Phylogenetic Relationships of the Gonostomatidae (Teleostei: Stomiiformes)

BULLETIN OF MARINE SCIENCE, 62(3): 715–741, 1998

PHYLOGENETIC RELATIONSHIPS OF THE GONOSTOMATIDAE (TELEOSTEI: STOMIIFORMES)

Antony S. Harold

ABSTRACT Recent studies have suggested that the family Gonostomatidae is monophyletic if Diplophos, Manducus, and Triplophos are excluded, but no supportive characters for this hypothesis have been described. The remaining four genera, Bonapartia, Cyclothone, Gonostoma, and Margrethia, are found to share such derived features as loss of IP photophores, a shortened premaxilla, a peculiar pattern of maxillary dentition, and modified pharyngobranchials. The current analysis shows Cyclothone to be a clade nested within Gonostoma, rendering the latter paraphyletic. With these results Cyclothone should be considered a junior synonym of Gonostoma but the classification is not amended at this time, pending the completion of other studies. The relationships of this restricted Gonostomatidae to other stomiiform subgroups is discussed. Diplophos and Manducus are proposed to be sister groups and together comprise the sister group of all other stomiiforms. The evidence for the interrelationships of Triplophos is contradictory but initial data presented here indicate that this genus is probably more closely related to the photichthyans than to gonostomatans.

The composition and relationships of the Gonostomatidae has been a continuing problem. Weitzman (1974) reviewed its history, while concentrating on the related Sternoptychidae, and provided a phylogeny and classification of stomiatoids (= stomiiforms) that was based on the principles of phylogenetic systematics. The main pur- poses of the present paper are to provide a phylogenetic diagnosis for the Gonostomatidae and an analysis of intrarelationships. Grey (1964) placed 21 genera into the Gonostomatidae. Weitzman’s (1974) treatment of the family was the most restrictive up until that time, including only six genera: Gonostoma Rafinesque (Fig. 1), Cyclothone Goode and Bean (Fig. 2), Bonapartia Goode and Bean (Fig. 3), Diplophos Günther (including Manducus Goode and Bean), Margrethia Jespersen and Tåning and Triplophos Brauer. He greatly reduced the size of the family by placing the “maurolicid” genera (e.g., Maurolicus Cocco, Thorophos Bruun) into the Sternoptychidae, and moving seven other genera (e.g., Polymetme McCulloch, Woodsia Grey) into a new family, the Photichthyidae. These had all been considered gonostomatids by Grey (1964). Weitzman was unable to find any derived characters that were shared by his six gonostomatid genera, contending that the family would continue to be a “catch basket of relatively primitive and advanced stomiatoid genera” until further phylogenetic studies could be completed. He stated that Diplophos, for example, possesses a series of primitive characters for stomiiforms, including a large, toothed basihyal. This genus, including the species here ascribed to Manducus, was later proposed by Fink (1984) as the sister group to other stomiiforms. Some character data suggest that one or more species of Diplophos may be more closely related to photichthyans than to other Diplophos species and Manducus (Ahlstrom et al., 1984). Further consideration of characters relating to the interrelationships of these species is clearly needed.

715 716 BULLETIN OF MARINE SCIENCE, VOL. 62, NO. 3, 1998 , USNM uncat., M/V Oregon Sta. 5688, 169.0 mm SL. , USNM uncat., M/V Oregon elongatum

Gonostoma Figure 1. Figure HAROLD: GONOSTOMATID PHYLOGENY 717 , USNM 149537, 54.0 mm SL. atraria Cyclothone Figure 2. Figure 718 BULLETIN OF MARINE SCIENCE, VOL. 62, NO. 3, 1998 , USNM 203294, 52.2 mm SL. pedaliota

Bonapartia Figure 3. Figure HAROLD: GONOSTOMATID PHYLOGENY 719

The Sternoptychidae and Gonstomatidae were placed as sister groups in Weitzman’s (1974) phylogeny, their clade collectively referred to the infraorder Gonostomata. This relationship was based on the presence of four pectoral radials and the occurrence of type Alpha or Beta photophores. Ahlstrom et al. (1984) discussed this evidence and reached the conclusion that neither was a synapomorphy of the Gonostomata. They did suggest, however, that protracted development, a derived feature shared by all sternoptychids and gonostomatids except Cyclothone, could be considered a diagnostic character of the group. The sister group of the Gonostomata, the infraorder Photichthya (Photichthyidae plus the barbeled Stomiatoidea), was diagnosed by Weitzman (1974) by the presence of type Gamma photophores and three pectoral radials. Fink (1984) and Ahlstrom et al. (1984) agreed that the Gonostomatidae should be restricted to Bonapartia, Cyclothone, Gonostoma and Margrethia, based on unspecified myological and osteological features of the head. In the present paper I describe a series of characters that support the monophyly of the group. Gonostomatid intrarelationships are proposed, and possible relationships of Diplophos, Manducus and Triplophos presented. Characters having a bearing on higher-level stomiiform relationships are described and optimized in the context of a cladogram presented by Harold and Weitzman (1996), who also deal with the photichthyans. The interrelationships of Triplophos appear to be most relevant to the photichthyans and are therefore discussed in greater detail by Harold and Weitzman (1996).

MATERIALS AND METHODS

Characters were polarized by outgroup comparison. Functional outgroups allowed characters that are unique to stomiiforms to be polarized. Watrous and Wheeler (1981) and Mooi (1989) explain and illustrate this method. A matrix of coded characters was analysed using Hennig86 (Farris, 1988) with the branch-swapping options “bb” and “ie-”. Multistate characters were run unordered: discussions of ordered transitions of these characters are based on their optimizations on the most parsimonious cladogram(s). Trees were rooted using an outgroup consisting of the following taxa, as listed in the matrix (Table 1): Diplophos, Manducus, Triplophos, Thorophos, Sternoptychidae minus Thorophos, and Yarrella. A complete character matrix in support of the gonostomatid-sternoptychid sister group relationship as well as other higher-level stomiiform relationships depicted in Figure 4 is given in Harold and Weitzman (1996). Their cladogram is used for the purpose of optimizing and discussing characters that are specific to the problem of hypothesiz- ing gonostomatid relationships. In the list of characters below the derived condition is briefly described, followed by the plesiomorphic condition, and its distribution if there is variability among other stomiiforms or outgroups. The description of the character is followed by homoplastic occurrences and any alternative optimizations implied by the cladograms. Characters exhibiting homoplasy are annotated by “c” if there is inferred convergence, “R” if the character is in a reversed state and “r” if the character reverses at a lower level of generality. The states of multi-state characters are given in parentheses. Characters with alternative, equally parsimonious optimizations are indicated as such in the character list by a Roman numeral suffix added to the character number. Terminology follows Fink and Weitzman (1982) for osteology and ligaments, Weitzman (1974: 1986) for photophores and Winterbottom (1974) for myology. Specimens were cleared and stained following the method described by Taylor and Van Dyke (1985) and modifications by Potthoff (1984). Stomiiform and outgroup representatives studied are listed below by catalog number or, if not available, by institutional acronym and locality data. Institutional abbreviations follow Leviton et 720 BULLETIN OF MARINE SCIENCE, VOL. 62, NO. 3, 1998 5 0 0 0 0 0 0 0 1 1 0 1 0 1 0 1 0 0 0 0 5 0 0 0 0 0 0 0 0 0 0 0 0 1 0 2 0 0 0 0 – 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 6 10 10 00 00 00 01 01 00 00 00 00 00 00 00 20 00 00 00 01 41 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 0 1 0 0 0 4 0 0 0 1 1 1 1 1 0 1 0 0 0 0 0 0 0 0 0 – 0 0 0 0 0 0 0 0 1 0 1 0 0 0 0 0 0 0 0 1 0? 0? 0? 11 11 01 11 00 01 00 11 00 00 0? 0? 00 00 0? 0? 40 0 1 0 0 0 0 1 0 1 0 1 0 1 0 0 0 0 0 0 0 0 4 0 0 0 1 1 1 1 1 1 1 2 0 0 0 0 0 0 0 0 – 0 0 0 1 1 1 1 1 0 1 0 0 0 0 0 0 0 0 0 6 0 01 01 10 10 10 10 10 11 10 11 00 00 00 00 00 00 00 00 35 .)txetnidenifedsretcarahC(spuorgbusmrofiimotsrehtodnasditamotsonogrofxirtametatsretcarahC.1elbaT 1 0 0 0 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 3 0 0 0 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 – 0 0 0 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 1 0 00 00 11 1 10 11 10 11 10 11 00 00 00 00 00 00 00 00 30 retcarahC 0 0 0 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 0 0 – 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 0 0 6 00 00 00 01 0 01 01 01 01 01 02 10 10 10 00 00 00 00 00 25 0 0 0 0 0 0 0 0 0 0 0 1 1 1 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 0 0 1 1 1 0 0 0 0 0 – 1 0 0 0 0 0 0 0 0 0 0 1 1 1 0 0 0 0 1 1 00 00 00 01 01 01 01 01 01 01 01 10 00 10 00 00 00 00 00 20 ? ? 0 0 0 0 1 1 1 1 0 1 1 1 2 2 1 1 1 2 1 2 1 1 1 2 2 2 2 2 2 2 2 2 1 2 0 0 0 – 1 1 0 0 0 1 1 1 1 1 1 1 1 1 0 0 0 0 0 6 10 11 00 00 00 10 10 10 10 10 10 10 11 11 00 00 00 00 00 15 0 0 0 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 1 0 0 0 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 – 0 0 0 1 1 1 1 1 1 1 1 1 1 1 0 0 0 2 0 1 00 00 00 10 10 10 10 10 10 10 10 11 11 11 00 00 00 00 00 10 0 0 0 1 1 1 1 1 1 1 0 1 1 1 1 1 0 0 0 1 0 0 0 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 – 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 65 00 00 00 01 01 01 01 01 01 01 01 01 01 01 00 00 10 10 10 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 5– 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 1 0 0 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 10 10 10 10 11 11 11 11 11 11 11 11 11 11 11 10 10 00 00 00 ) e a d ) i e a h a r c t e s d m e y i i s a a t u a s t y o n p c i d n o r i h i i i i o s t t e t l a s h r n n n h n a a i r c y u i e e c a t l i e d a y h l n d m t t t t t b s e a b e a i u o m S p h a o v p e m l a ( n h u i c t r o m u i t i a e a a n a s t h P n s t i i i i s s s g a e (1 r n o t a p o o m l h h p o o u n d e o r i t t i y h g h i h t o a c h h u c l t h a e e l g h p n p P S t u l p p t s r r e n a p n o o o e o d o o r e a l r o g g r l b a r l o l l r r r n e e l g e e d b p n c n r o p p i a a a h h ...... o i i y o a r h t t o1 Y T G G G G G G G C B M M o T M D D HAROLD: GONOSTOMATID PHYLOGENY 721 al. (1985). All material was cleared and stained unless annotated by “D” to indicate dissected only or “E” for external examination. The range of standard length (mm) is provided in parentheses following the number of specimens examined.

