epipleurites and the “The differentiated structure of dorsoan- ventral spiracle-bearing hypopleurites. As terior lower portion of the phallobase. It to the later evolutionary event on VIII, is tubular in form, permitting the the epipleurites fused with the tergite, ejaculatory duct runs through.” On page and the hypopleurites fused with the 710, “This structure is unrecognizable in sternite. Stenorrhyncha, Cicadoidea, Cercopoidea Schuh and Slater (1996) considered and Membracoidea.” On page 18, “The that the paired respiratory processes of structure unrecognizable are judged the Belostomatidae and Nepidae are based on phylogenetic tree undifferen- modified “abdominal tergum 8.” Herein tiated yet.” It is recognizable in the they are judged to be the hypopleurites. Fulgoroidea, Coleorrhyncha, and Heterop- The appendage-like structure is judged to

Preliminary Thoughts on the Phylogeny of Coleorrhyncha-Heteroptera 299 Table 1. Rearrangment data matrix Psy Col Eni Lep Cim Pen Dip Ger Nep 1 1 0 0 0 0 0 0 0 0 2 0 1 1 1 1 1 1 1 1 3 0 1 1 1 1 1 1 1 1 4 0 1 1 1 1 1 1 1 1 5 0 1 1 1 1 1 1 1 1 6 0 1 1 1 1 1 1 1 1 8 0 1 1 1 1 1 0 0 0 10 0 0 0 0 0 0 1 1 1 9 0 0 0 1 1 1 0 0 0 15 0 0 0 1 1 1 0 0 0 13 0 0 0 0 0 0 0 1 1 7 0 0 1 1 1 1 1 1 1 11 1 0 0 0 0 0 1 1 1 12 1 0 0 0 0 0 0 1 1 14 0 0 0 1 1 1 0 0 1 Psy – Psylloidea Pen – Pentatomomorpha Col – Coleorrhyncha Dip – Dipsocoromorpha Eni – Enicocephalomorpha Ger – Gerromorpha Lep – Leptopodomorpha Nep – Nepomorpha Cim - Cimicomorpha

be reduced as the later evolutionary sternite is fused and tube-shaped. event. In the Dipsocoromorpha: In the Enicocephalomorpha: Oncyloco- Ceratocombidae: The hypoleurites are tis basalis Westwood (Enicoce- appendage-like. phalidae) (Sweet, 1996: 127, figs.12- Dipsocoridae: The hypopleurite (right) is 13): The hypopleurites are promi- appendage-like (Shuh and Slater, nent. 1995: 78). In the Leptopodomorpha: Schizopteridae: The hypopleurites are Aepophilidae: Aepophilius bonnairei reduced. (Sing.) (Sweet, 1996: 129, fig.22): Stemmocryptidae: The hypopleurites are The hypopleurites are prominent. appendage-like (Schuh and Slater, Saldidae: Pentacora ligata (Say) (Sweet, 1995: 83). 1996: 129, figs. 23-24): The In the Gerromopha: The VIII tergite- hypopleurites are prominent. sternite is fused and tube-formed. Leptopodidae: Leptopodus hispanus Ramb. In the Nepomorpha: (Sweet, 1996: 129): The hypo- Nepoidea: The hypopleurites are pleurites are prominent. appendage-like. In the Cimicomorpha: Ochteroidea and Corixoidae: The VIII are Reduviidae: The VIII tergite-sternite is appendage-like. fused and tube-shaped. (7) 0 Pleurites of VIII are single, Miridae, Nabidae, and Cimicidae: The consisting of hypopleurites. tergite-sternite is separated. 1 Pleurites of VIII are double, In the Pentatomomorpha: The tergite- consisting of epipleurites and

ௐαഇס˟˩˟ᖪௐٿέ៉ 300 Fig. 1. Cladogram of the Coleorrhyncha-Heteroptera.

hypopleurites. separted; or tergite sternite fused, (8) 0 Pleurites of VIII are single; or ring-like. double, hypoleurites evolved to an (9) 0 Pleurites of VIII single; or double, appendage-like structure; or append- hypopleurites evolved to an age-like structure is reduced, tergite- appendage-like structure; or the sternite is fused; or tergite-sternite appendage-like structure is reduced, completely fused, tube-formed. the tergite-sternite is separated; or 1 Hypopleurites are prominent; or tergite-sternite incompletely fused; or epipleurites are fused with the tergite tergite-sternite completely fused, and hypopleurites are fused with the tube-formed; or hypopleurites are sternite, the tergite-sternite is prominent.

