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The trochoblasts in the pilidium larva break an ancient spiralian constraint to enable continuous larval growth and maximally indirect development
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The trochoblasts in the pilidium larva break an ancient spiralian constraint to enable continuous larval growth and maximally indirect development
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Journal Article
The trochoblasts in the pilidium larva break an ancient spiralian constraint to enable continuous larval growth and maximally indirect development
2017
Overview
Background
Nemertean embryos undergo equal spiral cleavage, and prior fate-mapping studies showed that some also exhibit key aspects of spiralian lineage-based fate specification, including specification of the primary trochoblasts, which differentiate early as the core of the prototroch of the spiralian trochophore larva. Yet it remains unclear how the nemertean pilidium larva, a long-lived planktotroph that grows substantially as it builds a juvenile body from isolated rudiments, develops within the constraints of spiral cleavage.
Results
We marked single cells in embryos of the pilidiophoran
Maculaura alaskensis
to show that primary, secondary, and accessory trochoblasts, cells that would make the prototroch in conventional spiralian trochophores (1q
2
, 1q
12
, and some descendants of 2q), fully account for the pilidium’s primary ciliary band, but without undergoing early cleavage arrest. Instead, the primary ciliary band consists of many small, albeit terminally differentiated, cells. The trochoblasts also give rise to niches of indefinitely proliferative cells (“axils”) that sustain continuous growth of the larval body, including new ciliated band. Several of the imaginal rudiments that form the juvenile body arise from the axils: in particular, we show that cephalic imaginal disks originate from 1a
2
and 1b
12
and that trunk imaginal disks likely originate from 2d.
Conclusions
The pilidium exhibits a familiar relation between identified blastomeres and the primary ciliated band, but the manner in which these cells form this organ differs fundamentally from the way equivalent cells construct the trochophore’s prototroch. Also, the establishment, by some progeny of the putative trochoblasts, of indeterminate stem cell populations that give rise to juvenile rudiments, as opposed to an early cleavage arrest, implies a radical alteration in their developmental program. This transition may have been essential to the evolution of a maximally indirect developing larval form—the pilidium—among nemerteans.