STOMIIFORMES GONOSTOMATIDAE.—Bonapartia pedaliota, MCZ 79861 (1, 37.2), USNM 316477 (1, 51.3); Cyclothone acclinidens, USNM 260174 (1, 40), USNM 316481 (2, 45.8–46.3); Cyclothone alba, MCZ 97809 (2, 21.6–25.3); Cyclothone braueri, MCZ 97810 (1, 31.2); Cyclothone livida, MCZ 55208 (2, 31.2–31.5); Cyclothone microdon, USNM 206847 (2, 51.9–53.4); Cyclothone pallida, MCZ 89568 (2, 31.5–49.8); Cyclothone parapallida, MCZ 97187 (1, 58.1); Cyclothone pseudopallida, MCZ 91734 (2, 36.5–37.2); Gonostoma atlanticum, CAS 28001 (1, 49.1); Gonostoma bathyphilum, USNM 206833 (1, 126.6), USNM 219951 (1, 126.9); Gonostoma denudatum, ROM 1626CS (1, 46.3); Gonostoma ebelingi, USNM 324457 (1, 139.6); Gonostoma elongatum, USNM 206788 (1, 88.4), USNM 313688 (1, 140.0), USNM 324459 (1, 49.9); Gonostoma gracile, BPBM 26090 (2, 45–61), BPBM 26136 (1, 81), USNM 135491 (2, 67.0–100.1); Gonostoma longipinnis, USNM 324458 (1, 54.7); Margrethia obtusirostra, USNM 248771 (1, 49.5); Margrethia valentinae, USNM 206761 (2, 56.3–63.6, 63.6 D only). UNPLACED (PREVIOUSLY GONOSTOMATIDAE).—Diplophos taenia, MCZ 52537 (1, 17.0), ROM 58061 (1, 57.4), USNM 206614 (1, 171.0), USNM 248764 (2, 114.9–128.4); Diplophos rebainsi, ISH 543/76 (1, 179.5), USNM 225012 (1, 252.0, CS part). Manducus greyae, USNM 135691 (1, 105.8, CS part), Manducus maderensis, MCZ 82187 (1, 24.3), MCZ 52541 (1, 51.8), USNM 186282 (1, 90.8), USNM 186364 (2, 107.1-111.5, 111.5 D only). Triplophos hemingi, USNM 199832 (1, 175), USNM 203384 (1, 83.5), USNM 316479 (1, 190). PHOTICHTHYIDAE.—Ichthyococcus ovatus, MCZ 59230 (1, 34.2, D), MCZ 60337 (7, 8.5–37.6), MCZ 89140 (1, 10.5); USNM 49337 (1, 38.4), USNM 316480 (1, 45.1); Photichthys argenteus, MCZ 62111 (4, 24.7-29.8), MCZ 81732 (2, 31.6–54.0), USNM 316478 (1, 65.7), USNM uncat., ANTON BRUUN Cr. 3, Hydro Sta. 157, (1, 70, D); Pollichthys mauli, MCZ 80815 (1, 13.3), USNM 203408 (2, 35.0-42.0), USNM 248981 (1, 39.9, D), USNM 248982 (2, 39.9–41.4); Polymetme corythaeola, USNM 203281 (1, 117.1, D), USNM 306167 (1, 112.8); Polymetme thaeocoryla, USNM uncat., OREGON II, Sta. 10200 (1, 129.7); Vinciguerria attenuata, MCZ 62109 (16, 21.0– 31.2), Vinciguerria lucetia, USNM 315776 (2, 18.9-43.9); Vinciguerria nimbaria, USNM 206762 (3, 32.3–47.6, 47.6 D only); Yarrella blackfordi, USNM 186280 (1, 138.7); Woodsia meyerwaardeni, ISH 454/76 (1, 80.0), LACM 11509–18 (1, 18.0, E); USNM 208349 (1 paratype, 48.3). STERNOPTYCHIDAE.—Material listed in Harold (1994) STOMIIDAE.—Astronesthes niger, USNM 301281 (1, 63.2); Astronesthes similis, USNM 257476 (1, 121.1); Bathophilus pawneei, USNM 159052 (2, 114.1–118.3); Borostomias antarcticus, USNM 199821 (1, 111.7); Chauliodus schmidti, USNM 225045 (4, 51.2–165.0); Chauliodus sloani, USNM 199500 (2, 154.8–163.1); Heterophotus ophistoma, USNM 225025 (1, 133.2); Malacosteus niger, USNM 199834 (1, 105.6); Neonesthes capensis, USNM 199823 (1, 114.8).

OUTGROUP TAXA ARGENTINIDAE.—Argentina sphyraena, USNM 238016 (1, 128.7); Argentina striata, USNM 188224 (2, 112–125); Glossanodon struhsakeri, USNM 36418 (1, 117.0). OSMERIDAE.—Mallotus villosus, USNM 306411 (1, 72.2); Spirinchus dilatus, USNM 104689 (1, 108.6); Thaleichthys pacificus, CAS 15378 (1, 104.4). GALAXIIDAE.—Galaxias maculatus, USNM 203872 (2, 44.0-56.4); Galaxias vulgaris, USNM 203886 (1, 58.1). SALMONIDAE.—Coregonus artedi, ROM 1022CS (2); Coregonus clupeaformis, ROM 1028CS (2, 45.3–53.5 TL); Coregonus nasus, ROM 1012CS (2, 38.8–42.5); Oncorhynchus gorbuscha, ROM 1005CS (4, 42.6–43.5 TL); Oncorhynchus mykiss, ROM 534CS (7), ROM 830CS (2); Prosopium cylindraeceum, ROM 0028CS (2, 72-78 TL); Salmo trutta, ROM 1013CS (2, 46.7–50.9 TL); 722 BULLETIN OF MARINE SCIENCE, VOL. 62, NO. 3, 1998

Figure 4. Cladogram showing interrelationships of major stomiiform subgroups. Characters defined in text. * indicates homoplastic character(s).

