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 [cirrophores] ofthe dorsal cirri) is considered homoplasious within the Nereididae. The synapomorphies 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 phylogenetic 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 (excluding 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 pharynx 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 monophyletic 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 setiger I I. greater than length setiger I 7. Tentacular cirri (number of pairs) O. 8 pairs 1. 6 pairs 2. 4 pairs 3. 3 pairs 8. Pharynx, Area I with (structure) O. no papillae I. papillae 2. conical paragnaths 9. Pharynx, Area II with (structure) O. no papillae I. papillae 2. conical paragnaths 10. Pharynx, Area III with (structure) O. no papillae I. papillae 2. conical paragnaths II. Pharynx, Area IV with (structure) O. no papillae 1. papillae (singly, rarely in tufts) 2. conical paragnaths 3. conical and bar-shaped paragnaths 12. Pharynx, Area V (structure) O. pad-like, with Areas V-VI fused I. as narrow groove 2. with papi1\ae 3. with conical paragnaths 13. Pharynx, Area VI with (structure) O. no papillae 1. papillae 2. conical paragnaths 3. a bar-shaped paragnath 14. Pharynx, Areas VII-VIII with (structure) O. no papi1\ae 1. papillae 2. conical paragnaths IS. Parapodia I and 2 with (types of aciculae) O. noto- and neuroaciculae I. neuroaciculae only 16. Dorsal aciculae supports (position in podia) O. notopodia or dorsal cirrus 1. neuropodia 17. Glandular patches on dorsal edge of parapodia (pres- O. absent ence) 1. present 18. Dorsal notopodialligule in setiger 10 (presence; form) O. absent I. present, simple 2. a series of arborescent filaments (branchiae) 562 BULLETIN OF MARINE SCIENCE, VOL. 48, NO.2. 1991

Table I. Continued

Character Stale 19: Pre-setal notopodiallobe in setiger 10 (presence) O. absent I. present 20. Median ligule in setiger IO (presence) O. absent I. present 21. Post-setal neuropodiallobe in setiger IO (presence) O. absent I. present 22. Ventral neuropodialligule in setiger IO (presence) O. absent 1. present 23. Dorsal cirri in mid-posterior segments (shape of cir- O. cylindrical rophore) 1. leaf-like I'. absent 24. Supra-acicular notosetae in setiger IO are (type) O. capillaries I. spinigers 2. absent 2'. falcigers 25. Supra-acicular notosetae in setiger IO (articulation) O. sesquigomph 1. homogomph 26. Supra-acicular neurosetae in post-acicular fascicle in O. falcigers setiger IO are (type) 1. spinigers 27. Supra-acicular neurosetae in post-acicular fascicle in O. heterogomph setiger IO (articulation) 1. sesquigomph 2. homogomph 28. Supra-acicular neurosetae in pre-acicular fascicle in se- O. falcigers tiger IO are (type) I. spinigers 29. Supra-acicular neurosetae in pre-acicular fascicle in se- O. heterogomph tiger IO (articulation) I. sesquigomph 30. Sub-acicular neurosetae in post-acicular fascicle in se- O. falcigers tiger IO are (type) I. spinigers 2. absent 31. Sub-acicular neurosetae in post-acicular fascicle in se- O. heterogomph tiger IO (articulation) I. sesquigomph 2. homogomph 32. Sub-acicular neurosetae in pre-acicular fascicle in seti- O. falcigers ger IO are (type) I. spinigers 33. Sub-acicular neurosetae in pre-acicular fascicle in seti- O. heterogomph ger IO (articulation) I. sesquigomph 34. Pygidium (shape) O. smooth ring I. incised ring 2. ring with paired lateral lobes and minute dorsal lobe 2'. ring with wing-like lateral lobes 35. Mature oocytes (maximum diameter) O. normal-sized (less than 150 ILm) I. giant-sized (greater than 300 ILm) 36. Mature oocytes (shapes) O. spherical I. ellipsoid ofa material that is easily preserved (Howell, 1962). However, according to Szaniawski (1974), there are no undisputed records of fossilized nereidid jaws. Character states were scored for the ingroup as follows: where two or more states applied to any particular taxon, the state was scored as unknown (?); inapplicable characters 'were scored as "-" (Table 2). Hennig86 treats both "?" and "-" in the same way, as missing data. In the outgroup, if character states varied among the three species, the state occurring in two of the species was scored as plesiomorphic (e.g., characters 7, 15, 17, 19,24,30,34). Three types of characters were recognized in the data: binary characters (0-1,3-6, 15-17, 19-22,25-26,28-29,32-33,35-36), multi state linear characters (7-14, 18,27,30-31) and multi state branched characters (2,23-24,34). Multistate characters were coded using additive binary coding (Table 2), a technique recommended by Farris (1969) and Carpenter (1988) if successive weighting is to be used. GLASBY: PHYLOGENETIC RELATIONSHIPS IN NEREIDIDAE 563

