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Evolution of Remarkable Structural Novelties in Its Jaws and External Genitalia^

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Evolution of Remarkable Structural Novelties in Its Jaws and External Genitalia^ OSTEOLOGY OF THE MALAYSIAN PHALLOSTETHOID FISH CfRATOSTETHUS BICORNIS, WITH A DISCUSSION OF THE EVOLUTION OF REMARKABLE STRUCTURAL NOVELTIES IN ITS JAWS AND EXTERNAL GENITALIA^ TYSON R. Roberts- Abstract. The osteology of the phallostethoid an externalized pelvic bone. Phallostetliidae ap- Ccratostethtis bicornis (Regan) is described and parently arose from Neostcthus. The toxactinium, figured. Comparative observations on osteology of the main externalized bony element in the atherinoids, cyprinodontoids, and other phallo- priapium of Phallostethidae, is derived from the stethoids are also given. Phallostethoids apparently inner pulvinular bone, which is the anteriormost originated from atherinids. The most closely internal liony element in tlie priapium of related atherinids are Taeniomembrasinae. The Neostetliidae. The inner pulvinular bone of Neo- osteological observations tend to support the idea stethus bears a small lateral projection, the that atherinoids and cyprinodontoids are related, pulvinular spine, which may be a rudimentary as in toxactinium. structure of the postulated ])y Rosen ( 1964 ) proposing the The papillary ])one, order Atheriniformes. Atherinifomis exhil^it a intimately associated with the genital pore, is widespread tendency to develop teeth with two relatively simple in Gulaphallinae and Phallo- and three cusps, especially on the pharyngeal stethidae, ])ut in Neostethinae it divides into bones. The trend is pronounced in cyprinodontoids, numerous thin processes each bearing a booklet at exocoetoids, and scomberesocids, practically absent its tip. A comprehensive definition is given for in atherinoids, and completely absent in phallo- the superfamily Phallostethoidea. All taxa used stethoids and belonids. in this paper were proposed l^y previous authors. The Phallostethoidea can be divided into two Oviparous Atheriniformes with internal fertiliza- families, Phallostethidae and Neostethidae. Neo- tion have external genitalia far more complicated stetliidae comprises two subfamilies, Neostethinae than the gonopodium of any of the viviparous and Gulaphallinae. These groups are distinguish- .\theriniformes. The explanation of this difference able on the basis of morphological differences in is sought in terms of selection pressures for and the jaws and external genitalia. The highly pro- against the evolution of liighly complicated ex- ternal in forms with internal fertilization. tractile jaws of Neostethinae ( as exemplified" ])y genitalia Ceratostethus and Neostethtis) are remarkalile in Neotenic characters probably played an important having several pairs of bones without homologues role in the origin of phallostethoids from Atherin- in other fishes. These new bones, invohed mainly idae. in protrusion of the jaws, evolved in soft structures already present in the jaws of atherinids. The INTRODUCTION functional anatomy of the jaws of phallostethoids is discussed. Phallostethidae and Gula- briefly Ichthyologists have marvelled at phallo- phallinae lack the neomorphic jaw bones found in stethoids since thev \\'ere first made known Neostethinae. Two ctenactinia formed from pelvic C. T. Males of fin spines or rays occur only in CeratostetJius. The by Regan (1913; 1916). so-called "second ctenactinium" of Gulaphallus is these delicate little fishes from Southeast Asia can be distinguished in an instant by ^ Published a from tlie Wetmore Colles by grant their strange subcephalic copulatory organ, Fund. - or as designated it. The Museum of Comparative Zoology, Harvard Uni- priapium, Regan have been divided versity, Cambridge, Massachusetts 02138 19 species now known Bull. Mus. Comp. Zool., 142(4): 393-418, December, 1971 393 394 Bulletin Museum of Comparative Zoology, Vol. 142, No. 4 into two families and ten genera, largely based on differences in the external arma- ture of the priapium (see Herre, 1942). H. M. Smith (1927) made the surprising an- nouncement that phallostethoids he ob- served in Thailand are oviparous. This discovery was confirmed in species from the Philippines by Villadolid and Manacop (1934) and Woltereck (1942a). Despite their outstanding interest, phallostethoids have remained virtually unknown to the a general zoological public. The present paper gives a relatively complete, illustrated account of the osteol- > Cerotostethu.s ])icornis o ogy of (Regan) (Fig. 1), with special attention to the hitherto undescribed jaws and their func- ,-K a c tional Previous work D anatomy. osteological .cU on Phallostethoidea (with the exception of brief observations by Regan [1913; 1916], skeletal who lacked adequate preparations ) has been almost totally restricted to the J3 O