Academic journal article Genetics

Genome Evolution and Meiotic Maps by Massively Parallel DNA Sequencing: Spotted Gar, an Outgroup for the Teleost Genome Duplication

Academic journal article Genetics

Genome Evolution and Meiotic Maps by Massively Parallel DNA Sequencing: Spotted Gar, an Outgroup for the Teleost Genome Duplication

Article excerpt

ABSTRACT Genomic resources for hundreds of species of evolutionary, agricultural, economic, and medical importance are unavailable due to the expense of well-assembled genome sequences and difficulties with multigenerational studies. Teleost fish provide many models for human disease but possess anciently duplicated genomes that sometimes obfuscate connectivity. Genomic information representing a fish lineage that diverged before the teleost genome duplication (TGD) would provide an outgroup for exploring the mechanisms of evolution after whole-genome duplication. We exploited massively parallel DNA sequencing to develop meiotic maps with thrift and speed by genotyping F^sub 1^ offspring of a single female and a single male spotted gar (Lepisosteus oculatus) collected directly from nature utilizing only polymorphisms existing in these two wild individuals. Using Stacks, software that automates the calling of genotypes from polymorphisms assayed by Illumina sequencing, we constructed a map containing 8406 markers. RNA-seq on two map-cross larvae provided a reference transcriptome that identified nearly 1000 mapped protein-coding markers and allowed genome-wide analysis of conserved synteny. Results showed that the gar lineage diverged from teleosts before the TGD and its genome is organized more similarly to that of humans than teleosts. Thus, spotted gar provides a critical link between medical models in teleost fish, to which gar is biologically similar, and humans, to which gar is genomically similar. Application of our F^sub 1^ dense mapping strategy to species with no prior genome information promises to facilitate comparative genomics and provide a scaffold for ordering the numerous contigs arising from next generation genome sequencing.

TELEOST fish provide numerous medical models. Some are induced mutant models, as in zebrafish and medaka (i.e., Moore et al. 2006; Schartl et al. 2010). Others are evolutionary mutant models, in which naturally occurring mutations lead to adaptive phenotypes that mimic human disease (Albertson et al. 2009), as in cichlids (craniofacial anomalies), platyfish (melanoma), mollies (premature puberty), cavefish (retinal degeneration), and icefish (osteopenia and anemia) (Eastman and Devries 1981; Streelman et al. 2003; Meierjohann and Schartl 2006; Near et al. 2006; Jeffery 2009; Valenzano et al. 2009; Albertson et al. 2010; Lampert et al. 2010; Zhang et al. 2010b). Teleost genomes differ from mammalian genomes, however, by a whole-genome duplication event, the teleost genome duplication (TGD) (Figure 1) (Amores et al. 1998; Postlethwait et al. 1998; Taylor et al. 2003; Jaillon et al. 2004). While the TGD can facilitate the dissection of ancestral gene functions due to the partitioning of ancestral subfunctions in the course of evolution (Force et al. 1999; Postlethwait et al. 2004), it can also obfuscate correlations between teleost disease models and their human counterparts because of the difficulty of ortholog assignment after lineage-specific loss of duplicated genes and the asymmetric evolution of gene duplicates. Genomic resources from a ray-fin (Actinopterygian) fish that diverged from teleosts before the TGD (Figure 1) would facilitate the connectivity of teleost and mammalian genomes. Unfortunately, candidate species for this role, including polypterus, paddlefish, sturgeons, bowfin, and gar (Blacklidge and Bidwell 1993; Inoue et al. 2003; Hardie and Hebert 2004) have virtually no genome resources and have life history traits inconvenient for the construction of large-scale genetic maps.

Teleost genomes possess substantially rearranged chromosomes with respect to mammalian chromosomes (Postlethwait et al. 1998; Nakatani et al. 2007), and although it has been suggested that chromosome rearrangements accelerated after the TGD, this idea is controversial (Comai 2005; Semon and Wolfe 2007; Hufton et al. 2008). Comparative analysis of a fish genome occupying a lineage that diverged from teleosts shortly before the TGD would test whether chromosome rearrangements detected in teleosts arose before or after the TGD. …

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