Salvelinus fontinalis, ROM 0998CS (1); Stenodus leucichthys, ROM 1016CS (1, 48.7 TL); Thymallus arcticus, ROM 0039CS (10, 70–90 TL). AULOPIDAE.—Aulopus filamentosus, USNM 225043 (2, 143–173). CHLOROPHTHALMIDAE.—Chlorophthalmus agassizi, USNM 159377 (1, 121), USNM 159385 (2, 56.2–85.1); Parasudis truculentus, USNM 159407 (2, 101.0–118.0). SYNODONTIDAE.—Synodus variegatus, USNM 217675 (1, 71.0). NEOSCOPELIDAE.—Neoscopelus macrolepidatus, USNM 317160 (1, 54.5). MYCTOPHIDAE.—Myctophum affine, USNM 317161 (1, 52.7).

CHARACTERS

The states of 51 characters for 19 taxa are listed in Table 1. Interpretations of these characters are made in the context of two cladograms, one for higher level stomiiform relationships documented by Harold and Weitzman (1996) and one for relationships among gonostomatids. Evidence for monophyly for various stomiiform clades follows. CLADE A: ORDER STOMIIFORMES (Fig. 4).—Monophyly of the order is presented and discussed by Fink and Weitzman (1982) and reviewed by Harold and Weitzman (1996). There are seven unequivocal synapomorphies for the order, which include a unique photophore structure, Type 3 tooth attachment, and subdivision of the medial section of the adductor mandibulae (A1β of Rosen, 1973) into two sections, one inserting dorsally onto the maxilla and the other onto the primordial ligament. CLADE B: ALL STOMIIFORMS MINUS DIPLOPHOS AND MANDUCUS (Fig. 4).—1r. Extensor proprius pelvicus muscle is vertically oriented, originating dorsolaterally in connective tissue associated with the pleural ribs in all stomiiforms except Diplophos and Manducus, and the three deep-bodied hatchetfish genera Argyropelecus, Polyipnus and Sternoptyx. Primitively this muscle lies horizontally, overlying the adductor superficialis and originating along the anterolateral border of the anterior process of the pelvic bone, as in HAROLD: GONOSTOMATID PHYLOGENY 723

Figure 5. Pharyngobranchials and epibranchials of Gonostoma elongatum, USNM 313688, 140.0 mm SL, right side, medial view, anterior to left. Inset: pharyngobranchial 1, right side, lateral view. EB1, epibranchial 1; EB2, epibranchial 2; EB3, epibranchial 3; EB4, epibranchial 4; PB1, pharyngobranchial 1; PB2, pharyngobranchial 2; PB3, pharyngobranchial 3; PB4, pharyngobranchial 4; UP5, upper pharyngeal tooth plate 5.

Diplophos, Manducus and outgroups (e.g., Oncorhynchus, Spirinchus). The pelvic girdle in the three hatchetfish genera is vertically oriented and the extensor proprius muscle apparently has been lost (Harold, 1993). 3r. The first pharyngobranchial is ventrally bifurcate (e.g., Gonostoma elongatum, Fig. 5). In some clade B members (e.g., Triplophos hemingi, Fig. 6) PB1 is basally flared but not bifurcated; internally there are two divergent rodlike components that are probably homologs of the two externally visible branches of this bone in Gonostoma. The first pharyngobranchial is primitively cylindrical or slightly flared towards its articulation with the first epibranchial in Diplophos, Manducus (Fig. 6) and outgroup taxa examined. The photichthyan Ichthyococcus has a cylindrical PB1 but this is interpreted to be a reversal in the context of parsimony (Harold and Weitzman, 1996). 4. The basihyal is elongate, approximately vertically oriented, and lacking teeth in clade B. The main exception is the family Sternoptychidae in which the bone is lacking in all members, except some species of Polyipnus (Harold, 1994). In Diplophos and Manducus the basihyal is a flattened bone that is horizontally oriented and bears a dentigerous plate. Weitzman (1967b; 1974:407, fig. 75) and Fink and Weitzman (1982) provide description of some outgroup conditions and discussions of their significance. The present polariza- tion is further supported by an analysis of aulopiform interrelationships by Baldwin and Johnson (1996). 5c. The second preural centrum has a long, fully developed neural spine in all members of clade B. A short NPU2 was suggested by Ahlstrom et al. (1984) as a possible derived character of Manducus and Diplophos. Evidence indicating a basal position for these genera within the order plus the occurrence of short NPU2 in the outgroups (e.g., osmerids, salmonids) indicates that a short NPU2 is plesiomorphic condition for stomiiforms. One 724 BULLETIN OF MARINE SCIENCE, VOL. 62, NO. 3, 1998

Figure 6. Pharyngobranchials and epibranchials of Triplophos hemingi, USNM 316479, 190 mm SL, right side, medial view, anterior to left. Inset: pharngobranchial 1, right side, lateral view. Abbreviations defined in Figure 5 caption.

species of Diplophos, D. rebainsi, has a well-developed NPU2, explained possibly by convergence or by the possibility that this species is more closely related to or even the sister group of all other stomiiforms. DIPLOPHOS PLUS MANDUCUS.—6. The nasal bones are enlarged, anteriorly overlying the lateral processes of the rostrodermethmoid. The small nasal of other stomiiforms is probably plesiomorphic, comparing well with osmerids, such as Spirinchus (Weitzman, 1967b: fig. 1) and Thaleichthys, as well as salmonids and aulopiforms. In the Stomiidae, particularly the basal genera like Neonesthes and Astronesthes (Weitzman, 1967a: fig. 3), the nasal is slightly enlarged but expanded laterally and not positioned over the lateral process of the rostrodermethmoid. This condition in stomiids is likely a specialization and derived at that level. 7. A row of small photophores is present on the posterior portion of the lower jaw in Diplophos and Manducus. This row of light organs is unique to these genera but it is possible that their loss is derived for all remaining stomiiforms. 51. The anterior pleural rib is associated with the fourth vertebra in Diplophos and Manducus (my observation agrees with Fink and Weitzman, 1982 and Patterson and Johnson, 1995). Most other stomiiforms and outgroup taxa have the first rib on the third, occasionally on the second, vertebra, as in the sternoptychids Thorophos, Araiophos, Danaphos and Valenciennellus (Harold and Weitzman, 1996). Patterson and Johnson (1995) and Baldwin and Johnson (1996) report a first rib on the fourth vertebra in Pseudotrichonotus, interpreted here as a homoplasy. CLADE C: INFRAORDER GONOSTOMATA (STERNOPTYCHIDAE PLUS GONOSTOMATIDAE).—2c. Accessory horizontal photophore rows dorsal to the OA series are absent in all Sternoptychidae, Gonostomatidae except G. elongatum, and all Photichthya except Yarrella. They are found in Diplophos, Manducus, Triplophos and Yarrella. There are two equally parsimonious optimizations: (1), independent losses in clade C (Gonostomata) and a clade HAROLD: GONOSTOMATID PHYLOGENY 725

Figure 7. Cheek musculature of Maurolicus sp., USNM 100696, 49.0 mm SL, left side. a, A2α muscle; b, A2β muscle; c, A1β muscle.

consisting of all Photichthya minus Yarrella, and (2), in support of clade B with independent gains in Triplophos and Yarrella. There are no structural details that refute the homology of the accessory photophores, in fact, their anatomical positions (one per scale) and size distributions strongly support it. Further anatomical studies are needed, especially of the innervation of these photophores and of the comparable body regions of taxa lacking such organs. These photophores may be derived from neuromasts and, therefore, the occurrence of relatively un- differentiated photophores over much of the body, as found in Diplophos, Manducus, Triplophos and Yarrella, is presumably the primitive condition with their loss in various body areas being derived. 8r. Lateral section of the adductor mandibulae is divided into separate dorsal (A2α) and ventral (A2β) sections in the Gonostomatidae and all sternoptychids (e.g., Maurolicus sp., Fig. 7) except the deep-bodied genera Argyropelecus, Polyipnus and Sternoptyx. The generalized configuration, with one continuous, fanlike lateral adductor has been described and illustrated for Diplophos taenia by Fink and Weitzman (1982:57–58, fig. 15). 9r. Metamorphosis of serial photophores and other aspects of morphology is protracted in Sternoptychidae and the gonostomatid genera Bonapartia, Gonostoma and Margrethia (Ahlstrom, 1974; Ahlstrom et al., 1984). The only homoplasy is Cyclothone which has virtually simultaneous development of serial photophores through a white phase only. 726 BULLETIN OF MARINE SCIENCE, VOL. 62, NO. 3, 1998

Figure 8. Cladogram showing interrelationships of the Gonostomatidae (sensu stricto). Characters defined in text. * indicates homoplastic character(s).

