Genomics and Mapping of Teleostei (Bony fish)
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Comparative and Functional Genomics Comp Funct Genom 2003; 4: 182–193. Published online 1 April 2003 in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/cfg.259 Featured Organism Genomics and mapping of Teleostei (bony fish) Melody S. Clark* HGMP Resource Centre, Genome Campus, Hinxton, Cambridge CB2 4PP, UK *Correspondence to: Abstract Melody S. Clark, HGMP Resource Centre, Genome Until recently, the Human Genome Project held centre stage in the press releases Campus, Hinxton, Cambridge concerning sequencing programmes. However, in October 2001, it was announced CB2 4PP, UK. that the Japanese puffer fish (Takifugu rubripes, Fugu) was the second vertebrate E-mail: [email protected] organism to be sequenced to draft quality. Briefly, the spotlight was on fish genomes. There are currently two other fish species undergoing intensive sequencing, the green spotted puffer fish (Tetraodon nigroviridis) and the zebrafish (Danio rerio). But this trio are, in many ways, atypical representations of the current state of fish genomic research. The aim of this brief review is to demonstrate the complexity of fish as a Received: 10 November 2002 group of vertebrates and to publicize the ‘lesser-known’ species, all of which have Revised: 5 December 2002 something to offer. Copyright 2003 John Wiley & Sons, Ltd. Accepted: 28 January 2003 Keywords: Teleostei; fish; genomics; BACs; sequencing; aquaculture Background the wild-caught fisheries production figures. The equivalents within the EU are trout, Atlantic Fish have the potential to be immensely useful salmon and sea bass/bream for aquaculture; model organisms in medical research, as evidenced with herring, mackerel and sprat for wild-caught by the genomic sequencing programmes mentioned fisheries. None of these species is the subject of a above. Indeed, there is an increasing number high-profile genomics programme. of alternative species, such as Xiphophorus and medaka, which are being promoted in this area. However, it is fair to say that, in general, Fish relationships fish are the poor relations of high-throughput molecular biology. To put fish into context, they The term ‘fish’ is not a taxonomic rank, but a con- comprise over half of all known vertebrates and are venient label for a diverse group of organisms (for a economically very important. They are a significant comprehensive review, see Nelson, 1994). Overall, source of revenue, with the fisheries industry this convenient grouping of ‘fish’ varies depend- (national fishing fleets, aquaculture and associated ing on different sources, but can include the jaw- processing) generating ¤20 billion per year for the less vertebrates (Agnatha), sharks and rays (Chon- EU alone (without taking into account recreational drichthyes), the lobe-finned fishes (Sarcopterygii) or game fishing and aquarium supplies). This and the ray-finned fishes (Actinopterygii, including contrasts with the fact that the species undergoing the Teleostei). sequencing programmes were chosen due to their The lobe-finned fishes are in an evolutionarily potential as model genomes/organisms, rather critical position leading to the human lineage. than their commercial importance. Globally in The ray-finned fishes diverged from this ‘main’ aquaculture, the three most important fish are lineage approximately 450 million years ago and carp, Atlantic salmon and trout; with anchoveta, have since undergone massive diversification Alaska pollock and Chilean jack mackerel leading in morphology, physiology and habitat. Their Copyright 2003 John Wiley & Sons, Ltd. Teleostei 183 Figure 1. Phylogenetic relationships among living teleosts. Fish coloured in grey represent orders in which species are undergoing intensive mapping or sequencing programmes. Reproduced from The Diversity of Fishes by Helfman, Collette and Facey, by permission of Blackwell Science Copyright 2003 John Wiley & Sons, Ltd. Comp Funct Genom 2003; 4: 182–193. 184 Featured organism genomes did not remain static and they are salmonids are the best known example of such, still evolving, with the phylogenetic relationships many other species, such as members of the Cobiti- uncertain in many cases. Within this particular class dae, Catostomidae and Asipenseridae also contain (Actinopterygii) are those regarded as the more different ploidy levels, even up to 8× (Ohno, 1974; ‘ancient fishes’. This latter category includes the Bailey et al., 1978, and references therein). Hence sturgeons, paddlefishes and bichirs, which have fish, as a group of vertebrates, do not seem to relatively few extant members when compared to have the same stringent genomic controls that exist the rest of the class. This review will be largely within other groups of vertebrates, a property which restricted