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A Phylogenetic Analysis of the Genus Eunice (Eunicidae, Polychaete, Annelida)

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A Phylogenetic Analysis of the Genus Eunice (Eunicidae, Polychaete, Annelida) Blackwell Publishing LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082© 2007 The Linnean Society of London? 2007 1502 413434 Original Article PHYLOGENY OF EUNICEJ. ZANOL ET AL. Zoological Journal of the Linnean Society, 2007, 150, 413–434. With 12 figures A phylogenetic analysis of the genus Eunice (Eunicidae, polychaete, Annelida) JOANA ZANOL1*, KRISTIAN FAUCHALD2 and PAULO C. PAIVA3 1Pós-Graduação em Zoologia, Museu Nacional/UFRJ, Quinta da Boa Vista s/n°, São Cristovão, Rio de Janeiro, RJ 20940–040, Brazil 2Department of Invertebrate Zoology, NMNH, Smithsonian Institution, PO Box 37012, NHB MRC 0163, Washington, DC 20013–7012, USA 3Departamento de Zoologia, Insituto de Biologia, Universidade Federal do Rio de Janeiro, CCS, Bloco A, Sala A0-104, Ilha do Fundão, Rio de Janeiro, RJ 2240–590, Brazil Received April 2006; accepted for publication December 2006 Species of Eunice are distributed worldwide, inhabiting soft and hard marine bottoms. Some of these species play sig- nificant roles in coral reef communities and others are commercially important. Eunice is the largest and most poorly defined genus in Eunicidae. It has traditionally been subdivided in taxonomically informal groups based on the colour and dentition of subacicular hooks, and branchial distribution. The monophyly of Eunice and of its informal subgroups is tested here using cladistic analyses of 24 ingroup species based on morphological data. In the phylo- genetic hypothesis resulting from the present analyses Eunice and its subgroups are paraphyletic; the genus may be divided in at least two monophyletic groups, Eunice s.s. and Leodice, but several species do not fall inside these two groups. Most of the traditional characters used in the taxonomy of Eunice are homoplasies; however, characters used for the first time in this study, such as certain jaw characters and characters derived from a close examination of cha- etal variation along the body, are promising sources of phylogenetic signal. © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 150, 413–434. ADDITIONAL KEYWORDS: branchial distribution – Eunicida – jaw – Leodice – mandible – maxillae – phylog- eny – subacicular hooks. Eunice Cuvier, 1817 is the most species rich of the ten mercial and leisure fishing (Gambi et al., 1994). Sex- genera of the family Eunicidae, comprising around ually mature Eunice specimens have a large size 220 species. It is distributed worldwide, but it is most range, varying from a few mm to 6000 mm in length common in shallow tropical waters (Fauchald, 1992). (Fauchald, 1992), and both very large and very small Species of Eunice inhabit soft and hard marine bot- species have been described without adequate knowl- toms, many burrow into hard corals and calcareous edge of ontogenetic variation. algae or live in their crevices, and play significant The taxonomy within Eunice is difficult because of roles in coral reef communities as bioeroders (Hutch- the poor knowledge of ontogenetic and intraspecific ings, 1986), but possibly also in assembling those com- variation of characters (Steiner, Nogueira & Amaral, munities (Roberts, 2005). Eunice includes some 2002). In addition, many species have been described commercially important species used as bait in com- based on incomplete specimens (Miura, 1986), and several species are known just from type specimens (Fauchald, 1992). Furthermore, definition of the genus *Corresponding author. Current addresses: Department of is problematic as it is based on the following plesio- Biological Sciences, The George Washington University, 2023 G morphies: presence of three antennae, a pair of palps, Street NW, Washington, DC 20052, USA, and Department of a pair of peristomial cirri, and a complete set of Invertebrate Zoology, NMNH, Smithsonian Institution, PO Box 37012, NHB MRC 0163, Washington, DC 20013–7012, chaetal types (limbate, pectinate, aciculae, compound, USA. E-mail: [email protected] and subacicular hooks) (Orensanz, 1990); features © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 150, 413–434 413 414 J. ZANOL ET AL. that are also present in the well-defined eunicid genus to test the monophyly of Eunice and/or root the phy- Euniphysa (Lu & Fauchald, 2000) and in another logenetic analyses were species of other eunicid gen- eunicean family, Onuphidae. era, Marphysa, Palola, and Lysidice, members of the The poor definition of Eunice and the insufficient other four best known families of the order Eunicida, understanding of character variation led to the Onuphidae, Dorvilleidae, Lumbrineridae, and Oenon- description of genera such as Leodice Lamarck, 