This reversal may be due to heterochronic development resulting in paedomorphosis, as was supposed by Ahlstrom et al. (1984). 18(2)r. The ventrolateral ramus of pharyngobranchial 1, in taxa that have a ventrally bifurcate PB1, is elongate. Other stomiiforms have either a very slight bifurcation or none at all. The first pharyngobranchial is ventrally bifurcate with an elongate ventrolateral limb in Bonapartia, Gonostoma, Margrethia and Thorophos (Sternoptychidae). It may be interpreted as either derived for Gonostomata or independently derived in gonostomatids on the one hand and Thorophos on the other. With the former explanation, inferred loss in the other sternoptychids would tend to corroborate other evidence to the effect that Thorophos may be the sister group of the remaining members of the family (Harold and Weitzman, 1996). CLADE E: GONOSTOMATIDAE (Fig. 8).—The strict consensus diagram in Fig. 8 is based on a set of 8 equally parsimonious trees (length = 71 steps; C.I. = 0.85). Lack of resolution among Gonostoma species appears to be due more to a lack of applicable characters rather than to homoplasy. Monophyly of the family is supported by the following nine synapomorphies. 10. IP photophores are absent in all Gonostomatidae. All other stomiiforms have a row of serial photophores on the isthmus. 11. The palatine has the posterior cartilaginous articular process for attachment to the mesopterygoid well-developed as in Diplophos and Manducus but the posterior shaft is moderately elongate, extending along about a quarter of the length of the ectopterygoid in Gonostomatidae (s. str.). In other stomiiforms, except some stomiids, the posterior shaft is relatively short. HAROLD: GONOSTOMATID PHYLOGENY 727

Figure 9. Premaxillae and maxillae of representative stomiiforms, right side, lateral view. A, Cyclothone microdon, USNM 206847, 53.4 mm SL; B, Triplophos hemingi, USNM 316479, 190 mm SL; C, Diplophos rebainsi, USNM 225012, 252.0 mm SL; D, Diplophos taenia, USNM 206614, 171.0 mm SL.

12(1). Maxillary teeth are short, straight and subequal and very closely spaced in Bonapartia, Cyclothone, Gonostoma (Fig. 9) and Margrethia species. Except for some species of Cyclothone (Fig. 10A), these taxa have longer straight teeth of about the same length regularly interspersed among the short teeth may be lost or reduced in length through developmental truncation in the other Cyclothone. Subequal jaw teeth also occur in Ichthyococcus and Astronesthes but without interspersed longer teeth. Other stomiiforms, such as Triplophos (Fig. 10B), have maxillary teeth of various lengths, with no distin- guishable pattern to their distribution. The situation in Diplophos is variable, D. rebainsi (Fig. 10C) having the generalized dentition whereas in D. taenia (character 18[2], Fig. 10D) there is a pattern similar to that of the gonostomatids. In this case there are only 3 or 4 elongate teeth and they are of various lengths. In gonostomatids there are predomi- nantly two discrete lengths of maxillary teeth arranged in a distinct pattern. 13. The premaxilla is very short. The length of the bone is less than about one quarter of the length of the maxilla (Figs. 9 and 10A). A short premaxilla is present in Ichthyococcus but the extreme reduction of the bone, including loss of the alveolar process, suggests nonhomology. This interpretation is also indicated by a consideration of overall parsimony. In most other stomiiforms the premaxilla is roughly one half of the length of the maxilla. In Yarrella and, especially, Triplophos (Fig. 10B) the premaxilla is elongate, in the latter extending laterally about three quarters of the length of the maxilla. 14. A strong ligament attaches the distal tip of the fifth ceratobranchial to the ventrolateral surface of the cleithrum. In other stomiiforms and the outgroups the fifth ceratobranchial is attached via a sheet of diffuse, less organized connective tissue to the cleithrum in roughly the same position. 15. The dorsal portion of the tooth plate associated with the fourth pharyngobranchial (UP5, according to Johnson, 1992) anteriorly has a median process extending dorsally to the third pharyngobranchial. The process is lacking in other stomiiforms and the outgroups. 16. The second pharyngobranchial articulates anteriorly with the medial, cartilaginous condyle of the second epibranchial and lacks the rod-like anterior extension (Fig. 5) which, primitively, reaches well anterior of the EP2 condyle. The situation in Triplophos (Fig. 6) exemplifies the condition in nongonostomatid stomiiforms. This generalized condition is 728 BULLETIN OF MARINE SCIENCE, VOL. 62, NO. 3, 1998

Figure 10. Jaws and suspensorium of Gonostoma elongatum, USNM 313688, 140.0 mm SL, right side, lateral view.

wide-spread among basal euteleosts, as shown by several of Rosen’s (1973) illustrations: Bramocharax baileyi (Characidae), “Salmo gairdneri” (= Oncorhynchus mykiss) (Salmonidae), Harpadon nehereus (Synodontidae), Paralepis speciosa (Paralepididae) and Myctophum obtusirostris (Myctophidae) (Rosen, 1973: figs. 3, 5, 8, 16 and 69, respectively). 17. The medial radial of the pelvic fin has an elongate posterior process adhering to but not fused with the ventral half of the medial fin ray. The character described as derived here appears to occur in many of the outgroups, such as the osmerid Spirinchus thaleichthys (Weitzman, 1967: fig. 5). All other stomiiforms examined have either a short posterior process, as in Neonesthes and Polymetme (Fink, 1985: figs. 61 and 66, respectively) or none at all, as in many stomiids (e.g., Trigonolampa; Fink, 1985: fig. 64). The parsimonious interpretation of the situation in stomiiforms is that evolutionary reduction of the process is a synapomorphy of the order and its occurrence in gonostomatids is a reversal and atavistic. 19(1)r. An elongate process of the parapophysis of the first vertebra is present in Gonostoma elongatum, G. atlanticum, G. denudatum, G. gracile, G. ebelingi, Margrethia, Diplophos, Manducus (Fig. 11A) and some Cyclothone (Fig. 12B). In Bonapartia there is some extension of the parapophysis but it does not approach the condition of some of these taxa (e.g., G. elongatum, Fig. 12A) and may represent a derived, reduced condition. This process is interpreted as a basal ossification of Baudelot’s ligament by Patterson and Johnson (1995). Among basal stomiids there are clearer cases of ossification of Baudelot’s ligament (e.g., Borostomias elucens; Fink, 1985: fig. 58) and these are not homologous with the situation described here for basal stomiiforms, based on both morphology and a consideration of parsimony. First parapophysis elongation is absent in other stomiiforms (e.g., Triplophos hemingi, Fig. 11B). There is much variation among outgroups with re- spect to ossification of Baudelot’s ligament (Patterson and Johnson, 1995) but overall the HAROLD: GONOSTOMATID PHYLOGENY 729

Figure 11. Anterior vertebral centra and associated structures; right side, first vertebra at right. A, Manducus maderensis, USNM 186364, 107.1 mm SL; B, Triplophos hemingi, USNM 199832, 175 mm SL. ANA, accessory neural arch; BL, Baudelot’s ligament; EN, epineural; NA1, neural arch of first vertebra; PAR, parapophysis; PL, pleural rib; SN, supraneural.

