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.
Highlights
Coleoid cephalopods are characterized by a highly derived body plan compared to the other molluscs, with the main novelties being a partial or complete loss of the shell, a crown of flexible arms provided with suckers (Boletzky, 2003), camera-type eyes, and a nervous system considered to be the most complex among invertebrates (Young, 1963)
About half of every sequenced coleoid cephalopod genome comprises repetitive DNA, whose composition significantly differs across lineages: Short Interspersed Nuclear Element (SINE) are the main components of Octopus bimaculoides and O. vulgaris transposomes; Long Interspersed Nuclear Element (LINE) prevail in O. minor and Euprymna scolopes, whereas mostly DNA elements are present in the Architeuthis dux genome (Albertin et al, 2015; Kim et al, 2018; Belcaid et al, 2019; Zarrella et al, 2019; Fonseca et al, 2020)
Transposable Element (TE) annotation was enhanced in terms of both sequence quantity and number of detected families; for instance, the second masking round allowed to identify SINEs in E. scolopes, which were completely unannotated after just one round
Summary
Coleoid cephalopods (squid, cuttlefish, and octopus) are characterized by a highly derived body plan compared to the other molluscs, with the main novelties being a partial or complete loss of the shell, a crown of flexible arms provided with suckers (Boletzky, 2003), camera-type eyes, and a nervous system considered to be the most complex among invertebrates (Young, 1963) Such phenotypic features are further closely related to the active predatory lifestyle and the wide variety of behaviors in extant cephalopods (Hanlon and Messenger, 2018). Our study aims to make a first step in this direction by providing a common repeat annotation of the main cephalopod lineages and extrapolating with a comparative approach the ancient TE landscape that possibly existed in the stem coleoid lineage To this end, we considered the genome assemblies of the coleoids O. vulgaris, O. bimaculoides, A. dux, E. scolopes, and N. pompilius. Using sequence similarity network approaches, we could reveal complements of closely related squid and octopus sequences among the most abundant TE families, possibly hinting at their common origin back in the coleoid lineage
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