8~82~282=~~~88~888 - !-=. 0 - ~. - - - 0 ~. ~. ~. - - ~. - - -

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c: o ~'" 564 BULLETIN OF MARINE SCIENCE, VOL 48, NO.2, 1991

To counteract the effect of the additional data entries (i.e., columns) resulting from coding multistate characters in an additive binary fashion, a priori weights were applied to the characters (Table 3). This involved giving increased weights to characters represented by one and two columns so that they had the same weight as characters represented by three columns. Thus, a character represented by a single column is given a six times weight, by two columns is given a three times weight, and by three columns is given a two times weight. In this way all characters had equal weighting prior to the analysis. Cladograms were generated using the option "mhennig*" followed by bb*. Both algorithms apply branch swapping to achieve a solution. The bb* algorithm performs "extended branch swapping" on all cladograms generated by mhennig*. This combination of commands is recommended by Fitzhugh (1989) and Platnick (1989) for large data sets. The "exact" algorithms in Hennig86, which find all minimum length trees, were too time consuming for this set of data and the computer hardware (Osborne 80286 computer with a 80387 coprocessor). The cladistic analysis was refined using a technique known as successive approximations character weighting (Farris, 1969). The technique, which appears as an option in Hennig86 (successive weighting), involves an a posteriori application of weights to the cladistic characters based on the degree of fit between the character and the phylogeny (reliable characters, or those that show little homoplasy, are given the greatest weight) (Table 3). For a rationale behind this form of weighting see Farris (1969) and Carpenter (1988).

ANALYSIS Selection of Outgroup. - The choice of outgroup cannot be made with any assur- ance as the higher level phylogeny of the superfamily Nereidoidea George and Hartmann-Schroder, 1985, is unknown. However, several authors consider the Nereididae to be closely related to the Hesionidae (Dales, 1962; Fauchald, 1977; Mileikovsky, 1977; Fitzhugh, 1987). The Hesionidae share in common with the Nereididae a pair of palps (rarely absent in the Hesionidae), both notoaciculae and neuroaciculae supporting the parapodia (notoaciculae rarely absent in the Hesionidae), and compound neurosetae. It is difficult to decide which of these attributes, if any, are synapomorphies. The Pilargiidae also share several characters in common with the Nereididae and are considered by Day (1967) to be closely related to the Hesionidae and intermediate between the Nereididae and the Syllidae. The Hesionidae may be conveniently divided into three groups based on the structure of the parapodia, which may be either uniramous, sub-biramous or biramous. The three genera chosen as outgroups represent each of these groups. Hesione has uniramous parapodia in which notopodiallobes, notoaciculae and notosetae are absent; Leocrates has biramous parapodia in which notopodiallobes, notoaciculae and notosetae are present; and Ophiodromus has sub-biramous parapodia in which the notopodiallobe is extremely reduced, notoaciculae are present and there are a few notosetae. This concept of Ophiodromus differs slight from the definition given by Fauchald (1977) in which the parapodia are described as biramous. For each genus one species was examined, chosen on the basis of availability of material (Appendix). Monophyly of the Nereididae. - The monophyly of the Nereididae has never been established using cladistic methods-to do so would require consideration of the Nereidoidea. However, in all recent major classifications of the Polychaeta (Day, 1967; Fauchald, 1977; George and Hartmann-Schroder, 1985) it is considered a natural group. The family has been recognized largely in its present state since 1867 (Banse, 1977b). The validity of the present analysis may depend upon the assumption that the Nereididae is monophyletic. The following analysis included 15 of the 40 genera of Nereididae considered by Fitzhugh (1987). The ingroup comprised eight gymnonereidine genera, two nereidine genera and five namanereidine genera (Appendix). Choice of the gymnonereidine and nereidine genera was based to some extent on the availability of GLASBY: PHYLOGENETIC RELATIONSHIPS IN NEREIDIDAE 565

