SCI. MAR., 60 (1): 17.33 S CIENTIA MARINAADVANCES IN HYDROZOAN BlOLOGYx S PIRAINO, F, BOERO, J. BOUILLON, P.F.S. CORNELIUS and .I.M. GILI (eds.)

1996

Classifìcation and phylogeny in theHydroidomedusae (Hydrozoa, Cnidaria)*

F. BOERO’, J, BOUILLONz and S. PIRAINO3

‘Dipartimento di Biolog?, Stazione di BiologIa Marina, Università dl Lecce, 73lCJJ Lecce, Italy.%dbomtoire de Zoologie, Unwersité Libre de Bruxelles, Ave. F.D. Roosevelt, 1050 Bruxelles, Belgiwn

‘Istituto Spernnentale Talassogmfico “A. Ceruti” del CNR, Via Roma 4, 74100 Taranto, Italy.

SUMMARY: Paraphyletic and polyphyletic taxa in the hydroidomedusae result in pa.rt from the traditional assignment ofsimdar speck to separate genera according to presente or absence of the medusa stage. Medusa reduction 15 wdespread inthe Antho- a n d Leptomedusae a n d has occurred repeatedly in the same clade. Petersen mised this issue far t h eA~thomedusae-Capitata, with a thorough taxonomic re-anangement of the whole group. Advancing !mowledge of lifecycles allows identification of poly- and paraphyly in other hydrozoan groups, so that phylogenetic interpretation of some“anomalies” in the classification of Antho- and Leptomedusae 1s possible. Most diffictdt cases are those leading to “incon-sistent” evolution. It 1s here stressed that the “inconsistency” 1s due to different rates of change of the two main morphs ofthe cycle, whereas it is obvious tkdt the species as a whole evolve consistently. The casa of supposed inconststent evolu-tion considered bere are: Zancleidae vs. Coryntdae (simila hydmids different medusae); Anthomedusae vs. swimmmggonophores (different hydroids similar medusae); Clycia vs. Ohelia (similar hydrolds different medusae); Si~mokxa vs.Hydnchthyx (sitnila hydroids different medusae); Zancleidae vs. Teissieridae (different hydroids simila medusae):C/ytia vs. Phialdla (dlfferent hydroids similar medusae); ~it~~~~mium-campa~e~ium vs. El,cheflota-L~vene~la (differenthydroids simdar medusae); Eutim-Eirene vs, Eu,yymnanthea (similar hydroids different medusae). In sane casa t h eresemblances are due to corwergence, in other cases 1t 1s possible to recognize homologies. Resolution of pamphylies, howe-va, may prove difficult. Laonwdea, far instante, could represent paedomoqzhic speck of both Clytia and Ohelia specie,since the hydroids are similax and the dlfference resides almost exclusively in the gonothecal content. Taxonomy trust repre-sax phylogenetic relationships anong taxa, but has also to be a useful tool to nane taxa and one of its included aims 1snomenclatura1 stabdity. These two goals are difficult to achxve in hydmidomedusan systematics, especially because the rateof dtscovery of new taxa and of new life cycle types is still vo high that the overal pictur? is far from being completed. Farthe s&e of stabihty, it 1s suggested not to emend generic distinctions leading to supposed paraphyly unti1 the fatures of thespecies of such genera have bee” fully studied.

Kq wsords; Hydrozoa, life cycles, paedomorphosis, phylogeny, evolution.

Introduction: delimitation of genera

The taxonomic significante of medusa reduction inthe Hydroidomedusae (see Boero and Bouillon, 1987,for a review on paedomorphosis, and Bouillon et ul.,1992, for a historical review about the many differentnames given to non-siphonophoran Hydrozoa) has

*Received November 18, 1994, Accepted June 9, 1995.

been debated during and since the last century (seeAllman, 1864). In the last decades, it was almost uni-versally agreed that differently developed medusaewere a feature of generic value in a group of specieswith similar hydroids (see Ree& 1957). This was for-malised in detail by Bouillon (1983, who detined ahrecent and fossi1 genera of Hydroidomedusae.Petersen (1979, 1990) criticised this practice of gene-ric distinction, because it leads to paraphyletic orpolyphyletic genera. His arguments, however, were

CLASSlFlCATlOk’ AND PHYLOGENY IN THE HYDROIDOMEDUSAE 17

POLYPHYLETIC GENUS _-_ _~_~__ ._ --_- --. .WTH FIXED I’ULYYHYLbllC- tibNUb

WlTH LIBERABLEMONOPHYLETIC GENUS

GONOPHORES

w=yr c;kkT

GyyEzA1

l ,medusa r e d u c e d t o - /-hberable eumedusoid 1fl

- /medusa reduced tol fixed gonophore \/

FIG. 1. - Hypothetical cladogmn showing possibk caos of paraphyly and polyphyly when using medusareduction as a generic chamcter (see test fm detailed explanamn).

somehow cryptic within the wide-scoped papers con-taining them, SO that few authors recognised theirvalue. The line of reasoning of Petersen could beexplained by the following example (Fig. 1): a species(A) with me-dusae is the ancestor of a clade compri-sing three species with different medusa expression: -Al still has medusae and, if not much modified, canstili be included in the ancestor’s genus; -B has medu-sae reduced to liberable eumedusoids (see Boero andBouillon, 1993, for a recent assessment of life cycletypes of Hydroidome-dusae), this should be enough toconsider it as the founder of a new genus, based on thedifferente between a long-lived medusa, with compli-cated structures, and a liberable eumedusoid, living afew hours and simply carrying the gametes; -C hasfixed gonophores, with complete suppression of themedusa stage, again an important morphological featu-re or, better, the absence of an important morph, also,this species should be the founder of a new genus.

This taxonomic treatment of the “tirst genera-tion” clade deriving from A is apparently logical,but implies a big phylogenetic inconveniente if a“second generation” evolves from the first one. The

18 F. BOERO et al.

three species, in fact, could be the ancestors of otherclades, for simplicity considered as composed ofthree species each,

The clade deriving from Al, the species whichretained the medusa stage, could show the same evo-lutionary pattern as the clade originated by theancestral species A, originating a species (A2) withmedusae, a species with liberable eumedusoids (D),and a species with fixed gonophores (E). At thispoint, a taxonomic distinction of genera with freemedusae, liberable eumedusoids and fixed gonopho-res would again be possible.

