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

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.

Looking across the gap: Understanding the evolution of eyes and vision among insects

“…We recently modeled and tested differences in vision between D. mauritiana and D. simulans resulting from the wider ommatidia of the former species. [5] As predicted, the behavioral experiments showed that D. mauritiana eyes have greater contrast sensitivity while those of D. simulans have enhanced acuity. While D. simulans is a cosmopolitan generalist, D. mauritiana is restricted to Mauritius and this finding may help to better understand their ecology and behavior, and why these differences may have been selected.…”

“…[7] Even within the eye of D. mauritiana we have observed facet size differences up to 35%. [5] Ommatidia length also differs considerably within and between species, for example, rhabdomere length can vary from 0.46 to 1.1 mm within the eye of a dragonfly. [9,10] Differences in ommatidia number, diameter, and length affect the inter-ommatidial angles and determine how much light enters each ommatidium thus directly affecting acuity and contrast sensitivity [11][12][13] (Figure 1; Box 1).…”

“…[3] Ommatidia diameter also varies considerably among species, within species and even across different regions of the eyes of individuals. [4][5][6][7] For example, male Chrysomya megacephala have wide ommatidia in the dorsal two thirds of the eye and much narrower ommatidia in the ventral third. [8] Differences in the relative number…”