plesiomorphic condition appears to be a parapophysis of the first centrum that is enlarged relative to that of the second as well as not showing ossification of Baudelot’s ligament. Ossification of Baudelot’s ligament appears to be correlated with the occurrence of an ossified accessory neural arch, a feature that is not treated here as an independent character. An ossified accessory neural arch occurs in Diplophos, Manducus, Triplophos and all gonostomatids except Cyclothone. Additionally, some photichthyans, such as Photichthys and Yarrella, have an accessory supraneural without its associated neural arch. This apparent ephemeral nature of the accessory neural arch and its associated structures makes it of doubtful value as an indicator of phylogenetic relationships. CLADE K: MARGRETHIA PLUS BONAPARTIA.—20. In Margrethia and Bonapartia the ventral section of the lateral adductor mandibulae (A2β) inserts on connective tissue associated with the coronoid process lateral to the dorsal section (A2α), over a small portion of its attachment. Other stomiiforms with divided A2 muscles show no overlap. Remaining stomiiforms, like Diplophos, and the outgroups do not have a comparable division of A2. 21r. In Bonapartia and Margrethia valentinae a paired longitudinal muscle, a branch of the infracarinales medius, inserts via fascia onto the posterodorsal region of the pelvic girdle. No such division of this muscle was seen in other taxa examined. Absence of the muscle in Margrethia obtusirostra is parsimoniously viewed as a reversal. 22c. Photophores have a pattern of radiating photocytes in Margrethia and Bonapartia (see Herring and Morin, 1978 for a review of photophore types). A similar pattern occurs in Diplophos rebainsi (but not Diplophos taenia) and in many photichthyans. These three instances of radiating photocytes are inferred to be independently derived, based mainly on a parsimony consideration. The radiating morphology may be terminal additions to the development of photophores in D. rebainsi (an autapomorphy), Bonapartia plus Margrethia (synapomorphy) and most photichthyans (synapomorphy). The ventral photophores of Margrethia and Bonapartia stain differently in alcian blue from those of 730 BULLETIN OF MARINE SCIENCE, VOL. 62, NO. 3, 1998

Figure 12. Anterior vertebral centra and associated structures; right side, first vertebra at right. A, Gonostoma elongatum, USNM 313688, 140.0 mm SL; B, Cyclothone microdon, USNM 206847, 53.4 mm SL. Abbreviations defined in Figure 11 caption.

photichthyids, suggesting the possibility of nonhomology. Photophores of stomiiforms are unique (Fink and Weitzman, 1982) and no outgroup comparisons are possible. Polar- izations of this and other photophore characters are made on the basis of overall parsimony. 23. Anterior rays of the anal fin are highly elongate in Bonapartia (Fig. 3) and Margrethia. Fin shapes in Gonostoma (Fig. 1) and Cyclothone (Fig. 2) are more typical of stomiiforms and exhibit the plesiomorphic condition. 24c. Bilateral flattened tooth plates occur superficial to the dorsal surface of basibranchial 3 (five pairs in Margrethia; three pairs and one median plate in Bonapartia). There is some similarity to the condition of large superficial plates in Vinciguerria and Pollichthys but on the weight of other evidence it is more plausible to propose that these two cases of tooth plates lying superficially and dorsally to the third basibranchial are independently derived. Most other stomiiforms, including Diplophos, Manducus and Gonostoma, have superficial tooth plates positioned laterally to the third basibranchial, associated with the ligament from the third hypobranchial. Such tooth plates do not occur in the outgroups. Tooth plates are lacking in Cyclothone, Triplophos, Ichthyococcus and Yarrella. 25. The anteromedian process of the UP5 tooth plate associated with the fourth pharyngobranchial has a broad dorsal groove which encloses an extension of the fourth pharyngobranchial cartilage. The other stomiiforms with this anteromedian process (i.e., Cyclothone and Gonostoma) lack a dorsal groove and an extension of PB4 cartilage. 26c. OA photophores are absent in Bonapartia, Margrethia, and in the sternoptychid Araiophos. In other stomiiforms these light organs are arranged in a row between the opercle and the anal fin just dorsal to the level of the pectoral fin base. It is parsimonious to conclude that a lack of OA is independently derived in Bonapartia and Margrethia on the one hand and Araiophos on the other. MARGRETHIA.—27. In both species, M. obtusirostra and M. valentinae, the premaxilla has a peculiar shape, being laterally expanded, and with a highly convex ventral margin. Other stomiiforms and the outgroups have a narrow premaxilla with a straight to very slightly convex ventral margin. HAROLD: GONOSTOMATID PHYLOGENY 731

Figure 13. Jaws and suspensorium of Cyclothone acclinidens, USNM 260174, 40.0 mm SL, right side, lateral view.

28. The rostral cartilage is elongate transversely, being produced into a cylindrical bar of cartilage attaching to the medial surface of the premaxilla by a ligament. The situation is about the same in the two species with the exception that in M. valentinae there is also a median posterior knoblike process serving as an attachment surface for the median rostrovomerine ligament. The rostral cartilage is nearly spherical in other gonostomatids, sternoptychids, Manducus, Diplophos, Triplophos but appears to be absent in some photichthyans (e.g., Photichthys). CLADE F: GONOSTOMA PLUS CYCLOTHONE.—29. The levator arcus palatini muscle (LAP) is divided from its origin on the sphenotic to its insertion on the hyomandibula and metapterygoid in Cyclothone and Gonostoma. In other stomiiforms the LAP is a single, undivided block of muscle. 30. The adductor arcus palatini muscle is absent in Cyclothone and Gonostoma (Fink, unpubl.). This muscle is present in other stomiiforms and is widespread among nonstomiiforms examined. 31. The vertebral centra are highly elongate. There is some indication of elongation in Triplophos (Fig. 11B) also, but not to the degree that it occurs in Gonostoma and Cyclothone (Figs. 12A and B, respectively). In other stomiiforms the centra vary from deeper than long as in Ichthyococcus and Woodsia to slight elongation, as in Diplophos. 32. A modified, probably paedomorphic form of type Beta photophore occurs in Cyclothone and Gonostoma. During ontogeny of Beta type photophores of other gonostomatids pigmentation begins dorsally on the main body of the organ and spreads ventrally. The terminal stage is a vertically elongate bulblike structure. In Cyclothone and Gonostoma with a full complement of photophores the pigmentation only forms a dorsal cap on the photophore. Such a pattern is similar to the early stage of Beta photophore development in Bonapartia and Margrethia and is therefore probably paedomorphic and therefore derived. 732 BULLETIN OF MARINE SCIENCE, VOL. 62, NO. 3, 1998

Figure 14. Jaws and suspensorium of Margrethia valentinae, USNM 206761, 63.6 mm SL, right side, lateral view.

33. In Gonostoma and some Cyclothone species paired ligaments extend from the anterolateral surface of the rostrodermethmoid to the anterolateral surface of the premaxilla. These ligaments are auxilliary to the typical arrangement in which only the medial surface of the premaxilla has ligamentous attachment to the rostrodermethmoid. Some species of Cyclothone seem to lack this anterolateral ligament, a situation that may be due to reduction rather than to plesiomorphy, an interpretation that is dependent on overall parsimony. 34. The opercular condyle of the hyomandibula is reduced, not extending posteriorly beyond the posterior margin of the hyomandibula, in Cyclothone (Fig. 13) and Gonostoma (Fig. 9). The general condition is present in Margrethia (Fig. 14) and Bonapartia (Fig. 15), among gonostomatids, and in Diplophos (Fink and Weitzman, 1982: fig. 8). 35(1). The ventral section of the lateral adductor mandibulae (A2β) is divided into dorsal and ventral slips. In other stomiiforms, except Cyclothone, there is a continuous lateral fanlike muscle in the ventral part of the cheek. In Cyclothone the dorsal slip of A2β is apparently lost (character 35[2]). 36. In Cyclothone (Fig. 13) and Gonostoma (Fig. 9) the hyomandibula is flexed anterodorsally, producing a long oblique limb leading to the articulation with the pterotic. Other stomiiforms (e.g., Margrethia valentinae, Fig. 14 and Bonapartia pedaliota, Fig. 15) have a relatively short, vertically oriented dorsal limb. 37r. There is a minute tooth plate adhering superficially to the ventral lateral surface of the first pharyngobranchial (Fig. 5, inset) (apparently reversed in G. bathyphilum and Cyclothone species). Such a tooth plate was not observed in other stomiiforms (Fig. 6, inset) and the outgroups. Most stomiiforms have a series of toothplates along the lateral HAROLD: GONOSTOMATID PHYLOGENY 733