The second species, B, with liberable eumedu-soids, could be the ancestor of a clade made by twospecies (B 1 and B2) with liberable eumedusoids, butone species (F) could undergo paedomorphosis andhave fixed gonophores.

The third species, C, with fixed gonophores,could be the ancestor of two species with fixedgonophores (Cl and C2), but the last species of theclade (G) might have evolved new motile sexual sta-ges, such as swimming gonophores (see Boero andBouillon, 1989a).

Monophyly, paraphyly and polyphyly

In this hypothetical phylogenetic pattern, thepolyp stage of al1 species remained conservative, SO

that the most “differentiated” set of characterswould be the strutture of the gonosome. But thegenus identified by the possession of fixed gonop-hores would comprise species deriving from the spe-cies C of the “first generation”, that is Cl, C2, butalso some deriving from Al and B, namely E and F,originated by independent paedomorphic processesin the “second generation”. This means that thegenus with fixed gonophores would comprise spe-cies derived from different ancestors, SO b e i n gpolyphyletic. The same is valid for the genus withliberable eumedusoids. However, the genus withmedusae would be paraphyletic because it wouldcomprise not al1 the species deriving from a singleancestor. Some of the species deriving from the firstancestor (A) would fa11 in the genera with liberableeumedusoids (B) and with tixed gonophores (C),and also would the species deriving from the firstspecies of the “second generation”(D, E).

Such a situation led Petersen (1979, 1990) torefrain from considering medusa reduction as ageneric feature if not accompanied by other impor-tant modification at the hydroid stage. This implieddeep alteration of the definition of genera, a task thatPetersen (1979, 1990) attempted for the Anthome-dusae, Capitata.

Petersen’s solution

TO solve such phylogenetic inconsistencies inhydroidomedusan systematics, Petersen (1979,1990) proposed a thorough re-evaluation of the cha-racter sets of both stages (where both exist), SO as tosingle out the apomorphic characters and have adouble check of the hypotheses of phylogenetic rela-tionships implied by generic classification. When aspecies with medusae is referred to the same genusas a species lacking them, the hydroid is the onlyfeature that allows comparison between the twotaxa. This is particularly evident in the classificationproposed by Petersen (1979, 1990) of theCorynidae, in which the distinctions among Coryne,,%u+L, and Dipurena allow identification to genuseven of sterile hydroid material. According toPetersen (1979, 1990), the medusae produced byhydroids with a consistent set of apomorphic cha-racters (besides the gonosome) should have a con-sistent set of apomorphic characters too. But recog-

nition of such apomorphic characters might prove dif-ficult and the above-mentioned phylogenetic hypot-hesis for the classification of the Corynidae isencountering problems in its application, as remarkedby BrinckmannVoss (1989) Kubota and Takashima(1992), Pagès et UL (1992), and Bouillon and Groh-man (1994) who found inconsistencies in Petersen’sprinciples when applied to their corynid material: thehydroid “apomorphic” character sets recognised byPetersen (1979, 1990) did not match those postulatedfor the medusae, nor did the distinction of differentfunctional regions in the manubrium of the differentgenera. This recalls what Naumov (1960) (recentlydiscussed by Boero and Bouillon 1987, Boero andSarà 1987) has already described as “inconsistentevolution” (see Rees, 1957), a concept recognizingthat the rate of hydroid evolution can be differentfrom that of the medusa. The plasticity of the group,with wide “freedom” of modification of the two sta-ges, could lead to completely different character setsin related species, or to such parallelisms to make dis-tant species look similar. This has caused difficulty ofinterpretation by taxonomists, causing problems informing valid genera for both hydroids and medusae.Petersen (1979, 1990) stated that proper characterchoice for both stages is the only solution and that“inconsistent evolution” is an artefact linked to cha-racter choice. It is out of the question that a monophy-letic group of species, sharing a “phylogeneticallyproximal” common ancestor, should be included in ataxon of higher rat& than species, reflecting theirseparation from other monophyletic clades. The nea-rest taxon to species is genus, SO such group of spe-cies should be included in the same genus, in spite ofmorphological differences.

It is not surprising that Petersen (1990) deniedthe value of “inconsistent evolution”: his system ofclassification works only if hydroids and medusaeevolve in a parallel way within the same clade,otherwise the clues that they provide are misleading,especially when the medusa is abolished and classi-fication is based on hydroids only. Petersen (1990)stressed how characters were not properly chosen bymany former authors and that good descriptions andfigures are the only method for detecting phylogenywhen doing systematics. But Petersen (1990, p.224), for instante, compared Zanclea with Te&eraon the basis of the different position of ocelli in thetwo genera (although Zancleu has no ocelli), or figu-red the medusa of Pterodava kreqfi as beingdeprived of exumbrellar nematocyst pouches (p.139), whereas these are present.

CLASSIFICATION AND PHYLOGENY IN THE HYDROIDOMEDUSAE 19

T h e conceptual f r amework introduced byPetersen (1979, 1990) appears soundly based whencriticising the current system of generic classifica-tion of hydroidomedusae, but the solution to the pro-blem, envisaging a constant evolutionary rate in bothhydroids and medusae, poses other questions, espe-cially when the rate of change is different in the twomain stages of the hydroidomedusan cycle.

