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Genes Genet. Syst. (2009) 84, p. 153–170 Comprehensive phylogeny of the family Sparidae (Perciformes: Teleostei) inferred from mitochondrial gene analyses Satoru N. Chiba1, Yukio Iwatsuki2, Tetsuo Yoshino3 and Naoto Hanzawa1* 1Graduate school of Science and Engineering, Yamagata University, 1-4-12 Kojirakawa-machi, Yamagata 990-8560, Japan 2Division of Fisheries Science, Faculty of Agriculture, University of Miyazaki, 1-1 Gakuen-Kibanadainishi, Miyazaki 889-2192, Japan 3Department of Marine Sciences, Faculty of Science, University of the Ryukyus, 1 Senbaru, Nishihara-cho, Okinawa 903-0213, Japan (Received 13 October 2008, accepted 3 February 2009) Sparid fishes consist of approximately 115 species in 33 genera that are broadly distributed in tropical and temperate coastal waters. Although several phyloge- netic analyses were conducted based on specific molecular markers, their classifi- cation remains unresolved. Here, we present the most comprehensive molecular phylogeny of the family Sparidae to date, based on cytochrome b (cyt-b) genes. We determined 18 sequences of sparids and conducted phylogenetic analyses among 72 individuals representing 66 sparids with 23 outgroup species. Phyloge- netic trees were constructed according to partitioned Maximum Likelihood (ML) and Bayesian methods. The phylogenetic analyses were conducted on two dif- ferent data sets (including all positions; RY-coding). The phylogenetic trees showed monophyly of the family Sparidae with a different taxon, centracanthid Spicara. The subfamilies in the Sparidae in all trees are non-monophyletic and do not agree with current classification of the subfamilies. The genera Acanthopagrus, Cheimerius, Dentex, Diplodus, Pagellus, Pagrus, and Spicara are also non-monophyletic and their classifications should be revised based on the phylogenetic relationships and reinvestigation of morphological characters. The sparids are divided into three major clades, A, B and C, respectively in the ML tree based on all codon positions, whereas clade C was paraphyletic in the other trees. The species in clade C are known to be present in the eastern Pacific to western Atlantic, whereas those in clades A and B are distributed in various oceanic regions. Some sub-clades in clades A and B consist of species that are dis- tributed in defined local regions. We further investigated evolutionary patterns of 87 morphological characters by ancestral character-state reconstruction accord- ing to the parsimony criteria. The results suggested high evolutionary plasticity of the characters in sparids, indicating that it causes species-diversity and taxo- nomic confusion at various taxonomic levels, and that such convergent evolution may occur more frequently also in other coastal fishes. Key words: sequence variation, ML, Bayes, character state reconstruction, convergent evolution because similar morphological characters among species INTRODUCTION are derived from convergent evolution, and speciation In most taxa of coastal fishes that are distributed patterns are quite complicated (Duftner et al., 2007; worldwide, it is difficult to infer accurate phylogenetic Westneat et al., 2005). One such coastal fish family, the relationships and to classify the fish appropriately Sparidae (Perciformes), which consists of approximately 115 species belonging to 33 genera, is the most diverse of Edited by Toshihiko Shiroishi the sparoid families (Nelson, 2006). The species in the * Corresponding author. E-mail: [email protected] Sparidae inhabit tropical and temperate coastal waters and 154 S. N. CHIBA et al. occasionally occur in estuaries as nurseries (Carpenter, feeding strategies and dentition. However, since they 2001). used only S. maena as the outgroup, their analysis The Sparidae, Nemipteridae, and Lethrinidae were rec- showed incorrect phylogenetic relationships among ognized their osteological close relationships and termed sparids and of the sparids to related families. Orrell et them as “spariform” fish (Akazaki, 1962). Additionally it al. (2002) and Orrell and Carpenter (2004) inferred the was found that the three families were also closely related phylogeny of representatives of all 33 sparid genera and osteologically to the family Centracanthidae and classi- a number of percoid outgroups using the mitochondrial fied all of them into the new superfamily Sparoidea cytochrome b (cyt-b) gene and 16S rRNA gene sequences. (Johnson, 1980). The phylogenetic position of the cent- They also found that the currently defined subfamilies racanthids, however, is still uncertain with respect to are not monophyletic and showed Spicara to be a member sparid genera (Carpenter and Johnson, 2002; Day, 2002; of the sparid ingroup. Day (2002) analyzed a numerical Orrell et al., 2002; Orrell