Figure 15. Jaws and suspensorium of Bonapartia pedaliota, USNM 316477, 51.3 mm SL, right side, lateral view.

surface of the first epibranchial, as in Diplophos taenia (Fink and Weitzman, 1982: fig. 11), but the series either terminates laterally or ventrolaterally to the pharyngobranchial. 38(1). The A3 muscle of the adductor mandibulae is partially divided or disjunct dors- oventrally along its origin, with the A1β muscle originating in the gap. The break in A3 is clearest in Gonostoma species (state 38[1]), appearing to be a specialized condition. The present interpretation requires a terminal character state (38 [2]) for the species of Cyclothone in which A3 is disjunct but its origin is not displaced posteriorly. The optimi- zation of this multistate character indicates that states 38(1) and 38(2) are both specialized and derived. In other stomiiforms and outgroup taxa the line of attachment at the origin of A3 runs parallel and medial to A1β. CLADE G: GONOSTOMA ELONGATUM, G. EBELINGI, G. LONGIPINNIS, G. GRACILE, G. BATHYPHILUM PLUS CYCLOTHONE.—50. Epineural and epipleural bones associated with caudal vertebrae are attached to the bases of, respectively, the neural or haemal spines or to the centra. Other stomiiforms have these bones progressively displaced distally on the spines from anterior to posterior, being attached as much as half way along the length of the spine. This displacement appears to be widespread among basal stomiiforms (e.g., Manducus) and in some sternoptychids (e.g., Maurolicus). Both conditions occur among other lower neoteleosts as well as argentinoids and certain salmonids (Patterson and Johnson, 1995). There is ambiguity, therefore, at the level of stomiiforms but the distal shift is probably primitive with regard to gonostomatids using the functional outgroup Manducus and Diplophos. CLADE H: GONOSTOMA EBELINGI, G. LONGIPINNIS, G. GRACILE, G. BATHYPHILUM PLUS CYCLOTHONE.—39. The posterior inferior OP photophore is absent in adults. This photophore, which is associated with the medial surface of the subopercle, is absent at all 734 BULLETIN OF MARINE SCIENCE, VOL. 62, NO. 3, 1998

stages of development in G. ebelingi, G. gracile and all species of Cyclothone examined. In G. bathyphilum the posterior inferior OP is present at 20 mm SL (Grey, 1964: fig. 42) but is absent in adults. All other stomiiforms, with the exception of Danaphos (Sternoptychidae) have the full complement of three OP photophores, a condition inferred here to be primitive within the order based on the presence of the condition in Manducus, Diplophos, Triplophos and Yarrella. There has been some indication in the literature (e.g., Ahlstrom et al., 1984:188, table 51) that there are only two OP photophores in the hatchetfish genera Argyropelecus, Polyipnus and Sternoptyx. That count does not reflect homology of the light organs because the photophore that was referred to as the “postorbital (PTO)” by Schultz (1961) is actually associated with the dorsal limb of the preopercle and therefore equivalent in position to and homologous with the superior OP photophore of other stomiiforms. The OP 2 condition in Danaphos is also not homologous with a similar photophore in the Gonostomata (clade B). In this case it is the superior photophore that is absent rather than the posterior inferior element. 40c. The neural spines are reduced, represented by the unfused, open arches only, throughout the postcranial axial skeleton (Fig. 12). The arches are similarly reduced in Ichthyococcus (Photichthyidae) and in Araiophos (Sternoptychidae), which are both thought to be convergent with the feature in gonostomatids. In other stomiiforms and the outgroups the neural arches are well developed, dorsally expanded structures meeting in the mid- line. 41r. The anus is located well anterior of the origin of the anal fin, about midway between the bases of the anal and pelvic fins in most of the species. The character is reversed in G. bathyphilum, in which the anus is located only slightly anterior to the anal fin origin. Other stomiiforms have the anus located immediately anterior to the anal fin origin or slightly in advance of it. 49. The dorsal- and anal-fin origins are in or close to a vertical passing through the first caudal vertebra. Most other stomiiforms have the dorsal origin well anterior to the anal origin (e.g., Triplophos, Polymetme) and the latter either immediately anterior to the first haemal spine (e.g., G. elongatum) or displaced posteriorly as in Manducus. The dorsal fin is well in advance of the anal fin in outgroup taxa, such as osmeroids, most argentinoids (not alepocephalids), salmonids, nearly all aulopiforms (not Omosudis). The exceptions here are possibly significant and require more study. CLADE J: GONOSTOMA BATHYPHILUM PLUS CYCLOTHONE.—42. The medial process of the pelvic bone is greatly expanded distally. In addition to the medial expansion, and possibly not an independent modification, the anterior shaft of the pelvic girdle (= pubic process of Weitzman, 1974) is short in comparison with the immediate outgroups. This arrangement is similar to that of Thorophos euryops (Weitzman, 1974:443, fig. 105) but not homologous in the context of the cladogram. The pelvic girdle in most other stomiiforms, such as G. elongatum, have elongate anterior shafts and with narrow, subcylindrical to moderately conical medial processes. This configuration agrees well with the situation in osmerids and salmonids. 43R. There is no tooth plate adhering to the lateral surface of the first pharyngobranchial. In other Gonostoma species there is a minute tooth plate adhering superficially to the ventral lateral surface of PB1. In no other taxa examined was such a tooth plate present. Its presence in Gonostoma is therefore considered derived, and its absence in Cyclothone and G. bathyphilum parsimoniously interpreted as a loss. HAROLD: GONOSTOMATID PHYLOGENY 735

44c. The third and fourth hypurals are fused into a single platelike element. Two other instances of independent derivation occur in Vinciguerria (Photichthyidae) and the Sternoptychidae. The third and fourth hypurals are separate in other stomiiforms (including all other Gonostoma species) and, generally, the outgroups. 45c. There are no superficial tooth plates associated with the second basibranchial. Similarly, there is a lack of such plates in Triplophos, Ichthyococcus and Yarrella. The character is interpreted as a synapomorphy of the species of Cyclothone and G. bathyphilum on the basis of parsimony. Tooth plates are found associated with the lateral surface of the second basibranchial via the ligament from the second hypobranchial in the other stomiiforms. In Vinciguerria there are fully developed gill rakers in the same positions as the above tooth plates and these are inferred homologues. 48(1). There are only three sets of epipleurals in G. bathyphilum and none in Cyclothone species (48[2]). Other gonostomatids have at least seven sets and in Manducus there are at least 20. The character is treated as an unordered multistate, with character state 48(1) being inferred a posteriori to be a step in a linear transition series terminating with complete absence of epipleurals in Cyclothone. 19R. The elongate process on the first parapophysis found in other gonostomatids (see Clade E) is absent in G. bathyphilum and some Cyclothone species. This is interpreted as a reversal in the context of the cladogram and suggests that the elongate process figured for C. microdon (Fig. 12B) is possibly not homologous with that of other gonostomatids. CYCLOTHONE.—46(2). A single large pectoral fin radial is present in all Cyclothone species examined. Presence of three pectoral radials was proposed by Weitzman (1974) as a synapomorphy of all Photichthya (character 46[1]). The four radials of other stomiiforms and outgroups is plesiomorphic at this level. 47. The fourth basibranchial is capped by a single edentate ossified plate. The presence of an ossification on the dorsal surface of the fourth basibranchial also occurs in Bonapartia, Margrethia, Triplophos, Vinciguerria and Pollichthys. In these other genera the plate bears teeth and there are other aspects of morphology which together suggest nonhomology. Other stomiiforms are without tooth plates on basibranchial 4, as are many of the outgroup taxa. 48(2). Epipleurals are absent in all Cyclothone species examined. See clade J, character 48(1) for other details. 35(2). The dorsal portion of the A2β section of the adductor mandibulae is absent. In other stomiiforms (except Gonostoma species), and the outgroups there is a continuous lateral fanlike body of muscle in the ventral part of the cheek corresponding to (and here considered homologous with) the A2β section. In Gonostoma species this ventral muscle is divided into dorsal and ventral sections. Presence of an additional subdivision is interpreted here as a step in a transition (character 35[1]), the loss of the dorsal slip being the terminal derived state in Cyclothone. 9R. Metamorphosis of photophores and other aspects of morphology is protracted or “extended” in Sternoptychidae plus Bonapartia, Gonostoma and Margrethia (Ahlstrom et al., 1984). In Cyclothone this is not the case, with the photophores developing rapidly through a “white” phase. This and other possibly paedomorphic features of Cyclothone could be related to the relatively small body size at which maturation and development of other structures is completed in this genus. 18R. The first pharyngobranchial is ventrally bifurcated with an elongate lateral limb in Bonapartia, Gonostoma, Margrethia and Thorophos. This character is either indepen- 736 BULLETIN OF MARINE SCIENCE, VOL. 62, NO. 3, 1998

