Giant genome of the vampire squid reveals the derived state of modern octopod karyotypes

Why some animal groups retain ancestral chromosomal complements while others change significantly is a fundamental question in evolutionary genomics. Few systems exist where accumulations of chromosomal changes can be studied in the context of morphological innovation. In coleoid cephalopods (octopus, squid, cuttlefish), an ancient coleoid chromosomal rearrangement event (ACCRE) has led to a substantial increase in the chromosome number and a new set of chromosomal homologies. Compared to typical molluscan or bilaterian genomes, ACCRE has enabled the origin of many novel regulatory regions in coleoid cephalopods. However, the discrepancies between extant octopodiform (octopus, [~]30 chromosomes) and decapodiform (squid and cuttlefish, [~]46 chromosomes) karyotypes and the direction of these evolutionary changes remain unexplained. Here we provide a draft genome assembly of the vampire squid Vampyroteuthis sp., the largest cephalopod genome sequenced to-date (over 10 gigabasepairs). Through syntenic comparisons, we infer that this basally branching octopodiform species shows partial retention of the chromosomal complement of Decapodiformes, indicating its more ancestral state and the derived nature of the octopod karyotype. Together with the analysis of a new chromosome-level assembly of the pelagic octopod Argonauta hians, we identified irreversible chromosomal fusion-with-mixing events followed by inter-chromosomal translocations in octopods. We show that this secondary reduction and mixing within octopod chromosomes has enabled the origin of a more entangled genomic configuration, shedding light onto the early evolutionary transitions within the clade. Our results offer broader insights into general patterns of chromosomal evolution following large-scale rearrangement events in animal genomes. Significance statementHow changes to the ancient animal synteny result in novel chromosomal homologies is difficult to dissect due to the lack of intermediate states. Here we report that the genome of Vampyroteuthis, one of the largest animal genomes sequenced to-date (over 11 gigabasepairs), despite its phylogenetic position within the octopodiform cephalopods, partially retains squid and cuttlefish chromosomal complement, reflecting an ancestral karyotypic state that existed at the time of divergence between these cephalopod lineages. Our findings reveal karyotype reductions through chromosomal fusions were followed by inter-chromosomal translocations in octopods, leading to a more specialized genomic and gene regulatory architecture. These data show how chromosomal fusions can act as drivers of further inter-chromosomal rearrangements in animal genomes.