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

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.

Insect Neurobiology: How a Small Spot Stops a Fly.

Animals often respond to small moving features very differently than they do to large moving fields. A new study finds that viewing small spots causes walking fruit flies to stop in their tracks, and identifies the cellular pathway that processes this signal.

Small eyes in dim light: Implications to spatio-temporal visual abilities in Drosophila melanogaster.

Fruit flies, Drosophila melanogaster, are active over a range of light intensities in the wild, but lab-reared flies are often tested only in bright light. Similarly, scarce feeding during larval stages-common in nature-generates smaller adults, and a wide range of eye sizes not found in well-fed lab colonies. Both dimmer light and smaller eyes limit light capture and have undetermined effects on visual behaviors such as flight. In this study, we used moving sinusoidal gratings to test spatial acuity, temporal acuity, and contrast threshold of female flies of varying eye sizes at different light intensities. We also investigated vision in the smaller and often neglected male fruit flies. As light intensity drops from 50.1 lx to 0.3 lx, flies have a reduced spatial acuity (females: from 0.1 to 0.06 cycles per degree, CPD, males: 0.1 to 0.04 CPD) and temporal acuity (females: from 50 Hz to 10 Hz, males: 25 Hz to 10 Hz), and an increased contrast detection threshold (females: from 10% to 29%, males: 19% to 48%). We find no major sex-specific differences after accounting for eye size. Visual abilities in both small (eye area of 0.1-0.17 mm2) and large flies (0.17-0.23 mm2) suffer at 0.3 lx compared to 50.1 lx, but small flies suffer more (spatial acuity: 0.03 vs 0.06 CPD, contrast threshold: 76% vs 57%, temporal acuity: 5 Hz vs 10 Hz). Our results suggest visual abilities of small flies suffer more than large flies at low light levels, possibly leading to size- and light intensity-dependent effects on foraging, navigation, and flight.

Miniaturisation reduces contrast sensitivity and spatial resolving power in ants.

Vision is crucial for animals to find prey, locate conspecifics and navigate within cluttered landscapes. Animals need to discriminate objects against a visually noisy background. However, the ability to detect spatial information is limited by eye size. In insects, as individuals become smaller, the space available for the eyes reduces, which affects the number of ommatidia, the size of the lens and the downstream information-processing capabilities. The evolution of small body size in a lineage, known as miniaturisation, is common in insects. Here, using pattern electroretinography with vertical sinusoidal gratings as stimuli, we studied how miniaturisation affects spatial resolving power and contrast sensitivity in four diurnal ants that live in a similar environment but vary in their body and eye size. We found that ants with fewer and smaller ommatidial facets had lower spatial resolving power and contrast sensitivity. The spatial resolving power was maximum in the largest ant Myrmecia tarsata at 0.60 cycles deg-1 compared with that of the ant with smallest eyes Rhytidoponera inornata at 0.48 cycles deg-1 Maximum contrast sensitivity (minimum contrast threshold) in M. tarsata (2627 facets) was 15.51 (6.4% contrast detection threshold) at 0.1 cycles deg-1, while the smallest ant R. inornata (227 facets) had a maximum contrast sensitivity of 1.34 (74.1% contrast detection threshold) at 0.05 cycles deg-1 Miniaturisation thus dramatically decreases maximum contrast sensitivity and also reduces spatial resolution, which could have implications for visually guided behaviours. This is the first study to physiologically investigate contrast sensitivity in the context of insect allometry.

Fairyflies.

A Quick Guide to fairyflies, miniature parasitoid wasps which have the smallest adult size known for any insect.

Miniaturisation decreases visual navigational competence in ants.

Evolution of a smaller body size in a given lineage, called miniaturisation, is commonly observed in many animals including ants. It affects various morphological features and is hypothesised to result in inferior behavioural capabilities, possibly owing to smaller sensory organs. To test this hypothesis, we studied whether reduced spatial resolution of compound eyes influences obstacle detection or obstacle avoidance in five different species of ants. We trained all ant species to travel to a sugar feeder. During their return journeys, we placed an obstacle close to the nest entrance. We found that ants with higher spatial resolution exited the corridor - the area between the two ends of the obstacle - on average 10 cm earlier, suggesting they detected the obstacle earlier in their path. Ants with the lowest spatial resolution changed their viewing directions only when they were close to the obstacle. We discuss the effects of miniaturisation on visual navigational competence in ants.