dently derived in gonostomatids and in Thorophos or it is derived basally in Gonostomata and reverses in Cyclothone, Araiophos and the remaining sternoptychids.

DISCUSSION

MONOPHYLY OF GONOSTOMATIDAE.—Fink (1984) and Ahlstrom et al. (1984) suggested that the Gonostomatidae should be restricted to Margrethia, Bonapartia, Gonostoma and probably Cyclothone. Problems with the placement of Cyclothone have been attributed to paedomorphosis but Ahlstrom et al. (1984) went as far as to say that this genus and Gonostoma have modifications of the head and jaws that are likely synapomorphic. Among significant features of Cyclothone that are possibly paedomorphic is the presence of rapid development of photophores, rather than the protracted mode, as occurs in the other three gonostomatid genera and the sternoptychids. Emphasizing photophores in a tentative subfamilial classification of the non-barbeled stomiiforms (Sternoptychidae in his terminology), Ahlstrom (1974) placed Cyclothone with Diplophos, Ichthyococcus, Manducus, Pollichthys, Vinciguerria, Woodsia and Yarrella, all of which have photophores forming essentially simultaneously through a “white” phase. Ahlstrom et al. (1984) concluded that such development is primitive and its occurrence cannot be used as an indication of phylogenetic relationship. Evidence from my analysis supports the later proposal of Ahlstrom et al. (1984) that Cyclothone belongs with the other three gonostomatid genera and that the lack of protracted photophore development in the former can be inferred to be paedomorphic. Stomiiforms that do not have protracted development have the full complement of photophores develop rapidly while still larval. Early maturation in the common ancestor of all Cyclothone species probably resulted in the larval-like overall morphology seen in this genus as well as the mechanism of photophore development as occurs in the early stages of basal stomiiform taxa such as Diplophos and Manducus. Monophyly of the Gonostomatidae is here supported by ten characters, including loss of IP photophores (character 10), elongation of posterior shaft of palatine (11), pattern of maxillary dentition (12), short premaxilla (13), configuration of PB2 (16) and presence of an elongate process of the parapophysis of the first vertebral centrum (19). Ahlstrom et al. (1984) mention possible derived features of the skull but did not specify them. Within the Gonostomatidae, Bonapartia and Margrethia are sister groups and they are together the sister group of the remaining Gonostoma and Cyclothone. According to the preliminary cladogram presented here (Fig. 8) Cyclothone is a monophyletic subgroup of Gonostoma but its precise relationships to those species is yet to be completely resolved. It is clear, however, that G. ebelingi, G. longipinnis, G. gracile and, especially, G. bathyphilum are more closely related to Cyclothone species than are G. atlanticum, G. denudatum and G. elongatum. The former species share with Cyclothone species derived reductions of the inferior OP photophore (39) and the neural arches (40), an anterior shift of the anus away from the anal fin origin (41), and vertical alignment of the dorsal and anal fins with the first caudal vertebra. Gonostoma bathyphilum appears to be the likely sister group of the Cyclothone clade based on an expanded medial pelvic process (42), loss of the tooth plate otherwise associated with the first pharyngobranchial (43), fusion of the third and fourth hypurals (44), loss of tooth plates otherwise associated with the second basibranchial (45), and reduction of epipleurals (49). These results give a strong HAROLD: GONOSTOMATID PHYLOGENY 737

indication that Gonostoma, as it is presently formulated, is paraphyletic. This conclusion is supported by a phylogenetic analysis of Cyclothone species based on molecular data (Miya, in litt.) which included Gonostoma atlanticum and G. gracile as outgroups. I resist synonymizing Cyclothone at this time, pending examination of additional material and further resolution of gonostomatid relationships. MONOPHYLY OF GONOSTOMATA.—Weitzman (1974) established the infraorder Gonostomata for the proposed sister groups Sternoptychidae and Gonostomatidae (including Diplophos, Manducus and Triplophos). However, this relationship was based on the presence of four pectoral fin radials, a plesiomorphic feature at this level. This was pointed out by Ahlstrom et al. (1984) who reinterpreted one of Ahlstrom’s (1974) characters, protracted photophore development (character 9, this study), as derived and supportive evidence for such a group if Diplophos, Manducus and Triplophos are excluded. As discussed above, Cyclothone did not have this character but was retained because of other characters. In examining the cheek musculature I found that virtually all Gonostomata possess lateral adductor mandibulae (A2) that are divided into dorsal and ventral sections (character 8). Rosen (1973) illustrated the cheek muscles of Maurolicus showing there to be only a single slip of muscle. All of the specimens of Maurolicus I have examined have the additional, although poorly developed, dorsal slip attaching to the coronoid process. The one exception appears to be in the hatchetfish clade consisting of Argyropelecus, Polyipnus and Sternoptyx in which the dorsal muscle has been lost. This being the case, such loss could be interpreted as another synapomorphy for those three genera (see Harold, 1993; Weitzman, 1974 for other evidence for monophyly). In the context of the cladogram presented here (Fig. 4) two other characters, albeit homoplastic, are potential synapomorphies of the Gonostomata. All members of the group lack accessory photophore rows (character 2), a condition thought to be independently derived in all Photichthya except Yarrella. It is equally parsimonious for this character to be optimized at the level of clade B (all stomiiforms minus Diplophos and Manducus) with independent gains in Triplophos and Yarrella. The other character is the presence of an elongate ventrolateral process of the first pharyngobranchial, which is found in most gonostomatids and Thorophos (a basal sternoptychid). This distribution, interpreted as a synapomorphy of the Gonostomata, requires losses in Cyclothone and all sternoptychids except the basal Thorophos. Neither of these two characters is reliable or consistent evidence of relationship and they are suggested only as possibly corroborative evidence of the details of cheek musculature and photophore development. RELATIONSHIPS OF DIPLOPHOS, MANDUCUS AND TRIPLOPHOS.—The species of Diplophos and Manducus are unquestionably similar to one another but there is no consensus as to their relatedness (Fink, 1984a; Ahlstrom et al., 1984). They have been treated as all species of Diplophos (e.g., Fink and Weitzman, 1982) but there is not much evidence for monophyly of such a group (evidence suggesting nonmonophyly was discussed by Ahlstrom et al., 1984). Monophyly is supported here by association of the first pleural rib with the fourth vertebra, rather than the third (character 51). Following Ahlstrom et al. (1984), I retain the two separate generic names, acknowledging that one or more of the species may be more closely related to other stomiiforms than to the remaining Diplophos and/or Manducus. Those authors stated that D. taenia and D. rebainsi have the cartilages of pectoral radials III and IV fused while all other stomiiforms with four pectoral radials have them separate. This was thought to be a possible stage in a character transition that terminates in the three radial condition of photichthyans. The suggestion that these spe- 738 BULLETIN OF MARINE SCIENCE, VOL. 62, NO. 3, 1998

