Evolution of compound eye morphology underlies differences in vision between closely related Drosophila species

Buffry, Alexandra D.; Currea, John P.; Franke-Gerth, Franziska A.; Palavalli-Nettimi, Ravindra; Bodey, Andrew J.; Rau, Christoph; Samadi, Nazanin; Gstöhl, Stefan J.; Schlepütz, Christian M.; McGregor, Alistair P.; Sumner-Rooney, Lauren; Theobald, Jamie; Kittelmann, Maike

Abstract

Background: Insects have evolved complex visual systems and display an astonishing range of adaptations for diverse ecological niches. Species of Drosophila melanogaster subgroup exhibit extensive intra- and interspecific differences in compound eye size. These differences provide an excellent opportunity to better understand variation in insect eye structure and the impact on vision. Here we further explored the difference in eye size between D. mauritiana and its sibling species D. simulans. Results: We confirmed that D. mauritiana have rapidly evolved larger eyes as a result of more and wider ommatidia than D. simulans since they recently diverged approximately 240,000 years ago. The functional impact of eye size, and specifically ommatidia size, is often only estimated based on the rigid surface morphology of the compound eye. Therefore, we used 3D synchrotron radiation tomography to measure optical parameters in 3D, predict optical capacity, and compare the modelled vision to in vivo optomotor responses. Our optical models predicted higher contrast sensitivity for D. mauritiana, which we verified by presenting sinusoidal gratings to tethered flies in a flight arena. Similarly, we confirmed the higher spatial acuity predicted for Drosophila simulans with smaller ommatidia and found evidence for higher temporal resolution. Conclusions: Our study demonstrates that even subtle differences in ommatidia size between closely related Drosophila species can impact the vision of these insects. Therefore, further comparative studies of intra- and interspecific variation in eye morphology and the consequences for vision among other Drosophila species, other dipterans and other insects are needed to better understand compound eye structure–function and how the diversification of eye size, shape, and function has helped insects to adapt to the vast range of ecological niches.

Citation

Buffry, A. D., Currea, J. P., Franke-Gerth, F. A., Palavalli-Nettimi, R., Bodey, A. J., Rau, C., …Kittelmann, M. (2024). Evolution of compound eye morphology underlies differences in vision between closely related Drosophila species. BMC Biology, 22(1), Article 67. https://doi.org/10.1186/s12915-024-01864-7

• Journal Article Type: Article
• Acceptance Date: Mar 7, 2024
• Online Publication Date: Mar 19, 2024
• Publication Date: Mar 19, 2024
• Deposit Date: Apr 16, 2024
• Publicly Available Date: Apr 16, 2024
• Journal: BMC Biology
• Publisher: BioMed Central
• Peer Reviewed: Peer Reviewed
• Volume: 22
• Issue: 1
• Article Number: 67
• DOI: https://doi.org/10.1186/s12915-024-01864-7
• Keywords: Ommatidia, Contrast, Acuity, Eye size, Optic lobe, Drosophila, Vision, Evolution, Field of view
• Public URL: https://durham-repository.worktribe.com/output/2346216