Stable genome structures in living fossil fishes

Genomic evolution can propel and restrict species diversification. Rapid molecular evolution and genomic rearrangement is often associated with increased species diversification, but whether genome structural evolution shows a slow tempo in long-lived, species-poor lineages remains unclear. Here, we present two chromosome-level genomes of gars, a lineage of seven living species of freshwater fishes that are nearly identical in anatomy to extinct species from tens of millions of years ago. Using the new genomes, we show that gars have the slowest rates of genomic structural and sequence evolution of all vertebrates. In species of the two living gar genera Atractosteus and Lepisosteus, 83.35% of the genomes remain identical even though they diverged over 100 million years ago. Genome size variation among gars is almost entirely attributable to single base pair insertions and deletions. Yet, we also detect inflated GC repeat numbers on Chromosomes 14 and 23 of Atractosteus spatula that are absent in Lepisosteus and show that gar microchromosomes and macrochromosomes display different rates of structural evolution. Our analyses suggest that the genomic stability of gars, which may explain the ability of deeply divergent gar species to hybridize and has contributed to their higher structural similarity to tetrapod genomes than those of the far more closely related teleost fishes, may result from very low rates of transposable element origination and high inactivity compared to other vertebrates. Beyond providing a reference point for comparative vertebrate genomic studies, the new gar genomes illuminate a structural component of slow genomic evolution in living fossils and molecular mechanisms that may underlie exceptional genome stability.