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Evolution of Odonata, with Special Reference to Coenagrionoidea (Zygoptera)

Evolution of Odonata, with Special Reference to Coenagrionoidea (Zygoptera)

Arthropod Systematics & Phylogeny 37

66 (1) 37 – 44 © Museum für Tierkunde Dresden, eISSN 1864-8312

Evolution of , with Special Reference to (Zygoptera)

Frank Louis Carle* 1, Karl M. Kjer 2 & Michael L. May 1

1 Rutgers, Department of , New Brunswick, New Jersey 08901 USA [[email protected]; [email protected]] 2 Rutgers, Department of Ecology, Evolution, and Natural Resources, New Brunswick, New Jersey 08901 USA [[email protected]]

* Corresponding author

Received 04.ii.2008, accepted 10.v.2008. Published online at www.-systematics.de on 30.vi.2008.

> Abstract A phylogeny including 26 families of Odonata is presented based on data from large and small subunit nuclear and mito- chondrial ribosomal RNAs and part of the nuclear EF-1α. Data were analyzed using Bayesian methods. Extant Zygoptera and Anisoptera are monophyletic. The topology of Anisoptera is ((, ) ( ( (( (Neopetaliidae, )) ((, ) ( (Corduli- idae s.s., ))))))). Each of the major groups among anisopterans is well supported except the grouping of Neopeta­ lia with Chloropetalia. and form a group sister to other Zygoptera, and Coenagrionoidea are also monophyletic, with the caveat that , although well supported as a family, was unstable but not placed among other coenagrionoids. are paraphyletic and partly polytomous, except for the recovery of (, Hetaerinidae) and also ( (Epallagidae (Diphlebiinae, Lestoidinae))). Support for Epallagidae as the of a (Diphlebiinae, Lestoideinae) is strong. Within Coenagrionoidea, several novel relationships appear to be well supported. First, the Old World disparoneurine protoneurids are nested within and well separated from the protoneurine, . The remaining coenagrionids are divided into two well-supported subdivisions. The first includes Pseudostigmatinae, stat. nov., Protoneurinae, a group of coenagrionids mostly characterized by having an angulate frons, and Argiinae (). The second division includes typical . > Key words Odonata, Zygoptera, Anisoptera, , phylogeny, RNA, Bayesian, parsimony.

1. Introduction

The phylogeny of Odonata has been a matter of con­ (1919; Zygoptera), Kennedy (1919; Zygoptera) and troversy for nearly a century and a half. Largely Needham & Broughton (1927; Libellulidae), all but due to the work of Baron de Selys-Longchamps, that of Kennedy based almost entirely on wing ve­ “the Father of Odonatology”, the families generally nation. Needham (1903) proposed, in modern terms, recognized today were established as “légions” and a paraphyletic Zygoptera with Calopterygoidea + first placed in Zygoptera or Anisoptera (1854a,b). Epiophlebia sister to a monophyletic Anisoptera and Selys treated “légions” as natural groupings and had with Aeshnidae the sister of Libellulidae. Tillyard’s a sense of their evolutionary position, but the first (1917) classification was similar but raised Lestidae to explicitly phylogenetic or “geneologic” study of Odo­ family status, and elevated “legions” now recognized nata was that of Needham (1903), followed by Munz as families of Coenagrionoidea to subfamily status. 38 Carle et al.: Evolution of Odonata

