Cladistic Analysis of Medusozoa and Cnidarian Evolution

Invertebrate Biology 123(1): 23–42. ᭧ 2004 American Microscopical Society, Inc. Cladistic analysis of Medusozoa and cnidarian evolution Antonio C. Marques1,a and Allen G. Collins2 1 Departamento de Zoologia, Instituto de Biocieˆncias, Universidade de Saõ Paulo. C.P. 11461, 05422-970, Saõ Paulo, SP, Brazil 2 ITZ, Ecology & Evolution, Tiera¨rtzliche Hochschule Hannover, Bu¨nteweg 17d, 30559 Hannover, Germany Abstract. A cladistic analysis of 87 morphological and life history characters of medusozoan cnidarians, rooted with Anthozoa, results in the phylogenetic hypothesis (Anthozoa (Hydrozoa (Scyphozoa (Staurozoa, Cubozoa)))). Staurozoa is a new class of Cnidaria consisting of Stau- romedusae and the fossil group Conulatae. Scyphozoa is redefined as including those medusozoans characterized by strobilation and ephyrae (Coronatae, Semaeostomeae, and Rhizosto- meae). Within Hydrozoa, Limnomedusae is identified as either the earliest diverging hydrozoan lineage or as the basal group of either Trachylina (Actinulida (Trachymedusae (Narcomedusae, Laingiomedusae))) or Hydroidolina (Leptothecata (Siphonophorae, Anthoathecata)). Cladistic results are highly congruent with recently published phylogenetic analyses based on 18S molecular characters. We propose a phylogenetic classification of Medusozoa that is consistent with phylogenetic hypotheses based on our cladistic results, as well as those derived from 18S analyses. Optimization of the characters presented in this analysis are used to discuss evolutionary scenarios. The ancestral cnidarian probably had a sessile biradial polyp as an adult form. The medusa is inferred to be a synapomorphy of Medusozoa. However, the ancestral process (metamorphosis of the apical region of the polyp or lateral budding involving an en- tocodon) could not be inferred unequivocally. Similarly, character states for sense organs and nervous systems could not be inferred for the ancestral medusoid of Medusozoa. Additional key words: Staurozoa, Scyphozoa, Hydrozoa, Cubozoa Cnidarian species are often used as model organisms ships among its component groups are known with in evolutionary studies (of development, cell biology, precision (Marques 1996; Nielsen et al. 1996; Jenner gene families, etc.) because Cnidaria diverged rela- & Schram 1999; Nielsen 2001; Collins 2002). tively early in the history of Metazoa. The presump- Prior studies focusing on relationships among cni- tion in these studies is that cnidarian species may ex- darian classes contain many contradictions (Salvini- hibit relatively underived character states that can be Plawen 1978, 1987; Petersen 1990; Bridge et al. 1992; compared with those of other animals, particularly bi- Bridge et al. 1995; Schuchert 1993; Odorico & Miller laterians. As an example, a recent study made infer- 1997; Marques 2001; Nielsen 2001; Collins 2002). ences about the ancestral paired domain (a conserved However, in the last decade Anthozoa has emerged as DNA-binding domain present in developmental con- the most likely sister group of the remaining cnidari- trol genes) in animals based on the condition of Pax ans, first dubbed Tesserazoa (Salvini-Plawen 1978), genes in a hydrozoan cnidarian (Sun et al. 2001). but more commonly known as Medusozoa (Petersen Though character states in cnidarians are possibly an- 1979). Monophyly of the medusozoans is particularly cient, features under study in a given cnidarian species well supported by their shared possession of linear may certainly be derived at some level within Cnidaria mtDNA, in contrast to anthozoans and other metazo- and to assume the opposite could be misleading. Thus, ans (Bridge et al. 1992). To move toward a consensus the utility of comparative studies is enhanced as more view of cnidarian phylogeny that will enlighten further taxa are investigated (Lowe et al. 2002) and as knowl- comparative studies using cnidarians, we present a cla- edge of phylogeny increases. In the case of Cnidaria, distic analysis of 87 morphological and life history neither its position within Metazoa nor the relation- characters to generate a hypothesis of relationships among medusozoan cnidarians. We compare the cladistic results with those of recent phylogenetic analy- a Author for correspondence. E-mail: [email protected] ses of Medusozoa using molecular characters (Collins 24 Marques & Collins 2002), and present a classification that is consistent not available was coded as a question mark (?) and with phylogenetic hypotheses derived from both anal- non-comparable structures were coded in the matrix as yses. Finally, we make inferences about the evolution N. Polymorphic characters were treated as uncertain- of morphological and life history traits within Cnidaria ties. based on our cladistic analysis. Cladistic