Gene Recruitments and Dismissals in the Argonaut Genome Provide Insights into Pelagic Lifestyle Adaptation and Shell-like Eggcase Reacquisition

Abstract

The paper nautilus or greater argonaut, Argonauta argo, is a species of octopods which is characterized by its pelagic lifestyle and by the presence of a protective spiral-shaped shell-like eggcase in females. To reveal the genomic background of how the species adapted to the pelagic lifestyle and acquired its shell-like eggcase, we sequenced the draft genome of the species. The genome size was 1.1 Gb, which is the smallest among the cephalopods known to date, with the top 215 scaffolds (average length 5,064,479 bp) covering 81% (1.09 Gb) of the total assembly. A total of 26,433 protein-coding genes were predicted from 16,802 assembled scaffolds. From these, we identified nearly intact HOX, Parahox, Wnt clusters, and some gene clusters that could probably be related to the pelagic lifestyle, such as reflectin, tyrosinase, and opsin. The gene models also revealed several homologous genes related to calcified shell formation in Conchiferan mollusks, such as Pif-like, SOD, and TRX. Interestingly, comparative genomics analysis revealed that the homologous genes for such genes were also found in the genome of the shell-less octopus, as well as Nautilus, which has a true outer shell. Therefore, the draft genome sequence of A. argo presented here has helped us to gain further insights into the genetic background of the dynamic recruitment and dismissal of genes to form an important, converging extended phenotypic structure such as the shell and the shell-like eggcase. Additionally, it allows us to explore the evolution of from benthic to pelagic lifestyles in cephalopods and octopods.

Multi-omic insights into the formation and evolution of a novel shell microstructure in oysters

“…4 b). This acidic matrix protein and its homologs were not only identified in molluscan shells [ 14 , 30 , 70 , 71 ], but also involved in the construction of other mineralized structures of molluscs, such as sclerites and shell-like eggcase [ 72 , 73 ]. Despite VWA and CB domains are common across metazoans, we found that Pif proteins were exclusively present in lophotrochozoans and two chordates ( Branchiostoma floridae and Ciona intestinalis ) (Fig.…”

Neo-functionalization and co-option of Pif genes facilitate the evolution of a novel shell microstructure in oysters

“…The well-known combination of VWA and CB domains is Pif protein (Suzuki, et al 2009). This acidic matrix protein and its homologs were not only identified in molluscan shells (Marie, et al 2012;Suzuki, et al 2013;Zhao, et al 2018), but also involved in the construction of other mineralized structures of molluscs, such as sclerites and shell-like eggcase (Varney, et al 2021;Yoshida, et al 2022). Despite VWA and CB domains are common across metazoans, we found that Pif proteins were exclusively present in lophotrochozoans and two chordates (Branchiostoma floridae and Ciona intestinalis) (fig.…”

How Rare Are Argonautoidea Octopuses in the Mediterranean? New Data from Stranding Events, Stomach Contents and Genetics

“…In both cases, the sequences of closest relatives seem to have been obtained by Japanese specimens, but unfortunately referred to an unpublished study; therefore, it is difficult to provide accurate evaluations. Recently, the NGS Illumina HiSeq approach was applied to gain more insight into the taxonomic position and lifecycle of A. argo found in Japanese waters, through full mitochondrial genome sequencing [ 75 , 76 ]. However, to the best of our knowledge, no data on full A. argo genomes are available for Mediterranean individuals.…”