The use of genetic characters

Cunningham and Buss (1993) opposed Peter-sen’s (1979, 1990) proposal for generic distinction,as applied by him to the Capitata, to the traditionalone, as applied by Boero and Sarà (1987) for theCampanulariidae. Boero and Sarà (1987), in fact,simply applied almost literally the practice of consi-dering the degree of medusa reduction as a soundgeneric character, arranging the genera of theCampanulariidae along a trend of decreasing medu-sa “expression”. Cunningham and Buss (1993) tes-ted the value of the two hypotheses by applyingthem to the main genera of the Hydractiniidae(Anthomedusae, Filifera), a family showing a clas-sica1 example of generic distinction based on medu-sa reduction: Podocoryne with medusae, Stylac-taria with liberable eumedusoids, and Hydractiniawith fixed gonophores. Comparison of fragments ofthe DNA sequence encoding mitochondrial largeribosomal subunit RNA of representatives of thethree nomina1 genera showed lack of consistency inthis generic distinction, supporting Petersen’shypothesis. It is to be expected, however, that medu-sa reduction is not a good taxonomic character in afamily such as the Hydractiniidae. In this family thedegree of medusa reduction is rather high in thethree main genera, even though their current dis-tinction is based mainly on medusa expression. Themedusae of many species of Podocoryne, in fact,are liberated with almost ripe gonads and live just afew days before spawning and die. It is probablethat such medusae are liable to further accelerationof gamete maturity, leading to reduction to liberableeumedusoids with a short life spari. Medusa reduc-tion to liberable eumedusoids may well have happe-ned independently in many species (Petersen,1990). The step from liberable eumedusoid to fixedgonophore might also have happened independentlymany times. In the Hydractiniidae, generic distinc-tion based on medusa reduction seems impracticaleven by considering morphology and life cycle pat-tem only.

Genetic analysis provides just an additional set ofcharacters and, while it can be conclusive in speciesdefinition, it is less clear in the definition of genera,If, for instante, two species (a, A) are near the bran-ching of two large clades (Fig. 2), they could begenetically (and phenetically) more similar to eachother than they would seem similar to distant speciesof their respective clades (g-a, A-D) (see discussionof Mitrocomium and Eucheilota below). Geneticanalysis operates somehow phenetically, a comple-tely different “philosophy” from cladistics. A smallchange in the genome might resuh in the evolution ofan apomorphic character involving the origin of anew clade (e.g. a genus), whereas other genomicchange might involve simple variation (e.g, specia-tion within the same clade-genus). This is particu-larly clear when considering that the magnitude ofthe phenotypic effect of genetic mutation can varywithin a morphogenetic tree (Arthur, 1988), SO that agenetic change occurring early in development mighthave greater effect than one of a genetic change of(apparently) the same magnitude but on a gene actinglater in development. Wray (199.5), however, pointedout how early developmental mechanisms related toecologica1 adaptation of an early stage in the lifecycle may not follow this rule.

The test by Cmmingham and Buss (1993) of thehypothesis giving generic weight to the degree ofmedusa reduction is thus not conclusive, eventhough it might be reasonable that the hypothesis isto be rejected if applied to the Hydractiniidae. But,in accordante to what was stressed by Buss (1987)who convincingly showed that some important para-digms of biology are good for some groups and badfor others, the same hypothesis could prove soundwhen applied to other families.

In the light of the above considerations, it isworthwhile reconsidering the Campanulariidae,attempting a phylogenetic reconstruction at genericleve1 by following Petersen’s (1979, 1990) practice.

The Campanulariidae

The Campanulariidae is a compact and well defi-ned family of Leptomedusae. It is probably the bestknown family of al1 Hydroidomedusae, due to itscosmopolitanism in coastal waters and to the nume-rical abundance of its representatives. Its main cha-racter is the peduncled hypostome of the hydranth.Its medusae have much differentiated features.Comelius (1977) remarked how the link of medusanand hydroid stages in the Campanulariidae goes

20 F. BOERO et al.

gf ed c ba A B C D E F G

F I G. 2. - Hypothetical cladogram showmg splitting of two clades, each witb a long “history”, so thatthe first species of the two clades, tbose near the branching, have a higher overalI similxity with each

other than wth phylogenetndly distant specxs of their same clades.

back to the times of the early recognition of complexlife cycles in the hydrozoans. The great resemblanceof hydroid stages caused keeping in the same familysome genera with much different medusae, such asClyliu and U&&Z. Such taxonomic decision impliesgiving more phylogenetic weight to resemblances ofthe hydroids than to differences of the medusa sta-ges and has been accepted by ah specialists, even bythose used to consider the medusa stage only. Al1agreed, and agree, in keeping ClyfL~ and ~LJ&u inthe Campanulariidae, accepting for this case thetaxonomic importance of hydroid over medusanmorphology.

Cly& formerly known as Phialidium by medu-san specialists, is a typical leptomedusa, with noparticular features allowing its distinction fromother genera, SO that, for instante, Russe11 (1953) inhis pictorial key of the medusae of the British Isles,reported Clytiu hemisphuerica as identica1 withPhiulellu quadrutu on the basis of general morpho-logy, the medusae of the two species being identifia-ble only because P. quadrutu has a fixed number ofstatocysts, whereas in C. hewkphuericu the numberof statocysts increases with age. Their hydroids, onthe other band, are much different: Clytiu has openhydrothecae and stalked hypostome, whereasPhiulellu has operculate hydrothecae and conicalhypostome. The medusae could well be referred tothe same genus, but the hydroids are cmrently refe-rred to separate leptomedusan suborders, Phiulellabeing included in the Conica and Clytiu in theProboscoidea (see Bouillon, 1985).

Obeliu (see Comelius, 1975, 1982, 199Oa) is oneof the most widespread hydrozoans, SO that classicaItextbooks (e.g, Barnes, 1980; Pearse et ul., 1987;Barnes er ul., 1988; Brusca and Brusca, 1990) provi-de detailed drawings of both the hydroid and themedusa stages as an example of altemation of “gene-rations” in the Hydrozoa. But the medusae of Obeliuare far from being typical hydromedusae. Their morphology is in fact SO particular that Boero and Sarà(1987) (but, before them, also Bouillon; Edwards;Petersen, unpublished) proposed that they could be acase of medusa re-expression from reduced medusae.The re-expression of features that were lost in the phe-notype indicates that they are stili coded in the genoty-pe and this phenomenon is known as atavism (seeMcKinney and McNamara, 1991 p. 185, for a reviewand examples, including limb re-expression in wha-les). This view was questioned by Comelius (199Ob).

The above mentioned resemblance betweenClytia and Obelia hydroids opposed to the differen-ces in their medusae, or the similarity betweenPhiulellu medusae with those of Clytia opposed tothe differences at the hydroid level, suggest thathydroids can remain conservative while medusaechange, or vice versa.

