Analysis of ciliary band formation in the mollusc Ilyanassa obsoleta

Gharbiah, Maey; Nakamoto, Ayaki; Nagy, Lisa M.

doi:10.1007/s00427-013-0440-1

Cited by 16 publications

(13 citation statements)

References 26 publications

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“…Although most recent authors believe that the feeding larvae are specializations of the ontogeny of an ancestral, direct development [56-58], the organization of ciliated larvae is still useful for evolutionary and phylogenetic deductions [20,21], especially with respect to the development and organization of the nervous and muscular systems. According to modern analysis [59-61], the last common bilaterally symmetrical ancestor had a centralized nervous system, which consisted of a nerve center and nerve cords that innervated the tentacles.…”

Section: Discussionmentioning

confidence: 99%

Development and organization of the larval nervous system in Phoronopsis harmeri: new insights into phoronid phylogeny

Temereva

Tsitrin

2014

Front Zool

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BackgroundThe organization and development of the nervous system has traditionally been used as an important character for establishing the relationships among large groups of animals. According to this criterion, phoronids were initially regarded as deuterostomian but have more recently been regarded as protostomian. The resolving of this conflict requires detailed information from poorly investigated members of phoronids, such as Phoronopsis harmeri.ResultsThe serotonin-like immunoreactive part of the P. harmeri nervous system changes during larval development. These changes mostly concern the nervous system of the hood and correlate with the appearance of the median and two marginal neurite bundles, the frontal organ, and the sensory field. The apical organ has bilateral symmetry. The tentacular neurite bundle passes under the tentacles, contains several types of perikarya, and gives rise to intertentacular bundles, which branch in the tentacle base and penetrate into adjacent tentacles by two lateroabfrontal bundles. There are two groups of dorsolateral perikarya, which exhibit serotonin-like immunoreactivity, contact the tentacular neurite bundle, and are located near the youngest tentacles. Larvae have a minor nerve ring, which originates from the posterior marginal neurite bundle of the hood, passes above the tentacle base, and gives rise to the mediofrontal neurite bundle in each tentacle. Paired laterofrontal neurite bundles of tentacles form a continuous nerve tract that conducts to the postoral ciliated band.DiscussionThe organization of the nervous system differs among the planktotrophic larvae of phoronid species. These differences may correlate with differences in phoronid biology. Data concerning the innervation of tentacles in different phoronid larvae are conflicting and require careful reinvestigation. The overall organization of the nervous system in phoronid larvae has more in common with the deuterostomian than with the protostomian nervous system. Phoronid larvae demonstrate some “deuterostome-like” features, which are, in fact, have to be ancestral bilaterian characters. Our new results and previous data indicate that phoronids have retained some plesiomorphic features, which were inherited from the last common ancestor of all Bilateria. It follows that phoronids should be extracted from the Trochozoan (=Spiralia) clade and placed at the base of the Lophotrochozoan stem.

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Section: Discussionmentioning

confidence: 99%

Development and organization of the larval nervous system in Phoronopsis harmeri: new insights into phoronid phylogeny

Temereva

Tsitrin

2014

Front Zool

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“…Many authors have favored the idea that the planktotrophic larvae are ancestral in the (eu)metazoans, for example [1-4], whereas most of the recent authors believe that the feeding larvae are specializations of the ontogeny of an ancestral, direct development, for example [5-7] (see Figure 1). There are many cases of intermediates between indirect development with lecithotrophic larvae and direct development, so in the following I will discuss development with planktotrophic larvae versus development with lecithotrophic larvae or direct development (Figure 2 and Table 1).…”

Section: Reviewmentioning

confidence: 99%

Life cycle evolution: was the eumetazoan ancestor a holopelagic, planktotrophic gastraea?

