Cephalic furrow paper

The peer-reviewed version of our cephalic furrow paper is out 🎉

It was published back-to-back with another cephalic furrow study:

Research mutualism

This was a wonderful collaborative effort to understand the developmental role and evolutionary origins of this prominent but overlooked tissue fold of fly embryos.

We were two teams working on a similar question, doing similar experiments, and observing similar results. But instead of competing and eventually scooping each other, we decided to join forces. The overlapping experiments became an asset as they were performed independently by different people in different labs. And since we were tackling the problem from different angles and using different approaches, the two studies neatly complemented each other and strengthened the main conclusions.

From the start, we posted the preprints and submitted the manuscripts together, and I’m delighted that the papers got to be published together back-to-back, as we had originally envisioned it.

To top this emotion, our findings and overarching story were carefully summarized in a great overview piece written by Thibaut Brunet:

Some thank yous

I have more to say about this cephalic furrow endeavor, but for now I’d like to highlight the immediate people who made it possible.

Marina Cuenca who performed crucial experiments and analyses that were a turning point for the project into tissue mechanics; Abhijeet Krishna, who did an outstanding job coding the model and running the simulations; and Alicja Szałapak who greatly contributed to the model and visualizations early in the project. Carl Modes, who supervised the theory part and could always explain so clearly the math and modeling intricacies to this biologist here. And, finally, Pavel Tomancak who provided all the support and input along the course of this project and was a guiding light for the entire endeavor. It was a pleasure to work with such talented scientists and wonderful people.

Additionally, I’d like to thank Steffen Lemke and Yu-Chiun Wang and their teams, who agreed to embark with us on this mutualistic scientific collaboration; our reviewers Thibaut Brunet, Alfonso Martinez-Arias, and an anonymous reviewer for their constructive feedback that helped shape and consolidate our work; the editor Henry Gee for handling our manuscripts during the revision process; and the Max Planck Society for paying the article processing charges to make the article open access.

There are many more people to thank. I’m writing it up on a new post, which I’ll link below when ready.

Some related posts

• The Great Divide
• Mechanobiology EMBL Symposium 2022
• The MeMoDEvo QBIO Symposium 2022
• Cephalic furrow on bioRxiv
• Cephalic furrow thread
• Improving Z-resolution of lightsheet data using CARE upsampling
• Cephalic furrow preLights
• In the spotLights
• EuroEvoDevo Helsinki 2024

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URL: https://brunovellutini.com/posts/cephalic-furrow-paper/

#cephalicFurrow #ceratitisCapitata #clogmiaAlbipunctata #diptera #drosophilaMelanogaster #evoDevo #mechanobiology #postdoc #publication

In the spotLights

spotLights is a podcast-like, interview series to highlight the people and stories behind the latest preprints. It is part of the preLights initiative organized by The Company of Biologists.

The first spotLights episode is out, and it features… me 🥸

The conversation was about the cephalic furrow preprint, which was also reviewed by preLighters earlier this year.

Participating in a podcast was something new for me!

It was a pleasure to be a part of such a fresh initiative. Big thanks to Reinier Prosée, Matthew Davies, and Ethan Ewe for the invitation and for hosting me.

You can hear the interview below. But, before that, I recommend reading the preLights post and the thread about the paper for context.

https://www.youtube.com/watch?v=rPfdCn9kScE

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URL: https://brunovellutini.com/posts/spotlights/

#cephalicFurrow #newspiece #postdoc #scienceOutreach

Cephalic furrow thread

I published a cephalic furrow thread about our paper on Twitter and Mastodon. We recently updated the manuscript on bioRxiv. In addition to the tissue mechanics, this new version includes gene expression data comparing Drosophila with Clogmia, a fly that has no cephalic furrow… It gives us some hints about the patterning changes associated with the evolution of this novel invagination.

1. Opening

Our paper on cephalic furrow mechanics got updated with an exciting evo-devo twist :)

From the labs of Pavel Tomancak and Carl Modes:

What can a fold tell us about the interplay between genetic patterning, tissue mechanics, and the evolution of morphogenesis?

https://www.biorxiv.org/content/10.1101/2023.03.30.534554v2

2. What’s the role?

The cephalic furrow is a puzzling fold.

While its formation is under strict genetic control, the invagination is transient and doesn’t give rise to specific tissues. It simply unfolds, leaving no trace.

It has no obvious function. Or does it?

3. Instability in mutants

To investigate, we analyzed the tissue dynamics in cephalic furrow mutants.

We found that without the invagination, the head-trunk epithelium becomes unstable and buckles, forming what we call ectopic folds (see bottom embryo).

What’s causing this instability?

4. Sources of stress

We identified two potential sources of mechanical stress…

Mitotic domains (groups of dividing cells in the head) and germ band extension (tissue movement towards the head).

…and analyzed their contribution using biophysical modeling and experimental perturbations.

5. Biophysical model

The model developed by Abhijeet Krishna and Alicja Szałapak from the Carl Modes lab allowed us to simulate epithelial dynamics in different conditions, and make predictions for what’s happening in vivo.