The medusu qf Obelia

The medusa of Obeliu is SO different from al1other hydromedusae that if its hydroid were unk-nown it could well be placed in a separate class ofCnidaria. The peculiarities of Obeliu are as follows:

CLASSIFICATION AND PHYLOGENY IN THE HYDROIDOMEDUSAE 21

e -gonadsYoung 0b&a l~~gis+ra medusae have gonads

developing from the four corners of the tnanubrium,where the radia1 canals originate. As the medusagrows, the gonads become separate from the manu-brium and become isolated on the radia1 canals. InObeliafimbriata they are peduncled.

In Leptomedusae, gonads usually derive from theradia1 canals and are seldom connected to the manu-brium (but see A4odeeria, some Laodiceidae andsome Melicertidae for exceptions). At least in someObelia, the position of the gonads is thus differentfrom almost al1 other Leptomedusae.

What is the medusa ofobelia?

Gravier-Bonnet (1992) described a hydroid(Zeulonies estrambordi) with deciduous hydranthsthat can live for some time in the water column andthen settle on a proper substratum to originate anew colony. The medusae of Zeulonies are similarto those of Clyfia, but the hydroid features areintermediate between the Haleciidae and theCampanulariidae. The discovery of Zeulorziesestrambordi demonstrates that hydranths of theca-te colonia1 hydroids can be released and live anindependent life in the plankton. On the one band,their ontogeny is different from that of medusaebecause they are not formed from a medusarynodule deriving from the lateral budding of apolyp. On the other band, polyps also derive fromother polyps by budding. In Zanclea (Gravili,unpublished observation) the hydranths can budother hydranths from the zone whence medusae arenormally budded.

The possibility of hydranth detachment in can-panulariid-like species leads to further speculationabout the nature of Obelia medusae.

Boero and Bouillon (1989a) proposed an inter-pretation of anomalous medusoid stages, invokingthe possibility of gonophore-medusa mosaics, lea-ding to already described structures that they calledswimming gonophores. The origin of the medusaof Obelia, a morph with an astonishing series ofhydranth (tentacles, hypostome), origina1 (absenceof velum, statocyst position, unique striated mus-cle, mode of swimming) and medusan (gastrovas-cular system, statocysts) features, could be explai-ned by a similar phenomenon. The medusa ofObelia might have originated from hydranthswhich became detached by a process similar to thatdescribed in Zeulonies estrambordi, and which,

together with features specialised for a planktoniclife, acquired also the possibility of becomingsexually mature (Fig. 3).

This alternative hypothesis to that of the “atavis-tic” origin of Obelia medusae (Boero and Sarà, 1987)will be substantiated or refuted by further detailedanalysis of the ontogeny of these medusae. But theillustrations of Ktihn (1913) (reproduced in Fig. 4)showed that in “normal” medusa development thevelum is formed from two ectodermal layers, enclo-sing a subumbrellar cavity that will open when thevelum is completely formed (Fig. 4A). But in Obelia(Fig. 4B), there is no velum even during develop-ment, and the subumbrellar cavity is virtual since it isclosed only by the outer membrane wrapping thedeveloping medusa. Such morphogenesis is astonis-hingly similar to that of developing hydranths.

FIG. 3. - Schematic reconstruct~~~ showing the similatities betweenfJ!x?k~ medusae (A) and campanulariid hydranths (BI.

The meconidia of Gonothyraea

Miller (1972) studied the functional morphologyof the meconidia of Gonothyraea, reporting on theexceptional feature of their tentacles, used to “cap-ture” the spermatozoa and direct them into themeconidium, where fertilization occurs. The tenta-cles of the meconidium are chordal, and SO o fhydranth affinity, as those of Obelia medusae.Furthermore, meconidia are deprived of radia1canals (but Allman, 1871-72, figured them) andhave gonads on the “manubrium”. If interpreted in

CLASSIFICATION AND PHYLOGENY IN THE HYDROIDOMEDUSAE 23

RC

FIO. 4. - Developmental stages of the medusae of Sarsk tubulosa (as Syncoryne w-sii) (A) and of Obeiiadichotoma CB). GC: gastra cavity; M outa membrane; RC; radia1 canal; SC: subumbrellar cavity;

T: tenta& bu& V velum (afta Ktih,,, 1913, A: p. 161; B: p. 156).

the light of Boero and Bouillon’s (1989a) proposal,meconidia do not have a manubrium but a spadix,and are in the series of swimming gonophores. Inthis case, however, besides producing the gametes,they work also as brood chambers, where fertiliza-tion and planula development occur.

Monophyly, polyphyly and paraphyly in theCampanulariidae

P!z~uMu, having almost identica1 medusae toClytia, is here considered as an outgroup to theCampanulariidae. Bouillon (1984) obtained a

24 F. BOERO et a/

hydroid with peduncled hypostome from the medu-s a o f Pkiuhcium mbenga. T h e medusae o fPkiuhcium differ from those of Clytia in havingrudimentary tentacular bulbs and excretoq pores.Both outgroups piace Clytia at the base of the cam-panulariid clade (Fig. 5).

Stolonal species of Clytiu represent a rather com-pact group, but some species (e. g. Clytiu lineuris)are erect and then in this resemble Luomedea,Gonofkyraea and 0beIia colonies. Furthermore, thecolonies of Clytia wziver&ah are fascicled, and itis possible that complication of colony architettureand increased hydroid efficiency made medusareduction advantageous, with the origin ofLaomedeu-like colonies with erect stem derivingfrom paedomorphic C.Iytia-like species which sup-pressed the medusa. This, according to the generalsuggestion of Petersen (1979, 1990) could haveoccurred independently in severa1 CLytia-like“ancestors”, SO that Luomedea could be polyphyle-tic (as suggested by differences in hydranth morp-hology such as, for instante, the presente of an

in te r t en tacu la r web; see Cornelius, 1987), andClytia could be paraphyletic. Some Luomedea-likespecies, with reduced gonophores, could have evol-ved the specialised meconidia that characteriseGonotkyruea. Meconidia are too specialised to haveoriginated independently in different species, andthe low number of known Gonotkyraea species sug-gests a recent origin. Of course, some Gonotkyrueaspecies might have reverted to fixed gonophores,thus retuming to a Laomedea-like strncture. Thiswould lead to paraphyly for Gonotkyraea, at presentan unavoidable risk.