Kennedy’s (1919, 1920) study of zygopteran pe- to other extant Anisoptera and Gomphidae sister to nes led him to depict modern Zygoptera as a poly­ . Lohmann (1996) proposed a phylogeny tomy comprising Calopterygidae (with basal Mega­ for Anisoptera much like Bechly’s but with Aeshnidae podagrioninae), , Lestidae, and Coen- as sister to other Anisoptera, in accord with Pfau’s ar- agrionidae, all arising “by radiation from the primi- guments. Carle & Kjer (2002), also based in part on tive lestid or hemiphlebiid stock”. Tillyard (1925) the work of Pfau, proposed yet another arrangement later described Kennedya mirabilis, a “small narrow of Anisoptera, ((Austropetaliidae, Aeshnidae) (Gom- winged” taxon characterized by petiolate phidae (Petaluridae, Libeluloidea))). The most recent wings, two antenodal crossveins, and without the computer-implemented morphological study (Rehn posterior arcular brace. Kennedya turned out to be an 2003) utilized diverse characters and again found important taxon, because these wing characteristics monophyletic Zygoptera and Anisoptera. Rehn’s re- caused a reinterpretation of polarities, which led Fra- sults placed or Philoganga + ser to propose a new classification system T( illyard as sister to other Zygoptera, with Amphipterygidae & Fraser 1938–1940) and finally to Fraser’s (1957) and (both sensu Fraser 1957) reclassification and phylogeny positing a paraphyletic forming a paraphyletic assemblage branching basal to Zygoptera originating from a Kennedeya-like ances- Calopterygoidea, which in turn was sister to a mono- tor. Hemiphlebia was placed at the base of extant Odo- phyletic (with Hemiphlebia branching at its nata with Coenagrionoidea branching next, followed base) plus a monophyletic Coenagrionoidea. Rehn’s by Lestinoidea (= Lestoidea), from which in turn arose Anisoptera form a pectinate array with Petaluridae the Calopterygoidea and its supposed sister taxon, An- and Gomphidae, successively, as sister to remaining isozygoptera + Anisoptera. In the absence of a gener- Anisoptera. ally agreed alternative this phylogeny has been widely Previous molecular studies of Odonata as a whole accepted (Davies & Tobin 1984, 1985; Bridges 1994; include those of Hovmöller et al. (2002), Ogden & Steinmann 1997a,b), despite being explicitly based Whiting (2003), Saux et al. (2003), Kjer (2004), Kjer on putative plesiomorphic character states (Fraser et al. (2006), and Hasegawa & Kasuya (2006). All 1954). but Kjer (2004), Kjer et al. (2006), and Hovmöller Nevertheless, several different phylogenetic hy- (2002) recovered a paraphyletic Zygoptera with potheses have been suggested more recently. Carle as sister to a monophyletic Anisoptera. Kjer (2004) (1982), using a wide variety of morphological charac- discussed the weakness of his hypothesis, which re- ters, concluded that Anisoptera and Zygoptera are each covered a paraphyletic Anisoptera. The molecular monophyletic, with Gomphidae the sister to remaining based topologies of Hovmöller et al. (2002) and Kjer Anisoptera. Chlorogomphidae, usually placed in Cor- et al. (2006) come closest to the phylogeny we present dulegastridae previously, was raised to family status in this paper. In all molecular studies, however, much and both families were considered basal Libelluloidea. of the phylogenetic diversity of Odonata is left un- Carle & Louton (1994) later modified this scheme, sampled. Almost the only features of odonate phylo- placing the newly defined Austropetaliidae as sister geny that currently enjoy consensus are the monophy- to Aeshnidae, and Neopetaliidae (Neopetalia only) ly of Anisoptera with Epiophlebia as its sister taxon, immediately basal to Chlorogomphidae, and Carle and the deeply nested position of Libellulidae within (1995) separated Gomphomacromiidae from Cordu- Anisoptera. Here we suggest a revised phylogeny of liidae. Pfau (1991) placed Aeshnidae as sister to all Odonata, with particular emphasis on new conclusions other Anisoptera based principally on detailed studies about relationships among the Coenagrionoidea. of genitalic functional morphology. Cordulegastridae, Petaluridae, and Gomphidae formed a new superfam- ily, Petaluroidea. Pfau (2002) also supported the para- phyly of Zygoptera based on morphology of caudal appendages and their muscles. Trueman (1996) pre- 2. Methods sented a computer-assisted phylogeny, based strictly on wing venation, very similar to Fraser’s, including Hemiphlebia as the sister taxon to the rest of Odona- ta, but with Petaluridae basal to Austropetaliidae and DNA was extracted, amplified, and purified using with many families, especially in Zygoptera, paraphy- standard techniques. Amplification products from letic. Bechly (1995), utilizing inferred ground plans both strands were generated, purified, and used as tem- and manual cladistic analysis, inferred a monophy- plates for cycle sequencing using Applied Biosystems letic Zygoptera (Calopterygoidea ((Coenagrionoidea, BigDye ReadyMix; fragments were sequenced on Megapodagrionidae) (Hemiphlebiidae, Lestoidea))), both ABI slab gel and capillary sequencers. Forward and monophyletic Anisoptera with Petaluridae sister and reverse sequences were edited and consensus se- Arthropod Systematics & Phylogeny 66 (1) 39

