Novel Morphological Traits in the Early Developmental Stages of Temnopleurus toreumaticus

Abstract

We have re-observed in detail the development of the sea urchin species Temnopleurus toreumaticus, which is considered to be a typical indirect-developing species with a feeding larval stage. In this re-observation, we discovered two new morphological traits in the early embryonic stages of T. toreumaticus. The first trait is that, immediately after fertilization, the egg enters a stage in which wrinkles form on its surface as a result of actin polymerization. The second new trait is that the blastulae form wrinkles; in sea urchins, this has previously been known only in direct-developing species that have a nonfeeding larval stage and form wrinkles during the blastula stage, before hatching. These phenomena indicate that after fertilization, the egg of T. toreumaticus undergoes a surface transformation that is unprecedented in echinoderms, and that an indirect-developing sea urchin can form a wrinkled blastula.

Morphological diversity of blastula formation and gastrulation in temnopleurid sea urchins

“…As features and reasons to form wrinkles in direct developers, like Heliocidaris erythrogramma , it is considered that their embryos develop under the narrow perivitelline space and form wrinkles depending on the early cell lineage, their blastomeres adhesive weakly and their wrinkled blastulae release small lipid droplets into the blastocoel (Henry et al, 1991). The results of the present and previous studies (Kitazawa et al, 2009, 2010) are coincident with the mechanism of direct developers except for lipid releasing. However, it was observed that there were some ECM granules instead of lipids in the blastocoel of embryos of T. toreumaticus (Fig.…”

“…Wrinkled blastula formation has been known in only direct developing species in sea urchins (Henry et al, 1991). However, embryos of T. toreumaticus in spite that is an indirect developing species, form wrinkled blastulae (Kitazawa et al, 2009, 2010). As features and reasons to form wrinkles in direct developers, like Heliocidaris erythrogramma , it is considered that their embryos develop under the narrow perivitelline space and form wrinkles depending on the early cell lineage, their blastomeres adhesive weakly and their wrinkled blastulae release small lipid droplets into the blastocoel (Henry et al, 1991).…”

“…10). Temnopleurus toreumaticus develops some species-specific features like wrinkled egg and wrinkled blastula formation at the early developmental stages (Kitazawa et al, 2009, 2010). Phylogenetic analysis based on allozyme data of temnopleurids suggest that T. toreumaticus and T. reevesii are more closely related than T. hardwickii and M. globulus (Matsuoka and Inamori, 1996).…”

“…We found that the indirect-developing temnopleurid Temnopleurus toreumaticus forms a wrinkled blastula with a thick blastular wall, whereas other indirect-developing species T. reevesii , T. hardwickii and Mespilia globulus form smoothed blastulae with a thin blastular wall (Kitazawa et al, 2009, 2010). Embryos of T. toreumaticus invaginate continuously to form an archenteron, whereas embryos of M. globulus have stepwise invagination such as that the archenteron elongates with two elongation steps and a lag phase between these steps (Takata and Kominami, 2004).…”

Effects of Nodal inhibition on development of temnopleurid sea urchins

“…Temnopleurid sea urchins pass the cleavage stages without acceleration, after which the embryos begin to show LR asymmetry through the formation of two PPCs, of which the right PPC eventually degenerates (Kitazawa, Nishimura, Yamaguchi, Nakano, & Yamanaka, 2009;Kitazawa, Tsuchihashi, Egusa, Genda, & Yamanaka, 2010, 2014. After this stage, the larvae develop a CM leading to adult rudiment formation.…”