The same argument runs for the few recognisedObeliu species, too specialised and origina1 to be ofconvergent origin, but again liable to have undergo-ne some events of paedomorphosis to fixed gonop-hores, thus resembling Luomedea, again with thepossibility of paraphyly for the genus.

The “weakest” genus in the whole clade isLaomedea, being derivable from independent pae-d o m o r p h i c events in Clytia, Gonotkyraeu andObelia.

CAMPANUIARIINAE

peduncled hypostome

FIG. 5. - Hypothetical relationships anong the recent genera of the Campanulariidae.

CLASSIFICATION AND PHYLOGENY 1N THE HYDROIDOMEDUSAE 25

T h e crucial character of this c lade ( theObeliinae) is the presente of a true diaphragm(Cornelius, 1982).

The clade with annular thickening, theCampanulariinae, not having true medusae, is of sim-pler analysis at generic level, and the hydroid-basedgenera Orthopyxis, Siliculurìa and Campanulariucan be retained as valid, as discussed by Comelius(1982) and re-defined by Bouillon (1985).

The phylogeny of the Campanulariidae proposedby Boero and Sarà (1987) seems only partly correct,and can be integrated with the scheme proposed byComelius (1982), to cape better with Petersen’s(1979, 1990) suggestions (Fig. 5). Gonothyraea, forinstante, has a problematic position in Boero andSarà’s (1987) diagram, since it is considered as anintermediate step between liberable eumedusoidsand fixed gonophores, whereas it is here interpretedas a specialised morph, possibly deriving from furt-her evolution of fixed gonophores. The presente of atrue diaphragm opposed to that of an annular thicke-ning and a subhydrothecal spherule in the hydroid, asaccepted by Cornelius (1982) (and, before him, bymany others), divides the family into two subfami-lies: the Campanulariinae (with annular thickening)and the Obeliinae (with true diaphragm).

Some taxonomic adjustments

The most reasonable outcome of the presentanalysis should be to merge Laomedeu into C!yriqbut we refrain from doing SO because Luomedeacould also contain Gonothyraea and Ohelia specieswhich lost by reduction their specialised gonoso-mes. This decision of retaining Luomedeu as validis due to conveniente, and is provisional, due tolack of knowledge of proper characters to infer affi-nities.

The genus Hartlaubella could der ive frommedusa reduction in Clytia or Ob&z-like fascicledcolonies. Al1 the above discussion shows that gene-ric distinction based on medusa reduction only isnot well grounded, and Hurtlaubellu is merged intoLaomedeu, here retained as a convenient “contai-ner” for Obeliinae with fixed gonophores. Sinceboth Laomedea and Hurtlaubella (referred to theObeliinae) could be merged into Clytiu, there are nogrounds to retain as valid a subfamily for Clytia (theClytiinae), as proposed by Comelius (1982) andsome other authors before him. Boero (unpublishedobservation) reared medusae which grew multiplemouths (SO resembling Gastroblasta) from a still

undescribed Mediterranean C/ytia hydroid symbio-tic with sponges. It is thus highly possible thatGastroblasta will be recognised as identica1 withClytia.

It is difficult, at present, to ascertain if the gene-ra of the Obeliinae are monophyletic. The specieswith Ob&z-like medusae are evidently of commonorigin, but it is impossible to decide, on the basis ofhydroid characters, if in some of these species thenewly originated medusae regressed again to fixedor swimming gonophores. It is evident, at this point,that other generic features must be searched for, butthey seem, at present, undetected. Al1 species of theObeliinae have a distinct diaphragm delimiting abasa1 hydrothecal chamber, but no other consistentfeatures (besides gonophore strutture) seem to iden-tify them. The unilìcation of al1 these species into asingle genus (as suggested by Broch, 1909) could atpresent be the only practical solution, representing,however, some sort of surrender to the difficulties ofthe case. The proposal of sub-genera with the namesof the formerly recognised genera is not practical,since they have the same inconveniente as the gene-ra. The Obeliinae represents too a heterogeneousclade to be ascribed to a single genus. Hydranthmorphology, as described by Comelius (1987), is ofspecific value but is not a good generic character, atleast in the Campanulariidae.

The genus Tulpu, included by Comelius (1982)into the Clytiinae, has an annular thickening and nota diaphragm (see Bouillon, 1985), thus fitting intothe Campanulariinae, an opinion already expressedby Calder (1991). Its main distinction fromCampanuluria, however, is based on the much largersize of the hydrotheca, This feature is here regardedas having doubtful generic value. Rhizocuulus (orVerticillina) is distinguished from Campanularia onthe presente of fascicled stems and to the verticilla-te arrangement of the hydrothecae. Vervoort (1987)remarked how Campanuluria volubilk is practicallyidentica1 with Rhizocuulus verticillutus in hydrothe-tal and gonosomal strutture, the two forms beingdistinguishable only because the tirst is stolonal andthe second is fascicled and has verticillate hydrothe-tal arrangement. In other genera, both in athecates(e, g. Eudendrium and Bouguinvillia) and thecates(e. g. Clytia, Obelia, Halecium and Sertularella) thepresenze of a fascicled stem is not an accepted gene-ric feature and it is unconvincing as such in theCampanulariinae, if not accompanied by some otherderived feature. This is accepted, for instante, forOhelia, comprising 0. dichotomu and 0. geniculatu

26 F. BOERO et al.

with simple stems, and 0. bidentatu and 0. longissi-ma with fascicled stem. The spira1 arrangement ofthecae is not only recognised as having no genericvalue in Obelia, and is even treated as having no spe-cific value, so that 0. spiralis was considered byCornelius (1975) as conspecific with 0. dichotoma.Boero (198 1) showed that the kirchenpaueriidVentromma halecioides can have simple or fascicledstems according to the intensity of water movement.Bavestrello and Ceriano (1992), furthermore, sho-wed that, at least in Eudendrium glomeratum, fasci-cled colonies derive from the gregarious behaviour ofplanulae and are SO colonies of colonies. Tbe onlycharacter allowing distinction of Rhizocaulus fromCampanzdariu is the verticillate arrangement of the-cae. The generic value of such feature is here retai-ned as doubtful, SO that Rhizocuulus is tentativelymerged into Campunulariu.