quences created as in Kjer et al. (2001). Consensus 3. Results sequences were evaluated and contaminated sequenc- es removed, based on BLAST searches, overlapping sequence fragment identities, and phylogenetic analy- ses of individual fragments. Sequences of rRNA were Anisoptera and Zygoptera were found to be monophy- aligned manually utilizing secondary structure models letic. Results are further summarized in Fig. 1. The (Gutell et al. 1994) and compensatory substitutions relationship of Odonata to other is still un- according to Kjer (1995, 2004). Ambiguously aligned resolved (Whitfield & Kjer 2007; Klass 2007), and regions are excluded from analyses according to the our results provide no further resolution to the Pa- criteria presented in Kjer et al. (2007). Portions of laeoptera question. The placement of Epiophlebiidae the large and small subunit nuclear ribosomal RNA’s was unstable, with support for a sister taxon relation- (28S and 18S rRNAs; 6228 aligned nts.), EF-1α (1074 ship with other Odonata, Zygoptera, or Anisoptera. exon nts.), mitochondrial rRNA’s (12S and 16S; 1181 We present a basal trichotomy (Fig. 1). Nevertheless, aligned nts.) were selected for analysis. Protein cod- our data recover, with very strong support, a mono- ing genes were length invariant, and alignment was phyletic Zygoptera, in agreement with Carle (1982), trivial. Introns in EF-1α were identified in compari- Bechly (1994, 1995), and Rehn (2003). The aniso- son to mRNA-generated sequences taken from Gen- pteran topology in Fig. 1 is very similar to that report- Bank. Outgroup taxa, taken from GenBank, included ed by Carle & Kjer (2002), based on morphology. It Tricholepidion, Ctenolepisma, Lepisma (Thysanura = supports placement of Neopetalia in Libelluloidea, Zygentoma), Calibaetis, Hexagenia, Caenis, Steno­ Austropetaliidae as sister to Aeshnidae as in Carle & nema and Centroptilum (Ephemeroptera), and the ne- Louton (1994) and the monophyly of Synthemistidae opterans, Gromphadorhina (Blattodea), and Isoperla + Gomphomacromiidae. The zygopteran topology (Plecoptera). The GenBank accession numbers for all is similar to that proposed by Kennedy (1919), with included taxa and genes are given in the Electronic the superfamily Lestoidea (not to be confused with Supplement. the unrelated Lestoidea Tillyard) as sister to all Two independent analyses were simultaneously other Zygoptera. Calopterygoid phylogeny remains performed with MrBayes (Huelsenbeck & Ronquist obscure. Based on this limited taxon sample, only the 2002). Each of the analyses consisted of 5,000,000 (Hetaerinidae, Calopterygidae), and (Epallagidae (Di- iterations, each with 4 chains, 1 cold, 3 hot. All pa- phlebiinae, Lestoideinae)) groups are well supported. rameters for the Bayesian analysis can be found in Isostictidae is monophyletic but often recovered with- the Nexus file available on Kjer’s website, and the in Calopterygoidea or as sister to coenagrionoids with journal’s online website. The program MODELTEST less than 50% probability. (Posada & Crandall 1998) was used to select a Coenagrionoidea are here more extensively sam- model from the combined data under the Akaike crite- pled and the framework of a phylogeny with some rion. The GTR+I+G model (Tavaré 1986; Yang 1994; strongly supported features is apparent. Two striking Yang et al. 1994; Gu et al. 1995) was used with each results are suggested. First, appear not of the three data sets (i.e., EF-1α nuclear rRNA, and to be monophyletic (e.g. Rehn 2003). The three dis- mitochondria rRNA) unlinked, and free to vary un- paroneurines (Chlorocnemis, , and Prodasi­ der their own characteristics. Plots of the likelihood neura) are grouped with Platycnemididae. This group- scores from the MrBayes “.p” files were examined ing is morphologically supported by a distinctly trans- with Tracer (Rambaut & Drummond 2003) to deter- verse adult head and small labial cleft. New World mine the appropriate “burn-in”, and after discarding Protoneuridae, which possess an angulate frons (re- the burn-in (the first 1000 from each run), all presented here by Neoneura), is part of a morphologi- near optimal trees were pooled. Posterior probabilities cally diverse group including Argia moesta, several were recorded from this pooled treefile from a majori- presumed coenagrionids mostly characterized also by ty-rule consensus , calculated in PAUP (Swofford having the frons angulate (Kennedy 1919; Demarmels 1999). In to illustrate a phylogram, the most 1985; O’Grady & May 2002), and , likely of all trees was identified, and imported into the also with an angulate frons. Second, this latter group Treeview (Page 1996) program. is well differentiated from a third group comprising Data are available on GenBank, and voucher other more typical Coenagrionidae that lack an angu- specimens are deposited in the Rutgers Entomologi- late frons, including and the large genera, cal Museum. Alignments and Nexus files are available , , and , among oth- on Kjer’s website http://www.rci.rutgers.edu/~insects/ ers. indexpersonnel.htm, and the journal’s website http:// globiz.sachsen.de/snsd/publikationen/ArthropodSys- tematicsPhylogeny/. 40 Carle et al.: Evolution of Odonata

