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The Phylogeny of Atherinomorphs: Evolution of a Novel Fish Reproductive System

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The Phylogeny of Atherinomorphs: Evolution of a Novel Fish Reproductive System The Phylogeny of Atherinomorphs: Evolution of a Novel Fish Reproductive System Lynne R. Parenti Division of Fishes, MRC NHB 159, Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA. Lynne R. Parenti • The Phylogeny of Atherinomorphs. Reproductive System 13 Abstract Resumen The Phylogeny of The fishes commonly known in English as Los peces comúnmente conocidos en inglés Atherinomorphs: silversides, rainbowfishes, phallostethids, como: silversides, rainbowfishes, phallostethids, killifishes, ricefishes, halfbeaks, needlefishes, killifishes, ricefishes, halfbeaks, needlefishes, Evolution of a flying fishes, and sauries were combined by flying fishes y sauries fueron integrados por Rosen (1964), into one taxon, now known as Rosen (1964) en un taxon ahora conocido Novel Fish the Atherinomorpha, largely using osteological como Atherinomorpha, utilizando and reproductive characters. Subsequent esencialmente caracteres osteológicos y Reproductive reviews have supported atherinomorph reproductivos. Revisiones posteriores han monophyly, adding characters to the sostenido que Atherinomorpha es un grupo System diagnosis. Today atherinomorphs are monofilético y han agregado otros caracteres a diagnosed as monophyletic by derived la diagnosis. Hoy, los aterinomorfos están characters of the testis, egg, reproductive definidos como monofiléticos por mode, circulatory system, jaw musculature, características derivadas del testículo, huevos, olfactory organ, and various parts of the formas reproductoras, sistema circulatorio, skeleton including the ethmoid region of the musculatura de la mandíbula, órgano skull, gill arches, pelvic girdle, among others. olfatorio, y varias partes del esqueleto, Support for monophyly of each of the three incluyendo la región etmoidea del cráneo, included taxa, now classified as the orders arcos branquiales, y cintura pélvica, entre Cyprinodontiformes, Beloniformes, and otros. El carácter monofilético de cada uno de Atheriniformes, and the relationships among los tres taxa incluidos actualmente, clasificados them, varies in quantity and quality. During en los órdenes Cyprinodontiformes, the past twenty years, reproductive and Beloniformes, y Atheriniformes, se define en Lynne R. Parenti molecular data used to infer atherinomorph sus relaciones entre ellos, con variaciones de relationships have grown significantly. In cantidad y calidad. Durante los últimos veinte general, molecular data support hypotheses años, ha aumentado significativamente el uso based on morphology, and, in some cases, de datos sobre reproducción y moleculares provide novel hypotheses and unique para inferir relaciones en los aterinomorfos. challenges to morphological data. A growing En general, datos moleculares apoyan body of data indicates that all atherinomorphs hipótesis basadas en la morfología y, en share a unique testis-type that is correlated algunos casos, sustentan hipótesis nuevas y with an array of reproductive modifications únicas referentes a los datos morfológicos. Un such as coupling during mating, relatively número creciente de datos indica que todos long developmental period, sperm-bundle los aterinomorfos tienen un tipo testicular formation, internal fertilization, superfetation, único, correlacionado con una serie de embryo retention, diapause, delayed hatching, modificaciones reproductivas, tales como el hermaphroditism, and live-bearing. apareamiento, un periodo relativamente largo Corroboration of an atherinomorph sister de desarrollo, formación de paquetes de group may include identification of some espermatozoides, fertilización interna, unique aspects of this reproductive system in superfetación, retención de los embriones, other taxa. diapausa, eclosión demorada, hermafroditismo y viviparidad. Corroborar que algún grupo de otro taxa, esté emparentado con los aterinomorfos, puede incluir la identificación de alguno de estos aspectos del sistema reproductor. • Viviparous Fishes • ViviparousMari Carmen Fishes Uribe and Harry J. Grier, book editors. 