Evolutionary change in developmental mode in sea urchins is closely tied to an increase in maternal provisioning. We examined the oogenic modifications involved in production of a large egg by comparison of oogenesis in congeneric sea urchins with markedly different sized oocytes and divergent modes of development. Heliocidaris tuberculata has small eggs (95 microm diameter) and the ancestral mode of development through feeding larvae, whereas H. erythrogramma has large eggs (430 microm diameter) and highly modified non-feeding lecithotrophic larvae. Production of a large egg in H. erythrogramma involved both conserved and divergent mechanisms. The pattern and level of vitellogenin gene expression is similar in the two species. Vitellogenin processing is also similar with the gonads of both species incorporating yolk protein from coelomic and hemal stores into nutritive cells with subsequent transfer of this protein into yolk granules in the developing vitellogenic oocyte. Immunocytology of the eggs of both Heliocidaris species indicates they incorporate similar levels of yolk protein. However, H. erythrogramma has evolved a highly divergent second phase of oogenesis characterised by massive deposition of non-vitellogenic material including additional maternal protein and lipid. Maternal provisioning in H. erythrogramma exhibits recapitulation of the ancestral vitellogenic program followed by a novel oogenic phase with hypertrophy of the lipogenic program being a major contributor to the increase in egg size.
BackgroundThe molecular mechanisms underlying the development of the unusual echinoderm pentameral body plan and their likeness to mechanisms underlying the development of the bilateral plans of other deuterostomes are of interest in tracing body plan evolution. In this first study of the spatial expression of genes associated with Nodal and BMP2/4 signalling during the transition to pentamery in sea urchins, we investigate Heliocidaris erythrogramma, a species that provides access to the developing adult rudiment within days of fertilization.Results
BMP2/4, and the putative downstream genes, Six1/2, Eya, Tbx2/3 and Msx were expressed in the earliest morphological manifestation of pentamery during development, the five hydrocoele lobes. The formation of the vestibular ectoderm, the specialized region overlying the left coelom that forms adult ectoderm, involved the expression of putative Nodal target genes Chordin, Gsc and BMP2/4 and putative BMP2/4 target genes Dlx, Msx and Tbx. The expression of Nodal, Lefty and Pitx2 in the right ectoderm, and Pitx2 in the right coelom, was as previously observed in other sea urchins.ConclusionThat genes associated with Nodal and BMP2/4 signalling are expressed in the hydrocoele lobes, indicates that they have a role in the developmental transition to pentamery, contributing to our understanding of how the most unusual body plan in the Bilateria may have evolved. We suggest that the Nodal and BMP2/4 signalling cascades might have been duplicated or split during the evolution to pentamery.Electronic supplementary materialThe online version of this article (doi:10.1186/s12861-017-0145-1) contains supplementary material, which is available to authorized users.
Development of the larval peptidergic system in the sea star Patiriella regularis and structure of the adult nervous system in Patiriella species were documented in an immunofluorescence investigation using antisera to the sea star neuropeptide GFNSALMFamide 1 (S1) and confocal microscopy. P. regularis has planktotrophic development through bipinnaria and brachiolaria larvae. In early bipinnaria, two groups of immunoreactive cells appeared on either side of the anterior region and proliferated to form a pair of dorsolateral ganglia. The ganglia gave rise to fine varicose fibres that innervated the preoral and adoral ciliated bands. Peptidergic cells also innervated the postoral ciliated band, and a nerve tract connected the pre- and postoral bands. Fully developed bipinnaria had a well-developed peptidergic system, the organisation of which reflected the bilateral larval body plan. As the brachiolar attachment complex differentiated at the anterior end, the ganglia became positioned on either side of the anterior projection, from which they innervated the complex. It is suggested, based on the distribution of S1-like immunoreactivity in association with ciliary and attachment structures, that the peptidergic system functions in modulation of feeding, swimming, and settlement. The larval peptidergic system degenerates as the larval body is resorbed during metamorphosis. In adults, S1-like immunoreactivity was intense in the axonal region of the ectoneural nervous system and in hyponeural perikarya. Immunoreactive cells in the neuroepithelium connected with the surface and may be sensory. Examination of immunoreactivity in several Patiriella species attests to the highly conserved organisation of the peptidergic system in adult asteroids.
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