The Spotted Gar Provides Connectivity Among Vertebrate Genomes and Insights into Evolution By Genome Duplication in Fish

Several whole genome duplication (WGD) events during vertebrate evolution complicate the analysis of vertebrate gene family history and gene function evolution. Following the genomic big bang of WGDs, subsequent lineage-specific genome reshuffling and loss of gene duplicates can obscure the distinction of orthologs and paralogs across lineages leading to false conclusions about the origin of vertebrate genes and their functions.

Here we show that the genome sequence of the ray-finned fish spotted gar (Lepisosteus oculatus) holds many clues to the ancestry of vertebrate gene functions and provides connectivity among vertebrate genomes. Gar diverged from teleost fish shortly before the teleost genome duplication (TGD), which had major impact on the evolution of genome structure and gene regulatory networks in teleosts. Using a chromosome-level genome assembly of spotted gar, we show that gar has retained an ancestral form of genome structure as well as many paralogs from the early two vertebrate WGDs that were differently lost in teleosts vs. lobe-finned vertebrates (coelacanth, tetrapods).

The spotted gar is also very helpful to identify cis-regulatory elements shared between teleosts and tetrapods. Such hidden orthology among regulatory elements could not be established by direct teleost-tetrapod comparisons due to elevated evolutionary rates in teleosts. Using whole genome alignments of teleosts, gar, coelacanth, and tetrapods, we identify conserved non-coding elements (CNEs) that were gained and lost at different times during vertebrate evolution. Adding information from analyzing differential retention of duplicated genes and linked CNEs among basally diverging teleosts further helps to infer regulatory targets of CNEs.