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Phylogenetic Relationships in the Nereididae (Annelida: Polychaeta), Chiefly in the Subfamily Gymnonereidinae, and the Monophyly

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Phylogenetic Relationships in the Nereididae (Annelida: Polychaeta), Chiefly in the Subfamily Gymnonereidinae, and the Monophyly BULLETIN OF MARINE SCIENCE, 48(2): 559-573, 1991 PHYLOGENETIC RELATIONSHIPS IN THE NEREIDIDAE (ANNELIDA: POL YCHAETA), CHIEFLY IN THE SUBFAMILY GYMNONEREIDINAE, AND THE MONOPHYLY OF THE NAMANEREIDINAE C. J. Glasby ABSTRACT The cladistic relationships of 15 genera in the Nereididae are investigated in order to establish whether the Namanereidinae is monophyletic and to develop an hypothesis of precise outgroup relationships for the Namanereidinae. The cladistic analysis is based on 37 morphological characters with character state polarity determined using the outgroup method. Outgroup taxa include the hesionid genera Hesione, Leocrales and Ophiodromus. The re- sultant cladistic hypothesis is similar to that proposed by Fitzhugh (1987). The Namanereidi- nae is monophyletic and the sister group of the remaining Nereididae. The gymnonereidine genera included in the analysis are relatively more plesiomorphic compared to the nereidine genera, and Stenoninereis is the most plesiomorphic gymnonereid. Further synapomorphies for the Namanereidinae (spherical pal po styles and dorsal aciculae supporting the neuropodia) are identified and the synapomorphy identified by Fitzhugh (the lack of ceratophores [cir- rophores] ofthe dorsal cirri) is considered homoplasious within the Nereididae. The synapo- morphies are discussed in relation to present theories on the origin of the Namanereidinae. The recent study of phylogenetic relationships within the Nereididae (Fitzhugh, 1987) represents the first investigation of the family using the methods of phy- logenetic systematics. I Such studies are rare in polychaete systematics. Apart from Fitzhugh's, other studies of polychaetes using cladistic methods include several by Westheide (1977; 1982; 1985), Westheide and Riser (1983), Fauchald (1982), ten Hove (1984), Paxton (1986) and Solis-Weiss and Fauchald (1989). The Nereididae consists of three subfamilies: Namanereidinae, Gymnonereidi- nae and Nereidinae (Fitzhugh, 1987). A fourth subfamily, the Notophycinae Banse, 1977, which contained a single genus Micronereis (and its synonyms Notophycus, Phyllodocella and Quadricirra) (Paxton, 1983) was synonymized with the Ner- eidinae by Fitzhugh (1987). Fitzhugh, perhaps unwisely, expanded the definition of the Gymnonereidinae to include all genera without hardened paragnaths (ex- cluding the Namanereidinae). As Banse (l977a) points out, these genera do not constitute a natural group, as they vary considerably in parapodial complexity and setal types. The Gymnonereidinae sensu Banse was defined on the basis of two features unique within the Nereididae (bifid neurocirri and the anterior body region with numerous setae) and included four genera: Tambalagamia, Gym- nonereis, Ceratocephale and Micronereides. These genera are highly unusual in a number of different characters, with each genus having its own characteristic pattern of parapodial features. They are not considered in the present study, however, as the type species were not available to study. The Namanereidinae was established by Hartman (1959) (as Namanereinae). According to Hartman (1959), the subfamily was distinguished by having a phar- ynx without papillae or paragnaths; parapodia which lacked notopodiallobes but which had both notoaciculae and neuroaciculae, one or a few slender notosetae [may be absent], and well developed neuropodia with two to three kinds of neu- I Phylogenetic systematics (or c1adism) can be defined as the recovery of phylogenetic (genealogical) relationships among groups of organisms and the classification of groups of organisms based only on monophyletic taxa (modified after Wiley, 1981). 559 560 BULLETIN OF MARINE SCIENCE, VOL. 48, NO.2, 1991 rosetae; a prostomium with a pair offrontal antennae and four eyes (usually); and an apodous first segment with three to four peristomial [=tentacular] cirri. Gibbs (1971) expanded the description by including Cryptonereis which lacks frontal antennae. Fitzhugh (1987) maintained this concept of the Namanereidinae as the results of a cladistic analysis indicated the group was monophyletic, defined by the lack of ceratophores [cirrophores] of the dorsal cirri. It is not the purpose of this paper to evaluate the subfamily classification. This would require the inclusion of all nereidid genera, which is beyond the scope of this study. I will, therefore, follow the most recent classification proposed by Fitzhugh (1987). While this classification may yet be improved, it offers the advantage of being based on a testable hypothesis of relationships underpinned by the logical concepts of phylogenetic systematics. In