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Fig. 1. Likelihood phylogram from the Bayesian analysis; all posterior probabilities are 100% unless given to the left of a node. This was the most likely tree from among many trees in the distribution, therefore there are some nodes, indicated by an “X”, on this “best” tree that are not present in the majority-rule consensus from which posterior probabilities were calculated. Con- ventional family groupings are indicated with the following abbreviations: AES – Aeshnidae, AMP – Amphipterygidae, AUS – Austropetaliidae, CAL – Calopterygyidae, CGA – Cordulegastridae, CHL – Chlorogomphidae, COE – Coenagrionidae, COR – , CYC – Chlorocyphidae, EPA – Epallagidae, EPI – Epiophlebiidae, GMA – Gomphomacromiidae, GOM – Gomphidae, HET – Hetaerinidae, ISO – Isostictidae, LES – Lestidae, LIB – Libellulidae, LTO – (Lestoi- deinae + Diphlebiinae), MAC – Macromiidae, NEO – Neopetaliidae, PCN – Platycnemididae, PET – Petaluridae, PRN – Proto- neuridae, PSE – Pseudostigmatidae, STH – Synthemistidae, SYN – Synlestidae. Arthropod Systematics & Phylogeny 66 (1) 41

4. Discussion Our hypothesis for Zygoptera includes support for Lestoidea as sister to other Zygoptera, as in Hov- möller et al. (2002), and Kjer (2004), and as implied by Kennedy (1920). The position of Hemiphlebia, The monophyly of Anisoptera has never been in ques- not included here, is still unclear. In his text Fraser tion, but the phylogenetic arrangment of included (1957), too, suggests a basal branching of Lestoidea groups has been a source of major disagreement (eg. from other Zygoptera (and indeed from all extant Odo- Carle 1995; Bechly 1996; Pfau 2005). Pfau (1991, nata). The accompanying tree and Fraser’s description 2005) proposed his unique Petaluroidea comprising of it, however, makes Coenagrionoidea the sister to Gomphidae, Petaluridae, and Cordulegastridae, based other Zygoptera. This appears to be a consequence of largely on his reconstruction of the evolution of the his view that Megapodagrionidae, and penis. The molecular evidence, however, strongly in- Amphipterygidae are “annectant” between Lestoidea dicates that Pfau’s Petaluroidea is paraphyletic, with and Calopterygoidea and that the latter are sister to or Cordulegastridae sister to all other Libelluloidea, as even progenitors of Anisoptera. Such an arrangement also inferred by most other authors (e.g., Fraser 1957; forces Coenagrionoidea to a position as sister to the Carle 1982; Misof et al. 2001; Rehn 2003). This result other taxa. implies that the biphasic function of the distal penile Our data strongly refute the placement of Calo­ chamber is a plesiomorphy within Libelluloidea, with pterygoidea as related to Anisoptera. If Isostictidae, subsequent development of a single phase pump in the the position of which is unstable, is excluded, the Calo­ monophyletic synthemistid (incl. gomphomacromi- pterygoidea (inc. Amphipterygida sensu Bechly 1995) ini), macromiid, corduliid, libellulid group. Placement form the sister group of Coenagrionoidea. However, of Neopetalia in Libelluloidea and establishment of traditional calopterygoids are not recovered as mono- Austropetaliidae as basal aeshnoids (Carle & Louton phyletic but are intermingled in a paraphyletic assem- 1994) is supported by both morphological and mole- blage with