“Inconsistent evolution” strikes back

Boero and Bouillon (1987) demonstrated that, inmany lineages, hydroids and medusae evolve in aconsistent way and used this evidente to discardNaumov’s (1960) proposal of “inconsistent evolu-tion”. In a note to their paper, however, Boero andBouillon (1987) recognised that cases existed inwhich hydroids apparently evolved differently frommedusae, as stressed also by Boero and Sarà (1987).The fact that in many cases the morphological evo-lution (i.e. change in anatomy) of hydroids andmedusae proceeds at the same pace does not implythat this has to be always SO. Petersen (1990, p. 224)said that “both stages (hydroids and medusae) showmorphological differences consistent with the con-cepts of their phylogeny, although these differencesare certainly different in magnitude between hydroidand medusa”. The concept of “inconsistent evolu-tion” does not imply that medusan phylogeny is dif-ferent from that of hydroids, and is exactly whatPetersen calls “differences of different magnitudebetween hydroid and medusa”. This means, for iris-tante, that a hydroid could “slow down” its evolu-tion in terms of morphological change betweenancestral and derived forms, whereas the medusacould “accelerate” its evolution in the same terms(or vice w-su). In summarising Naumov’s “incon-sistent evolution” Petersen (1990, p. 222) said“Naumov explained... the fact that closely relatedhydroids can produce very different medusae or Gceaeree... by differences in rate and direction of evolu-tion in the two generations depending on their diffe-

rent relations to environment”. Maybe the differen-ces envisaged by Petersen between “differente inrate and direction of evolution in the two genera-tions” (Naumov’s explanation) and “differences ofdifferent magnitude between hydroid and medusa”(Petersen’s explanation) referto the fact that he inter-preted Naumov’s ideas as if he were convinced thathydroids and medusae are phylogenetically dista@otherwise we cannot see any differente between themechanisms invoked by Naumov and Petersen toexplain the inconsistencies between hydroid andmedusan morphologies. The word “evolution” usedby Naumov does not mean “phylogeny” but simply“change”, since Naumov was SO aware that hydroidsand medusae are phylogenetically the same thingthat he was the first to publish a monograph mergingthe classification of the two stages!

It is obvious that hydroids evolve together withtheir medusae as a single phylogenetic unit, but thisdoes not mean that different rates of change actuallycause trouble to those attempting to reconstruct ataxonomic system reflecting phylogeny. Thus, weaccept the concept of “inconsistent evolution” interms of “inconsistent change” but we discard it if itis meant in terms of “inconsistent phylogeny”, aconcept that, however, no-one has expressed. Asimilar phenomenon has been referred to as “uncou-pled evolution” by Wray (1995): echinoid specieswith similar adults and different larva1 stages indica-te that environmental constraints acting on larvaemay cause changes in development which do notinfluente adult ecology and morphology.Hydroidomedusan life cycles, however, have a muchwider array of variation than echinoid life cycles and“inconsistencies” may occur both at the hydroid(larval) and medusan (adult) stage.

If the species and genera showing “inconsisten-cies” between hydroid and medusa morphologiesare phylogenetically related, their relationshipsshould be detectable by a careful analysis, asPetersen (1990) remarked, Otherwise, since theirapparent resemblance in one stage might be due toconvergent evolution, polyphyletic taxa might beaccepted.

Cases of inconsistent evolution can be explainedin two ways:

1: they represent events of convergent evolutionof unrelated species (the inconsistency being resol-ved by showing analogies),

2: they are the outcome of a differente in the rateof change in the two stages (the inconsistency beingresolved by detecting homologies).

CLASSIFICATION AND PHYLOGENY IN THE HYDROIDOMEDUSAE 2?

The two possibilities are not mutually exclusive,SO that both analogies and homologies can be foundin different characters in any one group.

Phylogenetic resolution of “inconsistentevolution”

The following is a series of examples in whichapparent phylogenetic inconsistency can be resolvedby character analysis.

Fully founed medusae vs reduced medusae

Al1 phylogenetically related species belonging toclades (classified as genera) in which medusa reduc-tion has occurred repeatedly are similar in theirhydroids but are different in the content of theirgonosomes: a fully formed medusa or a reducedmedusa. As remarked by Petersen (1979, 1990),

homology is thus apparent in the hydroid only, whe-reas the differences in the medusa are due to “incon-sistent evolution” in the sense accepted above.Homologies of hydroid leve1 should thus allowinclusion of species with and without medusae in thesame genus.

Zancleìdae vs Corynìdae

Naumov (1960) regarded the Zancleidae and theCorynidae as an example of inconsistent evolution,showing that their hydroids are similar, whereastheir medusae are much different. The differencesbetween zancleid and corynid hydroids, however,are currently recognised as being great (Bouillon,1985; Petersen, 1990), the shared character of scat-tered capitate tentacles being treated as plesiomorphic, and both cnidome and hypostome features asapomorphic.

LUKVX~U 2.tentacled Nudiclava

\ medusa

paedomorphosis\ /\

jdrichthys 5.6.tentacled\

suppressic

!\l Il \ medusa /

medusam

JJLStomotocu “normal” hydroid

. 2.tentacled medusa 7-4paedom>rp+oi 0 Ichthyoparasitic

.

FIG. 6. Hypahekal relatiomhips amm~ mmt ichthyopamitic hydroids and related form.

Anthomedusae vs swìmmitq gonophores

Boero and Bouillon (1989a) proposed a solutionto the taxonomic incongruente of severa1 thecatehydroids producing “medusae” with gonads on themanubrium, in that character state apparently resem-bling typical Anthomedusae. They interpreted suchmorphs as mosaics of fixed gonophores and medu-sae, their resemblance to Anthomedusae being dueto analogy.

