Genome and transcriptome mechanisms driving cephalopod evolution

Abstract

Cephalopods are known for their large nervous systems, complex behaviors and morphological innovations. To investigate the genomic underpinnings of these features, we assembled the chromosomes of the Boston market squid, Doryteuthis (Loligo) pealeii, and the California two-spot octopus, Octopus bimaculoides, and compared them with those of the Hawaiian bobtail squid, Euprymna scolopes. The genomes of the soft-bodied (coleoid) cephalopods are highly rearranged relative to other extant molluscs, indicating an intense, early burst of genome restructuring. The coleoid genomes feature multi-megabase, tandem arrays of genes associated with brain development and cephalopod-specific innovations. We find that a known coleoid hallmark, extensive A-to-I mRNA editing, displays two fundamentally distinct patterns: one exclusive to the nervous system and concentrated in genic sequences, the other widespread and directed toward repetitive elements. We conclude that coleoid novelty is mediated in part by substantial genome reorganization, gene family expansion, and tissue-dependent mRNA editing.

A single-cell atlas of bobtail squid visual and nervous system highlights molecular principles of convergent evolution

“…Interestingly, parallel expansions occurred independently in other spiralian lineages, such as the annelid Capitella teleta and the gastropod mollusc Aplysia californica (Figure 1J, Figure S1). We found extensive tandem arrays of C2H2 transcription factors on chromosomes 3, 6, 41, 46 and an expansion of both C2H2 transcription factors and protocadherins, on chromosome 20, paralleling findings in other cephalopod species (Albertin et al, 2022b) (Figure 1J). Moreover, the cephalopod lens is composed of glutathione-S-transferase proteins known as σcrystallins expanded in 193 copies in two hotspots on chromosomes 40 and 41.…”

“…As a foundation for single-cell transcriptomics, we assembled a highly contiguous chromosome-scale reference genome for the Japanese bobtail squid E. berryi by combining long-read sequencing with chromatin conformation capture data (Figure 1H, Figure S1A-B, Table S1). Our assembly of the E. berryi genome totals 5.5 Gb and captures the 46 chromosomes found in decapods in a more contiguous fashion (N50 chromosome length: 113.96 Mb, N50 contig length: 827 kb) than other available cephalopod genomes (Albertin et al, 2022a, 2015b; Belcaid et al, 2019; Kim et al, 2018; Zarrella et al, 2019; Zhang et al, 2021). For instance, we recovered the massive 17 Mb Hox cluster as an intact locus on chromosome 9 (Figure S1G).…”

“…E. berryi chromosomes are generally derived from the fusion of several ancestral linkage groups (ALGs) as shown by the comparison with the bivalve mollusc Pecten maximus : for instance, the tandem array-rich chromosome 20, corresponds to a mixture of ALGs I and G (Albertin et al, 2022b; Simakov et al, 2022) (Figure 1H-J). The karyotype of cephalopods is heavily affected by such fusion events and conceals multiple tandem expansion hotspots, whose respective contribution to the emergence of their unique features appears essential (Figure 1H-J).…”

“…The karyotype of cephalopods is heavily affected by such fusion events and conceals multiple tandem expansion hotspots, whose respective contribution to the emergence of their unique features appears essential (Figure 1H-J). However, the 46 chromosomes of E. berryi shows extensive conservation with the distantly related D. pealei the longfin inshore squid (Figure S1D) (Albertin et al, 2022c).…”

“…Direct cell type homology (in the sense of cell types in modern cephalopod and vertebrate eyes descending from specific ancestral cell types in their common ancestor (Arendt et al, 2016)) is therefore unlikely, since the last common ancestor of molluscs and chordates did not have an image forming eye (Nilsson, 2009;Salvini-Plawen et al, 1977). Instead, we must consider that convergent structures could arise by some combination of (1) parallel reuse of shared ancestral genes or networks (Shubin et al, 2009), perhaps following common organizational principles (Sanes and Zipursky, 2010) and (2) the parallel acquisition of new genes and pathways, such as novel adhesion molecules or transcriptional activators (Albertin et al, 2015a(Albertin et al, , 2022b. From this perspective, the a priori convergent cephalopod and vertebrate visual systems provide an ideal opportunity to begin to compare the genes and cell types underlying convergently evolved complex systems.…”