14 Systematics,New Life Biogeography, Publications, and Homestead, Evolution Florida, 2005. p 13-30. Introduction n 1964, Donn E. Rosen, then curator in the considered by Gosline to be “higher teleosts” Department of Ichthyology, American Mu- because they have characters such as two dorsal Iseum of Natural History, New York, pub- fins, both with anterior spines or thickened rays, lished a monograph as a Bulletin of the American and an I,5 pelvic-fin ray formula. In contrast, Museum of Natural History, in which he brought the Cyprinodontoidei and Exocoetoidei (Cy- together three disparate groups of teleost fishes prinodontiformes and Beloniformes, following in one order, the Atheriniformes (Rosen, 1964). Greenwood et al., 1966) were considered by The three suborders in Rosen’s Atheriniformes Gosline to be “intermediate teleosts.” Both have were the Atherinoidei (the silversides, rainbow- a single, soft-rayed dorsal fin and may have more fishes, and phallostethids), the Cyprinodon- than six pelvic-fin rays, among other characters, toidei (the killifishes and ricefishes), and the that they share with taxa that Gosline thought Exocoetoidei (the sauries, needlefishes, half- to be less advanced (see review by Parenti, 1993). beaks, and flying fishes). Support of this taxon Cyprinodontiformes and Beloniformes were not included evidence largely from two systems, os- considered closely related by Gosline (1971), teology and reproductive biology, which Rosen who postulated that they were derived from, or described in an essay, as was common then, most closely related to the Beryciformes and rather than enumerating putative synapomor- Myctophiformes, respectively. phies. Skeletal characters that Rosen considered Monophyly of atherinomorphs and mono- diagnostic of his Atheriniformes included a disc- phyly and relationships of the three included shaped dorsal and ventral ossified mesethmoid taxa was reviewed by Rosen and Parenti (1981) and decoupling of the rostral cartilage from the in conjunction with a phylogenetic analysis of ascending processes of the premaxillae. Repro- Cyprinodontiformes by Parenti (1981). The ductive characters included a large, demersal egg first explicitly cladistic analyses of atherino- with long, adhesive chorionic filaments and morph phylogeny were presented in these two large oil globules (Rosen, 1964:253-255). papers. Atherinomorph monophyly was sup- The new taxon, classified as the series ported by ten characters, again largely those of Atherinomorpha by Greenwood et al. (1966), the skeleton, but also including two reproduc- was not accepted readily by all systematic ich- tive characters (Rosen and Parenti, 1981:20), thyologists. In particular, Gosline (1971, Fig. one of the egg (“a large dermersal egg with long 28B) argued that Rosen had brought together adhesive and short filaments and many lipid fishes from different evolutionary grades that did globules that coalesce at the vegetal pole”), and not share an evolutionary history. Atherinoids one of the testis (“the spermatogonia forming (now classified as the order Atheriniformes fol- only at the blind end of the tubule near the lowing Dyer and Chernoff, 1996; Table 1) were tunica albuginea”). Lynne R. Parenti • The Phylogeny of Atherinomorphs. Reproductive System 15 Table 1. Annotated classification of Atherinomorph fishes (following Rosen and Parenti, 1981; Collette et al, 1984; Parenti, 1993; Costa, 1998a; Dyer and Chernoff, 1996). Series Atherinomorpha Greenwood et al., 1966 [= Atheriniformes of Rosen, 1964] Order Atheriniformes sensu Dyer and Chernoff, 1996 [= Atherinoidei of Rosen, 1964; Division I of Rosen and Parenti, 1981] Classification is sequenced. Family Atherinopsidae Suborder Atherinoidei Family Notocheiridae (including Isonidae) Infraorder Atherines Family Melanotaeniidae (including Bedotiidae, Pseudomugilidae) Family Atherionidae Superfamily Atherinoidea Family Phallostethidae (including Dentatherinidae) Family Atherinidae Superorder Cyprinodontea of Dyer and Chernoff, 1996 [Division II of Rosen and Parenti, 1981, order Cyprinodontiformes of Nelson, 1984, not recognized by Rosen, 1964] Order Cyprinodontiformes [= Cyprinodontoidea of Rosen, 1964] Suborder Aplocheiloidei Family Aplocheilidae Family Rivulidae Suborder Cyprinodontoidei Superfamily Funduloidea Family Profundulidae Family Fundulidae Family Goodeidae Superfamily Valencioidea of Costa, 1998a [= Sept 1 of Parenti, 1981] Family Valenciidae Unranked category including superfamilies Cyprinodontoidea and Poecilioidea Superfamily Cyprinodontoidea Family Cyprinodontidae Superfamily Poecilioidea of Parenti, 1981 [= unnamed clade of Costa, 1998a] Family Anablepidae Family Poeciliidae Order Beloniformes [not recognized by Rosen, 1964] Suborder Adrianichthyoidei [= Adrianichthyoidea of Rosen, 1964] Family Adrianichthyidae (including Horaichthyidae and Oryziidae) Suborder Exocoetoidei Superfamily Exocoetoidea Family Exocoetidae Family Hemiramphidae Superfamily Scomberesocoidea Family Belonidae Family Scomberesocidae • Viviparous Fishes 16 Systematics, Biogeography, and Evolution Figure 1. The many, unique characteristics of the Diagrammatic representation of two atherinomorph egg are correlated with reproduc- different testis-types in higher tive and developmental modifications. Filaments teleosts: A: testis lobule in representative atherinomorph, with are derived from the secondary or outer layer of spermatogonia restricted to the the zona pellucida which is secreted
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