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Oryzias[/I] and Relatives (Beloniformes, Adrianichthyidae)

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Oryzias[/I] and Relatives (Beloniformes, Adrianichthyidae) Zoological Journal of the Linnean Society, 2008, 154, 494–610. With 58 figures A phylogenetic analysis and taxonomic revision of ricefishes, Oryzias and relatives (Beloniformes, Adrianichthyidae) LYNNE R. PARENTI FLS* Division of Fishes, Department of Vertebrate Zoology, National Museum of Natural History, MRC 159, Smithsonian Institution, PO Box 37012, Washington, DC 20013-7012, USA Received 25 March 2007; accepted for publication 27 September 2007 Ricefishes, known best by the model organism, the medaka, Oryzias latipes Temminck & Schlegel, 1846, comprise the family Adrianichthyidae, which ranges broadly throughout fresh and brackish waters of Central, South and Southeast Asia and the Indo-Malay-Philippines Archipelago as far east as Timor. Twenty-eight Recent species are recognized here in two monophyletic genera, Adrianichthys and Oryzias. Xenopoecilus and Horaichthys are placed in synonymy of Oryzias for the first time. Adrianichthys comprises four species from Lake Poso, Sulawesi, Indonesia. Oryzias comprises 24 species that live throughout the range of the family. A fossil genus and species, †Lithopoecilus brouweri from the Miocene of central Sulawesi, is included tentatively in the Adrianichthyidae. Evidence for the sister group relationship of adrianichthyids and exocoetoids is reviewed briefly and that relationship corroborated. Monophyly of adrianichthyids is likewise strongly supported here. Species groups within Oryzias are diagnosed as monophyletic largely based on osteology, colour pattern and meristic variation. They correspond only in part to species groups previously recognized based on chromosome constitution. Miniature species do not comprise a monophyletic group; disjunct absolute size in close relatives has evolved repeatedly. Oryzias latipes is a member of a species complex that includes O. luzonensis, O. curvinotus and the miniatures O. sinensis and O. mekongensis. A new species, Oryzias bonneorum sp. nov., is described from Lake Lindu, Sulawesi, Indonesia. Lectotypes are designated for Haplochilus celebensis Weber, 1894 and Haplochilus timorensis Weber & de Beaufort, 1922. No claim to original US Government works. Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154, 494–610. ADDITIONAL KEYWORDS: comparative morphology – homology – medaka – model organisms – miniaturization – phylogeny. INTRODUCTION common there in stagnant waters, such as flooded rice paddies, particularly in the summer.] When placing Oryzias latipes has been known broadly by its Poecilia latipes Temminck & Schlegel, 1846, in a new Japanese name, medaka, and is identified with genus, Oryzias, 60 years later, Jordan & Snyder rice paddies, suggesting the English common name, (1906) coined a name based on the Latin word for rice, ricefish, since Temminck & Schlegel (1846: 225) Oryza, also a genus of rice plants. concluded their species description: ‘On désigne ce The medaka has been one of the most widely used poisson au Japon sous le nom de Medaka. Il y est species in experimental vertebrate biology for over très-commun dans les eaux stagnantes, telles que les a century. Attributes of the medaka that encouraged champs de riz inondés, notamment en été’ [This fish is its laboratory use include small size, external sexual known in Japan by the name medaka. It is very dimorphism, relatively large and clear eggs, long development time, ease of maintenance in freshwater aquaria, wide availability and reasonable cost. The *E-mail: [email protected] medaka is the first fish in which Mendelian laws of 494 No claim to original US Government works. Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154, 494–610 PHYLOGENY OF RICEFISHES 495 inheritance were demonstrated (Toyama, 1916) and partially Y-linked inheritance was established (Aida, 1921). It is the first animal in which complete rever- sal of sex differentiation was induced by hormone administration (Yamamoto, 1952; see also Yamamoto, 1967, 1975). In 1959, Briggs & Egami compiled a bibliography of over 350 citations covering the use of the medaka in fields such as embryology, genetics, toxicology, comparative anatomy, endocrinology, systematics and taxonomy. Nearly one thousand sci- entific papers were compiled in a subsequent medaka bibliography by Egami & Yamamoto (1975). A com- plete, up-to-date bibliography of the medaka, well beyond the scope and purpose of the present study, would include several thousand scientific and popular articles (see Iwamatsu, 1997, 2006). Today, the medaka is one of the three most impor- Figure 1. Oryzias dancena (Hamilton, 1822), the first tant model organisms among bony fishes along with