Gene and genome duplications are considered to be the main evolutionary mechanisms contributing to the unrivalled biodiversity of bony fish. New studies of vitellogenin yolk proteins, including a report in BMC Evolutionary Biology, reveal that the genes underlying key evolutionary innovations and adaptations have undergone complex patterns of duplication and functional evolution

Braasch, Ingo

Salzburger, Walter

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MinireviewIn ovo omnia: diversification by duplication in fish and other vertebratesIngo Braasch* and Walter Salzburger†Addresses: *University of Würzburg, Physiological Chemistry I, Biocenter, Am Hubland, 97074 Würzburg, Germany. †Zoological Institute,University of Basel, Vesalgasse 1, 4055 Basel, Switzerland.Correspondence: Walter Salzburger. Email: walter.salzburger@unibas.chSince the publication of Charles Darwin’s The Origin ofSpecies a century and a half ago, evolutionary biologists havebeen concerned with the identification of the processes thatgovern the emergence of new species and, thus, oforganismal diversity. Because of variation in the rate ofspeciation and extinction, evolution inevitably leads to anunequal distribution of morphological diversity andspecies-richness across taxonomic lineages. Some lineageshave remained morphologically uniform and are species-poor, whereas others have diversified rapidly. It is thesemore ‘successful’ and species-rich lineages in particular thatenable insights into the process of diversification.In vertebrates, the most species-rich group is that of thefishes: at least one in two vertebrate species is a fish, or -more precisely - a teleost fish. There are at least 26,000living teleost species [1], which show a remarkable varietyof ecological, morphological and behavioral adaptations.Among the characteristics that distinguish the teleost cohortfrom the only 50 or so species of basal ray-finned fishes andthe rest of the vertebrates are genomic features such as geneand genome duplications and higher rates of chromosomalrearrangements and molecular evolution [2].Are gene and genome duplications the fuel thatdrives biodiversity in fish?A fish-specific genome duplication (also known as the 3Rduplication) occurred in an ancestor of the teleost lineagearound 300-350 million years ago [3]. This event, whichendowed teleosts with additional new genes, has beenhypothesized to be at least partly responsible for theirbiodiversity and species richness [2,4,5]. Not all genes thatemerged from the duplication are still present, however. Infact, the majority of duplicated genes (about 70-90%) havesince been degraded and/or lost (a process termed nonfunc-tionalization). But because this massive post-duplicationgene loss followed different routes, different teleost lineagesnow have different complements of paralogous genesderived from the original genome duplication. This processis called divergent resolution [4,5]. Empirical support fordivergent resolution between teleost lineages that divergedAbstractGene and genome duplications are considered to be the main evolutionary mechanismscontributing to the unrivalled biodiversity of bony fish. New studies of vitellogenin yolkproteins, including a report in BMC Evolutionary Biology, reveal that the genes underlying keyevolutionary innovations and adaptations have undergone complex patterns of duplication andfunctional evolution.Journal of Biology 2009, 8:25Published: 5 March 2009Journal of Biology 2009, 8:25 (doi:10.1186/jbiol121)The electronic version of this article is the complete one and can befound online at http://jbiol.com/content/8/3/25© 2009 BioMed Central Ltd very early comes from a recent comparative genome-wideanalysis of paralog loss in zebrafish and the green spottedpufferfish [6].In many cases where both copies have been maintained in agenome, the functions of the ancestral gene are now distri-buted among the duplicates - a process called subfunctiona-lization. Given that retention of duplication-derived genecopies also followed different routes