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'" MO 'o:tNO "'MO ~ '" N 'o:t '~ -

'e:: N MO MNN 'o:t..,o 0 N 'o:t 'e:: - ~OJ,...,•.. '"o~OJ \00 NNO M\OO 0.<'> N 'o:t 01 E! - - '1:;lCll c'5 \00 -NM N\OO 0 N 'o:t 'e::01 •.•OJ - 0.1 'e::,~ 0.':::::s nereis, Laeonereis, Kinberginereis, Micronereides, Ceratocephale, Gymnonereis, Tambalagamia, and Websterinereis. Sinonereis Wu and Sun, 1979 and Lycas- tonereis Nageswara-Rao, 1981 also belong to the Gymnonereidinae, however their relationships within this subfamily were not discussed by Fitzhugh (1987) and no material was available for this study.

RESULTS Topology. -An initial analysis, prior to the application of successive weighting, yielded three cladograms with length, 1 = 388, consistency index, ci = 57 and retention index, ri = 74. In all three cladograms the outgroup Leocrates emerged together with the Gymnonereidinae and Nereidinae as a monophyletic group. The trees were not further considered as some very homoplasious characters were having an undue influence on the topology. A subsequent analysis, utilizing successive weighting, yielded three minimum length trees (l = 403; ci = 85; ri = 92). The three trees differed in the arrangement of taxa at the base of the clade Namanereidinae. In one, Namalycastis was the sister group to the remaining namanereids, in the second both Lycastoides and Namalycastis formed a joint sister group to the remaining namanereids; and in the third Namalycastis, Lycastoides and the remaining namanereidine clade formed a trichotomy. A "Nelson" consensus tree (Fig. 1), which represents the information on grouping shared by all cladograms, had the same topology as the third cladogram. Relationships within the Nereididae. -In the following analysis, characters indicated in brackets are discussed in the order in which they occur on the cladogram (Fig. 1) and are grouped according to their occurrence below each node (roman numerals). Relationships within the Namanereidinae are not discussed, as a character set with a lower level of universality is used to elucidate the relationships within this subfamily (Glasby, 1990). The cladogram (Fig. 1) suggests that, of the three hesionid outgroups, Leocrates is the sister group of the Nereididae. Leocrates shares with the Nereididae the derived condition of having spinigers present in the post-sub-acicular fascicle of the neuropodia (30). The other two hesionids considered here have falcigers in this position. I. NEREIDIDAE.The Nereididae share the following derived character states: four pairs of tentacular cirri (7/); dorsal cirri with leaf-like or no cirrophores (23); supra-acicular notosetae are spinigers (24); supra-acicular neurosetae in the post- acicular fascicle are spinigers (26); supra-acicular neurosetae in the post-acicular fascicle being sesquigomph (27). II. NAMANEREIDINAEANDSISTERGROUP(GYMNONEREIDINAEPLus NEREIDINAE). The Gymnonereidinae and the Nereidinae are defined on the basis of two synapomorphies: dorsal notopodialligule present (18) and median ligule present (20). Acceptance of the first synapomorphy means that we must also accept a reversal to the ancestral state (dorsal notopodialligule absent) in two taxa, Tylorrhynchus and Profundilycastis. Acceptance of the second synapomorphy results in a reversal in Tylonereis (median ligule absent). GLASBY: PHYLOGENETIC RELATIONSHIPS IN NEREIDIDAE 567

