Evolution of the cephalopod head complex by assembly of multiple molluscan body parts: Evidence from Nautilus embryonic development.
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.
Shigeno
Shuichi
S
Group for Evolutionary Regeneration Biology, Center for Developmental Biology, RIKEN Kobe, Chuo-ku, Kobe 650-0047, Japan. sshigeno@uchicago.edu
Sasaki
Takenori
T
Moritaki
Takeya
T
Kasugai
Takashi
T
Vecchione
Michael
M
Agata
Kiyokazu
K
D000818:Animals; D005075:Biological Evolution; D019521:Body Patterning; D004625:Embryo, Nonmammalian / Q000196:embryology / Q000502:physiology / Q000648:ultrastructure; D047108:Embryonic Development; D006257:Head / Q000196:embryology / Q000502:physiology; D018398:Homeodomain Proteins / Q000378:metabolism*; D008855:Microscopy, Electron, Scanning; D009024:Morphogenesis; D049850:Nautilus / Q000196:embryology* / Q000502:physiology / Q000648:ultrastructure; D038081:Organogenesis
D018398:Homeodomain Proteins; C093990:engrailed protein, mollusca