contrast, previous subfamily classifications ofthe Nereididae have been based on what can be subsumed under phenetic principles (Hartman, 1959; Pillai, 1961; Banse, 1977a, 1977b). The aims of this study are firstly to test whether the Namanereidinae is mono- phyletic and, if so, to identify the synapomorphies defining the group; and secondly to elucidate the phylogenetic relationship in some Gymnonereidinae (sensu Fitz- hugh) and in some Nereidinae (sensu Fitzhugh). The topology established here was used in a cladistic analysis of the Namanereidinae (Glasby, 1990) to polarize characters using the method of Maddison et al. (1984). METHODS Thirty-seven morphological characters and 18 terminal taxa were used in this study (Tables I and 2). Features were observed using a Zeiss dissecting microscope and a Zeiss compound microscope. Measurements of prostomium outline (length and width) and peristomium length were made using an ocular graticule with the dissecting microscope, while measurement of oocyte diameter used an ocular graticule and the compound microscope. Oocytes were distinguished as being "normal-sized" (maximum diameter less than 150 /Lm) or "giant-sized" (maximum diameter greater than 300 /Lm). The terminologies used for the morphology are standard (Day, 1967; Fauchald, 1977), with the folIowing exceptions. The term tentacular cirri rather than peristomial cirri is used for the head end sensory appendages of the Nereididae and the Hesionidae as in the former, the origin of alI of the cirri from the peristomium is questionable (Glasby, 1990). Parapodial lobe terminologies folIow HylIeberg, Nateewathana and Bussarawit (1986) and Hutchings and Reid (1990), except that the superior notopodiallobe is referred to here as the pre-setal notopodiallobe. Terminologies for setal types have prefixes supra- and sub-, depending on their position in relation to the aciculae. In addition, the setae are defined as being either post-acicular or pre-acicular. The setal positions are discussed further in Glasby (1990). The terminology for setal morphology is standard except that the less commonly used term sesquigomph sensu Perkins (1980), rather than hemigomph sensu Fauchald (1977), is used to describe the articulation of compound setae intermediate between heterogomph and homogomph. Sesquigomph refers to an articulation with sides in the ratio 3:2, whereas hemigomph is ambiguous, referring either to a ratio of 1:2 or, in the sense that Fauchald used it, to mean "partialIy" (i.e., the articulation is nearly at right angles to the long axis of the shaft). Systematic Procedures. - The relationships within the Nereididae were analyzed using methods of phylogenetic systematics (cladistics), as conceptualized by Hennig (1950; 1966) (see also Wiley (1981) for a comprehensive review of the goals and philosophies behind phylogenetic systematics). EssentialIy the method involves the grouping of taxa, on the basis of shared, derived characters (synapomorphies), into a series of nested, hierarchical units. The phylogenetic method of argumentation used is based on the principle of parsimony which, when applied to phlogenetic reconstruction, involves minimizing the number of character transformations (steps). The specific form of parsimony employed, Wagner parsimony, alIows reversals to the ancestral state. A microcomputer program, Hennig86 (Farris, 1989) was used to implement this principle. Character polarity was determined using outgroup comparison (Watrous and Wheeler, 1981). Other methods of determining polarity such as the ontogenetic method and the paleontological method were not suitable for this group. Apart from Feuerborn's (1931) article, there is very little ontological data for species of Namanereidinae and Gymnonereidinae (Reish, 1957). The paleontological record of "worms" is poor, and consists mainly of fossilized tubes, burrows, and jaws (scolecodonts) composed GLASBY: PHYLOGENETIC RELATIONSHIPS IN NEREIDIDAE 561 Table 1. Characters and character states used in the cladistic study. 0, plesiomorphic state; I, I', 2, 2', 3 apomorphic states. A prime (') following a state value indicates that the state is part of a branching sequence and is equally apomorphic with the corresponding non-prime state Character State O. Setigers (maximum number) O. less than ISO 1. greater than 150 l. Prostomium (ratio of width at base of prostomium rel- O. relatively compact (greater than ative to length medially) 1.3) 1. relatively elongate (less than 1.3) 2. Antennae (shape) O. conical I. subconical I'. absent 3. Antennae (basally) O. distinct from prostomium I. produced from prostomium 4. Palpophores (shape) O. compact, unarticulated 1. large, articulated 5. Palpostyles (shape) O. conical-subconical 1. spherical 6. Peristomium length (mid-dorsal length) O. equal to or less than length se- tiger I I. greater than length setiger I 7. Tentacular cirri (number of pairs) O. 8 pairs 1. 6 pairs 2. 4 pairs
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