11 ",13" 30

5,16

o reversals

Il homoplasies (convergences & parallelisms)

• synapomorphies & autapomorphies

Figure 1. Cladogram of selected Nereididae and outgroups. Arabic numerals represent characters, roman numerals refer to the branch points discussed in the Relationships section of the Results. Synapomorphies (and autapomorphies), homoplasies and reversals are indicated separately. 568 BULLETIN OF MARINE SCIENCE, VOL. 48, NO.2, \99\

The hypothesis presented here is that the Namanereidinae is the sister group of the Gymnonereidinae plus Nereidinae. The presence of spherical palpostyles (5) and of dorsal aciculae supporting the neuropodia (16) are synapomorphies holding the Namanereidinae together. III. STENONINEREISAND SISTERGROUP.Stenoninereis is the most plesiomorphic Gymnonereidinae. It is defined by a single autapomorphy, pygidium with wing- like lateral lobes (34'). There are two non-congruent characters that must be considered homoplasies on the basis of overall parsimony. These are supra-acicular neurosetae in the pre-acicular fascicle are spinigers (28), and the presence of giant-sized oocytes (35). The spinigers (28) are also present in Tylonereis and the giant-sized oocytes are present in the namanereids Namanereis, Cryptonereis and Lycastopsis. Both features are thought to be easily acquired, with giant-sized oocytes often associated with direct development, presumably an adaption for life in low-salinity environments (Schroeder and Hermans, 1975). The sister group of Stenoninereis is defined by nine synapomorphies: the pos- session of papillae in Areas I, II, III, IV, VI, and VII and VIII (8-11, 13-14); parapodia 1 and 2 with neuroaciculae only (15); post-setal neuropodia 1lobe present (21); and sub-acicular neUTOsetae in the post-acicular fascicle being sesquigomph (31). This is perhaps an overestimate of the real number of synapomorphies as characters 8-11 and 13-14 are very closely correlated and may have been better treated as a single character. Acceptance of the synapomorphy indicated by character 21 results in four reversals to the plesiomorphic condition (post-setal neuropodiallobe absent) in Tylorrhynchus, Olganereis, Perinereis-Neanthes and Pro- fundilycastis. Character 31 forces a reversal in the same four taxa (sub-acicular neurosetae in the post-acicular fascicle being heterogomph). IV. DENDRONERElDES-TYLORRHYNCHUSAND SISTERGROUP.The next most pie- siomorphic group in the Gymnonereidinae comprises Dendronereides-Tylorrhyn- chus. This group may be defined on the basis of the acquisition of papillae on Area V of the pharynx (12'). The sister group is characterized by five synapomorphies: pTOstomium relatively elongate (1); glandular patches on the dorsal edge of the parapodia (17); ventral neuropodialligule in setiger 10 present (22); supra-acicular notosetae being homogomph (25); and supra-acicular neurosetae in the post-acicular fascicle being homogomph (27'). V. AUSTRAWNEREISAND SISTERGROUP.There are no autapomorphies defining Australonereis as recognized in this cladistic hypothesis, however the presence of a series of paired, transversely arranged ventral papillae (not included in the present analysis), which is unique to Australonereis and not present in the outgroup, is a good autapomorphy (Hartman, 1954). The sister group of Austra/o- nereis is united by a single synapomorphy, peristomium length greater than the length of setiger 1 (6). VI. OLGANEREISAND SISTERGROUP. Similarly the hypothesis presented here shows no autapomorphies for Olganereis. Three reversals define O/ganereis (9, 21, 31) as indicated in Figure 1. However, an equally parsimonious interpretation of character state changes in character 9 would be a reversal to the ancestral condition (no papillae) in the vicinity of node V and a synapomorphy involving two state changes (no papillae --> papillae --> conical paragnaths) for Neanthes and Perinereis (node VII). Considering the strength of the relationships (i.e., numbers of synapomorphies) defining groups at the base of the cladogram, I feel the place- ment of O/ganereis is reasonable. Further analyses, at a lower level of universality, may reveal autapomorphies for this taxon. The sister group of O/ganereis is defined by one synapomorphy, palpophores large and articulated (4). GLASBY: PHYLOGENETIC RELATIONSHIPS IN NEREIDIDAE 569

