Contributions to Zoology, 67 (2) 125-141 (1997) SPB Academic Publishing bv, The Hague Phylogeny of the Anomura (Decapoda, Crustacea): Spermatozoa and spermatophore morphological evidence Christopher+C. Tudge Crustacean Laboratory, Museum of Victoria, 71 Victoria Crescent, Abbotsford, Vic. 3067, Australia Keywords: Anomura, phylogeny, spermatozoa, spermatophore, ultrastructure, hermit crabs le Abstract un taxon monophylétique: genre lomoïde Lomis est exclu de ce tandis le groupe, que genre thalassinide Thalassina y est La indu. -synapomorphie pour la des taxons conven- A of majorité phylogenetic analysis selected anomuran, thalassinidean, tionnels d’Anomures.(Lomis exclu) est l’origine cytoplasmique and other decapod crustacean taxa, based on spermatozoal des branches microtubulaires. Si des représentants des ultrastructural characters and spermatophore morphological Palinurides des Thalassinoïdes et sont séparément désignés characters, was performed and the following relationships of comme “outgroups”, les Astacidea + the Brachyura forment un taxa are elucidated from the trees produced. The Anomura groupe-frère pour les Anomura. Les superfamilles Thalassi- are not a monophyletic assemblage, with the lomoid Lomis noidea, Paguroidea et Galatheoideane sont des exclusive of pas groupes being the remainderof the anomurantaxa, and the monophylétiques. Les montrent thalassinid analyses que les familles Thalassina included in the anomuran clade. The d’Anomures Coenobitidae et Porcellanidae sont des the groupes synapomorphy joining majority of the conventional ano- monophylétiques. La famille de Paguroïdes Diogenidae est muran taxa (Lomis excluded) is the cytoplasmic origin of the paraphylétique, les Clibanarius et Cancellus devant être microtubular genres arms. When the palinurid and thalassinoid du clade contenant le des Les séparés reste genres diogenides. representatives are separately designated as outgroups, the et familles Paguridae Parapaguridae forment un mono- Astacidea clade and Brachyura jointly formed a sister group to the - à du phylétique l’exception genre Porcellanopagurus. Les Anomura. The superfamilies Thalassinoidea, Paguroidea, and deux représentants de la famille Chirostylidae Eummida et Galatheoidea not In all the ( are monophyletic groups. analyses Uroptychus) ne peuvent pas être associés avec les autres anomuran families Coenobitidaeand Porcellanidae each form a espèces des Galatheoidea. Les taxons de la familleGalatheidae The is monophyletic group. paguroid family Diogenidae para- ne forment pas un groupe monophylétique. Le seul with the Clibanarius and Cancellus Hippoïde phyletic, genera separate étudié. Hippa, est considéré comme groupe-frère des autres from a the single clade containing remaining diogenid genera. taxons d’Anomures Lomis The (. excepté). families Paguridae and Parapaguridae form a mono- phyletic clade with the exception of Porcellanopagurus. The two representatives of the family Chirostylidae ( Eumunida and Uroptychus ) fail to associate with the other species in the Introduction Galatheoidea. taxa The in the family Galatheidae are not a monophyletic assemblage. The only investigated hippoid The of use spermatozoal ultrastructure in tax- is sister the remainder of the Hippa portrayed as the group to and is onomy phylogeny now firmly established anomuran taxa (with the exception ofLomis). as a valid means of investigating phylogenetic in various animal There relationships groups. are Résumé many phyla in which advances have been made in phylogenetic studies by using spermatozoal ultra- Une Recent include studies analyse phylogénétique d’une sélection de taxons d’Ano- structure. examples in the mures, de Thalassinides d’autres et Décapodes, basée sur des Platyhelminthes (Ehlers, 1985; Justine, 1991); caractères ultrastructuraux des des spermatozoïdes et sur Polychaeta (Jamieson & Rouse, 1989); Oligo- caractères morphologiques du spermatophore, a été entreprise, chaeta (Jamieson, 1981, 1983); Mollusca et les arbres (Healy, produits permettent d’élucider plusieurs aspects fish 1991b; Mattel, and concernant la entre taxons. Les Anomures 1988); (Jamieson, 1991), parenté ne sont pas 126 C.C. Tudge - Phylogeny of the Anomura Amniota (Healy & Jamieson, 1992; Jamieson & have been the subject of several investigations at Healy, 1992; Jamieson, 1995a, b). the morphological and molecular level. Of note Within the Crustacea, studies on spermatozoal are the phylogenetic analyses of the constituent ultrastructure in representatives of the Penta- families of the Anomura using adult and larval stomida (Wingstrand, 1972; Storch & Jamieson, somatic morphology (McLaughlin, 1983b; Martin 1992) have confirmed that the pentastomids are & Abele, 1986; Richter & Scholtz, 1994; Scholtz view crustaceans, a