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A ddRAD-based genetic map and its integration with the genome assembly of Japanese eel (Anguilla japonica) provides insights into genome evolution after the teleost-specific genome duplication.

ABSTRACT: BACKGROUND: Recent advancements in next-generation sequencing technology have enabled cost-effective sequencing of whole or partial genomes, permitting the discovery and characterization of molecular polymorphisms. Double-digest restriction-site associated DNA sequencing (ddRAD-seq) is a powerful and inexpensive approach to developing numerous single nucleotide polymorphism (SNP) markers and constructing a high-density genetic map. To enrich genomic resources for Japanese eel (Anguilla japonica), we constructed a ddRAD-based genetic map using an Ion Torrent Personal Genome Machine and anchored scaffolds of the current genome assembly to 19 linkage groups of the Japanese eel. Furthermore, we compared the Japanese eel genome with genomes of model fishes to infer the history of genome evolution after the teleost-specific genome duplication. RESULTS: We generated the ddRAD-based linkage map of the Japanese eel, where the maps for female and male spanned 1748.8 cM and 1294.5 cM, respectively, and were arranged into 19 linkage groups. A total of 2,672 SNP markers and 115 Simple Sequence Repeat markers provide anchor points to 1,252 scaffolds covering 151 Mb (13%) of the current genome assembly of the Japanese eel. Comparisons among the Japanese eel, medaka, zebrafish and spotted gar genomes showed highly conserved synteny among teleosts and revealed part of the eight major chromosomal rearrangement events that occurred soon after the teleost-specific genome duplication. CONCLUSIONS: The ddRAD-seq approach combined with the Ion Torrent Personal Genome Machine sequencing allowed us to conduct efficient and flexible SNP genotyping. The integration of the genetic map and the assembled sequence provides a valuable resource for fine mapping and positional cloning of quantitative trait loci associated with economically important traits and for investigating comparative genomics of the Japanese eel.

SUBMITTER: Kai W

PROVIDER: S-EPMC3986909 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:Gene duplication is considered important to increasing the genetic diversity in animals. In fish, visual pigment genes are often independently duplicated, and the evolutionary significance of such duplications has long been of interest. Eels have two rhodopsin genes (rho), one of which (freshwater type, fw-rho) functions in freshwater and the other (deep-sea type, ds-rho) in marine environments. Hence, switching of rho expression in retinal cells is tightly linked with eels' unique life cycle, in which they migrate from rivers or lakes to the sea. These rho genes are apparently paralogous, but the timing of their duplication is unclear due to the deep-branching phylogeny. The aim of the present study is to elucidate the evolutionary origin of the two rho copies in eels using comparative genomics methods. RESULTS:In the present study, we sequenced the genome of Japanese eel Anguilla japonica and reconstructed two regions containing rho by de novo assembly. We found a single corresponding region in a non-teleostean primitive ray-finned fish (spotted gar) and two regions in a primitive teleost (Asian arowana). The order of ds-rho and the neighboring genes was highly conserved among the three species. With respect to fw-rho, which was lost in Asian arowana, the neighboring genes were also syntenic between Japanese eel and Asian arowana. In particular, the pattern of gene losses in ds-rho and fw-rho regions was the same as that in Asian arowana, and no discrepancy was found in any of the teleost genomes examined. Phylogenetic analysis supports mutual monophyly of these two teleostean synteny groups, which correspond to the ds-rho and fw-rho regions. CONCLUSIONS:Syntenic and phylogenetic analyses suggest that the duplication of rhodopsin gene in Japanese eel predated the divergence of eel (Elopomorpha) and arowana (Osteoglossomorpha). Thus, based on the principle of parsimony, it is most likely that the rhodopsin paralogs were generated through a whole genome duplication in the ancestor of teleosts, and have remained till the present in eels with distinct functional roles. Our result indicates, for the first time, that teleost-specific genome duplication may have contributed to a gene innovation involved in eel-specific migratory life cycle.

Project description:Long-term (1967-2008) glass eel catches were used to investigate climatic effects on the annual recruitment of Japanese eel to Taiwan. Specifically, three prevailing hypotheses that potentially explain the annual recruitment were evaluated. Hypothesis 1: high precipitation shifts the salinity front northward, resulting in favorable spawning locations. Hypothesis 2: a southward shift of the position of the North Equatorial Current (NEC) bifurcation provides a favorable larval transport route. Hypothesis 3: ocean conditions (eddy activities and productivity) along the larval migration route influence larval survival. Results of time series regression and wavelet analyses suggest that Hypothesis 1 is not supported, as the glass eel catches exhibited a negative relationship with precipitation. Hypothesis 2 is plausible. However, the catches are correlated with the NEC bifurcation with a one-year lag. Considering the time needed for larval transport (only four to six months), the one-year lag correlation does not support the direct transport hypothesis. Hypothesis 3 is supported indirectly by the results. Significant correlations were found between catches and climate indices that affect ocean productivity and eddy activities, such as the Quasi Biennial Oscillation (QBO), North Pacific Gyre Oscillation (NPGO), Pacific Decadal Oscillation (PDO), and Western Pacific Oscillation (WPO). Wavelet analysis reveals three periodicities of eel catches: 2.7, 5.4, and 10.3 years. The interannual coherence with QBO and the Niño 3.4 region suggests that the shorter-term climate variability is modulated zonally by equatorial dynamics. The low-frequency coherence with WPO, PDO, and NPGO demonstrates the decadal modulation of meridional teleconnection via ocean-atmosphere interactions. Furthermore, WPO and QBO are linked to solar activities. These results imply that the Japanese eel recruitment may be influenced by multi-timescale climate variability. Our findings call for investigation of extra-tropical ocean dynamics that affect survival of eels during transport, in addition to the existing efforts to study the equatorial system.

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A ddRAD-based genetic map and its integration with the genome assembly of Japanese eel (Anguilla japonica) provides insights into genome evolution after the teleost-specific genome duplication.

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