VII. TYLONEREIS-NICON-PROFUNDILYCASTIS ANDSISTERGROUP(NEREIDINAE). The grouping together of the remaining Gymnonereidinae is tenuous, according to this hypothesis, due to the lack of a synapomorphy. The reversal of character 9 is not the only most parsimonious interpretation (see above). Nevertheless, the position of this group as the most derived Gymnonereidinae would appear reasonable based on the strength of the cladogram near the base. The sister group, the two nereidines (Neanthes and Perinereis) are defined by seven synapomorphies as follows: pharynx with Areas I, II, III, IV, V, VI, VII and VIII with paragnaths (8'-14'). Perinereis is defined by two autapomorphies, pharynx with Areas IV and VI with bar-shaped paragnaths (11", 13").

DISCUSSION Some controversy exists over whether the Namanereidinae are derived from an ancestor with biramous or uniramous parapodia. The parapodia of the Nereidi. dae vary in complexity from fully biramous (two-three notopodialligules internally supported by a dorsal acicula; and two neuropodialligules internally supported by a ventral acicula) to sub-biramous (neuropodialligule only, supported by a dorsal acicula and a ventral acicula). Some genera have an intermediate development of the parapodia between these two extremes (e.g., Tylorrhynchus). The reduced notopodial condition of the namanereids is considered by some to be ancestral (Saint-Joseph, 1900; Gravier, 1902; Fitzhugh, 1987) and by others to be derived (Southern, 1921; Banse, 1977a). C<;>rrea(1948) repeats Feuerborn's (1931) observation that the presence of reduced notopodia in adult namanereids represents an ontogenetic reduction, but neither offer an explicit opinion on wheth· er the namanereids are ancestral to, or derived from, biramous nereidids. In this study I have recognized that parapodial morphology may be usefully divided into two components: the position ofthe dorsal aciculae in the parapodia (16) and the form taken by the notopodiallobe and 1igu1es(18-20). In the Na- manereidinae the position of the dorsal aciculae in supporting the neuropodia is derived. The other nereidids share the ancestral condition with the Hesionidae of having the dorsal aciculae supporting the notopodia (or, in the case of Ophiod- romus, the dorsal cirrus). The Namanereidinae are symplesiomorphic with the Hesionidae in the absence of no to podia I lobes and ligules. I feel justified in dealing with the parapodia as components of the aciculae and lobes/ligules as the presence of dorsal aciculae is not always correlated with the maximum development of notopodial lobes/ligules (e.g., Tylorrhynchus, Profundilycastis, and Tylonereis) although they may be co-variant. The other synapomorphy of the Namanereidinae, indicated in the proposed cladistic hypothesis (Fig. 1), is spherical palpostyles. The function of the palps (palpophores plus palpostyles) is probably sensory. A spherical palpostyle would have less surface area than a conical palpostyle of corresponding size, and presumably a decreased sensory capability. The Namanereidinae show a general evolutionary trend toward compactness and reduction of many head end sensory appendages including palps, antennae, tentacular cirri and eyes (Glasby, 1990). The absence of ceratophores [cirrophores] of the dorsal cirri, identified by Fitzhugh (1987) as a synapomorphy for the Namanereidinae, is homoplasious in his preferred cladogram (fig. 1), defining also most of the Gymnonereidinae and Nereidinae. I believe that it is more parsimonious that either the absence of cirrophores (23,1') or cirrophores leaf-like (23,1) are derived from cirrophores present (23,0), and further that both are synapomorphies at a higher level, for the 570 BULLETIN OF MARINE SCIENCE, VOL. 48, NO.2, 1991