Nielsen

2013

BMC Evol Biol

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BackgroundTwo theories for the origin of animal life cycles with planktotrophic larvae are now discussed seriously: The terminal addition theory proposes a holopelagic, planktotrophic gastraea as the ancestor of the eumetazoans with addition of benthic adult stages and retention of the planktotrophic stages as larvae, i.e. the ancestral life cycles were indirect. The intercalation theory now proposes a benthic, deposit-feeding gastraea as the bilaterian ancestor with a direct development, and with planktotrophic larvae evolving independently in numerous lineages through specializations of juveniles.ResultsInformation from the fossil record, from mapping of developmental types onto known phylogenies, from occurrence of apical organs, and from genetics gives no direct information about the ancestral eumetazoan life cycle; however, there are plenty of examples of evolution from an indirect development to direct development, and no unequivocal example of evolution in the opposite direction. Analyses of scenarios for the two types of evolution are highly informative. The evolution of the indirect spiralian life cycle with a trochophora larva from a planktotrophic gastraea is explained by the trochophora theory as a continuous series of ancestors, where each evolutionary step had an adaptational advantage. The loss of ciliated larvae in the ecdysozoans is associated with the loss of outer ciliated epithelia. A scenario for the intercalation theory shows the origin of the planktotrophic larvae of the spiralians through a series of specializations of the general ciliation of the juvenile. The early steps associated with the enhancement of swimming seem probable, but the following steps which should lead to the complicated downstream-collecting ciliary system are without any advantage, or even seem disadvantageous, until the whole structure is functional. None of the theories account for the origin of the ancestral deuterostome (ambulacrarian) life cycle.ConclusionsAll the available information is strongly in favor of multiple evolution of non-planktotrophic development, and only the terminal addition theory is in accordance with the Darwinian theory by explaining the evolution through continuous series of adaptational changes. This implies that the ancestor of the eumetazoans was a holopelagic, planktotrophic gastraea, and that the adult stages of cnidarians (sessile) and bilaterians (creeping) were later additions to the life cycle. It further implies that the various larval types are of considerable phylogenetic value.

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“…This suggests that shell gland specification either initially requires N signaling, or requires N signaling for its maintenance and proper morphogenesis. The cells in the shell field are clonal descendants of all of the 2nd quartet cells (Cather, 1967;Render, 1997;Gharbiah et al, 2013;Chan and Lambert, in press) and the shell is missing in 3D deletions (Clement, 1962) and reduced in deletions of 4d (Rabinowitz et al, 2008). Thus, failure to appropriately specify the shell field in the DAPT treated animals could either result from a failure to properly specify the 2nd quartet cells or a failure to maintain their specification at a later time.…”

Section: N Signaling Is Required For Shell Gland Specificationmentioning

confidence: 99%

Ilyanassa Notch signaling implicated in dynamic signaling between all three germ layers

et al. 2014

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Two cells (3D and 4d) in the mud snail Ilyanassa obsoleta function to induce proper cell fate. In this study, we provide support for the hypothesis that Notch signaling in Ilyanassa obsoleta functions in inductive signaling at multiple developmental stages. The expression patterns of Notch, Delta and Suppressor of Hairless (SuH) are consistent with a function for Notch signaling in endoderm formation, the function of 3D/4d and the sublineages of 4d. Veligers treated with DAPT show a range of defects that include a loss of endodermal structures, and varying degrees of loss of targets of 4d inductive signaling. Veligers that result from injection of Ilyanassa Delta siRNAi in general mimic the defects observed in the DAPT treated larvae. The most severe DAPT phenotypes mimic early ablations of 4d. However, the early specification of 4d itself appears normal and MAPK activation in both 3D/4d and the micromeres, which are known to activate MAPK as a result of 3D/4d induction, are normal in DAPT treated larvae. Treating larvae at successively later timepoints with DAPT suggests that Notch/Delta signaling is not only required during early 4d inductive signaling, but during subsequent stages of cell fate determination as well. Based on our results, combined with previous reports implicating the endoderm in maintaining induced fate specification in Ilyanassa, we propose a speculative model that Notch signaling is required to specify endoderm fates and 4d sublineages, as well as to maintain cell fates induced by 4d.

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Analysis of ciliary band formation in the mollusc Ilyanassa obsoleta

Cited by 16 publications

References 26 publications

Development and organization of the larval nervous system in Phoronopsis harmeri: new insights into phoronid phylogeny

Development and organization of the larval nervous system in Phoronopsis harmeri: new insights into phoronid phylogeny

Life cycle evolution: was the eumetazoan ancestor a holopelagic, planktotrophic gastraea?

Ilyanassa Notch signaling implicated in dynamic signaling between all three germ layers

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