Novel Relationships Among Ten Fish Model Species Revealed Based on a Phylogenomic Analysis Using Ests
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J Mol Evol (2006) 62:772–784 DOI: 10.1007/s00239-005-0170-8 Novel Relationships Among Ten Fish Model Species Revealed Based on a Phylogenomic Analysis Using ESTs Dirk Steinke, Walter Salzburger, Axel Meyer Lehrstuhl fu¨ r Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, 78457 Konstanz, Germany Received: 8 July 2005 / Accepted: 17 February 2006 Reviewing Editor: Dr. Rafael Zardoya] ½ Abstract. The power of comparative phylogenomic physi and Acanthopterygii are monophyletic and the analyses also depends on the amount of data that are Protacanthopterygii and Ostariophysi are sister included in such studies. We used expressed sequence clades. In addition, and contrary to the traditional tags (ESTs) from fish model species as a proof of phylogenetic hypothesis, our analyses determine that principle approach in order to test the reliability of killifish (Cyprinodontiformes), medaka (Belonifor- using ESTs for phylogenetic inference. As expected, mes), and cichlids (Perciformes) appear to be more the robustness increases with the amount of se- closely related to each other than either of them is to quences. Although some progress has been made in pufferfish (Tetraodontiformes). All 10 lineages split the elucidation of the phylogeny of teleosts, rela- before or during the fragmentation of the supercon- tionships among the main lineages of the derived fish tinent Pangea in the Jurassic. (Euteleostei) remain poorly defined and are still de- bated. We performed a phylogenomic analysis of a Key words: Teleost phylogeny — Phylogenomics set of 42 of orthologous genes from 10 available fish — Euteleostei — Molecular clock — EST — Pangea model systems from seven different orders (Salmoni- — Gondwana formes, Siluriformes, Cypriniformes, Tetraodonti- formes, Cyprinodontiformes, Beloniformes, and Perciformes) of euteleostean fish to estimate diver- gence times and evolutionary relationships among those lineages. All 10 fish species serve as models for Introduction developmental, aquaculture, genomic, and compara- tive genetic studies. The phylogenetic signal and the The relative importance of increasing the number of strength of the contribution of each of the 42 or- analyzed taxa and the number of characters for thologous genes were estimated with randomly cho- accuracy of phylogenetic inferences remains an issue sen data subsets. Our study revealed a molecular of debate (Hillis 1998; Hillis et al. 2003; Rosenberg phylogeny of higher-level relationships of derived and Kumar 2003; Gadagkar et al. 2005; Cummings teleosts, which indicates that the use of multiple genes and Meyer 2005; Rokas et al. 2005). Large-scale produces robust phylogenies, a finding that is ex- phylogenetic analyses inevitably involve a trade-off pected to apply to other phylogenetic issues among between taxon sampling and gene sampling. However, distantly related taxa. Our phylogenomic analyses recent simulation and empirical studies suggest that confirm that the euteleostean superorders Ostario- increased gene sampling, in general, might have a greater beneficial effect on the rigor of the estimation of phylogenetic topologies than more extensive taxon Correspondence to: Axel Meyer, Department of Biology, University of Konstanz, Postbox 5560 M618, D-78457 Konstanz, Germany; sampling (Mitchell et al. 2000; Rosenberg and Kumar email: [email protected] 2001; Rokas and Carroll 2005). The benefits of sam- 773 pling several independent gene genealogies to infer an Table 1. Diversity and classification of ray-finned fish and species organismal phylogeny with confidence are widely used in this study: The classification follows Nelson (1994) recognized (Cummings et al. 1995; Takezaki et al. Class Actinopterygii (23,681 species, 42 orders) 2003; Chen et al. 2004) because a more complete Division Teleostei (23,637 species, 38 orders) representation of the whole genome is highly desirable Subdivision Euteleostei (22,262 species, 32 orders) and stochastic errors occurring in data with small Superorder Acanthopterygii (13,414 species, 13 orders) sample size will decrease with increasing sample size. Order Beloniformes (191 species, 5 families) Oryzias latipes Comparative phylogenomic analyses using ex- Order Cyprinodontiformes (807 species, 8 families) pressed sequence tags (ESTs) from taxa across the Fundulus heteroclitus spectrum of animal diversity promise to yield reliable Order Perciformes (9,293 species, 148 families) and robust results. ESTs also provide an economical Haplochromis sp. approach to identify large numbers of genes that can Order Tetraodontiformes (339 species, 9 families) Takifugu rubripes be used in gene expression and phylogenomic studies Tetraodon nigroviridis (Gerhold