taxa generally placed within Amphipte- cular results. Consequently, similarities between Aus- rygida and possibly also including Isostictidae. This tropetaliidae and Neopetaliidae are either plesiomor- region of the phylogeny is characterized mostly by phies (abdominal color pattern, separated compound long terminal branches and short deeper internodes, so ), or convergences (reddish wing spots, quadrate it is likely that considerably more taxon sampling, and epiproct). Additionally, similarities between Aeshni- possibly use of additional genes and/or more appro- dae and Libellulidae, including the elongate male epi­ priate models, will be required to resolve this group. proct, contiguous compound eyes, hoodlike interocellar Dumont et al. (2005) provide a detailed analysis of lobe, well developed median and radial planates, elon- Calopterygidae which agree exactly with the results gate double anal loop, and lateral abdominal carina, presented here. Our results also justify family rank for are due to convergence (contra Needham 1903; Carle Isostictidae as proposed by Lieftinck (1975) and indi- 1982). Loss of an endophytic ovipositor apparently is cate that it is not phylogenetically close to Protoneu- an independent autapomorphy of Gomphoidea and Li- ridae. The group (Epallagidae (Diphlebiinae, Lestoi- belluloidea (contra Bechly 1994; Lohmann 1996; Rehn deinae)) is strongly supported and indicates that a 2003). However, shifts in ovipositor form and function close relationship between (not included has perhaps enhanced coevolution of male and female in this study) and Epallagidae proposed by Kennedy genitalia leading to the independent numerical domi- (1919) may be due to the convergent acquisition of nance of Gomphidae and Libellulidae in comparison to larval lateral abdominal . their near sister groups as shown in Fig. 1. Coenagrionoidea excluding Isostictidae (ie. Coen- The question of whether Zygoptera is monophy- agrionidae, Platycnemididae, Protoneuridae, and Pseu- letic has been perhaps the principal unresolved issue dostigmatidae; all sensu Fraser 1957, except that Pro- in higher level phylogeny of Odonata. As noted in the toneuridae excludes Isostictidae), reveal several unex- introduction, several authors have supported a para- pected but well supported relationships. Protoneuridae phyletic Zygoptera. Each of these analyses suffers, appears to be polyphyletic, with New World protoneu- however, from limited taxon or character sampling rids (Neoneura) closely associated with Argia, the an- or, in the case of Fraser’s work, by prephylogenetic gulate-frons Coenagrionidae (the -Teleba­ systematic methods. Our results provide strong inde- sis Series of Kennedy 1920), and Pseudostigmatidae. pendent validation of zygopteran monophyly from a Nososticta, Chlorocnemis, and , placed large taxon sample and extensive molecular data, and by Fraser (1957) in Disparoneurinae, are recovered they agree in this respect with the most detailed mor- within Platycnemididae (Fig. 1). Fragmentary data phological analyses performed using modern system- (not shown) from other New World protoneurids place atic principles (Carle 1982; Bechly 1994, 1995; Rehn them with Neoneura. The strong molecular differ- 2003; Klass 2008). ences between protoneurines and disparoneurines are 42 Carle et al.: Evolution of Odonata

