Friday Cephalopod: It's not really an alien

a, Schematic of Octopus bimaculoides anatomy, highlighting the tissues sampled for transcriptome analysis: viscera (heart, kidney and hepatopancreas), yellow; gonads (ova or testes), peach; retina, orange; optic lobe (OL), maroon; supraesophageal brain (Supra), bright pink; subesophageal brain (Sub), light pink; posterior salivary gland (PSG), purple; axial nerve cord (ANC), red; suckers, grey; skin, mottled brown; stage 15 (St15) embryo, aquamarine. Skin sampled for transcriptome analysis included the eyespot, shown in light blue. b, C2H2 and protocadherin domain-containing gene families are expanded in octopus. Enriched Pfam domains were identified in lophotrochozoans (green) and molluscs (yellow), including O. bimaculoides (light blue). For a domain to be labelled as expanded in a group, at least 50% of its associated gene families need a corrected P value of 0.01 against the outgroup average. Some Pfams (for example, Cadherin and Cadherin_2) may occur in the same gene, however multiple domains in a given gene were counted only once. Bfl, Branchiostoma floridae; Cel, Caenorhabditis elegans; Cgi, Crassostrea gigas; Cte, Capitella teleta; Dme, Drosophila melanogaster; Dre, Danio rerio; Gga, Gallus gallus; Hsa, Homo sapiens; Hro, Helobdella robusta; Lch, Latimeria chalumnae; Lgi, Lottia gigantea; Mmu, Mus musculus; Obi, O. bimaculoides; Pfu, Pinctada fucata; Xtr, Xenopus tropicalis.

Well, cool. We've got preliminary analysis of the octopus genome, and it's full of tantalizing goodies, but it's very preliminary, and the Nature news and comment left me unimpressed. One of the things they seemed to think was a big deal was that Octopus has more genes than we do.

Surprisingly, the octopus genome turned out to be almost as large as a human’s and to contain a greater number of protein-coding genes — some 33,000, compared with fewer than 25,000 in Homo sapiens.

But why would that be surprising? Humans aren't the measure of all things, and we aren't necessarily going to see any correlation between number of genes and complexity in multicellular organisms like people and octopuses. What is interesting in the paper, though, is how they achieved that greater number of genes. In vertebrates, what we see is the result of multiple rounds of whole genome duplication, followed by pruning away. There is no evidence of genome duplication at all in octopus; instead, select gene families underwent expansion. The two major families were protocadherins and a specific zinc finger gene group.

That's interesting and suggestive! Protocadherins are important homophilic cell adhesion molecules mostly expressed in the developing nervous system -- diverse protocadherins seem to be important in permitting more elaborate patterns of synaptic specificity. Vertebrates also have increased numbers of protocadherins, associated with greater neural complexity, and here we have an animal with the largest nervous system size among the invertebrates, and they too have a correlated increase in protocadherin number.

The zinc finger genes are transcription factors -- they bind to DNA to regulate the expression of other genes. Octopus has 1800 different C2H2 ZNF genes! They are also a significant gene factor in humans, but we have only 500-700, and other molluscs have only a few hundred. These genes would permit greater and more complex developmental modulation.

You can see why a developmental biologist would find these differences provocative.

Another interesting difference is in the organization of the Hox genes. We have what is considered the approximately primitive condition, with the genes arranged in a tight cluster with colinear expression relative to the body plan -- they are laid out in the same order on the genome as they will be expressed along the length of the body. I am not surprised at this result, however: the octopus Hox genes are scattered and fragmented, no longer arranged in a tidy linear array. The coleoid cephalopods have undergone some genuinely radical morphological transformations during evolution, so it is perhaps only to be expected that their genome shows some similarly radical rearrangements.

Go read the whole paper! It's open access!

Coleoid cephalopods (octopus, squid and cuttlefish) are active, resourceful predators with a rich behavioural repertoire. They have the largest nervous systems among the invertebrates and present other striking morphological innovations including camera-like eyes, prehensile arms, a highly derived early embryogenesis and a remarkably sophisticated adaptive colouration system. 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 lineage. 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 previously thought to be uniquely enlarged in vertebrates: the protocadherins, which regulate neuronal development, and the C2H2 superfamily of zinc-finger transcription factors. Extensive messenger RNA 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 remodelling of genome linkage and repetitive content, played a critical role in the evolution of cephalopod morphological innovations, including their large and complex nervous systems.

Albertin AB, Simakov O, Mitros T, Wang ZY, Pungor JR, Edsinger-Gonzales E, Brenner S, Ragsdale CW, Rokhsar DS (2015) The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature 524:220–224.