to a sub-set of the ray-finned fishes, may be due in part to their lack of a rigid sex chro- the Teleostei or bony fishes (Figure 1), where the mosome system. Data on the more common species model and (most) commercial species are found. is given in Table 2. Table 1 lists the more commonly known members of each order (Nelson, 1994). Polyploidy and fish-specific duplications Genome sizes and karyotypes It is known that many fish are polyploid, the prime example given above being that of the Fish certainly appear to have a much more dynamic salmonids, in which members such as trout and and plastic genome than that of mammals, with salmon are actually partial tetraploids, 2n = 4× genome sizes varying from 400 Mb in some of (Lee and Wright, 1981; Wright et al., 1983; Allen- the Tetraodontidae to over 1000 Mb in the African dorf and Thorgaard, 1984). The term ‘partial’ lungfishes (Hinegardner, 1968; Hinegardner and means that the species have undergone an ancient Rosen, 1972; Ohno, 1974; Tiersch et al., 1989). extra whole genome duplication (i.e. in addition This wide range of genome sizes is also reflected to the two rounds of whole genome duplication in huge karyotypic variation, with diploid num- which occurred in the vertebrate lineage, pro- bers as low as 2n = 22–26 in some Nototheriidae posed by Ohno, 1970) and are currently revert- (Ozouf-Costaz et al., 1997), up to 2n = 240–260 ing to diploidy via a process of gene loss. How- in some anadromous Acipenseridae (Fontana et al., ever, there is currently much debate as to whether 1997). However, these diploid numbers hide the the whole of the Euteleostei have undergone an fact that many species are polyploid. Although the extra whole genome duplication, or just isolated Table 1. Main orders of the Teleostei accompanied by their more commonly known family members. Most examples are listed against the Percomorpha, as these comprise approximately 50% of all known extant fishes. Species discussed in this review are also indicated Teleostei sub-division Common families Family members Osteoglossomorpha Elephantfishes, mooneyes Elopomorpha Tarpons, eels Clupeomorpha Herrings, anchovies Ostariophysi Carps, suckers, loaches, catfishes Catfish, zebrafish Protocanthopterygii Pikes, mudminnows, smelts, salmonids Salmon, trout Stenopterygii Lightfishes, bristlemouths Cyclosquamata Telescopefishes, greeneyes Scopelomorpha Lanternfishes Lampridiomorpha Ribbonfishes, oarfishes Polymixiomorpha Beardfishes Paracanthopterygii Cavefishes, cods, hakes, rattails, anglerfishes Mugilomorpha Mullets Atherinomorpha Killifishes, rainbowfishes, flying fishes, silversides, Medaka, Xiphophorus medakas Percomorpha Basses, perches, jacks, chubs, snappers, cichlids, Tilapia, Tetraodon, Fugu, sea mackerels, flounders, pufferfishes, swordfishes, tunas bass, sea bream Copyright 2003 John Wiley & Sons, Ltd. Comp Funct Genom 2003; 4: 182–193. Teleostei 185 Table 2. Fish genome sizes and chromosome complements of some of the more commercially important species. X indicates data not known. Where possible, species discussed in this review have been included. Brackets indicate that the chromosome number given is that of a closely related family member, not the exact species named (data taken from Bejar et al., 1997; Hinegardner, 1968; Hinegardner and Rosen, 1972; Ohno, 1974; Sola et al., 1993; Tiersch et al., 1989; http://www.genomesize.com/fish.htm; http://www.fishbase.org; Angelo Libertini, personal communication). In perspective; the coho salmon, carp and pacific herring are 90%, 50% and 28%, respectively, of the size of the human genome Common Haploid Diploid Sub-division Latin name name DNA content (Mb) chromosome no. Elopomorpha Anguilla rostrata Atlantic eel 1400 38 Clupeomorpha Engraulis mordax Californian anchovy 1500 46–48 Clupea pallasi Pacific herring 770 52 Ostariophysi Cyprinus carpio Common carp 1700 50 Danio rerio Zebrafish 1800 50 Ictarulus punctatus Channel catfish 1050 58 Protocanthopterygii Onchorhynchus kisutch Coho salmon 3000 60 Onchorhynchus tshawytscha Chinook salmon 3300 68 Salmo salar Atlantic salmon 3100 60 Onchorhynchus mykiss Rainbow trout 2600 60 Salmo trutta Brown trout 2800 80 Paracanthopterygii Merluccinus bilinearis Silver hake 930 — Atherinomorpha Oryzias latipes Medaka 800 48 Xiphophorus maculatus Xiphophorus 950 48 Percomorpha Dicentrarchus labrax European sea bass 1600 48 Lutjanus campechanus Red snapper 1400 — Sparus aurata Gilthead sea bream 1650 48 Tilapia nilotica Nile tilapia 1200 44 Scomber scombrus Atlantic mackerel 970 (48) Pseudopleuonectes americus Winter flounder 700 48 Fugu rubripes Japanese pufferfish 365 44 Tetraodon nigroviridis Freshwater Pufferfish 380 42 species. This debate arose mainly from the results be complete agreement between the two sides, of mapping studies of zebrafish, which showed even with the imminent sequencing