Size-Correlated Polymorphisms in Phyllotaxis-Like Periodic and Symmetric Tentacle Arrangements in Hydrozoan Polyps

Abstract

AbstractIntroductionPeriodic organ arrangements occur during growth and development and are widespread in animals and plants. In bilaterian animals, the organs can be interpreted as being periodically arranged along the two-dimensional space and defined by two body axes; on the other hand, in radially symmetrical animals and plants, organs are arranged in the three-dimensional space around the body axis and around plant stems, respectively. The principles of periodic organ arrangement have primarily been investigated in bilaterians; however, studies on this phenomenon in radially symmetrical animals are scarce.MethodsIn the present study, we combined live imaging, quantitative analysis, and mathematical modeling to elucidate periodic organ arrangement in a radially symmetrical animal,Coryne uchidai(Cnidaria, Hydrozoa).ResultsThe polyps ofC. uchidaisimultaneously formed multiple tentacles to establish a regularly angled, ring-like arrangement with radial symmetry. Multiple rings periodically appeared throughout the body and mostly maintained symmetry. Furthermore, we observed polymorphisms in symmetry type, including tri-, tetra-, and pentaradial symmetries, as individual variations. Notably, the types of radial symmetry were positively correlated with polyp diameter, with a larger diameter in pentaradial polyps than in tetra- and triradial ones. Our mathematical model suggested the selection of size-correlated radial symmetry based on the activation-inhibition and positional information from the mouth of tentacle initiation.DiscussionOur established quantification methods and mathematical model for tentacle arrangements are applicable to other radially symmetrical animals, and will reveal the widespread association between size-correlated symmetry and periodic arrangement principles.