1818, idae, and members of Amphinomida, a probable sister and Nicidion Kinberg, 1865, both of which were later group to Eunicida (Rouse & Fauchald, 1997; but see considered junior synonyms of Eunice. Leodice, named Struck et al., 2006 for a discussion) (Table 3). for Leodice antennata Lamarck, 1818, was not clearly Each specimen was examined under stereo and differentiated from Eunice, and both names were used compound microscopes. Specimens were dissected as interchangeably through the first third of the 20th described by Day (1967) in order to code the characters century (Hartman, 1944). Nicidion included Eunice of the buccal apparatus. To determine chaetal varia- species lacking branchiae, a character not considered tion along the body, six parapodia of each specimen acceptable at either the generic (Hartman, 1944) or were examined, one from the first and last 2.5% subgeneric levels (Fauchald, 1970) because it is highly (determined by number of chaetigers) of the body, variable, and individuals within the same ‘Nicidion’ respectively, and four from the median chaetiger of species may or may not lack branchiae. each quarter of the body. We quantified branchial dis- Currently Eunice is subdivided into taxonomically tribution as the percentage of continuous chaetigers in informal groups based on colour and dentition of which branchiae are present, as used by Fauchald subacicular hooks (Ehlers, 1868; Hartman, 1944) (1992). and branchial distribution patterns (Fauchald, 1970). Miura (1986) suggested that the Eunice informal groups based on the characteristics of subacicular SPECIMENS hooks could correspond to genera or subgenera; he The material examined in this study came from the also suggested that the presence of few branchial fil- following institutions: ECOSUR, Colecion de Referen- aments present along the whole body was the ances- cia ECOSUR, Chetumal, Mexico; IBUFRJ, Departa- tral branchial distribution pattern in Eunice. mento de Zoologia, Instituto de Biologia, UFRJ, Rio de The monophyly of Eunice is currently disputed. Janeiro, Brazil; IRSNB, Institut Royal des Sciences Studies on the phylogeny of the order Eunicida using Naturelles de Belgique, Brussels, Belgium; SMNH, molecular data resulted in paraphyletic Eunice and Swedish Museum of Natural History, Stockholm, Swe- Eunicidae (Struck, Westheide & Purschke, 2002; den; USNM, National Museum of Natural History, Struck, Purschke & Halanych, 2006). Fauchald (1992) Smithsonian Institution, Washington, DC, USA. attempted a phylogenetic analysis of Eunice based on morphological features of the type specimens to test the relationships within the genus. His results were PHYLOGENETIC ANALYSES generally inconclusive and the only consistent clade in We coded two different character matrices, one all trees was a group that included all species with yel- with composite characters (composite analyses) and low hooks. another with reductive characters (reductive analy- The purposes of the present study are to test the ses) (sensu Strong & Lipscomb, 1999), to check the monophyly of the genus Eunice, as well as of its infor- sensitivity of our data set to the coding methods, mal groups, based on colour and dentition of the sub- which differ in the number of inapplicable characters acicular hooks and branchial distribution patterns, and in the underlying assumptions about primary and to provide a hypothesis of phylogeny for Eunice hypotheses of homology. that can be used as a framework for future studies on A matrix of 59 composite (74 reductive; Appendix 1) Eunice and Eunicidae in general. For this we used an morphological characters coded for 37 taxa (24 Eunice expanded morphological character set, compared with ingroup taxa plus 13 outgroup taxa) (Table 4; the one used by Fauchald (1992), and better preserved Appendix 2) was analysed under maximum parsimony material than represented by the types. optimization criteria. Eleven characters (20 in the reductive matrix) are uninformative autapomorphies or polymorphisms; however, these were included in the MATERIAL AND METHODS analyses because they have been observed in other species of the appropriate genus or family (J. Zanol & TAXONOMIC SAMPLING K. Fauchald, pers. observ.) not included here because of We examined 24 Eunice species (Table 1) representing the limited taxonomic sampling. Alternatively, some of all taxonomically informal groups (Table 2) and the these characters represent polymorphic variation that morphological diversity within these. Outgroup taxa is uninformative because of the way current analytic © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 150, 413–434 PHYLOGENY OF EUNICE 415 Table 1. Ingroup taxa examined in the present study (see Table 2 for a description of the groups) Group Species Number, collection, and locality of specimens examined A1 Eunice pennata
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