analyses were carried out using the branch and bound algorithm of the software PAUP* 4.0 Methods (Swofford 2001). First, we searched for most parsi- monious trees without weighting any of the characters. In our cladistic analysis, we used the class Anthozoa Strict and semi-strict consensus trees were calculated as an outgroup, a position supported by previous mor- from the trees obtained in these primary analyses. phological and molecular studies. As terminal taxa, we Then, a complementary analysis was performed using adopted the class Cubozoa (Werner 1975; Franc successive approximation weighting (Farris 1969, see 1994b), the fossil group Conulatae (Wade 1994), the also Carpenter 1988, 1994) by maximum values of re- 4 orders of Scyphozoa (after Franc 1994a), and the 8 scaled consistency indices (RC). Bootstrap indices subclasses of Hydrozoa (following Bouillon 1994a,b were calculated for 500 replicate searches using both with 2 exceptions). Higher-level hydrozoan taxonomy weighted and unweighted characters, and Bremer sup- has suffered from the legacy of early specialists of port indices were calculated using unweighted char- hydroids and hydromedusae, who developed indepen- acters. dent naming schemes. To be inclusive, we use the names Anthoathecata and Leptothecata (Cornelius Results 1992) rather than relicts of older classifications, such as Anthomedusae, Athecata, Leptomedusae, and The- The unweighted analysis of the data matrix (Appen- cata. As in any parsimony analysis, all terminals are dix 2) yielded 48 trees (14 trees using ‘‘amb-’’ option considered to be monophyletic. Although hydrocorals of PAUP; Lϭ126; CIϭ0.730; RIϭ0.728), for which and velellids are sometimes classified as higher taxo- the strict and semistrict consensus trees have the same nomic groups of Hydrozoa (e.g., Milleporina, Stylas- highly polytomic topology, including only 3 mono- terina, Chondrophora, etc.), these groups are well es- phyletic groups: (1) (Coronatae (Semaeostomeae, Rhi- tablished as part of Anthoathecata, based on their zostomeae)); (2) (Siphonophorae, Anthoathecata); and morphology (e.g., Bouillon 1985; Schuchert 1996) and (3) (Actinulida, Trachymedusae (Narcomedusae, Lain- on molecular evidence (Collins 2002). Hydridae and giomedusae)). The successive weighting analysis re- Otohydra are difficult hydrozoan groups and were con- sulted in 3 fully resolved trees (3 using ‘‘amb-’’; sidered here to be part of Anthoathecata and Actinu- Lϭ76.65; CIϭ0.928; RIϭ0.925), in which Limnome- lida respectively. Neither of these inclusions impact dusae appears in 3 different positions: (1) sister-group our scoring of Anthoathecata and Actinulida. That of all other hydrozoans; (2) sister-group of (Actinulida said, if future work indicates that any of our terminal (Trachymedusae (Narcomedusae, Laingiomedusae))); taxa are not monophyletic, our analyses should be and (3) sister group of (Leptothecata (Siphonophorae, emended accordingly. Anthoathecata)). The phylogenetic hypothesis (strict For each taxon, we scored 87 characters, of which consensus) generated by this cladistic analysis (Fig. 1) 48 were informative (Appendices 1 and 2). Non- suggests that Hydrozoa is the monophyletic sister informative characters either have incomplete docu- group of all other medusozoans. Within Hydrozoa, mentation or were judged to be shared by all terminals. Limnomedusae has an unstable position, whereas the We hope that including these characters here will in- other hydrozoan groups form 2 clades (Actinulida spire further studies. Scoring characters for supraspe- (Trachymedusae (Narcomedusae, Laingiomedusae))) cific taxa requires some generalizations unless one in- and (Leptothecata (Siphonophorae, Anthoathecata)). cludes only characters that are constant for all species Non-hydrozoan medusozoans are also monophyletic, in higher taxa or relies on a phylogenetic hypothesis but Scyphozoa, as traditionally circumscribed is not. of the group that permits optimization of all ancestral Instead, 3 scyphozoan groups form a clade (Coronatae states (Whiting et al. 1997). In general, the character (Rhizostomeae, Semaeostomeae)) that is the sister states scored were represented uniformly in each of the group to the clade ((Stauromedusae, Conulatae) Cu- terminals (see Appendix 1 for exceptions and discus- bozoa). sion). Because of the taxonomic breadth of this study, This cladogram (Fig. 1) represents hypotheses that characters and their states were taken mostly from the are both consistent with and contradictory to various literature. Characters were coded as binary or multi- views of cnidarian relationships that have been pro- state and considered unordered. Information that was posed in the past. Conulatae, which is comprised of Cladistic analysis of Medusozoa 25

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