
ビートルの胚性第二型神経芽細胞系譜は、ハエのものよりも大きく、より成熟した中間前駆細胞を含んでおり、これが胚性期の中枢複合体早期発達に寄与している。


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Background Despite its conserved basic structure, the morphology of the insect brain and the timing of its development underwent evolutionary adaptions. However, little is known on the developmental processes that create this diversity. The central complex is a brain centre required for multimodal information processing and an excellent model to understand neural development and divergence. It is produced in large parts by type-II neuroblasts, which produce intermediate progenitors, another type of cycling precursor, to increase their neural progeny. These neural stem cells are believed to be conserved among insects, but their molecular characteristics and their role in brain development in other insect neurogenetics models, such as the beetle Tribolium castaneum have so far not been studied.

Results Using CRISPR-Cas9 we created a fluorescent enhancer trap marking expression of Tribolium fez/earmuff , a key marker for type-II neuroblast derived intermediate progenitors. Using combinatorial labelling of further markers including Tc-pointed , Tc-deadpan , Tc-asense and Tc-prospero we characterized the type-II neuroblast lineages present in the Tribolium embryo and their sub-cell-types. Intriguingly, we found 9 type-II neuroblast lineages in the Tribolium embryo while Drosophila produces only 8 per brain hemisphere. In addition, these lineages are significantly larger at the embryonic stage than they are in Drosophila and contain more intermediate progenitors, enabling the relative earlier development of the central complex. Finally, we mapped these lineages to the domains of early expressed head pattering genes. Notably, Tc-otd is absent from all type-II neuroblasts and intermediate progenitors, whereas Tc-six3 marks an anterior subset of the type-II-lineages. The placodal marker Tc-six4 specifically marks the territory where anterior medial type-II neuroblasts differentiate.

Conclusions Homologous type-II neuroblasts show a conserved molecular signature between fly and beetle. Enhanced activity of the embryonic beetle neuroblasts-type-II and intermediate progenitors is associated with an earlier central complex development when compared to the fly. Our findings on the differentiation of beetle type-II neuroblasts and on specific marker genes open the possibility to decipher the cellular and molecular mechanisms acting at the stem cell level that contribute to evolutionary divergence in developmental timing and neural morphology.

### Competing Interest Statement

The authors have declared no competing interest.

Differences in size and number of embryonic type-II neuroblast lineages are associated with divergent timing of central complex development between beetle and fly

ビートルとハエの中枢複合体発達のタイミング差は-胚性第二型神経芽細胞系譜の大きさと数の違いに関連している


ビートルとハエの中枢複合体発達のタイミング差は、胚性第二型神経芽細胞系譜の大きさと数の違いに関連している


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分節特異的な軸索誘導の分子メカニズムが、ショウジョウバエ幼虫の運動コマンドの多様化に寄与する。


Functional diversification of homologous neuronal microcircuits is a widespread feature observed across brain regions as well as across species, while its molecular and developmental mechanisms remain largely unknown. We address this question in Drosophila larvae by focusing on segmentally homologous Wave command-like neurons, which diversify their wiring and function in a segment-specific manner. Anterior Wave (a-Wave) neurons extend axons anteriorly and connect to circuits inducing backward locomotion, whereas posterior Wave (p-Wave) neurons extend axons posteriorly and trigger forward locomotion. Here, we show that Frizzled receptors DFz2 and DFz4, together with the DWnt4 ligand, regulate the segment-specific Wave axon projection. DFz2 knock-down (KD) not only reroutes Wave axons to posterior neuromeres but also biases its motor command to induce forward instead of backward locomotion as tactile response. Thus, segment-specific axon guidance diversifies the function of homologous command neurons in behavioral regulation. Since control of anterior-posterior (A-P) axon guidance by Wnt/Fz-signaling is evolutionarily conserved, our results reveal a potentially universal molecular principle for formation and diversification of the command system in the nerve cord. Furthermore, this work indicates that sensorimotor transduction can be rerouted by manipulating a single gene in a single class of neurons, potentially facilitating the evolutionary flexibility in action selection.

Impact statement Rewiring the command neurons in the tactile circuit suffices to change the behavioral strategy of a whole animal, implying a “plug-and-play” flexibility in sensorimotor circuits.

### Competing Interest Statement

The authors have declared no competing interest.

Segment-specific axon guidance by Wnt/Fz signaling diversifies motor commands in Drosophila larvae

波長-フリッツレセプター-シグナリングによる分節特異的な軸索誘導がショウジョウバエ幼虫の運動コマンドを多様化させる


波長/フリッツレセプター シグナリングによる分節特異的な軸索誘導がショウジョウバエ幼虫の運動コマンドを多様化させる



単一神経前駆細胞における Sonic Hedgehog 応答ダイナミクスと細胞運命決定の間には大きな不均一性が存在する。


During neural tube patterning, a gradient of Sonic hedgehog (Shh) signaling specifies ventral progenitor fates. The cellular response to Shh is processed through a genetic regulatory network (GRN) to specify distinct fate decisions. This process integrates Shh response level, duration and other inputs and is affected by noise in signaling and cell position. How reliably Shh response profile predicts the fate choice of a single cell is unclear. Here we use live imaging to track neural progenitors in developing zebrafish and quantify both Shh and fate reporters in single cells over time. We found that there is significant heterogeneity between Shh response and fate choice in single cells. We quantitatively modeled reporter intensities to obtain single cell response levels over time and systematically evaluated their correlation with cell fate specification. Motor neuron progenitors (pMN) exhibit a high degree of variability in their Shh responses, which is particularly prominent in the posterior neural tube where the Shh response dynamics are similar to those of the more ventrally fated lateral floor plate cells (LFPs). Our results highlight the precision limit of morphogen-interpretation GRNs in small and dynamic target cell fields.

### Competing Interest Statement

The authors have declared no competing interest.

Heterogeneity of Sonic Hedgehog response dynamics and fate specification in single neural progenitors

単一の神経前駆細胞における-sonic-hedgehog-応答ダイナミクスと運命決定の不均一性


単一の神経前駆細胞における Sonic Hedgehog 応答ダイナミクスと運命決定の不均一性


ビートルとハエの中枢複合体発達のタイミング差は、胚性第二型神経芽細胞系譜の大きさと数の違いに関連している

波長/フリッツレセプター シグナリングによる分節特異的な軸索誘導がショウジョウバエ幼虫の運動コマンドを多様化させる

単一の神経前駆細胞における Sonic Hedgehog 応答ダイナミクスと運命決定の不均一性

波長/フリッツレセプターシグナリングによる分節特異的な軸索誘導がショウジョウバエ幼虫の運動コマンドを多様化させる