The octopus genome and the evolution of cephalopod neural and morphological novelties

Abstract

Coleoid cephalopods (octopus, squid, and cuttlefish) are active, resourceful predators with a rich behavioral repertoire1. They have the largest nervous systems among the invertebrates2 and present other striking morphological innovations including camera-like eyes, prehensile arms, a highly derived early embryogenesis, and the most sophisticated adaptive coloration system among all animals1,3. To investigate the molecular bases of cephalopod brain and body innovations we sequenced the genome and multiple transcriptomes of the California two-spot octopus, Octopus bimaculoides. We found no evidence for hypothesized whole genome duplications in the octopus lineage4–6. The core developmental and neuronal gene repertoire of the octopus is broadly similar to that found across invertebrate bilaterians, except for massive expansions in two gene families formerly thought to be uniquely enlarged in vertebrates: the protocadherins, which regulate neuronal development, and the C2H2 superfamily of zinc finger transcription factors. Extensive mRNA editing generates transcript and protein diversity in genes involved in neural excitability, as previously described7, as well as in genes participating in a broad range of other cellular functions. We identified hundreds of cephalopod-specific genes, many of which showed elevated expression levels in such specialized structures as the skin, the suckers, and the nervous system. Finally, we found evidence for large-scale genomic rearrangements that are closely associated with transposable element expansions. Our analysis suggests that substantial expansion of a handful of gene families, along with extensive remodeling of genome linkage and repetitive content, played a critical role in the evolution of cephalopod morphological innovations, including their large and complex nervous systems.

Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties

“…other hand, the cephalopod mollusk Octopus bimaculoides has lost several Hox genes and lacks a Hox cluster (22), and the clitellate annelids Helobdella robusta and Eisenia fetida do not have a Hox cluster but have greatly expanded certain Hox classes (16,17).…”

“…Hox genes are prone to gains (15-17) and losses (18)(19)(20)(21), and their arrangement in a cluster can be interrupted, or even completely disintegrated (22)(23)(24)(25). Furthermore, the collinear character of the Hox gene expression can fade temporally (24,26,27) and/or spatially (28).…”

Phylogenomic Synteny Network Analysis of MADS-Box Transcription Factor Genes Reveals Lineage-Specific Transpositions, Ancient Tandem Duplications, and Deep Positional Conservation

“…For example, the origin of morphological novelty has been linked to the duplication of key regulatory transcription factors in the case of the Hox genes in animals, but also the MADS-box genes in plants ( Alvarez-Buylla et al, 2000b;Airoldi and Davies, 2012;Soshnikova et al, 2013). However, gene clusters are frequently dispersed or "broken up" in certain lineages, like the Hox cluster in the genomes of octopus (Lemons and McGinnis, 2006;Duboule, 2007;Albertin et al, 2015) and brachiopods (Schiemann et al, 2017), and this dispersion contributes to divergent gene expression and morphological novelties.…”

Genome‐wide comparisons reveal a clinal species pattern within a holobenthic octopod—the Australian Southern blue‐ringed octopus, Hapalochlaena maculosa (Cephalopoda: Octopodidae)

“…This is most likely due to the general paucity of genomic sequencing studies in octopods and the lack of annotation within octopod genomes (c.f. Albertin et al., 2015; Ogura, Ikeo, & Gojobori, 2004). The increasing availability of genetic markers and techniques may enable future studies to easily link loci under directional selection to biologically meaningful regions of cephalopod genomes.…”

“…A third NJ tree was also constructed, using the same methodology as above, but using all neutral loci for comparison. Finally, the sequences of all identified directional outlier loci were compared against the NCBI nucleotide database and the Octopus bimaculoides genome assembly (Albertin et al., 2015) for biologically relevant matches using Blast2Go™ software.…”