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.
We report for the first time the development and morphological characteristics of the spleen thymus, lymph nodes and liver of the northern brown bandicoot, Isoodon macrourus. To date few marsupial species have been studied. The development and morphological characteristics of the organs shared the typical features of those few other marsupials studied as well as those of eutherians. These suggest comparative functional properties with the eutherian immune system. The thymus differentiated within the first week of pouch life and showed evidence of immunolymphopoiesis up to juvenile stages. The spleen, though seeded by lymphocytes within the first week of pouch life, was slower to mature, but differentiated and showed signs of immunocompetency by the time young left the pouch. The mature spleen displayed the same anatomical blood filtering and immunosurveillance properties as that of the eutherian spleen, with evidence of erythrocyte destruction, thrombopoietic activity, activation and differentiation of immunocompetent lymphocytes. However, the absence of sheathed capillary structures in the spleen may indicate differences in the humoral response to circulating antigens. Similarly, lymph nodes also mature by this stage with anterior nodes appearing before posterior nodes. The mature lymph nodes displayed structural features of secondary immuno-lymphoid organs consistent with production of immune responses. Finally, the liver displayed haemopoietic activity for the first four weeks of pouch life. The pattern of development in the bandicoot appears to parallel the pattern reported for other marsupials, yet the thymus matures considerably earlier than previously reported and may be of significance in the development and onset of cell-mediated immunity. Current studies to characterise cellular components, such as T/B lymphocyes and accessory cells of these organs will help to define the mechanisms of immune recognition, activation and hence outline the basis of the marsupial humoral and cellular immunity.
The Cryptasterina group of asterinid sea stars in Australasia comprises cryptic species with derived life histories. C. pentagona and C. hystera have planktonic and intragonadal larvae, respectively. C. pentagona has the gonochoric, free-spawning mode of reproduction with a planktonic lecithotrophic brachiolaria larva. C. hystera is hermaphroditic with an intragonadal lecithotrophic brachiolaria, and the juveniles emerge through the gonopore. Both species have large lipid-rich buoyant eggs and well-developed brachiolariae. Early juveniles are sustained by maternal nutrients for several weeks while the digestive tract develops. C. hystera was reared in vitro through metamorphosis. Its brachiolariae exhibited the benthic exploration and settlement behavior typical of planktonic larvae, and they attached to the substratum with their brachiolar complex. These behaviors are unlikely to be used in the intragonadal environment. The presence of a buoyant egg and functional brachiolaria larva would not be expected in an intragonadal brooder and indicate the potential for life-history reversal to a planktonic existence. Life-history traits of species in the Cryptasterina group are compared with those of other asterinids in the genus Patiriella with viviparous development. Modifications of life-history traits and pathways associated with evolution of viviparity in the Asterinidae are assessed, and the presence of convergent adaptations and clade-specific features associated with this unusual mode of parental care are examined.
The organization of the peptidergic system in the larvae of Patiriella species with divergent ontogenies was compared to determine which aspects of neurogenesis are conserved and which are altered in the evolution of development in these sea stars. P. regularis has ancestral-type feeding bipinnaria and brachiolaria larvae and the organization of the nervous system, in association with feeding structures, paralleled the bilateral larval body plan. P. calcar and P. exigua have non-feeding planktonic and benthic brachiolariae, respectively, and there was no trace of the neuronal architecture involved with feeding. The nervous system in the attachment stage brachiolaria was similar in all three species and neuronal organization reflected larval symmetry. Delayed expression of peptidergic lineages to the brachiolaria stage in the lecithotrophs indicates heterochronic change in the timing of neurogenesis or deletion of the ancestral early neurogenic program. The bipinnarial program is suggested to be a developmental module autonomous from the brachiolar one. With a divergence time of less than 10 Ma, the evolution of development in Patiriella has resulted in extensive reduction in the complexity of the larval nervous system in parallel with simplification in larval form. There is, however, strong conservation in the morphology and neuronal architecture of structures involved with settlement.
We documented expression of the pan-metazoan neurogenic gene engrailed in larval and juvenile Patiriella sea stars to determine if this gene patterns bilateral and radial echinoderm nervous systems. Engrailed homologues, containing conserved En protein domains, were cloned from the radial nerve cord. During development, engrailed was expressed in ectodermal (nervous system) and mesodermal (coeloms) derivatives. In larvae, engrailed was expressed in cells lining the larval and future adult coeloms. Engrailed was not expressed in the larval nervous system. As adult-specific developmental programs were switched on during metamorphosis, engrailed was expressed in the central nervous system and peripheral nervous system (PNS), paralleling the pattern of neuropeptide immunolocalisation. Engrailed was first seen in the developing nerve ring and appeared to be up-regulated as the nervous system developed. Expression of engrailed in the nerve plexus of the tube feet, the lobes of the hydrocoel along the adult arm axis, is similar to the reiterated pattern of expression seen in other animals. Engrailed expression in developing nervous tissue reflects its conserved role in neurogenesis, but its broad expression in the adult nervous system of Patiriella differs from the localised expression seen in other bilaterians. The role of engrailed in patterning repeated PNS structures indicates that it may be important in patterning the fivefold organisation of the ambulacrae, a defining feature of the Echinodermata.
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