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Our analyses reveal that the nautilus genome is the smallest when compared to published genomes of coleoid cephalopods it contains the least number of encoding genes and hitherto the lowest evolutionary rate in the group. pompilius would not only shed light on the origin and evolution of cephalopod genomic novelties but also incentivize research on their biology and inform sustainable conservation. However, its population has recently declined dramatically due to a mix of unfavourable circumstances, including commercial exploitation of ornamental shells, a lack of legal protection and very slow sexual maturation 16. pompilius is the most widespread species among nautiluses and has distributions in the Indo-Pacific region 15. In this study, we sequenced the complete genome of Nautilus pompilius in the hope of providing a critical reference for the evolution of cephalopods. However, genomic sequence availability is still limited in coleoid species 9– 12 and a non-coleoid cephalopod genome is urgently needed. Moreover, transcriptomic analyses have pointed out that RNA editing could allow high plasticity of transcripts, which is associated with thermal adaptation and neural functions 13, 14. Recently, genomic sequencing efforts in coleoids revealed that specific gene family expansions and genome rearrangements may drive the evolution of morphological novelties in these organisms 9– 12.
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Thus, investigating the nautilus genome could furnish valuable insights into the evolutionary drivers of cephalopod innovations. As a sister group to nautilus, coleoid cephalopods (such as the octopus, squid and cuttlefish) are perhaps the most intelligent and extraordinarily complex invertebrates with striking morphological and behavioural innovations including sophisticated camera eye, external shell internalization, unusual learning and problem-solving abilities 6– 8. Additionally, nautilus is adept in spatial learning and temporally separated biphasic memory even though its brain is disproportionately simple among extant cephalopods 4, 5. Nautilus possesses a unique and simple pinhole eye without lens or cornea, which provides an excellent prototypical model for illuminating the evolution of the eye. Moreover, the elegant architecture of the nautilus chambered shell takes the form of a logarithmic spiral conforming to the golden ratio and is composed of sturdy arrays of aragonite crystals, leading to its high degree of hydrostatic stability 3. A phenotypic peculiarity of the adult nautilus shell is that it consists of over 30 chambers: the soft body is accommodated and protected in the outermost chamber, whereas the remaining chambers act as a constant volume hydrostatic apparatus to maintain buoyancy. Palaeobiological evidence shows that the nautilus lineage has preserved plesiomorphic phenotypes such as a chambered shell and primary lens-less eye (pinhole eye) 2. Nautilus is the only surviving externally shelled cephalopod among hundreds of extinct cephalopod genera since the Palaeozoic it is deemed unique for its persistent ancestral features despite a long evolutionary history 1. The nautilus genome constitutes a valuable resource for reconstructing the evolutionary scenarios and genomic innovations that shape the extant cephalopods. The conserved molluscan biomineralization toolkit and lineage-specific repetitive low-complexity domains are essential to the construction of the nautilus shell. Importantly, multiple genomic innovations including gene losses, independent contraction and expansion of specific gene families and their associated regulatory networks likely moulded the evolution of the nautilus pinhole eye. Nautilus shows a compact, minimalist genome with few encoding genes and slow evolutionary rates in both non-coding and coding regions among known cephalopods. Here, we present a complete Nautilus pompilius genome as a fundamental genomic reference on cephalopod innovations, such as the pinhole eye and biomineralization. It is unique within cephalopod genealogy and critical to understanding the evolutionary novelties of cephalopods. Nautilus is the sole surviving externally shelled cephalopod from the Palaeozoic.