The sex of organ geometry

Laura Blackie, Pedro Gaspar, Salem Mosleh, Oleh Lushchak, Lingjin Kong, Yuhong Jin, Agata P. Zielinska, Boxuan Cao, Alessandro Mineo, Bryon Silva, Tomotsune Ameku, Shu En Lim, Yanlan Mao, Lucía Prieto-Godino, Todd Schoborg, Marta Varela, L. Mahadevan and Irene Miguel-Aliaga ()
Additional contact information
Laura Blackie: MRC Laboratory of Medical Sciences
Pedro Gaspar: MRC Laboratory of Medical Sciences
Salem Mosleh: Harvard University
Oleh Lushchak: MRC Laboratory of Medical Sciences
Lingjin Kong: MRC Laboratory of Medical Sciences
Yuhong Jin: MRC Laboratory of Medical Sciences
Agata P. Zielinska: MRC Laboratory of Medical Sciences
Boxuan Cao: MRC Laboratory of Medical Sciences
Alessandro Mineo: MRC Laboratory of Medical Sciences
Bryon Silva: MRC Laboratory of Medical Sciences
Tomotsune Ameku: MRC Laboratory of Medical Sciences
Shu En Lim: University College London
Yanlan Mao: University College London
Lucía Prieto-Godino: The Francis Crick Institute
Todd Schoborg: University of Wyoming
Marta Varela: Imperial College London
L. Mahadevan: Harvard University
Irene Miguel-Aliaga: MRC Laboratory of Medical Sciences

Nature, 2024, vol. 630, issue 8016, 392-400

Abstract: Abstract Organs have a distinctive yet often overlooked spatial arrangement in the body1–5. We propose that there is a logic to the shape of an organ and its proximity to its neighbours. Here, by using volumetric scans of many Drosophila melanogaster flies, we develop methods to quantify three-dimensional features of organ shape, position and interindividual variability. We find that both the shapes of organs and their relative arrangement are consistent yet differ between the sexes, and identify unexpected interorgan adjacencies and left–right organ asymmetries. Focusing on the intestine, which traverses the entire body, we investigate how sex differences in three-dimensional organ geometry arise. The configuration of the adult intestine is only partially determined by physical constraints imposed by adjacent organs; its sex-specific shape is actively maintained by mechanochemical crosstalk between gut muscles and vascular-like trachea. Indeed, sex-biased expression of a muscle-derived fibroblast growth factor-like ligand renders trachea sexually dimorphic. In turn, tracheal branches hold gut loops together into a male or female shape, with physiological consequences. Interorgan geometry represents a previously unrecognized level of biological complexity which might enable or confine communication across organs and could help explain sex or species differences in organ function.

Date: 2024
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DOI: 10.1038/s41586-024-07463-4

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