Clytia vs Obelia

A similar case is that of Clytiu and Obelia, withsimilar hydroids and much different medusae. Thismight be explained alternately by medusa re-expres-sion by atavism, or by considering the medusa ofObeliu to be derived from detached hydranths whichacquired both sexuality and adaptations to plankto-nic life (see above).

Stomotoca vs Hydrichthys (Fig. 6)

The medusae referred to the nomina1 speciesStomotoca pterophylla and Stomotoca atra, sharingthe feature of having just two tentacles, have beenshown to have much different hydroids. Larson(1982) described a Hydrichthys-like hydroid ofStomotoca pterophylla, whereas Boero and Bouillon(1989b) described a non parasitic hydroid ofStomotoca atra. Boero et al., (1991) described themedusa of Hydrichthys mirus, clearly related toLeuckarzìura, and considered the resemblance bet-ween Stomotoca atru and Stomotoca pterophylla asdue to convergent paedomorphosis: al1 pande idmedusae are released with only two tentacles, S O

that such a morphology could be easily acquired byheterochrony. Hydrichthys hydroids vvere interpre-ted as having originated from the Leuckurtiuru line-age (as suggested by the medusa of H. mirus) withspecialisation of hydroids to parasitic life on tìshes.The clade of parasitic hydroids remained conserva-tive at the hydroid level, whereas the medusae chan-ged morphology through paedomorphic events,becoming similar, by convergent evolution, toStomotoca. This case demonstrates both analogiesof the medusa between Stomotoca and Lursonia,proposed by Boero et al. (1991) to accommodatespecies with ichthyoparasitic hydroids and paedo-morphic medusa, and homologies betweenHydrichthys and Larsonia, in which the hydroidshave maintained a constant morphology, whereas

the medusae have changed. This is a clear case inwhich evolution (in terms of change) has proceededat a faster pace in the medusae than in the extremelyspecialised hydroids.

Zancleidae vs Teissieridae

The medusae of Zunclea and Teissieru are iden-tical in their general body plan, the only recogniza-ble differente being the presente of ocelli inTeissiera, a feature of no family value in otherhydromedusae. But their hydroids are SO differentthat family distinction is universally accepted (seeBouillon, 1985 and Petersen, 1990).

The differente between Zuncleu and Teissierahydroids, and the resemblance between their medu-sae, can be related to the similar environments of themedusae (a planktonic life) and to the different envi-ronments of the hydroids (association with serpulidopercula in Teissieru and with bryozoans or molluscshells in Zancleu). TO explain such differences with“differente in rate and direction of evolution in thetwo generations” or with “differences of differentmagnitude between hydroid and medusa” is exactlythe same.

It is out of question that Teissieru and Zuncleaare phylogenetically related, but it is highly probablethat the modified hydroids of Teissiera derive from asingle evolutionary event, so that they form amonophyletic clade, distinct from that of Zuncleu.The hydroids suggest analogy leading to splitting,whereas the medusae suggest homology leading todumping: a quite inconsistent pattern. The opinion ofBouillon (1985) of keeping Zunclea and Teissiera inthe same superfamily (the Zancleoidea) explains thehomology of the medusae, whereas their assignmentto distinct families (the Zancleidae and theTeissieridae) is consistent with the differences in thehydroid stages.

Clytia w Phialella

As remarked above, Clytiu and Phialella havemedusae which can be distinguished (at the leve1 ofgross morphology) only by constancy of statocystnumber in Phìalella and increase in statocyst num-ber with age in Clytiu. At present no other diffe-rences are known between the medusae, whichmight be placed in the same genus if their hydroidswere unknown The comparison of the hydroidsshows two main differences that will be analysedseparately.

CLASSIFICATION AND PHYLOGENY IN THE HYDROIDOMEDUSAE 29

1 - The hydrotheca of Phialellu is operculate,whereas that of Clytia is not. This differente is notas great as it seems. Clytia hydranths develop in clo-sed hydrothecae that open when the hydranth is fullygrown. The lines of rupture of the formerly closedhydrotheca conform to the cusps of the hydrothecalrim. The hydrothecal cusps remain erect and caotcontract anymore in the position that they had whenthe theca was sealed. In Phiulella the cusps formingthe operculum can close even after rupture of theoperculum. Such differente involves a small evolu-tionary step, SO that Clytia and Phialella could beconsidered as phylogenetically strictly related.

2 - The other differente is the presente of apeduncled hypostome in Clytia, a feature shared byal1 Campanulariids. Its presente sharply separatesClytia from Phialella and accounts for assignmentof Clytia to the Proboscoidea and of Phiulella to theConica. At present it is not clear if the resemblancesbetween the medusae are due to convergente, or ifthe differences at the hydroid stage are due to“inconsistent evolution”, with conservative medusaeand rapidly changing hydroids.

Mitrocomium-Campalecium vs Eucheilota-Lovenella

Calder (1991) resurrected the genus Mitro-comium to accommodate the species with haleciidhydroids and with &&ze~lotu-like medusae. Heascribed Mitrocomium to the Haleciidae (Halecioi-dea) due to the morphology of the hydroid, but themorphology of the medusa suggests placement inthe Lovenelloidea. Boero and Sarà (1987) proposedan exphmation for this inconsistency, postulatingthat Eucheilota and Campalecium were phylogene-tically related but that their medusae remained simi-lar whereas their hydroids underwent great diver-gence, Wemer (1968) showed that 10~s of hydrothe-ca is frequent in Eucheilota, and such loss makesthe hydrothecae resemble those of the haleciids.Boero and Sarà (1987) suggested that the ancestorof the haleciids was an eucheilotid which lost thehydrotheca and acquired strong nematocyst protec-tion, thus “becoming” a haleciid. The phylogeneticrelationship between haleciids and eucheilotidsremains evident in the medusae, whereas it is theirseparation which is evident in the hydroids. If theproposed interpretation is correct, this example isimportant to show how species referable to phylo-genetically separated clades can still remain moresimilar to each other than to species of their same

clade. The resemblances between Mitrocomìumand Eucheilota (assigned to different clades), infact, are greater than those between Mitrocomiumand Halecium (assigned to the same clade). Whenclades split, the species which are near the separa-tion might maintain an overall similarity somehowmasking the change that led to clade separation.Only further morphological diversification withinthe separated clades might lead to great overalldivergences, SO that the extremes of the same cladeseem more differentiated than the adjacent ones oftwo separate clades.

