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Argonauts or paper nautiluses are pelagic octopod cephalopods with a cosmopolitan distribution in tropical and subtropical waters around the world. Unlike other species of octopus, these are characterized by the fact that the female has a shell that serves as the breeding chamber for the eggs. Over time, this structure has been used as a taxonomic diagnostic character, causing problems in the systematics of this genus, with around 50 synonymies reported. Only two species, Argonauta argo and A. nouryi, have been reported in the Northern Humboldt Current System; however, there is taxonomic uncertainty regarding these species, which is reflected in the paralarvae (the first stage of life after hatching). In the paralarvae, the chromatophore patterns are considered to be conservative and reliable taxonomic characteristics. The objective of this study is to demonstrate the extensive variability in the chromatophore arrangement of Argonauta paralarvae in the Northern Humboldt Current using DNA barcoding and five species delimitation models. Our results include up to 11 different paralarvae morphotypes according to the pattern of chromatophores (number and arrangement) and 2 shell morphotypes. Species delimitation methods divided the 13 Argonauta morphotypes into two consensus molecular taxonomic units (MOTUs), A. argo and A. nouryi. Additionally, the results revealed an extensive morphological variability in the paralarvae and female shells of A. nouryi, demonstrating the importance of molecular data in studies involving species with different life stages, especially when this extensive morphological variability obscures conventional analyses.

The greater argonaut Argonauta argo is a species of the paper nautilus (Argonautidae), which is a family in Octopoda. In this paper, we report its full mitogenome sequence, which was obtained from a specimen collected in the Japan Seas near Oki Island, Shimane Prefecture, in Japan. The sequence was determined using the NGS Illumina HiSeq platform. With its 37 genes, the mitogenome shows a typical metazoan and Octopoda genomic structure, and similar to the mitogenome of the previously reported congener, A. hians. To confirm A. argo phylogenetic position in Octopoda, we conducted maximum likelihood phylogenetic analysis, using a data set including publicly available 17 Octopodiformes, five Decapodiformes, three Nautiloids and two outgroup Conchiferans. The result confirmed the affinity of Argonautidae to Tremoctopus, and the sister group position of this clade against the rest of incirrate Octopods. The mitogenome and phylogeny of A. argo reported here will be useful for future studies involving this enigmatic species, including on the reacquisition of external calcified shell structures in mollusks.

Argonauts (Cephalopoda: Argonautidae) are a group of rarely encountered open-ocean pelagic octopuses with benthic ancestry. Female argonauts inhabit a brittle ‘paper nautilus’ shell, the role of which has puzzled naturalists for millennia. The primary role attributed to the shell has been as a receptacle for egg deposition and brooding. Our observations of wild argonauts have revealed that the thin calcareous shell also functions as a hydrostatic structure, employed by the female argonaut to precisely control buoyancy at varying depths. Female argonauts use the shell to ‘gulp’ a measured volume of air at the sea surface, seal off the captured gas using flanged arms and forcefully dive to a depth where the compressed gas buoyancy counteracts body weight. This process allows the female argonaut to attain neutral buoyancy at depth and potentially adjust buoyancy to counter the increased (and significant) weight of eggs during reproductive periods. Evolution of this air-capture strategy enables this negatively buoyant octopus to survive free of the sea floor. This major shift in life mode from benthic to pelagic shows strong evolutionary parallels with the origins of all cephalopods, which attained gas-mediated buoyancy via the closed-chambered shells of the true nautiluses and their relatives.

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One of the distinguishing morphological features of conchiferan mollusks is the presence of a calcified exterior shell. Despite being conchiferans, most extant cephalopods have lost, internalized, or degraded their shells, with the exception of the basally divergent nautiloids. We compiled the shell matrix protein (SMP) data from several Nautilus pompilius studies and compared them with publicly available conchiferan SMP data, including those of Sepia pharaonis and Spirula spirula, two decapodiform cephalopods with internalized and partially internalized calcified shells, respectively. The recompilation of N. pompilius data revealed the presence of 85 distinct SMPs. Reciprocal homology searches suggested that N. pompilius shares 27 proteins known for their significant roles in shell formation and biomineralization, such as Pif/Pif-like, with other conchiferans. This is in agreement with our previous results, which suggested that the main functional domains of the SMPs in N. pompilius were also found in the conchiferans, suggesting that the domains were present in the ancestral conchiferans, with some recruited ancestrally, and some taxon-specifically. Meanwhile, 16 N. pompilius proteins are shared among the conchiferans, with only six proteins present in the cephalopods. indicating that some proteins were lost or co-opted in the course of their evolution. Three proteins shared among the conchiferans (CD109 antigen, Chitinase, and Tyrosinase) and one shared among the cephalopods (SOUL Domain-containing protein) apparently have dual functions of immunity and shell biomineralization. Intriguingly, four proteins are shared only between the two decapodiforms, indicating that they were co-opted in the decapodiform lineage with internalized shells.

Shell calcification in argonauts is unique. Only females of these cephalopods construct the paper nautilus shell, which is used as a brood chamber for developing embryos in the pelagic realm. As one of the thinnest (225 μm) known adult mollusc shells, and lacking an outer protective periostracum-like cover, this shell may be susceptible to dissolution as the ocean warms and decreases in pH. Vulnerability of the A. nodosa shell was investigated through immersion of shell fragments in multifactorial experiments of control (19 °C/pH 8.1; pCO₂ 419; ΩCa = 4.23) and near-future conditions (24 °C/pH 7.8-7.6; pCO₂ 932-1525; ΩCa = 2.72-1.55) for 14 days. More extreme pH treatments (pH 7.4-7.2; pCO₂ 2454-3882; ΩCa = 1.20-0.67) were used to assess tipping points in shell dissolution. X-ray diffractometry revealed no change in mineralogy between untreated and treated shells. Reduced shell weight due to dissolution was evident in shells incubated at pH 7.8 (projected for 2070) after 14 days at control temperature, with increased dissolution in warmer and lower pH treatments. The greatest dissolution was recorded at 24 °C (projected for local waters by 2100) compared to control temperature across all low-pH treatments. Scanning electron microscopy revealed dissolution and etching of shell mineral in experimental treatments. In the absence of compensatory mineralization, the uncovered female brood chamber will be susceptible to dissolution as ocean pH decreases. Since the shell was a crucial adaptation for the evolution of the argonauts' holopelagic existence, persistence of A. nodosa may be compromised by shell dissolution in an ocean-change world.

Cephalopods are a large and ancient group of marine animals with complex brains. Forms extant today are equipped with brains, sensors, and effectors that allow them not to just exist beside modern vertebrates as predators and prey; they compete fiercely with marine vertebrates at every scale from small crustaceans to sperm whales. We review the evolution of this group’s brains, learning ability and complex behavior. We outline evidence that although competition with vertebrates has left a deep impression on the brains and behavior of cephalopods, the original reorganization of their complex brains from their molluscan ancestors might have been forged in ancient seas millions of years before the advent of bony fishes.

In the course of research for a larger work on the history of molluscan studies in Japan, the author has translated a number of papers and notes from Japanese for the first time. Several are relevant in various ways to the molluscan collections of the Academy of Natural Sciences of Philadelphia, and a number of them concern the Academy’s best-known malacologist, Henry A. Pilsbry. The paper presented here in translation is by Tokubei Kuroda. It appeared in the Venus almost fifty years ago, and sheds some new light on one of the most productive relationships of Pilsbry’s early career.