and that subfunc-tionalization can be neutral and stochastic, the partitioningof gene functions can also occur lineage-specifically. Finally,it is possible that one of the duplicates continues to fulfillthe ancestral functions while the other acquires a com-pletely new function (neofunctionalization). Differentialfunctional evolution between teleost lineages has so farbeen shown for zebrafish, stickleback and medaka [4].Together, the fish-specific genome duplication and thedivergent resolution, subfunctionalization and neofunc-tionalization that followed it created a large evolutionaryplayground within teleost genomes. The duplication-diversification hypothesis predicts that gene and genomeduplication and subsequent reciprocal gene loss and/ordifferential paralog evolution in divergent populationsleads to genomic incompatibilities between isolated popu-lations and, consequently, to postzygotic isolation andspeciation. That is how the fish-specific genome duplicationmight have facilitated the radiation of teleosts [4,5].Vitellogenin gene duplications and marine teleostradiationsBesides the overall impact of gene and genome duplicationon reproductive isolation and thus on speciation, neo-functionalization of a duplicated gene copy can lead to theorigination of a key evolutionary innovation that enables agroup to radiate, for example in a new environment. In twonew articles, one in BMC Evolutionary Biology [7] and theother in Molecular Biology and Evolution [8], Finn andcolleagues examine an example of a cluster of genes thatemerged by duplication and that apparently has enabled awhole group of fishes to diversify.Finn and Kristoffersen had already in earlier studies [1]reconstructed the evolution of the vitellogenin (vtg) genefamily in teleost fishes. Vitellogenins are yolk proteinssynthesized in the liver and deposited in the maturingoocyte. Finn and Kristoffersen [1] suggested that neo-functionalization of the vtgAa gene in acanthomorphs, themost species-rich group of teleosts (comprising about16,000 species, 78% of which are marine), was an impor-tant step towards adapting to a new spawning strategy in themarine realm. Proteolysis of the VtgAa yolk protein leads toan increase in the levels of free amino acids in the maturingoocyte and causes water influx. In this way, the hydratedeggs are protected against leakage of water into thehyperosmolar marine environment, so that the eggs float onthe water surface. This is an important adaptation thatmakes pelagic (‘floating’) spawning strategies possible.The initial phylogenetic analysis of teleost vitellogenins [1]suggested that the three vtg genes in acanthomorphs, vtgAa,vtgAb and vtgC, evolved through a progressive series of geneduplications and subsequent gene losses, involving the fish-specific genome duplication and the two earlier rounds ofwhole genome duplication in vertebrates (called 1R and2R), and also an acanthomorph-specific duplication of thevtgA gene that generated the vtgAa and vtgAb duplicates.According to this scenario, lineage-specific neofunctionali-zation of the newly arising vtgAa paralog in acanthomorphsfacilitated their conquest of the marine ecosystem fromtheir original habitats in freshwaters.New data presented by the same group in BMC EvolutionaryBiology [7], as well as an earlier article by Babin [9], take thelocation of vitellogenin genes in vertebrate genomes intoaccount and turn the duplication history of teleost vtg genesupside down. In acanthomorphs, vtgAa, vtgAb, and vtgC arelocated close to each other on the same chromosome. Thisis consistent with the arrangement of vitellogenin genes inother teleosts and in more distantly related vertebratelineages, such as frog and chicken [7,9]. The most parsi-monious explanation for this arrangement is thus that avitellogenin gene cluster consisting of three genes (Vtg1,called vtgC in fish, Vtg2, called vtgAb in fish, and Vtg3, calledvtgAa in fish) was already present in the last commonancestor of fish and tetrapods about 450 million years ago(Figure 1). An ancestral