cies might, together, form the sister group to the Photichthya (Ahlstrom et al., 1984:185) seems not to be supported by other characters which indicate that Photichthya and Gonostomata are sister groups. The fused radial condition of Diplophos is most parsimomiously regarded as independent of the complete loss of the fourth radial in the Photichthya. Diplophos taenia and D. rebainsi also have the distal pectoral radials “out of line” (Ahlstrom et al., 1984:185). While this feature has no bearing on higher level relationships of the genus it does present, along with the pectoral radial fusion, a diagnostic character for the genus. Diplophos was identified by Weitzman (1974) as a stomiiform genus with many primitive attributes, and which probably did not belong in his Gonostomatidae. My survey of the stomiiforms is in agreement with the suggestion of Fink and Weitzman (1982:32) that Diplophos plus Manducus probably comprises the sister group of all other stomiiforms. One feature described by Fink and Weitzman (1982), in particular, that indicates such phylogenetic relationship is the large, toothed basihyal present in all Diplophos and Manducus species (see character 4, this study). Unlike the remaining stomiiforms, the basihyal of Diplophos and Manducus resembles that of other lower euteleosts, such as osmerids, salmonids and some aulopiforms. The form of the basihyal varies widely in the Aulopiformes (see Baldwin and Johnson, 1996), among which some taxa have a cylindrical, edentate basihyal very much like that of non-Diplophos/Manducus stomiiforms. Given other, supportive evidence for the basal position of Diplophos and Manducus and Baldwin and Johnson’s (1996) aulopiform analysis it is parsimonious to conclude that the occurrence of the edentate, cylindrical basihyal in the Stomiiformes and the Aulopiformes is convergent. Among other characters that suggest that all stomiiforms minus Diplophos and Manducus (clade B) form a monophyletic group are: vertically oriented extensor proprius pelvicus muscle (character 1) and basal bifurcation of the first pharyngobranchial (3). Ahlstrom et al. (1984) discussed the relative development of the neural spine of the “preural centrum” and its bearing on the relationships of Diplophos and Manducus. I take this to mean the neural spine associated with the second preural centrum (NPU2) which does vary in length among stomiiforms. It was suggested that the presence of a short neural spine was primitive for stomiiforms and I concur, suggesting that Diplophos and Manducus are basal stomiiforms (character 5, this study). Diplophos rebainsi, however, has a fully developed NPU2. Whether this condition is independently derived and autapomorphic, or is homologous with the full NPU2 in other stomiiforms cannot be determined on morphological grounds but it is much more parsimonious to hypothesize that it is not. Absence of an adipose fin, indicated by Ahlstrom et al. (1984) as a possible shared specialization of Diplophos and Manducus, also occurs in Gonostoma atlanticum, Triplophos, Yarrella, and in the sternoptychids Sonoda and Polyipnus latirastrus (Last and Harold, 1994). This amount of homoplasy makes this character a poor indicator of relationships. I agree that presence of an adipose fin is likely primitive at the stomiiform node but losses (and possible subsequent acquisitions) have occurred within the order. It also seems plausible that absence of an adipose fin is a derived feature of the Stomiiformes, as it is lacking in many basal stomiiforms, and that it re-appears atavistically more than once. HAROLD: GONOSTOMATID PHYLOGENY 739

Triplophos has a problematical mosaic of primitive and putatively derived characters. Ahlstrom et al. (1984) discussed some aspects of its pectoral radial structure and photophore development and reached the conclusion that this genus has all plesiomorphic conditions. It was suggested that Triplophos may share some derived aspects of pectoral girdle and head anatomy with certain photichthyans (Ahlstrom et al., 1984:198). Grey (1964) thought that Triplophos was most closely related to Yarrella (a gonostomatid in her classification) based on an elongate premaxilla and the presence of “additional” (= accesory) rows of photophores on the body. The premaxilla is exceptionally long in Triplophos, occupying much of the upper jaw. This elongate premaxilla, which is unique among stomiiforms, approaches its form in aulopiforms and myctophiforms, but the same bone in Yarrella is only moderately elongate, resembling that of other photichthyids, Diplophos and Manducus. The occurrence of the accessory photophore rows is shared with Yarrella, among Gonostoma at least G. elongatum, Diplophos and Manducus, giving a strong likelihood of plesiomorphy at this level. I agree with Grey (1964) that Triplophos shares some unusual characters with Yarrella but their meaning is not clear. These two genera both have a very elongate PU1 + U1 caudal centrum. Weitzman (1974) described this morphology for Triplophos, ascribing to it a possible function related to the elongate body and presumed modified locomotory mechanism. A modification of the pelvic girdle is also shared by Triplophos and Yarrella, in which the anterior processes lack the lateral and medial platelike laminae that otherwise occur throughout the Stomiiformes and the outgroups I have examined. These possible shared, derived characters are contrasted by pectoral radial morphology which places Yarrella among the Photichthya (three radials), whereas Triplophos has traditionally been regarded a gonostomatid (four radials). Also, Triplophos has type Beta photophores (plesiomorphic for stomiiforms) whereas Yarrella presumably has type Gamma (a photichthyan synapomorphy). Several alternative explanations are possible: (1) Triplophos may possess a reversed condition of four pectoral radials (as reported by Fink [1985] for certain stomiids) and is not only a photichthyan but is the sister group of Yarrella, (2) Triplophos is the sister group of the Photichthya based on the two characters described above, which are then lost in all Photichthya except Yarrella, (3) the apparent derived similarities of Triplophos and Yarrella are convergent. The problem of these relationships has been considered further and in the light of other characters of relevance to the Photichthya, in another paper (Harold and Weitzman, 1996).

ACKNOWLEDGMENTS

This work was made possible by the National Museum of Natural History, Smithsonian Institu- tion: in this regard I am particularly indebted to S. H. Weitzman who made time and resources available throughout the study. I am also grateful to S. H. Weitzman for making available the previously unpublished drawings by Marion Johnson Dalen of Gonostoma elongatum, Cyclothone atraria and Bonapartia pedaliota (Figs. 1,2,3, respectively). I thank R. Winterbottom for making available for study and publication his drawings and observations of stomiiform musculature. I also wish to thank the following museum staff who made material available for study: D. Catania (CAS), K. Ditz (ROM), K. E. Hartel (MCZ), E. Holm (ROM), T. Iwamoto (CAS), S. L. Jewett (USNM), R. Lavenberg (LACM), L. Palmer (USNM), N. V. Parin (IOAN), A. Post (IHS), J. Randall (BPBM), A. Suzumoto (BPBM), S. H. Weitzman (USNM) and R. Winterbottom (ROM). Financial support was gratefully received in the form of a Natural Sciences and Engineering Research Council of Canada Postdoctoral Fellowship and a Tilton Postdoctoral Fellowship from the California Academy of Sci- 740 BULLETIN OF MARINE SCIENCE, VOL. 62, NO. 3, 1998 ences, San Francisco. Preparation of the manuscript was made possible with the aid of staff and resources of the Department of Ichthyology and Herpetology, Royal Ontario Museum, Toronto, Canada. The manuscript was improved through critical reviews by W. L. Fink and S. H. Weitzman.

LITERATURE CITED

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DATE SUBMITTED: April 18, 1995. DATE ACCEPTED: June 20, 1996.

ADDRESS: Department of Ichthyology and Herpetology, Royal Ontario Museum, 100 Queen’s Park, Toronto, Ontario M5S 2C6, Canada. PRESENT ADDRESS: Grice Marine Biological Laboratory, College of Charleston, South Carolina, 205 Fort Johnson, Charleston, South Carolina 29412.

APPENDIX

LIST OF CHARACTERS BY MORPHOLOGICAL SYSTEM.—The following list of character num- bers, in conjunction with the annotated cladograms (Figs. 4 and 8), is provided as a cross- reference for the retrieval of characters and other anatomical information relating to specific morphological systems. Numerical order corresponds, with some exceptions (2, 18, 48–51), to the sequence in which characters are described in the text.

Alimentary tract: 41 Ethmoid region: 6, 28, 33 Fins and supports: 17, 23, 42, 46, 49 Gill arches: 3, 4, 14, 15, 16, 18, 24, 25, 37, 43, 45, 47 Jaws and suspensorium: 11, 12, 13, 27, 34, 36 Musculature: 1, 8, 20, 21, 29, 30, 35, 38 Photophores: 2, 7, 9, 10, 22, 26, 32, 39 Postcranial axial skeleton: 5, 19, 31, 40, 44, 48, 50, 51