Preliminary Thoughts on the Phylogeny of Coleorrhyncha-Heteroptera 301 1 Epipleurites are fused with the seemingly not separated from the tergite, and hypopleurites are fused remainder, but this is doubtful in with the sternite, the tergite-sternite some Notonectidae. If Nepomorpha is separated; or tergite-sternite fused, is truly a monophyletic taxon, the ring-like. tergite not been separated from the (10) 0 Pleurites of VIII are single; or remainder is reasonably the double, hypopleurites are prominent; reversal. or epipleurites are fused with the (11) 0 IX is ring-shaped. tergite and hypopleurites are fused 1 Abdominal tergite nine (IXt) is with the sternite, the tergite-sternite separated from the remainder and is is separated; or tergite- sternite fused, not fused with X; or IXt is separated ring-like. from the remainder and is fused with 1 Hypopleurites evolved to an X; or the IXt is not separated from appandage-like structure; or the remainder and is not fused with appendage-like structure is reduced, with X, ring-formed. tergite-sternite separated; or tergite- (12) 0 IX is ring-shaped; or IXt it sternite incompletely fused; or separated from the remainder and is tergite-sternite completely fused, not fused with X. tube-formed. 1 IXt is separated from the remainder 7. Abdominal segment nine (IX) and is fused with X; or IXt is not (pygophore sensu Schuh and separated from the remainder and is Slateer, 1995) not fused with X, ring-formed. In Psylloidea: Yang and Chang (2000: 8. Extension IX 59) stated: “Abdominal segment IX The base of IX protruding cephalad with tergite separated from the into the body cavity for various length, is remainder and tergite fused with termed the extension of IX. the X.” This character is found in the In Coleorrhyncha, Enicocephalomor- Psylloidea and many families of the pha, Leptopodomorpha, Cimi- Fulgoroidea: some species of Flatidae, comorpha and Pentatomomorpha: Nogodinidae, Issidae, Acanaloniidae, Ix is ring-like and the tergite is not Fulgoridae, Dictyopharidae, Meenoplidae, separated from the remainder. and Achilidae. But it is never overly In Dipsocoromorpha: developed as in Gerromorpha or Ceratocombidae and Schizoptera: The Nepomorpha. tergite is separated from the The extension is difficult to judge in remainder, and each side has a some taxa in the Nepomorpha, but it process dirceted mesad. The tergite easily assessed in Gerromorpha. In is not fused with X. Gerromorpha, it is always rather In Gerromorpha: transparent, without setae. In Nepo- Mesoveliidae, Hydrometridae, Veliidae, morpha, it is easily judged in Paraplea and Gerridae: The tergite of IX is indistinguenda Matsumura (Pleidae). separated from the remainder and is When other taxa are compared with the fused with X. Pleidae, one can roughly take the In Nepomorpha: anterior margin of X as the borderline of Nepoidea: The tergite of IX is separated IX. This is the way I herein judged the from the remainder and is fused extension of IX. with X. The extension of IX is unrecog- Ochteroidea, Coroxoidea, Naucoridae, and nizable, or it is more or less recognizable Notonectoidea: The tergire of IX is in the Notonectidae, are judged to be the