vitellogenin gene (proto Vtg) wasduplicated, giving rise to Vtg1 and Vtg2/3. The latter genewas then duplicated in tandem, generating Vtg2 and Vtg3(Figure 1a). In the fish lineage, two vitellogenin geneclusters were present after the fish-specific genome dupli-cation, but one of them degenerated so that this round ofgenome duplication did not increase the number of func-tional vtg genes.In theory, phylogenetic reconstruction of the vitellogeningene or protein family should reveal these three ancestralgene duplications. However, published vitellogenin phylo-genies [1,7,8,10] consistently suggest that the differentvertebrate Vtg2 and Vtg3 genes have been generated inparallel but independently through lineage-specific tandemduplications (Figure 1b). One explanation for the failure ofphylogenies to reconstruct the common duplication of theVtg2/3 precursor could be that gene conversion has occurredbetween Vtg2 and Vtg3, keeping them alike. The new results25.2 Journal of Biology 2009, Volume 8, Article 25 Braasch and Salzburger http://jbiol.com/content/8/3/25Journal of Biology 2009, 8:25by Finn et al. [7] and Babin [9] therefore illustrate howimportant it is to include synteny data for the correctinference of gene family evolution.Use it or lose it (or duplicate or delete)The evolutionary significance of vitellogenins is furthersubstantiated by the high frequency of true lineage-specificduplication events in teleost fishes. In acanthomorphs,Vtg2/vtgAa has been duplicated in medaka, whereasVtg3/vtgAb has multiple copies in marine labrids (wrasses).In the zebrafish, an ostariophysian, both Vtg3/vtgAb andVtg2/vtgAa have been duplicated, the latter being present inas many as five copies [7-9]. Nevertheless, acanthomorphsare special in their processing of the Vtg2/VtgAa protein andthe exceptionally high expression of Vtg2/vtgAa in marine,pelagically spawning species [7]. Although yolk proteolysisevolved before the divergence of Acanthomorpha andOtocephala (such as zebrafish and herring), it was not untilthe neofunctionalization of Vtg2/vtgAa in the acanthomorphhttp://jbiol.com/content/8/3/25 Journal of Biology 2009, Volume 8, Article 25 Braasch and Salzburger 25.3Journal of Biology 2009, 8:25Figure 1Evolution of the vertebrate vitellogenin cluster. (a) The vertebrate vitellogenin cluster was generated by two ancestral gene duplications (1 and 2).(b) The phylogeny of vertebrate Vtgs should reconstruct the ancestral gene duplications correctly (left), but observed phylogenies (right, merged anddeduced from [1,7,8,10]) indicate multiple, independent duplications (black circles) of Vtg2/3. Gene names are as used in the literature. A unifyingnomenclature is shown to the right of the expected phylogeny. The remaining functional platypus VtgX gene is most likely a Vtg2 [9,10].Ancestral gene duplication Lineage-specific gene duplicationStickleback vtgAaWrasse vtgAaStickleback vtgAbWrasse vtgAb1/vtgAb2Herring vtAbHerring vtgAaFrog VtgBFrog VtgAChicken Vtg3Chicken Vtg2Platypus VtgXChicken Vtg1Herring vtgCStickleback vtgCWrasse vtgCObserved phylogeny:Vtg1 Vtg3 Vtg2Proto VtgVtg2/3Gene conversion?(a)121Chicken Vtg1Herring vtgCStickleback vtgCWrasse vtgCChicken Vtg3Herring vtgAbStickleback vtgAbWrasse vtgAb1/vtgAb2Chicken Vtg2Herring vtgAaStickleback vtgAaWrasse vtgAaFrog VtgBFrog VtgAPlatypus VtgXExpected phylogeny:(b)12Vtg1Vtg3Vtg2lineage that highly hydrated marine pelagic eggs were madepossible, thereby triggering the teleost radiation in theoceans. This happened at least 400 million years after theevolution of the Vtg2/vtgAa gene itself [7,8].In another part of the vertebrate phylogeny, some lineagesevolved that do not seem to have any use for yolk proteinssuch as vitellogenins: mammals have evolved placentationand lactation to nourish their offspring [10]. It thereforedoes not come as a surprise that all three vitellogenin geneshave been lost from the evolutionary lineage leading to theplacental mammals and marsupials. Only the egg-layingmonotremes have retained a single functional Vtg gene(Figure 2) [10]. The