Copepods are among the most abundant organisms on the planet and play critical functions in aquatic ecosystems. Populations of the copepod Eurytemora affinis species complex are numerically dominant and highly invasive, with the extraordinary capacity to rapidly invade novel salinities. Prior studies from my laboratory revealed parallel selection acting on the same sets of ion transporter genes during independent saline to freshwater invasions by populations from genetically distinct clades. Our chromosome-level genomes of three genetically divergent clades of this species complex revealed peculiar genome architectures that might contribute to their remarkable capacity to acclimate and evolve during salinity invasions. The genomes, assembled using high-coverage PacBio and Hi-C sequencing of inbred lines (10-30 generations of full-sib mating), consisted of 521-671 Mb anchored onto variable numbers of chromosomes. Remarkably, we found striking patterns of chromosome fusions in the E. affinis complex, with the Europe clade (E. affinis proper) having 15 chromosomes, fusing independently into 7 chromosomes in the Gulf clade (E. gulfia) and 4 chromosomes in the Atlantic clade (E. carolleeae). We explored signatures of selection at the chromosomal fusion sites. Crossing between these clades resulted in varying levels of reproductive isolation, with asymmetric hybrid inviability or sterility between reciprocal crosses. Of the predicted ~20-24K protein-coding genes, we found an extraordinary expansion of ion transporter gene families in the E. affinis complex based on comparative analyses of 13 arthropod genomes. Notably, we found genome-wide signatures of extremely high historical methylation levels of the ion transporter gene bodies, suggesting transcriptional robustness of these genes. These high-quality genomes provide an invaluable resource that could help yield fundamental insights into the capacity of populations to expand their ranges into novel habitats.
Genome Architecture Evolution in the Copepod Eurytemora affinis Species Complex