and Carpenter, 2004). The four phylogeny of the interrelationships among most extant families form a monophyletic clade and can be placed in genera in the sparid using morphological data. The the superfamily Sparoidea by a cladistic analysis of 54 morphological data support their hypothesis that the morphological characters (Carpenter and Johnson, 2002). currently defined subfamilies are non-monophyletic and However, the Lethrinidae was a sister taxa to the that Spicara is nested deeply within the ingroup, but a Sparidae (Orrell et al., 2002). Therefore the superfamily few analyzed sparid genera are known to be non- Sparoidea was not recognized as the formal superfamily monophyletic based on molecular studies to date. in classification pending more study of other percoid fam- Because mitochondrial cyt-b genes are relatively easy ilies in hopes of presenting a comprehensive and mono- to amplify and sequence (Nishida et al., 1998), they con- phyletic classification of the entire group (Nelson, 2006). tain both slowly and rapidly evolving codon positions (e.g. Sparid species are classified based on morphological Saitoh et al., 2006; Yamanoue et al., 2007), and a signif- characters, such as dentition, spinous and soft fin ray icant amount of sequence data is available in GenBank counts, scalation and body color (e.g. Akazaki, 1962; and other DNA databases, these genes are very useful Bauchot and Hureau, 1986; Smith and Smith, 1986). In and convenient markers to clarify the evolutionary his- particular, dentition has been used by many researchers tory of fishes at various phylogenetic levels (e.g. Sasaki et to distinguish genera (e.g. Cuvier, 1817, 1829; Smith, al., 2006; Kuriiwa et al., 2007; Pérez et al., 2007; Timm et 1938; Munro, 1948, 1949; Akazaki, 1962) and to provide al., 2008). Most recent studies have focused on resolving subfamily classification (Smith, 1938; Smith and Smith, phylogeny conflicts at a higher taxonomic level mostly by 1986; Akazaki, 1962). Smith and Smith (1986) erected adding characters rather than taxa, and this has not four subfamilies, Sparinae, Denticinae, Pagellinae, and improved our understanding of lower taxonomic level Boopsinae, using dentitional characters, which are con- relationships. Mitogenomic data, for example, is known sidered to reflect trophic specialization. Akazaki (1962) to be a powerful genetic marker to resolve uncertainties further subdivided the Sparinae into two new subfami- at various phylogenetic levels. However, mitogenomic lies, Diplodinae and Pagrinae. Fiedler (1991) distin- data is available only for five sparid species despite the guished only three subfamilies, Sparinae (includes Smith fact that sparid classification needs a comprehensive phy- and Smith’s Pagellinae and Sparinae), Denticinae, and logenetic study that focuses on various phylogenetic Boopsinae. levels. These data well provide better tools for detailed In previous molecular studies of the relationships evolutionary studies, and are necessary to test existing among sparids and between the family Sparidae and morphological phylogenetic hypotheses, and current other percoids deduced from isozymes and their expres- sparid classification. Furthermore, adding more taxa, sion patterns and sequence analysis, taxon sampling was together with adding characters to molecular phyloge- limited mainly to sparids from the eastern Atlantic and/or netic data, can be an efficient way to overcome phyloge- Mediterranean or Japanese waters (Taniguchi et al., netic uncertainty (Graybeal, 1998; Hillis, 1996, 1998; 1986; Basagila, 1991; Garrido-Ramos et al., 1995, 1998, Hillis et al., 2003; Pollock et al., 2002; Zwickl and Hillis, 1999; Jean et al., 1995; Allegrucci et al., 1999; Hanel and 2002; but see Miller and Hormiga, 2004; Rosenberg and Sturmbauer, 2000; Summerer et al., 2001; de la Herrán Kumar, 2001, 2003; Rokas and Caroll, 2005). However, et al., 2001). Hanel and Sturmbauer (2000) analyzed it is obvious that combining multiple genes is beneficial mitochondrial 16S rDNA (16S) sequences of all 24 sparid to any phylogenetic problem. species described from the northeastern Atlantic and Here, we determined 18 cyt-b gene sequences for 15 Mediterranean, and used the centracanthid Spicara species of the 68 sparid taxa and estimated their phylog- maena as the outgroup. Their analysis indicated that eny with 23 outgroups. This data set covers approxi- some sparid genera and the currently defined subfamilies mately 60% of sparid species. The protein coding cyt-b are not monophyletic and that there are three major mito- gene that was employed is a useful marker for phyloge- chondrial lineages, each comprising species with different netic analysis among many species. The codon parti- Molecular phylogeny of sparid

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