evolution of vitellogenins in vertebratesnicely demonstrates an association between geneduplication and functional need. It also shows thatadaptively very important genes underlying keyevolutionary innovations can lose their relevance once anew innovation arises, with the consequence that suchgenes can vanish entirely from a genome. ‘Use it or lose it’ isthe motto, or - in the context of genome evolution -duplicate it or delete it. An intriguing question remains:were there functional necessities of reproduction that wereassociated with the duplications of the vertebrate proto Vtggene in the first place? The answer might, once more, befound in the oceans, where ancestral vertebrates used tospawn.References1. Finn RN, Kristoffersen BA: Vertebrate vitellogenin gene duplica-tion in relation to the “3R hypothesis”: correlation to the pelagicegg and the oceanic radiation of teleosts. PLoS ONE 2007, 2:e169.2. Ravi V, Venkatesh B: Rapidly evolving fish genomes and teleostdiversity. Curr Opin Genet Dev 2008, 18:544-550.3. Meyer A, Van de Peer Y: From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 2005, 27:937-945.4. Postlethwait J, Amores A, Cresko W, Singer A, Yan YL: Subfunc-tion partitioning, the teleost radiation and the annotation of thehuman genome. Trends Genet 2004, 20:481-490.25.4 Journal of Biology 2009, Volume 8, Article 25 Braasch and Salzburger http://jbiol.com/content/8/3/25Journal of Biology 2009, 8:25Figure 2Evolution of reproductive modes and vitellogenins in bony vertebrates. White circles indicate the ancestral gene duplications (1 and 2) that led to theestablishment of the vitellogenin cluster (VGC). Yellow stars indicate innovations in the reproductive mode; crosses indicate Vtg gene losses. FSGD,fish-specific genome duplication; MYA, million years ago. The timing of establishment of the vitellogenin cluster in relation to the emergence ofvertebrates and the occurrence of the 1R/2R genome duplications remain elusive and will require additional data from cartilaginous fishes, agnathansand non-vertebrate chordates. Adapted from [10] and revised and expanded using fish data from [7,8].Acanthomorpha (medaka, stickleback, pufferfish, wrasse etc.)  Otocephala (zebrafish, herring etc.)Amphibians ( including clawed frogs)Birds (including chicken)Monotremes (including platypus)Marsupials (including opossum and wallaby)Placentals (including human, mouse and dog)ActinopterygiiTeleosteiHydrated  pelagic     eggNutritivelactation   ViviparityPlacentationVGCProto VtgSarcopterygiiFSGDMYA450 0100200300400Loss of Vtg1Loss of Vtg2Loss of Vtg3Loss of second cluster      Yolkproteolysis  Vtg2/Aaneofunctionalization1 25. Volff JN: Genome evolution and biodiversity in teleost fish. Heredity2005, 94:280-294.6. Semon M, Wolfe KH: Reciprocal gene loss between Tetraodonand zebrafish after whole genome duplication in their ancestor.Trends Genet 2007, 23:108-112.7. Finn RN, Kolarevic J, Kongshaug H, Nilsen F: Evolution and differ-ential expression of a vertebrate vitellogenin gene cluster. BMCEvol Biol 2009, 9:2.8. Kristoffersen BA, Nerland A, Nilsen F, Kolarevic J, Finn RN:Genomic and proteomic analyses reveal non-neofunctionalizedvitellogenins in a basal clupeocephalan, the Atlantic herring, andpoint to the origin of maturational yolk proteolysis in marineteleosts. Mol Biol Evol 2009, doi:10.1093/molbev/msp014.9. Babin PJ: Conservation of a vitellogenin gene cluster in oviparousvertebrates and identification of its traces in the platypus genome.Gene 2008, 413:76-82.10. Brawand D, Wahli W, Kaessmann H: Loss of egg yolk genes inmammals and the origin of lactation and placentation. PLoS Biol2008, 6:e63.http://jbiol.com/content/8/3/25 Journal of Biology 2009, Volume 8, Article 25 Braasch and Salzburger 25.5Journal of Biology 2009, 8:25

In ovo omnia: diversification by duplication in fish and other vertebrates : [minireview]

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In ovo omnia: diversification by duplication in fish and other vertebrates

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