endorsed by molecular biol- & Richter, 1995) and the analyses of several based ogy (Abele et al., 1989). Similarly, spermatozoal members of the Anomura on 18S rRNA nucleotide Abele ultrastructure has been shown (Jamieson & sequences by Spears & (1988) Tudge, 1990; Jamieson, 1991a, 1994; Jamieson et and Spears et al. (1992), 16S rRNA by al., 1995) to support Guinofs re-classification of Cunningham et al. (1992), and 16S rRNA and the Brachyura (Guinot, 1977, 1978) into cytochrome oxidase I genes by Tam et al. (1996). Podotremata, Heterotremata (sensu lato), and Richter & Scholtz (1994: 197) state that “the Thoracotremata, based on differential location of phylogenetic relationships (within the asymmetri- cal hermit unresolved and be the male and female gonopores. crabs) are seem to of While the of The phylogenetic significance crustacean very complex". recognizing validity spermatozoa had been recognized by Koltzoff the taxon “Anómala”, particularly as used by (1906) and later, Wielgus (1973). Koltzoff (1906: Scholtz & Richter (1995), and not wishing to 424) was one of the first workers to construct a enter into debate over terminology, I prefer to use phylogeny of crustaceans based on spermatozoal the term “Anomura” for the infraorder containing structure at the light microscope level. To the the superfamilies Galatheoidea, Paguroidea, Hip- encountered he and different sperm types assigned a poidea, Lomoidea, as argued by McLaughlin binomen consisting of the “generic” name & Holthuis (1985). and and The value of such Spermia a descriptive “species” name computer programs, as placed this binomen on the nodes and branches of PAUP (Phylogenetic Analysis Using Parsimony) his phylogenetic tree. The crustacean taxa in- (Swofford, 1993), for phylogenetic analysis of cluded in his study were Mysis, Euphausia, spermatozoal and molecular characters has been well demonstrated in animal Natantia, Galatheidea, Paguridea, Thalassinidea, many groups (Jamie- & Astacus, Loricata, Brachyura, Oxystomata, and son et al., 1987; Kim Abele, 1990; Abele, Dromiidea. Some of the significant relationships 1991; Jamieson, 1991b, 1993, 1994, 1995a, b; apparent in Koltzoff s phylogenetic tree were the Spears et al., 1992; Jamieson & Grier, 1993; separation of Mysis from the decapods at the Jamieson et al., 1995). The present study investi- 42 node Spermia flagellifera, recognizing the pres- gates the interrelationships of species of ence of what is now termed a pseudoflagellum anomuran crab, three species of thalassinidean (Jamieson, 1987) in the spermatozoa of Mysis. shrimp, and six species of other decapods using The Galatheidea and similar and anomuran groups Paguridea parsimony analysis procedures em- in 26 were designated Spermia erecta, recognition of ploys spermatozoal and 6 spermatophore char- the superiorly positioned, generally elongate acters. acrosome vesicle. The Brachyura, Oxystomata, and Dromiidea were labelled Spermia cepha- lacantha. The latter binomen probably refers to Materials and methods the nuclear and that many arms spikes project The taxa included in this analysis, with sources of character laterally from around the acrosome vesicle of the information, are displayed in Table I. Appendices A & B spermatozoa in these groups. describe the characters used in the parsimony analysis and the The relationships among the families in the complete data matrix, respectively. Of the 32 characters infraorder Anomura “Anomala” of Boas, (the employed in the analysis only one (character 19) is considered and within uninformative. 1880), among representatives families, at present phylogenetically Contributions to Zoology, 67 (2) - 1997 127 Table I. Taxa included in the analysis. [ ] = source of character information. InfraorderInfraorder Thalassinidea Strigopagurus boreonotusboreonotus Forest, 19951995 [Tudge, 1995a, 1996] Axiidae: Axius glyptocercus Von Martens, 1868 [Tudge, Galatheidae: Allogalathea eleganselegans (Adams & White, 1848)1848) 1995a, b] [Jamieson, 1991a;1991a;Tudge,Tudge, 1995a] Callianassidae: australiensis Munida Trypaea (Dana, 1852) [Tudge,[Tudge, sp. [Tudge, 1995a, b] 1995a] Munidopsis sp.sp. [Tudge, 1995a] Thalassinidae: ThalassinaThalassina squamifera De Man, 1915 [Tudge,[Tudge, Hippidae; Hippa pacifica (Dana, 1852) [Matthews, 1956; 1995a, b]b] Tudge,Tudge, 1995a,b] Lomidae:Lomidae: Lomis hirta (Lamarck, 1810) [Tudge, 1995a, b, Infraorder Anomura 1997]1997] Chirostylidae: Eumunida sternomaculata St. Laurent & Paguridae;Paguridae; Pagurus bernhardus (Linnaeus, 1758) [Tudge,[Tudge, Macpherson, 1990 [Tudge, 1995a, b] 1995a]1995a] chevreuxi Uroptychus sp.sp. [Tudge, 1995a] Pagurus chevreuxi (Bouvier,(Bouvier, 1896) [Tudge,[Tudge, 1995a,1995a, b] Coenobitidae: Birgus latro (Linnaeus, 1758) [Tudge[Tudge & Pagurus hirtimanusMiers,