ௐαഇס˟˩˟ᖪௐٿέ៉ 302 reversal. anterior portion and a membranous In Psylloidea: It is more or less posterior portion.” recognizable. (14) 0 Forewings have a uniform texture. In Coleorrhyncha, Enicocephalomor- 1 Forewings are in the form of pha, Leptopodomorpha, Cimi- hemelytra. comorpha, Pentatomomorpha, 10. Capitate processes Dipsocoromorpha: it is unrecog- Yang and Chang (2000: 7) stated: nizable. “capitate processes – the processes of the In Gerromorpha: support bridge.” This is a new-born Mesoveliidae: It is subquadrate, higher structure. than long, and slightly shorter than (15) 0 The capitate processes are the length of IX. undifferentiated. Hydrometridae: It is subquadrte, longer 1 The capitate processes are already than high, and distinctly longer differentiated. than the length of IX. Veliidae: It is subquadrate, as high as Cladistic analysis long, and slightly shorter than the length of IX. Character 1 and the combination of Gerridae: It is subquadrate, as high as characters 2, 3, 4, 5, and 6 as borne by long, and slightly shorter than the the largest number of taxa are selected length of IX. as the basal branch. Here the Psylloidea In Nepomorpha: is determined to be a monophyletic taxon Nepoidea: It is slender and longer than by the possession of a synapomorphy, i.e., high. character 1. Coleorrhyncha and Hetero- Ochteroidea: It is triangular, narrowed ptera are determined to be a mono- dorsally, and distinctly shorter than phyletic taxon by the possession of the length of IX. synapomorphies, i.e., characters 2-6. Corixoidea: According to the above The combination of character, 8 and standard of judgment the real IX 10 as borne by the second largest number should be very small, and most part of taxa is selected as the second branch. of the so-called IX should be the Here Coleorrhyncha, Enicocephalomorpha, extension. Leptopodomorpha, Cimicomorpha, and Notonectidae: It is more or less Pentatomomorpha are determined to be a recognizable in some species, but monophyletic taxon by the possession of a unrecognizable in others. It should synapomorphy, i.e., character 8; and be the reversal. Dipsocoromorpha, Gerromorpha and Pleidae and Helotrephidae: It is nearly as Nepomorpha are determined to be a long as the length of IX. monophyletic taxon by the possession of a (13) 0 The extension of IX is unrecogniz- synapomorphy, i.e., character 10. able; or more or less recognizable. Character, 9 and 15 as borne by the 1 The extension of IX is overly third largest number of taxa are selected developed; or reduced. as the third branch. Here Leptopo- 9. Forewings domorpha, Cimicomorpha, and Pentato- Schuh and Slater (1995: 43) stated: momorpha are determined to be a “The forewing may be either of uniform monophyletic taxon by the possession of texture (tegminal) – as in the synapomorphies, i.e., characters 9 and 15. phylogenetically more promitive group – Character 13 as borne by the fourth or in the form of Hemelytra, that is, largest number of taxa is selected as the divided into a distinctly coriaceous fourth branch. Here Gerromorpha and

Preliminary Thoughts on the Phylogeny of Coleorrhyncha-Heteroptera 303 Nepomorpha are determined to be a Wheeler, W. C., Shuh, R. T. and Bang, R. monophyletic taxon by the possession of a 1993. Cladistic relationships among synapomorpha, i.e., character 13. higher groups of Heteroptera: con- Finally, characters 7, 11, 12, and 14 gruence between morphological and of parallel evolution are added. molecular data sets. Ent. Scand. 24: 121-137. References Wygodzinsky, P. M. 1996. A monograph of the Emesinae (Reduviidae, Hemi- Schuh, R. T. and J. A. Slater. 1995. True ptera). Bull Amer. Mus. Nat. Hist. Vol. bugs of the world (Hemiptera: Hetero- 133: 31. ptera). Cornell University Press: 1- Yang, C. T. and T. Y. Chang. 2000. The 336. external male genitalia of Hemiptera Sweet, M. H. 1996. Comparative external (Homoptera-Heteroptera). Shih Way morphology of the pregenital abdomen Publication: 1-746. of the Hemiptera. Thomas Say Publication: Studies on Hemiptera Received Aug. 28, 2002 Phylogeny: 119-146. Accepted Nov. 5, 2002

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Preliminary Thoughts on the Phylogeny of Coleorrhyncha-Heteroptera 305