Development of the sea urchins Temnopleurus toreumaticus Leske, 1778 and Temnopleurus reevesii Gray, 1855 (Camarodonta: Temnopleuridae)

Abstract

Background: Sea urchin larvae near metamorphosis form an adult rudiment that is a complex of the juvenile structures. However, the details of the mechanisms that form the adult rudiment are unknown. The temnopleurid sea urchins Temnopleurus toreumaticus and Temnopleurus reevesii occur in Japan, but the development of their juvenile morphology has not been described. In this study, we observed their development by light and scanning electron microscopy to follow the adult rudiment formation and to consider the mechanisms of evolution of juvenile morphology in sea urchins. Results: The prism embryos of both species formed two primary pore canals that elongated from the left and right coelomic sacs; the left canal connected the presumptive water vascular system to the hydropore. These organs were formed bilaterally and symmetrically in T. toreumaticus and with left-right asymmetry in T. reevesii. The right canal of both species had degenerated by the four-armed larval stage. At the prism stage, about six cells from the left oral ectoderm located between the left post-oral arm and the oral lobe formed a cell mass. The cell mass grew in diameter stepwise in T. toreumaticus by cell migration and by the formation of an epithelial pouch during the four-to six-armed larval stages and more rapidly in T. reevesii by the formation of a thin epithelium during the six-armed larval stage. In both species, the adult rudiment was formed by attachment of the cell mass to the hydrocoel. The larvae of T. toreumaticus metamorphosed from a tiny hole on the left ectoderm between the post-oral and postero-dorsal arms.Conclusions: These findings suggest that the developmental process involving the formation of two primary pore canals and a cell mass may have been acquired and conserved as common traits in the early development of indirect-developing temnopleurid species during evolutionary divergence from the Cidaroida.

Morphological diversity of blastula formation and gastrulation in temnopleurid sea urchins

“…The final degree of invagination is about 94% (Fig. 5B) and the primary pore canals of this species do not maintain the body width (Kitazawa et al, 2014). We suggest that the continuous invagination occurs by elongation of the archenteron itself.…”

“…These results indicate that the feature at the tip of the archenteron may cause species-specific invagination or the formational process of the coelomic pouches. This conclusion is supported by findings that the pattern of formation of the primary pore canal from the coelomic pouches is different among these species (Kitazawa et al ., 2012, 2014). …”

“…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). However, gastrulation of T. reevesii and T. hardwickii is not fully understood, and in T. reevesii development until metamorphosis was described only recently (Kitazawa et al, 2014). Therefore, details of morphogenesis are still unknown.…”

Effects of Nodal inhibition on development of temnopleurid sea urchins

“…Recently, however, we reported that adult rudiment formation in larvae of Mespilia globulus, Temnopleurus toreumaticus, and T. reevesii depends on a cell mass (CM) instead of the amniotic cavity (Kitazawa et al, 2012(Kitazawa et al, , 2014, as likewise identified in T. hardwickii (Fukushi, 1959) and Genocidaris maculata (Ubisch, 1959). Recently, however, we reported that adult rudiment formation in larvae of Mespilia globulus, Temnopleurus toreumaticus, and T. reevesii depends on a cell mass (CM) instead of the amniotic cavity (Kitazawa et al, 2012(Kitazawa et al, , 2014, as likewise identified in T. hardwickii (Fukushi, 1959) and Genocidaris maculata (Ubisch, 1959).…”

“…Morphologically, a primary pore canal (PPC) forms and elongates from the left coelomic pouch to the dorsal ectoderm, and then becomes a duct-like structure connecting the juvenile water vascular system to a madrepore (Kitazawa, Kobayashi, Kasahara, Takuwa, & Yamanaka, 2012;MacBride, 1914;Okazaki, 1975); some species form two PPCs initially, but thereafter the right PPC degenerates (Hara, Kuraishi, Uemura, & Katow, 2003;Kitazawa et al, 2012Kitazawa et al, , 2014. Morphologically, a primary pore canal (PPC) forms and elongates from the left coelomic pouch to the dorsal ectoderm, and then becomes a duct-like structure connecting the juvenile water vascular system to a madrepore (Kitazawa, Kobayashi, Kasahara, Takuwa, & Yamanaka, 2012;MacBride, 1914;Okazaki, 1975); some species form two PPCs initially, but thereafter the right PPC degenerates (Hara, Kuraishi, Uemura, & Katow, 2003;Kitazawa et al, 2012Kitazawa et al, , 2014.…”