For example, would ectopic folds appear if there was no germ band extension?

6. Germ band cauterization

To test this, Marina Cuenca mechanically blocked the germ band extension by laser cauterization in cephalic furrow mutants. No ectopic folds appear.

This indicates that mitotic domains alone cannot induce buckling, only when combined with the germ band push.

7. One double mutant

Similarly, inhibiting mitotic domains in cephalic furrow mutants (double mutant btd–stg) also abolishes ectopic folds.

This indicates that germ band extension alone cannot induce buckling, only when combined with mitotic domains.

8. Head–trunk under stress

These data suggests that, without the cephalic furrow, the simultaneous formation of mitotic domains and germ band extension generates mechanical instability.

Could the cephalic furrow be counteracting these increased compressive stresses during gastrulation?

9. Early fold prevents buckling

Our simulations point in this direction, showing that an early head invagination can effectively absorb these stresses and prevent epithelial instabilities at the head-trunk boundary.

10. A mechanical role

Putting all the data together, we propose the cephalic furrow has a function, it plays a mechanical role during Drosophila gastrulation.

This raised an intriguing evolutionary question for us: Could the cephalic furrow have evolved in response to these mechanical stresses?

11. Evolutionary novelty

We were lucky that Steffen Lemke and Yu-Chiun Wang had been working on the cephalic furrow from an evolutionary perspective because they reveal a crucial insight:

The cephalic furrow is an evolutionary novelty limited to a derived group of dipteran flies.

https://www.biorxiv.org/content/10.1101/2023.10.09.561568v1

12. Instability impacts development

They also provide evidence that other flies experience increased head-trunk stresses, and that this instability may impact developmental robustness, supporting the idea that the cephalic furrow evolved in response to mechanical conflict. Their thread:

https://twitter.com/VerenaJKaul/status/1717472879850528915

13. Patterning evolution

Now, we wondered.

The cephalic furrow is a patterned fold. The initiator cells driving the invagination are specified genetically by the narrow overlap between btd and eve domains.

So, which genetic changes are associated with the evolution of this novel invagination?

14. Novel head-trunk domain of btd

We compared gene expression between Drosophila and Clogmia, a fly that has no cephalic furrow.

Clogmia lacks btd expression at the head-trunk, a domain crucial for cephalic furrow formation, suggesting the appearance of this domain was a key event in cephalic furrow evolution.

15. Evolutionary scenario

Altogether, the integrative scenario we are establishing is that mechanical instability acted as a selective pressure for the evolution of the cephalic furrow, and that this occurred through the cooption of a new molecular player at the head-trunk boundary.

16. Mechanoevolution

To us, the cephalic furrow case illustrates an example of a possibly more widespread mechanism on how mechanical forces can influence the evolution of patterned morphogenetic innovations in early development.

17. Thank yous

I’d like to thank Pavel Tomancak, Marina Cuenca, Abhijeet Krishna, Alicja Szałapak, Carl Modes for their crucial contributions, the MPI-CBG facilities for support, and the Steffen Lemke and Yu-Chiun Wang teams for this unique collective effort on such ephemeral but remarkable invagination ;)

18. Data availability

For more the details: https://www.biorxiv.org/content/10.1101/2023.03.30.534554v2

For high-res figures/videos: https://zenodo.org/record/7781916

For main data/analyses: https://zenodo.org/record/7781947

For model/simulations: https://zenodo.org/record/7784906

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URL: https://brunovellutini.com/posts/cephalic-furrow-thread/

#cephalicFurrow #clogmiaAlbipunctata #diptera #drosophilaMelanogaster #embryo #evoDevo #mechanobiology #postdoc #preprint #publication #tweet

Hi everyone, we updated our paper on cephalic furrow mechanics with an exciting evo-devo twist :)

What can this fold tell us about the interplay between genetic patterning, tissue mechanics, and the evolution of morphogenesis?

https://www.biorxiv.org/content/10.1101/2023.03.30.534554v2

#Paper #PrePrint #DevBio #EvoDevo #Mechanobiology #Evolution #CephalicFurrow

I'm excited to announce that our cephalic furrow paper is out! We investigated the function of this enigmatic invagination using live imaging and modeling and found that it plays a mechanical role during fly gastrulation https://www.biorxiv.org/content/10.1101/2023.03.30.534554

#CephalicFurrow #Drosophila #MechanoBiology #TissueMechanics #Flies #PrePrint #DevBio #Lightsheet

Hi #ScienceMastodon, time for an #introduction!

I'm an #EvoDevo biologist interested in how tissue #mechanics influences the #evolution of #morphogenesis. I study a deep and mysterious epithelial invagination that forms at the head-trunk boundary of #flies during #gastrulation, known as the #CephalicFurrow (see video below!). Currently, based in Germany as a postdoc in the Tomancak Lab at MPI-CBG. Looking forward to meeting you!

#DevBio #mechanobiology #microscopy #lightsheet #embryos