described ricefish species, USNM 313908, adult female, the zebrafish, Danio rerio (Hamilton, 1822) and the 23.8 mm SL, above; adult male, 25.0 mm SL, below. Sri Japanese pufferfish, Takifugu rubripes (Temminck & Lanka. Female is carrying a cluster of embryos. Schlegel, 1850) (see Clark & Elgar, 2000; Ishikawa, 2000; Wittbrodt, Shima & Schartl, 2002). It is among Despite, or perhaps because of, the popularity of the first teleost species to have its genome sequenced the medaka, knowledge of Oryzias biology has been (Kasahara et al., 2007). Inducing and characterizing limited until relatively recently to O. latipes and just mutations (Shimada et al., 2002), detecting mutations several congeners, such as O. dancena (Fig. 1), the in transgenic individuals (Ozato, Wakamatsu & first described ricefish species (Roberts, 1998), Inoue, 1992; Winn et al., 2000), generating transgenic O. javanicus (viz. Iwamatsu et al., 2003) or O. sara- individuals (Tanaka & Kinoshita, 2001), identifying sinorum (viz. Sovrano et al., 1999; Sovrano, Bisazza & the role of the neural crest during development Vallortigara, 2001; Sovrano, 2004), classified formerly (Langille & Hall, 1988), and documenting spontane- in the genus Xenopoecilus (see below). Oryzias com- ous tumour development (Masahito et al., 1989) are prised just ten species according to Yamamoto (1975; just several, varied examples among many of biologi- Table 1): Oryzias latipes, O. melastigma (now recog- cal investigation and experimentation using the nized as O. dancena or O. carnaticus, following medaka during the past two decades. Roberts, 1998), O. celebensis, O. timorensis, O. jav- The popularity of the medaka as a laboratory anicus, O. curvinotus, O. minutillus, O. luzonensis, animal remains strong and interest in its natural O. matanensis and O. marmoratus. A note on electro- history is seemingly unlimited. Four medaka, two phoretic comparison of proteins among Oryzias males and two females, were aboard the US space species was introduced by Sakaizumi (1985: 521) as shuttle COLUMBIA for 15 days in 1994 and per- follows: ‘Recently several Japanese zoologists have formed the first successful vertebrate mating in begun comparative studies of the phylogeny of space, captured on videotape (Ijiri, 1995). The devel- Oryzias. The aim of this joint effort is to reexamine opment and swimming behaviour of medaka fry each nominal species morphologically, karyologically, under microgravity was observed on a subsequent biochemically and genetically.’ COLUMBIA mission in early 2003 (Niihori et al., The late Hiroshi Uwa (1986, 1991a, b, 1993), 2004). Living stocks of Oryzias species have long been Shinshu University, Matsumoto, Japan, and col- maintained in Japanese universities (Iwamatsu et al., leagues (e.g. Uwa & Ojima, 1981; Uwa & Jeon, 1987; 1993). A World Medaka Aquarium at the Nagoya Uwa & Parenti, 1988; Magtoon et al., 1992; Takata Higashiyama Zoo, Nagoya, Japan, has maintained et al., 1993) described some of the remarkable varia- Oryzias species and Oryzias latipes mutants tion in cytogenetic characters among Oryzias species, (Matsuyama, 1994). A journal devoted to the biology including chromosome number and constitution and of the medaka, The Fish Biology Journal MEDAKA, cellular DNA content. Investigations by Uwa and was published by the Laboratory of Freshwater Fish colleagues also included description of a new species, Stocks, Nagoya University, Japan. The medaka has a Oryzias mekongensis Uwa & Magtoon, 1986, and a homepage, http://biol1.bio.nagoya-u.ac.jp:8000/ (Hori new subspecies, Oryzias latipes sinensis Chen, Uwa & & Watanabe, 1995), with links to other popular Chu, 1989, recognized herein at the species level, as medaka web-sites. in Kottelat (2001a, b). No claim to original US Government works. Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154, 494–610 496 L. R. PARENTI Table 1. Classification of ricefishes, family Adrianichthy- Lake Lindu, Sulawesi, in 1939. Ricefishes as a group idae, as recognized in the present study are ‘under-described’ (Roberts, 1998: 213), and it is likely that more, detailed studies of population varia- Family Adrianichthyidae Weber, 1913 tion within some of the wide-ranging taxa recognized Genus Adrianichthys Weber, 1913 here, such as O. sinensis, O. latipes, O. dancena A. kruyti Weber, 1913 (Fig. 1) and O. carnaticus (see Roberts, 1998), will A. oophorus (Kottelat, 1990a) comb. nov. result in description of additional species. As I A. poptae (Weber & de Beaufort, 1922) comb. nov. was completing this monograph, Tyson R. Roberts A. roseni Parenti & Soeroto, 2004 informed me of his discovery of additional new species Genus Oryzias Jordan & Snyder, 1906 from south Asia, and Renny Hadiaty (MZB) informed O. latipes (Temminck & Schlegel, 1846) me of collections
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