and Caskey 1996; Renn et al. 2004; Hughes Superorder Ostariophysi (6,507 species, 5 orders) et al. 2006). For this reason, and because of the rapid Order Cypriniformes (2,662 species, 5 families) automated way of data collection and the relatively Cyprinus carpio low costs associated with this technology, many Danio rerio Order Siluriformes (2,405 species, 34 families) individual scientists as well as large genome Ictalurus punctatus sequencing centers have generated large numbers of Superorder Protacanthopterygii (312 species, 3 orders) ESTs that are publicly available and their numbers Order Salmoniformes (66 species, 1 family) continue to increase rapidly. Oncorhynchus mykiss However, the use of ESTs for phylogenetic anal- Salmo salar yses is limited to the rather small number of species for which EST and genome projects have been con- ducted. In order to test to test the power of multilo- cus approaches to reveal phylogenies, it was 16,000 species. These are placed into 32 orders and necessary to choose a group of species for which nine superorders. Currently used fish model species extensive EST datasets are available. Here we chose for developmental, genomic, and comparative genetic teleost fish to conduct EST-based analyses with dif- studies are assigned to three superorders of the Eu- ferent phylogenetic approaches such as Bayesian teleostei: the Ostariophysi, the Protacanthopterygii, inference and maximum likelihood in an effort to and the Acanthopterygii (Table 1). Ostariophysi are overcome possible pitfalls of one particular method. basal euteleosts characterized by the presence of the A recent theoretical study (Mossel and Vigoda 2005) Weberian apparatus. Protacanthopterygii is a super- revealed that Bayesian MCMC methods for phylog- order that was established by Greenwood et al. (1966) eny reconstruction could be misleading when the data and originally included a wide array of basal eu- are generated from a mixture of datasets. Thus, in teleosts. Since then, Rosen and Patterson (1969), cases of datasets that contain potentially conflicting Rosen and Greenwood (1970), and Rosen (1973, phylogenetic signals, phylogenetic reconstruction 1974) have repeatedly removed several of the orders should be performed separately on each subset that were originally included in the Protac- according to Mossel and Vigoda (2005). anthopterygii by them. The resulting Protac- There are more than 25,000 species of teleost fish, anthopterygii (sensu Rosen 1974) is the basis of amounting to nearly half of the extant vertebrate subsequent discussions on monophyly, interrelation- species, and about 96% of all extant fish are classified ships, and intrarelationships (e.g., Fink and Fink as teleosts (Nelson 1994). Since the pioneering work 1996; Ishiguro et al. 2003). Among the euteleosts the, on the systematics of fish by Greenwood et al. (1966), by far, most diverse lineage are the Acanthopterygii many studies have proposed novel hypotheses about (spiny rayed fish), comprising approximately 14,800 the relationships among basal teleosts, but the rela- species, in which both the dorsal and the pelvic fins tionships among the derived teleosts are still debated. have true fin spines as well as rays. The majority of One particular species-rich monophyletic group of Protacanthopterygii has ctenoid scales, and the pelvic derived teleosts is the Euteleostei, currently ranked as fins are thoracic, and the jaws protrusible. To the one of the four subdivisions of the Teleostei, along Acanthopterygii, Johnson and Patterson (1993) as- with the more basal groups, Osteoglossomorpha, signed five orders (Perciformes, Dactylopteriformes, Elopomorpha, and Clupeomorpha (Nelson 1994; Scorpaeniformes, Pleuronectiformes, and Tetra- de Pinna 1996; Arratia 1999; Miya et al. 2003, Inoue odontiformes) as a single clade and putative sister et al. 2004). group to the Smegmamorpha (which contains the The Euteleostei are the most derived and species- lineages Synbranchiformes, Mugiloidei, Elassomati- rich group of teleost fish, comprising approximately dae, Gasterosteiformes, and the Atherinomorpha). 774 Table 2. GenBank, JGI, and ENSEMBL accession numbers of the sequences and numbers of amino acids used for the phylogenetic analyses Amino acid EST used in Cyprinus Fundulus No. Annotation analyses Cichlid ESTs carpio Danio rerio heteroclitus 1 Adenylate kinase 2 189 BJ678728 CF662232 ENSDARP00000010686 CN983450 2 60S ribosomal protein L23a 130 BJ679384 AU240353 ENSDARP00000006624 CN979291 3 60S ribosomal protein L27a 131 BJ682982 CA965998 ENSDARP00000024203 CN983839 4 Triosephosphate isomerase 1 176 BJ683057 CF662476 ENSDARP00000008240 CV816996 5 snRNP core protein 134 BJ683377 CA970312 ENSDARP00000011550 CV819764 6 Acetoacetyl coenzyme A 187 BJ685403 CA968898 ENSDARP00000018064 CN970611 7 Eukaryotic translation 180 BJ686392 CA965942