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Comparative Analysis Reveals That Polyploidy Does Not Decelerate Diversification in fish

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Comparative Analysis Reveals That Polyploidy Does Not Decelerate Diversification in fish doi: 10.1111/jeb.12308 Comparative analysis reveals that polyploidy does not decelerate diversification in fish S. H. ZHAN*,L.GLICK†,C.S.TSIGENOPOULOS‡,S.P.OTTO§ &I.MAYROSE† *University of British Columbia, Vancouver, BC, Canada †Department of Molecular Biology and Ecology of Plants, Tel Aviv University, Tel Aviv, Israel ‡Institute of Marine Biology and Genetics, Hellenic Centre for Marine Research, Crete, Greece §Department of Zoology, University of British Columbia, Vancouver, BC, Canada Keywords: Abstract Acipenseridae; While the proliferation of the species-rich teleost fish has been ascribed to binary state speciation and extinction; an ancient genome duplication event at the base of this group, the broader Botiidae; impact of polyploidy on fish evolution and diversification remains poorly chromosome number; understood. Here, we investigate the association between polyploidy and Cyprinidae; diversification in several fish lineages: the sturgeons (Acipenseridae: Salmoniformes; Acipenseriformes), the botiid loaches (Botiidae: Cypriniformes), Cyprininae teleost fish. fishes (Cyprinidae: Cypriniformes) and the salmonids (Salmonidae: Salmoni- formes). Using likelihood-based evolutionary methodologies, we co-estimate speciation and extinction rates associated with polyploid vs. diploid fish lineages. Family-level analysis of Acipenseridae and Botiidae revealed no significant difference in diversification rates between polyploid and diploid relatives, while analysis of the subfamily Cyprininae revealed higher poly- ploid diversification. Additionally, order-level analysis of the polyploid Sal- moniformes and its diploid sister clade, the Esociformes, did not support a significantly different net diversification rate between the two groups. Taken together, our results suggest that polyploidy is generally not associated with decreased diversification in fish – a pattern that stands in contrast to that previously observed in plants. While there are notable differences in the time frame examined in the two studies, our results suggest that polyploidy is associated with different diversification patterns in these two major branches of the eukaryote tree of life. mals (instances summarized in Otto & Whitton, 2000; Introduction Mable et al., 2011). Nevertheless, genomewide analyses From vertebrates to fungi, polyploidy (or whole gen- have revealed several ancient genome duplications in ome duplication) is widely recognized as a key feature animals: two episodes early in vertebrate evolution of eukaryotic genomes (Taylor et al., 2003; Jaillon et al., (Dehal & Boore, 2005) and one specific to teleost fish 2004; Kellis et al., 2004; Dehal & Boore, 2005). Poly- (Taylor et al., 2003). Evolutionarily recent cases are ploidy reaches its zenith in plants, with all seed plants reported in amphibians and reptiles, and most notably thought to have experienced one or more genome in fish where entire polyploid lineages have been duplications in their evolutionary past (Bowers et al., described (reviewed in Otto & Whitton, 2000; Mable 2003; Cui et al., 2006; Soltis et al., 2009; Van de Peer et al., 2011). Polyploids often differ markedly from their et al., 2009; Jiao et al., 2011). While polyploidy is wide- diploid progenitors in morphological, physiological spread in plants, it is more sparsely documented in ani- and life-history characteristics (Levin, 1983; Ramsey & Schemske, 2002), and these differences may contribute to the establishment and success of polyploid species in Correspondence: Itay Mayrose, Department of Molecular Biology and Ecology of Plants, George S. Wise Faculty of Life Sciences, Tel Aviv novel ecological settings. It is thus hypothesized that University, Tel Aviv 69978, Israel. Tel.: +972 3 640 7212; polyploidy may serve as an important mechanism for fax: +972 3 640 9380; e-mail: [email protected] niche differentiation and ecological diversification, ª 2014 THE AUTHORS. J. EVOL. BIOL. 27 (2014) 391–403 JOURNAL OF EVOLUTIONARY BIOLOGY ª 2014 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 391 392 S. H. ZHAN ET AL. especially in harsh environments (reviewed in Otto, diversify less rapidly, this hypothesis has not been rig- 2007; Fawcett & Van de Peer, 2010). orously investigated in animals. A long-standing debate concerning polyploidy is Among animals, fish exhibit the most appreciable whether it influences a lineage’s evolutionary success. degree of polyploid incidence (reviewed in Leggatt & Historically, researchers have focused on plants because Iwama, 2003; Le Comber & Smith, 2004; Mable et al., of the rich documentation of polyploidy in this group. 