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Webster, N. B.

Publications and source records attributed to Webster, N. B..

3 recordsLinked to original sources

Evidence of autonomous neural specification for both brain and ventral nerve cord tissue in Annelida

Evolution of nervous systems is a long debated topic, and similar mechanisms of conditional neural specification linked to dorsal-ventral (D-V) axis formation across some taxa have been used to support homology. We tested for autonomous versus conditional neural specification in two distantly related annelids, Capitella teleta and Platynereis dumerilii, using blastomere isolations. Our results support previous work in C. teleta and further demonstrate that the autonomous specification of anterior neural tissue and for the first time in trunk neural tissue for both annelids. In C. teleta, we found evidence for conditional pro-neural and anti-neural signals for the VNC. Animal caps lacking vegetal macromeres at the 16-cell stage form a brain and a D-V axis but not a VNC while the addition of any single macromere rescues VNC fate. This suggests that animal micromeres other than 2d produce an anti-neural signal while a pro-neural signal is produced vegetally and that VNC specification is decoupled from D-V axis formation. Taken together, our study suggests possible conservation of autonomous specification of the brain and VNC within Annelida, raising interesting questions of how mechanisms controlling neural specification evolved in Spiralia.

developmental biology↗

Capitella teleta gets left out: Possible evolutionary shift causes loss of left tissues rather than increased neural tissue from dominant-negative BMPR1

BackgroundThe evolution of centralized nervous systems (CNSs) a fascinating and complex topic; further work is needed to understand the genetic and developmental homology between organisms with a CNS. Research into a limited number of species suggests that CNSs may be homologous across Bilateria. This hypothesis is based in part on similar functions of BMP signaling in establishing fates along the dorsal-ventral (D-V) axis including limiting neural specification to one region of ectoderm. From an evolutionary-developmental perspective, the best way to understand a system is to explore it in a wide range of organisms to create a full picture. MethodsHere we expand our understanding of BMP signaling in Spiralia, the third major clade of bilaterians, by examining phenotypes after expression of a dominant-negative BMP Receptor 1 and after knock-out of the putative BMP antagonist Chordin-like using CRISPR/Cas9 gene editing in the annelid Capitella teleta (Pleistoannelida). ResultsEctopic expression of the dominant-negative Cte-BMPR1 did not increase CNS tissue or alter overall D-V axis formation in the trunk. Instead, we observed a unique asymmetric phenotype: a distinct loss of left tissues including the left eye, brain, foregut, and trunk mesoderm. Adding ectopic BMP4 early during cleavage stages reversed the dominant-negative Cte-BMPR1 phenotype, leading to a similar loss or reduction of right tissues instead. Surprisingly, a similar asymmetric loss of left tissues was evident from CRISPR knock-out of Cte-Chordin-like but concentrated in the trunk rather than the episphere. ConclusionsWe further solidify the hypothesis that the function of BMP signaling during establishment of the D-V axis and CNS is fundamentally different in at least Pleistoannelida, possibly in Spiralia, and is not required for nervous system delimitation in this group. Our results support hypotheses of either multiple evolutionary origins of CNSs across Bilateria or divergence in the molecular mechanisms of CNS specification and D-V axis formation in annelids.

developmental biology↗

Role of BMP signaling during early development of the annelid Capitella teleta

The mechanisms regulating nervous system development are still unknown for a wide variety of taxa. In insects and vertebrates, bone morphogenetic protein (BMP) signaling plays a key role in establishing the dorsal-ventral (D-V) axis and limiting the neuroectoderm to one side of that axis, leading to speculation about the conserved evolution of centralized nervous systems. Studies outside of insects and vertebrates show a more diverse picture of what, if any role, BMP signaling plays in neural development across Bilateria. This is especially true in the morphologically diverse Spiralia (~Lophotrochozoa). Despite several studies of D-V axis formation and neural induction in spiralians, there is no consensus for how these two processes are related, or whether BMP signaling may have played an ancestral role in either process. To determine the function of BMP signaling during early development of the spiralian annelid Capitella teleta, we incubated embryos and larvae in BMP4 protein for different amounts of time. Adding exogenous BMP protein to early-cleaving C. teleta embryos had a striking effect on formation of the brain, eyes, foregut, and ventral midline in a time-dependent manner. However, adding BMP did not block brain or VNC formation or majorly disrupt the D-V axis. We identified three key time windows of BMP activity. 1) BMP treatment around birth of the 3rd-quartet micromeres caused the loss of the eyes, radialization of the brain, and a reduction of the foregut, which we interpret as a loss of A- and C-quadrant identities with a possible trans-fate switch to a D-quadrant identity. 2) Treatment after birth of micromere 4d induced formation of a third ectopic brain lobe, eye, and foregut lobe, which we interpret as a trans-fate switch of B-quadrant micromeres to a C-quadrant identity. 3) Continuous BMP treatment from late cleavage (4d + 12h) through mid-larval stages resulted in a modest expansion of Ct-chrdl expression in the dorsal ectoderm and a concomitant loss of the ventral midline (neurotroch ciliary band). Loss of the ventral midline was accompanied by a collapse of the bilaterally-symmetric ventral nerve cord, although the total amount of neural tissue did not appear to be greatly affected. Our results compared to those from other annelids and molluscs suggest that BMP signaling was not ancestrally involved in delimiting neural tissue to one region of the D-V axis. However, the effects of ectopic BMP on quadrant-identity during cleavage stages may represent a non-axial organizing signal that was present in the last common ancestor of annelids and mollusks. Furthermore, in the last common ancestor of annelids, BMP signaling may have functioned in patterning ectodermal fates along the D-V axis in the trunk. Ultimately, studies on a wider range of spiralian taxa are needed to determine the role of BMP signaling during neural induction and neural patterning in the last common ancestor of this group. Ultimately, these comparisons will give us insight into the evolutionary origins of centralized nervous systems and body plans.

developmental biology↗