Eutima-Eirene V.Y Eugymnanthea (Fig. 7)

Kubota (1983) reconstructed the evolution ofbivalve-inhabiting hydroids, showing that they deri-ved from l%timu-like hydroids which acquired acommensal habit. In some species the medusae didnot change much, SO that there are Eutima specieswith free colonia1 hydroids and species with bivalve-inhabiting hydroids similar to Eugymnanthea, bothhaving ,%&nu-like medusae. Evolution went “fas-ter” for the hydroid stage, whereas the medusa wentsomehow “slower” in morphological change.Further changes in the medusa might have presu-mably did then led to Eugymnantheu. Relevant isBouillon’s (1983) description of the life cycle ofEirene hexunemulis, an eirenid species with a soli-tary planktomc hydroid morphologically similar tothe hydroid of Eugymnunthea. Solitary planktonicpolyps may somehow be preadapted to a commensallife which might require little modification in theirbody plan. A solitary planktonic life could have faci-litated their entrante in the mantle cavity of bival-ves, whereas this seems more difficult for colonieswith reptant stolons. It is here proposed thatEugymnanthea-like hydroids evolved from free-living solitary planktonic eirenid hydroids, the restof Kubota’s (1983) explanation being completelyaccepted.

CONCLUSION

As in al1 hydroidomedusan families comprisingspecies with both hydroids and medusae, the recog-nition of genera in the Campanulariidae is proble-matic according to current use of medusa reductionas a generic character, a serious problem concemingthe validity of Laomedeu. The situation, however, isfurther complicated by the possibility of character

30 F. BOERO CZ al.

Eugymnanthea inquilina

\

reduced medusae

Eutirna comrnensalis Eirene hexanemalìsdeveloped medusae

I developed medusae

Eutima

EIRENIDAEcolonia1 benthic polvps

developed med&L

reversal, so that specialised features such as themeconidium of Gonothyraea or the medusa ofObe!ia could return to a less-specialised status offixed gonophores. The danger of paraphyly inLuomedeu could be resolved by referring al1Luomedea species to Clytia which, thus, wouldcomprise species with both medusae and fixedgonophores. This solution, consistent with the posi-tion of Petersen (1979, 1990), is not adopted here forpure conveniente. Character reversal in Gonothy-raea and Obel& in fact, could a lso lead toLaomedea-like species, but this inconvenientewould be unavoidable at this stage of knowledge andi& evaluation calls for further investigation based onother characters, as attempted in the Hydractiniidaeby Cunningham and BUS (1993). It is suggestive,however, that Cunningham and BUS (1993) did nottake any taxonomic position after their treatment ofthe Hydractiniidae, probably because the outcomeof their results would be to merge the three maingenera of the Hydractiniidae into a single genus.

The information content of hydroids in taxonomy

is indisputable when considering that hydroids arethe only clue for infening afflnities among specieswith and without medusa stages (the presente of thehydroid is a constant, that of the medusa is a varia-ble). This could lead to classifications such asNaumov’s (1960), where medusae have been disre-garded in taking taxonomic decisions, but such posi-tion has been corrected by Petersen (1979, 1990)who explicitly said that the features of the medusaehave to be matched with those of hydroids and thathydroids with no medusae have to be linked to simi-lar hydroids with medusae. We have shown above,however, how “inconsistent evolution” has operatedwidely in hydroidomedusan evolution and thathydroid and medusa morphologies Fan vary withoutapparent consistency within the same clade. Theseinconsistencies can be resolved, as Petersen showed,by drastic changes in the definition of genera, but weare convinced that this will be correct only after thecomplexity of life cycles and of parallel events inAntho- and Leptomedusae has become clearer bothfrom life-cycle elucidation and from molecular

CLASSIFICATION AND PHYLOGENY IN THE HYDROIDOMEDUSAE 31

investigation.The main goal of life cycle research on the

Hydroidomedusae has been to create a single classi-fication of hydroids and medusae. This was achie-ved by Naumov (1960) and thoroughly modified byBouillon (1985) who, however (p. 30), stated thatplacing species with medusae in the same genus ofspecies without medusae would have caused “moreperturbations than simplifications” due to still-incomplete knowledge of life cycles. Bouillon’s(1985) classification was thus based on convenienterather than on phylogeny, at least in problematictaxa. The present goal of life cycle studies, as remar-ked and attempted by Petersen (1979, 1990), is toavoid the compromise between a unified classifica-tion based on phylogeny and a unified classificationbased on conveniente.

The possible resolution of some cases of “incon-sistent evolution” given above derives mainly fromwork carried out since 1985 and shows how muchcan be gained from life cycle elucidation Severa1apparent inconsistencies remain to be fully explainedor could be solved only by drastic changes, such aslumping together the three main genera of theHydractiniidae. The taxonomic decisions to be takenwhen inconsistencies in morphology are resolvedare, however, not always clear: “intermediate” formssuch as A4itrocomiw-n and Eucheilotu, Clytia a n dPhiulella, Teissiera and Zanclea could be treated in adifferent way from the currently accepted ones, Newtindings often reveal former mistakes in the unifiedsystem of hydroids and medusae, but correction ofsuch mistakes on the basis of new (but in-complete)findings often leads to thoroughly revised systemswhich will be proven incorrect by yet further disco-veries. While fully accepting Petersen’s (1979, 1990)critiques of the currently adopted “convenient” sys-tem proposed by Bouillon (1985), we cannot fullyaccept his revised system as being “phylogenetic”,especially due to widespread lack of knowledge evenin the Capitata, as remarked by Boero et al,, (1995)when describing the life cycle of Pteroclava krernpj?and discussing its inclusion in the system proposedby Petersen (1990).

ACKNOWLEDGEMENTS

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