priapium (Bailey, 1936; Aurich, 1937; The is U Woltereck, 1942a, b). priapium derived mainly from pelvic bones and fin with contributions from the anterior- o rays, 3 most ribs and pectoral girdle. The pelvic 'K elements are so excessively modified that their homologies remain unresolved. This copulatory organ is perhaps even more on specialized than the copulatory organs derived from the anal fin in the U cyprin- odontoids Horaichthi/s and Tomeunis. — and o Interestingly enough, Iloraichthys ,^ E Tomeunis are also oviparous, and they exhibit numerous morphological and eco- logical similarities to phallostethoids. Tlie E do not E morphological similarities, however, CO extend to the jaws of Ceratostethtis: al- though basically similar to the jaws of atherinoids, they are even more highly t;r: protractile and possess two major and two 3 minor paired bones found so far in no other o fishes except the closely related Neostethus also in 0) (probably present SolenophaUm and Plectrostethus and possibly Phallo- 0) but absent in PJienacostethus and k_ stethus, Guhphallus). No observations have evei Ceratostethus—Osteology and Structural Novelties • Roberts 395 been made on the feeding movements of toids. The most closely related forms ap- Ceratostethus or any other phallostethoids; pear to be Stenatherina and its Indo-Pacific I have tried to detemiine the main features allies (placed by Schultz, 1948, in the of their functional atherinid anatomy by manipula- subfamily Taeniomembrasinae ) . tion of alizarin-stained specimens macerated If one considers only zoogeographic dis- in potassium hydroxide and cleared in 50 tribution and priapial morphology (which percent glycerine. has been worked out in considerable detail My initial objectives in studying the for almost all of the genera by Bailey [1936] osteology of Ceratostethus were to provide and especially by Aurich [1937]), a rel- information that might lead to a better atively simple picture of phyletic relation- of 1 of Phallo- \\'ithin understanding ) relationships ships Phallostethoidea emerges. stethoidea to other fish groups, and 2) There are two families: Phallostethidae and relationships among phallostethoid genera. Neostethidae. Phallostethidae, presumably I chose Ceratostethus because, judging most highly modified from the primitive from priapial stiiicture, it seemed to repre- or ancestral type of phallostethoid, com- sent a relatively primitive phallostethoid, prise two genera, Phallostethus and Fhena- and I had an abundant supply of fresh costethus, confined to the Malay Peninsula material from Thailand. Regan (1913; 1916) and adjacent parts of the mainland of regarded the phallostethoids as an aberrant Southeast Asia. Neostethidae comprise six subfamily of Cyprinodontidae, and noted to eight genera (Herre, 1942, probably that their osteology was "typically cyprin- went too far in splitting genera) belonging odontid." He did not indicate to which to two subfamilies, Neostethinae and Gula- cyprinodontids they might be most closely phallinae. Gulaphallinae are restricted to related. Subsequent to the discovery by the Philippines. Neostethinae, which in- Herre 1925 that clude ( ) phallostethoids possess Ceratostethus, SoJenophaUus, Plectro- a spiny (al]:)eit minute) first dorsal fin, stethus, and Neostethus, are more widely most followed 1928 distributed. Neostethus ichthyologists Myers ( ) and Ceratostethus in relating them to the Atherinidae. Myers occur in the Philippines, Borneo, and intimated that Atherinidae and Cyprin- both sides of the Malay Peninsula.^ The odontidae might actually be fairly closely priapium of Neostethinae, in which the related, a suggestion generally viewed with only externalized elements are derised from disfavor (cf. Hubbs, 1944) until Rosen pelvic spines and rays, is evidently more (1964) pointed out a large number of primitive than are the priapia of Phallo- stethidae and anatomical, morphological, and reproduc- Gulaphallinae. In phallo- tive characters and trends commoj! to stethid priapia the main externalized atherinoids, cyprinodontoids, and allied element is homologous witli the neostethid forms outer (including Phallostethoidea ) and pulvinular (Bailey, 1936; Roberts, united them in a new order, Atherinifonnes. 1971), which is the anteriormost internal While placing the superfamily Phallo- element in the priapium of Neostethidae. stethoidea in the suborder Atherinoidei Neostethus, alone among Neostediidae, has {ibid.: 261), he suggested that it might be a single spur near the base of its cten- more closely related to cyprinodontoids actinium, resembling the series of spurs on than to atherinoids after all {ibid.: 242). the ctenactinium of PhaUostethus (the During the course of the present study ctenactinium of Phenacostethus is absent or numerous supplemental observations were ^ made on cyprinodontoids and atherinoids. There are two
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