Repeat Age Decomposition Informs an Ancient Set of Repeats Associated With Coleoid Cephalopod Divergence

Abstract

In comparison with other molluscs and bilaterians, the genomes of coleoid cephalopods (squid, cuttlefish, and octopus) sequenced so far show remarkably different genomic organization that presumably marked the early evolution of this taxon. The main driver behind this genomic rearrangement remains unclear. About half of the genome content in coleoids is known to consist of repeat elements; since selfish DNA is one of the powerful drivers of genome evolution, its pervasiveness could be intertwined with the emergence of cephalopod-specific genomic signatures and could have played an important role in the reorganization of the cephalopod genome architecture. However, due to abundant species-specific repeat expansions, it has not been possible so far to identify the ancient shared set of repeats associated with coleoid divergence. By means of an extensive repeat element re-evaluation and annotation combined with network sequence divergence approaches, we are able to identify and characterize the ancient repeat complement shared by at least four coleoid cephalopod species. Surprisingly, instead of the most abundant elements present in extant genomes, lower-copy-number DNA and retroelements were most associated with ancient coleoid radiation. Furthermore, evolutionary analysis of some of the most abundant families shared in Octopus bimaculoides and Euprymna scolopes disclosed within-family patterns of large species-specific expansions while also identifying a smaller shared expansion in the coleoid ancestor. Our study thus reveals the apomorphic nature of retroelement expansion in octopus and a conserved complement composed of several DNA element types and fewer LINE families.

Multiple and diversified transposon lineages contribute to early and recent bivalve genome evolution

“…The phylum Mollusca shows a high level of organism diversity and includes species that are important for both their ecological and economic value. Although genomic studies are accumulating and comparative analyses are becoming more common for these organisms, a deep analysis of the mobilome is still limited to single genomes or to a few comparative studies with only a handful of species [ 24 , 25 ]. As could be expected, this also resulted in a scarce representativity of molluscan TEs in the public databases which makes their automated annotation less reliable.…”

“…Despite being extensively analyzed among vertebrates and arthropod genomes, TEs are surprisingly understudied in the phylum Mollusca, a large and diverse group of metazoans with many ecologically and economically important species. To date, TE studies in molluscs are limited to the characterization of one or a few elements [ 12 – 22 ] or to the whole mobilome, i.e., the full complement of TEs in the genome, but in a few species [ 23 – 25 ]. A direct consequence of the lack of genome-scale analyses of TE content in mollusc genomes is that public repositories and databases only harbor scarce information about them, making de novo assembled genome annotations less reliable [ 26 , 27 ].…”

The dynamic genomes of Hydra and the anciently active repeat complement of animal chromosomes

“…We find that the metazoan core cluster #2 is present but not as prominently active in the zebrafish genome as in the brown hydra genomes. Similarly, nine out of 14 core eukaryotic TEs have contributed to the ancient coleoid cephalopod genome expansion and evolution 31 . However, we also find other TE clusters that are expanded in species-specific manners, that are not covered by A-TEs and may thus constitute divergent lineage-specific active TE core sets that were not captured in our hydra-centric analysis.…”

Epigenetic machinery is functionally conserved in cephalopods

“…The vast majority of the O. bimaculoides genome is intergenic and nearly half of the genome is occupied by repetitive sequences [ 26 , 29 , 71 ]. Over 85% of CpGs in the octopus genome were intergenic (Fig.…”