Nereididae. In particular, I disagree with Fitzhugh who indicates that Stenoni- nereis, Tylorrhynchus and Micronereis have cirrophores. The so called cirrophores in Tylorrhynchus are more ventral than usual and, according to Pettibone (1971), correspond to the usual upper [dorsal] notopodialligule. The "cirrophores" of Stenoninereis are interpreted here as being leaf-like and resemble those of some namanereids; the cirrophores of Micronereis are not mentioned by either Banse (1977b) or Paxton (1983). If my interpretation of this structure is correct, then the only true cirrophores in the Nereididae occur in Ceratocephale, Gymnonereis, Tambalagamia and questionably in Lycastoides (observations from the literature). Therefore, a more parsimonious explanation of the phylogeny of this character in Fitzhugh's cladogram would be a synapomorphy defining the Nereididae and reversals for the Ceratocephale-Gymnonereis-Tambalagamia group and for Ly- castoides. This study supports Fitzhugh's (1987) finding that the Namanereidinae is derived from a phyllodociform ancestor over the alternative hypothesis that the Namanereidinae has evolved from a nereidid ancestor (Banse, 1977a). However, I do not agree that the ancestor necessarily had reduced notopodia (Fitzhugh, 1987: 180). It is equally conceivable that the ancestor resembled the biramous Leocrates. A taxonomic revision and phylogenetic study of the Hesionidae is required to further resolve the outgroup phylogeny, especially in regard to the parapodial attributes. Also a comparative anatomical study on the position ofthe dorsal aciculae in the parapodia of nereid ids and hesionids may shed further light on whether this structure is homologous in the two groups.

ACKNOWLEDGMENTS

This work is taken from my Ph.D, thesis on the taxonomy and phylogeny of the Namanereidinae (Nereididae: Polychaeta), which was conducted under an Australian Postgraduate Research Award. I would like to thank my Ph.D. supervisors Dr. P. Hutchings (Australian Museum) and Prof. D. Anderson (University of Sydney) for their help and encouragement. I would also like to thank, for the loan of polychaete specimens, Ms L. Harris (AHF), Dr. D. George and Mr. A. Muir (BMNH), Dr. G. Hartmann-Schroder (HZM), Dr. K. Fauchald (USNM), and Dr. G. Hartwich (ZMB).

LITERATURE CITED

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Watrous, L. E. and Q. D. Wheeler. 1981. The out-group comparison method of character analysis. Syst. Zool. 30( I): 1-11. Westheide, W. 1977. Phylogenetic systematics of the genus Microphthalmus (Hesionidae) together with a description of M. hartmanae nov. sp. Pages 103-113 in D. J. Reish and K. Fauchald, eds. Essays on polychaetous annelids in memory of Dr. Olga Hartman. Allan Hancock Found., U. South. Calif., Los Angeles. --. 1982. Ikosipodus carolensis gen. et sp. n., an interstitial polychaete from North Carolina, U.S.A., and its phylogenetic relationships within the Dorvilleidae. ZoOI. Scr. 11(2): 117-126. --. 1985. The systematic position of the Dinophilidae and the archiannelid problem. Pages 310- 326 in S. Conway Morris, J. D. George, R. Gibson and H. M. Platt, eds. The origin and relationships of lower invertebrates. Oxford University Press. -- and N. W. Riser. 1983. Morphology and phylogenetic relationships of the neotenic interstitial polychaete Apodotrocha progenerens n. gen., n. sp. (Annelida). Zoomorph. 103: 67-87. Wiley, E. O. 1981. Phylogenetics. The theory and practice of phylogenetic systematics. John Wiley and Sons, New York. XV + 439 pp.

DATEACCEPTED: June 5, 1990.

ADDRESS: Australian Museum, Division of Invertebrate Zoology, P.O. Box A285, Sydney South. N.S. w.. 2000. Australia.

ApPENDIX

Material examined for the cladistic analysis of the Nereididae.

