Dataset Information

Development to metamorphosis of the nemertean pilidium larva.

ABSTRACT:

Background

The nemertean pilidium is one of the most notable planktotrophic larval types among marine invertebrates. The juvenile forms inside the larva from a series of isolated rudiments, called the imaginal discs. The development culminates in catastrophic metamorphosis, in which the larval body is consumed by the juvenile worm. Although the pilidium was first described in 1847, and is commonly found among marine plankton, there is not a single complete description of its development. The few published studies of pilidial development are based on observations of typically unidentified larvae opportunistically collected from plankton at various developmental stages.

Results

The development of Micrura alaskensis, a common Northwest Pacific coast intertidal nemertean, is described from fertilization to metamorphosis. A staging scheme is proposed based on characteristic developmental milestones. Three pairs of imaginal discs develop as invaginations of larval epidermis. The cephalic discs invaginate from the larval epidermis above the ciliated band, while the cerebral organ discs and the trunk discs invaginate below the ciliated band. All paired imaginal disc invaginations are closely associated with different portions of the larval ciliated band. In addition, two unpaired rudiments contribute to the juvenile - the proboscis rudiment and the dorsal rudiment, which do not develop as invaginations. A pair of thick-walled esophageal pouches previously thought to represent nephridial rudiments give rise to the juvenile foregut. Branched rudiments of protonephridia, and their efferent ducts are also described. Larval and juvenile serotonergic nervous systems are briefly described. Development of the juvenile is completed by 5-8 weeks at 11-15 degrees C. During the rapid metamorphosis the juvenile emerges from and devours the larva.

Conclusions

This study is the first description of pilidial development from fertilization to metamorphosis in a single species. It is illustrated with photomicrographs of live larvae, diagrams, confocal images, and videos. The findings are discussed in the context of previously published accounts of pilidial development, with which they disagree on several accounts. The results described here indicate a different number, origin and fate of various juvenile rudiments. The proposed staging scheme will be useful in subsequent studies of pilidial development.

SUBMITTER: Maslakova SA

PROVIDER: S-EPMC3014920 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe life cycle of many animals includes a larval stage, which has diversified into an astonishing variety of ecological strategies. The Nemertea is a group of spiralians that exhibits a broad diversity of larval forms, including the iconic pilidium. A pelagic planktotrophic pilidium is the ancestral form in the Pilidiophora, but several lineages exhibit deviations of this condition, mostly as a transition to pelagic lecithotrophy. The most extreme case occurs, however, in the Pilidiophoran Lineus ruber, which exhibits an adelphophagic intracapsular pilidium, the so-called Schmidt's larva.ResultsWe combined confocal laser scanning microscopy and gene expression studies to characterize the development and metamorphosis of the Schmidt's larva of L. ruber. The larva forms after gastrulation, and comprises a thin epidermis, a proboscis rudiment and two pairs of imaginal discs from which the juvenile will develop. The cells internalized during gastrulation form a blind gut and the blastopore gives rise to the mouth of the larva and juvenile. The Schmidt's larva eats other siblings that occupy the same egg capsule, accumulating nutrients for the juvenile. A gradual metamorphosis involves the differentiation of the juvenile cell types from the imaginal discs and the shedding of the larval epidermis. The expression of evolutionarily conserved anterior (foxQ2, six3/6, gsc, otx), endomesodermal (foxA, GATA456-a, twi-a) and posterior (evx, cdx) markers demonstrate that the juvenile retains the molecular patterning of the Schmidt's larva. After metamorphosis, the juveniles stay over 20 days within the egg masses, until they are fully mature and hatch.ConclusionsThe evolution of the intracapsular Schmidt's larva involved the loss of the typical feeding structures of the planktotrophic pilidium and a precocious formation of the imaginal discs, as also observed in other pelagic lecithotrophic forms. However, no special adaptations are observed related to adelphophagy. As in planktotrophic pilidium, the molecular mechanism patterning the juvenile is only active in the imaginal discs and not during the early development of the larva, suggesting two separate molecular programs during nemertean embryogenesis. Our results illuminate the diversification of larval forms in the Pilidiophora and Nemertea, and thus on the developmental mechanisms underlying metazoan larval evolution.

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