Cephalopod head parts are among the most complex occurring in all invertebrates. Hypotheses for the evolutionary process require a drastic body-plan transition in relation to the life-style changes from benthos to active nekton. Determining these transitions, however, has been elusive because of scarcity of fossil records of soft tissues and lack of some of the early developmental stages of the basal species. Here we report the first embryological evidence in the nautiloid cephalopod Nautilus pompilius for the morphological development of the head complex by a unique assembly of multiple archetypical molluscan body parts. Using a specialized aquarium system, we successfully obtained a series of developmental stages that enabled us to test previous controversial scenarios. Our results demonstrate that the embryonic organs exhibit body plans that are primarily bilateral and antero-posteriorly elongated at stereotyped positions. The distinct cephalic compartment, foot, brain cords, mantle, and shell resemble the body plans of monoplacophorans and basal gastropods. The numerous digital tentacles of Nautilus develop from simple serial and spatially-patterned bud-like anlagen along the anterior-posterior axis, indicating that origins of digital tentacles or arms of all other cephalopods develop not from the head but from the foot. In middle and late embryos, the primary body plans largely change to those of juveniles or adults, and finally form a "head" complex assembled by anlagen of the foot, cephalic hood, collar, hyponome (funnel), and the foot-derived epidermal covers. We suggest that extensions of the collar-funnel compartment and free epidermal folds derived from multiple topological foot regions may play an important role in forming the head complex, which is thought to be an important feature during the body plan transition.
Coleoid cephalopods show remarkable evolutionary convergence with vertebrates in their neural organization, including (1) eyes and visual system with optic lobes, (2) specialized parts of the brain controlling learning and memory, such as vertical lobes, and (3) unique vasculature supporting such complexity of the central nervous system. We performed deep sequencing of eye transcriptomes of pygmy squids (Idiosepius paradoxus) and chambered nautiluses (Nautilus pompilius) to decipher the molecular basis of convergent evolution in cephalopods. RNA-seq was complemented by in situ hybridization to localize the expression of selected genes. We found three types of genomic innovations in the evolution of complex brains: (1) recruitment of novel genes into morphogenetic pathways, (2) recombination of various coding and regulatory regions of different genes, often called "evolutionary tinkering" or "co-option", and (3) duplication and divergence of genes. Massive recruitment of novel genes occurred in the evolution of the "camera" eye from nautilus' "pinhole" eye. We also showed that the type-2 co-option of transcription factors played important roles in the evolution of the lens and visual neurons. In summary, the cephalopod convergent morphological evolution of the camera eyes was driven by a mosaic of all types of gene recruitments. In addition, our analysis revealed unexpected variations of squids' opsins, retinochromes, and arrestins, providing more detailed information, valuable for further research on intra-ocular and extra-ocular photoreception of the cephalopods.
Coleoid cephalopods have an elaborate camera eye whereas nautiloids have primitive pinhole eye without lens and cornea. The Nautilus pinhole eye provides a unique example to explore the module of lens formation and its evolutionary mechanism. Here, we conducted an RNA-seq study of developing eyes of Nautilus and pygmy squid. First, we found that evolutionary distances from the common ancestor to Nautilus or squid are almost the same. Although most upstream eye development controlling genes were expressed in both species, six3/6 that are required for lens formation in vertebrates was not expressed in Nautilus. Furthermore, many downstream target genes of six3/6 including crystallin genes and other lens protein related genes were not expressed in Nautilus. As six3/6 and its controlling pathways are widely conserved among molluscs other than Nautilus, the present data suggest that deregulation of the six3/6 pathway led to the pinhole eye evolution in Nautilus.
Extreme sexual size dimorphism is one of the most striking phenomena in evolutionary biology. While the origin has been well discussed and some causes have been suggested, the evolutionary history remains unclear. We found a new species of deep‐sea scale worm (Annelida: Polynoidae) inside gastropod shells, either empty or occupied by hermit crabs collected at 140–306 m in depth, Mie Prefecture, Japan. This highly specialized habitat, together with the fact that it has never been found free‐living, led us to consider the scale worm to be an obligate symbiont. The species is characterized by males being dwarf, with their minute bodies (ca. one‐fourth the length of females) always riding on the dorsal side of females, being thus the first case of extreme sexual size dimorphism in scale worms. Based on a detailed morphological, histological, and molecular phylogenetic approach we are here describing a new species, Eunoe issunboushi sp. nov.
̶ A new species of Bathyceradocus, one of the maerid amphipods, is described based on the specimens collected from sunken wood on the bottom of the Kumano-nada, central Japan. Bathyceradocus japonicus sp. nov. can be distinguished from its congeners by the number of the accessory spines on the pleonite 1, the number of articles on the accessory flagellum, and the strongly oblique palm of the gnathopod 2 with the dentate margin. A brief note on the behavior of the new species and a key to species of the genus are provided.
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