Ingroup Taxa

Nereididae: Namanereidinae Cryptonereis malaitae Gibbs (paratype) 7 BMNH ZB 1970.31 Solomon Islands, Malaita, Alite Har- bour, Langa-Langa Lagoon. Lycastopsis beumeri Augener, 1922 (syntypes) 3 HZM V-7061 Cuba, Habana. Namalycastis abiuma (Millier in Grube, 1872) (holotype) I 2MB Q3436 Brazil, Desterro (now Santa Catarina Island). Namanereis quadraticeps (Blanchard in Gay, 1849) (neotype) I AM WI98509 Chile, Straits of Magellan, just north of Bahia San Gregorio.

N ereididae: Gymnonereidinae Stenoninereis martini Wesenberg-Lund, 1958 (syntypes) 2(2) USNM 29726 St. Martin, Devil's Hole Swamp, near Simson Bay Bridge = Nicon lackeyi Hartman, 1958 (holotype) l(l) 29627 Rorida, Sarasota County. Tylorrynchus heterochetus (Quatrefages, 1865) [=Nereis (Leptonereis) distorta Treadwell, 1936 (holotype of distorta) 1(1) USNM 20118 China, near Amoy. Olganereis edmondsi (Hartman, 1954) (non-type) 2(2) AM W12247, 2(2) AM W18290, 1(1) AM W 18294 Australia, South Australia, Kangaroo Island, American Bay (type locality). Nicon maculata Kinberg, 1866 (non-type) 1(1) AM W202509 Tasmania, offSt. Patrick's Head. Australonereis ehlersi (Augener, 1913) (non-type) 16(4) AM W5615 Australia, Western Australia, Bunbury, Leschenault estuary (near type locality). Dendronereides heteropoda Southern, 1921 (non-type) 9(3) NTM W2013 Australia, Northern Terri- tory, Daly River, Palmerston Island; 1(1) NTM W2735 Daly River, Woolianna Station; 5(5) BMNH ZK 1920.12.15.1-4 Thailand, Bangkok (as Dendronereides sp.) Tylonereis bogyawleskyi Fauvel, 1911 (non-type) many(2) AM unreg.; many(2) AM unreg. Hong Kong, Sai Kong. Profundilycastis profundus (Hartman, 1965) (holotype) AHF nlO980 off Bermuda; (non-type) 1(1) AHF unreg. off Bermuda?

Nereididae: Nereidinae Neanthes vaalii Kinberg, 1866 (non-type) 3(3) AM WI8306 Australia, South Australia, Kangaroo Island, 3 km SW of Cape Rouge (near type locality). GLASBY: PHYLOGENETIC RELATIONSHIPS IN NEREIDIDAE 573

Perinereis novae-hol/andiae Kinberg, 1866 [=Perinereis amblyodonta Schmarda, 1861] (non-type) 7(3) AM W4859 Australia, New South Wales, Port Jackson (type locality).

Outgroup Taxa

Hesionidae Ophiodromus didymocerus (Schmarda, 1861) [=Podarke didymocerus] (non-type) 1(1) AM W4489 Australia, New South Wales, Port Jackson (type locality); 1(1) AM W4492 Australia, New South Wales, Long Reef. Leocrates chinensis Kinberg, 1857 (non-type) 2(2) AM W198152 Australia, Queensland, Calliope River (type locality, China). Hesione splendida Savigny, 1820 (non-type) 1(1) AM W7439 New Caledonia, Aquarium de Noumea (type locality, Red Sea). The ingroup species examined and listed below are type species for their respective genera. Character state information for the namanereidine species (excluding C. malaitae and L. alticola) was supplemented by a large series of non-type material (see Glasby, 1990). The only material of C. malaitae known to exist is the type material. Character state data for L. alticola were taken from the type description as the types are lost and no other specimens are known to exist. Character state data for other ingroup species were supplemented by descriptions in the literature. The number of specimens examined is indicated in brackets after the number of specimens in the lot. The outgroup (hesionid) species, Ophiodromus didymocerus. is a non-type species and the specimens examined are also non-type. The outgroups, Hesione splendida and Leocrates chinensis, are type species for their respective genera and the specimens examined are non-type.