supported by several morphological characters; for - group is paraphyletic (as also example, platycnemidids and disparoneurines have found by Demarmels 2007) relative to - the adult frons rounded, tibial spurs long, labial cleft tidae and is represented here by Ceriagrion and Dice­ shallow, and head transversely elongate, while in pro- ratobasis; the larval habitat of Diceratobasis is again toneurines, the frons is angulate, the spurs short, the in bromeliad axils. labial cleft deep, and the head not unusually elongate In summary, we suggest that Disparoneurinae be transversely. Possession of an angulate frons, short regarded as a subfamily of Platycnemididae, pending tibial spurs, and a deep labial cleft appear to be syn­ further analysis to confirm its monophyly. Pseudostig- apomorphies of Protoneuridae (sens. nov.) while the matinae stat. nov. are considered highly autapomorphic transversely elongated head, at least, unites Platy­ Coenagrionidae related to the angulate-frons coenagri- cnemididae + Disparoneurinae. Thus it appears that onid taxa, including Teinobasini Tillyard (Demarmels protoneurines and disparoneurines have been hitherto 2007), the “Ceriagrion-Telebasis-Metaleptobasis Se- placed in one family due mainly to convergent simi- ries” (Kennedy 1920), and probably the Protoneuridae larity resulting from reduced venation, but they are and Argiinae, although the distinctive morphological not actually close relatives. We lack sequence data for features of the last group suggest the need for further Caconurinae, but they share the same morphological study. We note the placement of a supposed Argia characteristics as noted for disparoneurines. Note, too, vivida among the Coenagrionidae s.s. The latter data that the shape of the discoidal cell evidently has little were obtained from GenBank and we did not verify if any systematic significance above the subfamily or the specific identification of the voucher specimen. tribal level. The topological positions of narrow winged Zy- The coenagrionoid group comprising Neoneura goptera suggest that Kennedy’s narrow wing ancestor through Megaloprepus in Fig. 1 includes a number of theory for Zygoptera is more plausible than ever. The taxa that have not commonly been associated by most narrow wing and stalked wing base appear likely to be recent workers, and the suggestion that protoneurines a synapomorphy of Kennedya + extant Odonata. So, and Argia belong here has not, to our knowledge, been too, may be possession of two antenodal crossveins, considered previously. Most of these are dis- although Carle (1982) points out that the frequent tinguished from typical coenagrionids by their angu- lack of alignment of “primary antenodals” in Protozy- late frons (Argia is a notable exception), and in many, goptera may imply that these are not homologous with the larval caudal lamellae are very strongly nodate, the costal braces of extant Odonata. Certainly our re- or pedunculate. Santos (1966), however, suggested sults suggest independent evolution of unstalked wing that Pseudostigmatidae may have been derived from bases and numerous antenodal crossveins in Aniso­ coenagrionids similar or identical to Leptagrion (a ge- ptera and Calopterygoidea. nus with the frons angulate), based on their common larval habitat of phytotelmata, especially leaf axils of bromeliads. Ramírez (1997), too, based on larval morphology, argued for evolution of Pseudostigma- tidae from within Coenagrionidae, although he noted 5. Acknowledgments that similarity in larval caudal lamellae among species inhabiting phytotelmata may be due to convergence. Demarmels (1985, 2007) elaborated this idea in two papers that have received less attention than they de- For the gift or loan of Odonata specimens we thank: Diana serve. His morphological analysis based on larval and Carle, Kristina Carle, Viola Clausnitzer, Rory Dow, Carlos adult characters, although not including Neoneura and Esquivel, Oliver Flint, David Furth, Rosser Garrison, Paul Argia, is fully consistent with our conclusions. He rec- Grant, Andre Gunther, Jochen Lempert, Bill Mauffray, ognized the validity of Kennedy’s subdivision of the John Michalski, Rodolfo Novelo, Elyse O’Grady, Den- Nehalennia-Telebasis Series into a “-Ne­ nis Paulson, David Pryce, Graham Reels, Richard Rowe, Jeff Skevington, Gunther Theischinger, and Keith Wilson. halennia- Series”, characterized principally Supported by NSF Grant DEB-0423834 and the New Jer- by an articulated ventrobasal spur on each male cer- sey Agricultural Experiment Station; NJAES Publication # cus, a structure absent in the “Ceriagrion-Telebasis- D-08-08190-03-08. Metaleptobasis Series”. The former is represented in our phylogeny by a group comprising Chromagrion and Nehalennia. Note that, although clearly placed in this subgroup by virtue of their articulated cercal spur, the frons of Bromeliagrion, Chromagrion and Pyr­ rhosoma is rounded, with vestigial angulation only in the median frontal emargination of the latter two. The Arthropod Systematics & Phylogeny 66 (1) 43

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