2011). Polyploid assemblages have been well docu- Polyploids were traditionally regarded as evolutionary mented in Acipenseridae (Birstein et al., 1997; Ludwig ‘dead ends’ because of the hypothesized deleterious et al., 2001), Ostariophysi [e.g. Botiidae [Slecthtov a effects associated with ploidy level increase, such as et al., 2006)], and most notably in Cyprinidae (Machor- gene dosage imbalance of the sex chromosomes (Orr, dom & Doadrio, 2001a; Tsigenopoulos et al., 2002, 1990), reduced fertility in heteroploid hybrids (Ramsey 2010; Levin et al., 2012). In addition, the families Sal- & Schemske, 2002), and inefficiency of selection when monidae (Allendorf & Thorgaard, 1984; Johnson et al., genes are masked by multiple copies (Haldane, 1933; 1987) and Catostomidae (Uyeno & Smith, 1972; Ferris, Fisher, 1935; Wright, 1969). It was further argued that 1984) are thought to have undergone genome duplica- if polyploids were more successful than their diploid tion in their ancestry. Genomic analyses established relatives, polyploidy should have replaced diploidy as that the exceptionally species-rich ray-finned fish des- the predominant genetic system in extant eukaryotes cended from a polyploid ancestor, highlighting the (Stebbins, 1971). Supporting these views, a statistical potentially profound impact of polyploidy on fish evo- analysis showed that the high prevalence of polyploidy lution (Taylor et al., 2003). A later study by Hoegg et al. in plants can be explained by frequent polyploid (2004) narrowed the phylogenetic window of formation and slow reversal to diploidy rather than the ancient polyploidization event, pinpointing it to the elevated lineage diversification following polyploidy branch leading to the radiation of the teleost fish – the (Meyers & Levin, 2006). Recent comparative analyses main constituent of the ray-finned fish clade. Hoegg of plant genomes, however, revealed signatures of and colleagues suggested that the teleost-specific ancient polyploidization events (i.e. palaeopolyploidy) ancient polyploidy was linked to the evolutionary suc- that occurred multiple times during flowering plant cess and phenotypic diversification of teleost fish. More evolution (Van de Peer et al., 2009; Jiao et al., 2011), recently, Santini et al. (2009) tested the same associa- indicating that all extant flowering plants have experi- tion using a model-based method that incorporates enced at least one round of polyploidy in their evolu- both phylogenetic and diversity information. Their tionary past. This suggests that rather than being analysis detected a significant rise in diversification rate evolutionary ‘dead ends’, polyploids can indeed persist around the timing of the ancient polyploidization and even blossom into diverse and successful clades. event. However, the authors cautioned that the ancient Greater genetic degrees of freedom, increased heterosis, polyploidization event (or any other transition along different niche tolerances and altered colonizing abili- the same branch in the tree) may explain merely ~10% ties, as well as molecular mechanisms such as func- of extant teleost diversity, as much of the remaining tional divergence of duplicated genes and buffering of diversity may be ascribed to two subsequent radiations crucial functions, are a few of the hypotheses proposed that are not associated with known genome duplication to explain the success of polyploid lineages (Werth & events. Importantly, these studies focused on a single Windham, 1991; Soltis & Soltis, 2000; Taylor et al., ancient polyploidy event, whose link to higher diversi- 2001; Comai, 2005; Chapman et al., 2006; Otto, 2007; fication may be coincidental. To improve our under- Semon & Wolfe, 2007). standing of the contribution of polyploidy to fish Although genomic evidence has rekindled the ‘poly- evolution, more events must be considered and the ploid-success’ view, large-scale phylogenetic investiga- generality of the association robustly investigated. tions have suggested otherwise, at least for relatively In the current study, we assess the link between short evolutionary time scales. Using a comprehensive polyploidy and diversification in a few fish lineages phylogenetic and cytological data set of vascular plants, where polyploid species have been extensively docu- Wood et al. (2009) reported that polyploidy accompa- mented. By applying likelihood-based phylogenetic nied 15% and 31% of speciation events in angiosperms methodologies, we estimate the diversification rates of and in ferns, respectively. However, they discovered no polyploids and their diploid kin, and explore the rela- significant association between polyploid incidence and tive contribution of speciation and extinction to the elevated diversification in plants. Using likelihood-based evolutionary fate of polyploid fish lineages. As our methodologies, Mayrose et al. (2011) further found that methods are comparable to those used by Mayrose recently formed polyploid
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