Cell Dynamics Drive Dramatic Shape Changes in Insect Development

A small leg might uncover significant insights into how closely related insect species can exhibit dramatic differences in body shape, according to a new study led by researchers at the University of Tokyo.

By using time-lapse microscopy to observe live fruit fly cells, the team discovered a novel structure that forms and disappears during the final stages of development. This structure seems to play a role in shaping a segment of the fly’s leg.

These findings could enhance the understanding of the mechanisms determining insect body shape and offer valuable insights into the processes influencing the body shapes of other organisms.

With fruit fly leg development as a model, the research team used the current study to shed light on how specific cells determine an organism's final shape.

Researchers discovered a transient structure in the fly's leg that is important in determining the final shape of the limb by imaging the live cells of the common fruit fly, Drosophila melanogaster, over several days to analyze changes in the cells during the last stages of development. They named this formation the "Parthenon-like structure" due to its resemblance to the ancient Greek ruin.

Cells change their shape more dramatically than ever thought during the final shape formation process. Especially in the case of the fruit fly’s leg, cells transiently form the fascinating structure. Because the Parthenon-like structure is seen in tissues other than the leg and seems to appear in other insects, its transient formation may be a fundamental process that forms the final shape of the insect’s body.”

Tetsuya Kojima, Study Co-Author and Associate Professor, Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo

According to the researchers, the fundamental processes by which cells choose which genes to express and contribute to the developed form of the organism are said to be conserved among closely related species. What these cells do to contribute to the shape of the form is still unknown.

Since shapes can differ dramatically between closely related species that are expected to share the basic mechanisms of cell fate determination, differences in final shape formation processes should greatly contribute to making the shape differences. Understanding the mechanisms of final shape formation is of great importance to understanding the mechanisms of formation and diversification of organisms’ shapes.”

Reiko Tajiri, Study Co-Author, Associate Professor, Chiba University

 Tajiri was a Researcher at the University of Tokyo during the study.

The researchers imaged the developing legs of fruit flies over several days using an inverted confocal microscope, which images the specimens from underneath and provides clearer visuals to comprehend the mechanisms of final shape formation.

The tarsus, or leg segment furthest from the insect's body, was the subject of their particular attention. The tarsus can appear flat and wide in male diving beetles, whereas in mosquitoes, it can appear long and slender. Additionally, the tarsus has its own segments, which vary greatly among species.

This diversity in morphology (form and structure) makes the insect tarsus a good model for studying the mechanisms of final shape formation and its diversification. In this study, we found unexpected and dramatic shape changes in epithelial cells — cells that line the surface of structures — and the basement membrane, which give rise to the structures that differentiate into the tarsal segments. We also saw interesting behavior of macrophage-like cells, which typically help clean up waste cells.”

Tetsuya Kojima, Study Co-Author and Associate Professor, Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo

The scientists noticed that the epithelial cells changed from a columnar shape to a more cube-like shape, capturing almost the entire shaping process of the adult tarsus during the fly's pupal stage.

The cells underwent additional alteration, "dramatically" forming the unexpected, ephemeral Parthenon-like structure. The diameter of the tarsus rapidly decreased as that structure formed and then vanished. The layer of epithelial cells thinned after the diameter shrank.

“Our results contribute to elucidating the mechanism for the final shape formation of the adult tarsus,” said Kojima, mentioning that to gain a better understanding of how the Parthenon-like structure contributes to the final leg shape, the team is currently conducting more in-depth research on its formation and disappearance.