Date Published: June 12, 2019
Publisher: Public Library of Science
Author(s): Christoffer Rozenfeld, Jose Blanca, Victor Gallego, Víctor García-Carpintero, Juan Germán Herranz-Jusdado, Luz Pérez, Juan F. Asturiano, Joaquín Cañizares, David S. Peñaranda, Hubert Vaudry.
Paralogues pairs are more frequently observed in eels (Anguilla sp.) than in other teleosts. The paralogues often show low phylogenetic distances; however, they have been assigned to the third round of whole genome duplication (WGD), shared by all teleosts (3R), due to their conserved synteny. The apparent contradiction of low phylogenetic difference and 3R conserved synteny led us to study the duplicated gene complement of the freshwater eels. With this aim, we assembled de novo transcriptomes of two highly relevant freshwater eel species: The European (Anguilla anguilla) and the Japanese eel (Anguilla japonica). The duplicated gene complement was analysed in these transcriptomes, and in the genomes and transcriptomes of other Actinopterygii species. The study included an assessment of neutral genetic divergence (4dTv), synteny, and the phylogenetic origins and relationships of the duplicated gene complements. The analyses indicated a high accumulation of duplications (1217 paralogue pairs) among freshwater eel genes, which may have originated in a WGD event after the Elopomorpha lineage diverged from the remaining teleosts, and thus not at the 3R. However, very similar results were observed in the basal Osteoglossomorpha and Clupeocephala branches, indicating that the specific genomic regions of these paralogues may still have been under tetrasomic inheritance at the split of the teleost lineages. Therefore, two potential hypotheses may explain the results: i) The freshwater eel lineage experienced an additional WGD to 3R, and ii) Some duplicated genomic regions experienced lineage specific rediploidization after 3R in the ancestor to freshwater eels. The supporting/opposing evidence for both hypotheses is discussed.
Large accumulations of gene duplications can originate from one single event, like a whole genome duplication (WGD)  or from multiple small duplication events such as small segmental duplications (SDs) , which are often found in tandem. Any of these duplication events may contribute to species evolution by providing raw genetic material for new phenotypic variation [1–3].
The present study found more than one thousand gene families in which the gene family tree topology indicates a duplication in a common ancestor of freshwater eels sometime after the split of Elopomorpha and Osteoglossomorpha. Only phylogenetic species tree branches with previously documented WGDs (Fig 4, Nodes 1, 3, 4, and 16) and the zebrafish specific branch (Fig 4, Node 7) were assigned more duplications than the basal freshwater eel branch (Fig 4, Node 9). The vast majority of the assigned zebrafish specific duplications formed a 4dTv local density maximum at ~0 and were found “close” in the genome, thus these duplications appear to be tandem SDs, the presence of which concurs with previous studies [8,11,65].
The data presented in this study support the hypothesis that a remarkably high amount of paralogues pairs started to diverge in a common ancestor of the freshwater eel lineage after the split from the Osteoglossomorpha lineage. The 4dTv and phylogenetic analyses revealed a clear clustering of these paralogues in the basal freshwater eel branch with a 4dTv mode at ~0.4. The synteny of these paralogue pairs suggests they originated in large portions, most likely from a WGD event. However, the results do not unequivocally support/oppose whether i) These paralogues originated from the 3R but are located in genomic regions which have experienced protracted rediploidization; ii) These paralogues originated in a 4R WGD in a common ancestor to freshwater eels; or iii) Both i and ii have contributed to the evolution of these paralogues. The present results offer robust information on the duplicated gene complement of freshwater eels, thus providing novel insights into the peculiar biology of the critically endangered European eel. However, additional high quality genome resources of other Elopomorpha members are needed to further study the dynamics of gene duplication and conservation in early teleost evolution.