Small fruit flies sacrifice temporal acuity to maintain contrast sensitivity

Holometabolous insects, like fruit flies, grow primarily during larval development. Scarce larval feeding is common in nature and generates smaller adults. Despite the importance of vision to flies, eye size scales proportionately with body size, and smaller eyes confer poorer vision due to smaller optics. Variable larval feeding, therefore, causes within-species differences in visual processing, which have gone largely unnoticed due to ad libitum feeding in the lab that results in generally large adults. Do smaller eyes have smaller ommatidial lenses, reducing sensitivity, or broader inter-ommatidial angles, reducing acuity? And to what extent might neural processes adapt to these optical challenges with temporal and spatial summation? To understand this in the fruit fly, we generated a distribution of body lengths (1.67-2.34 mm; n = 24) and eye lengths (0.33-0.44 mm; n = 24), resembling the distribution of wild-caught flies, by removing larvae from food during their third instar. We find smaller eyes (0.19 vs.0.07 mm²) have substantially fewer (978 vs. 540, n = 45) and smaller ommatidia (222 vs. 121 μm²;n = 45) separated by slightly wider inter-ommatidial angles (4.5 vs.5.5°; n = 34). This corresponds to a greater loss in contrast sensitivity (<50%) than spatial acuity (<20%). Using a flight arena and psychophysics paradigm, we find that smaller flies lose little spatial acuity (0.126 vs. 0.118CPD; n = 45), and recover contrast sensitivity (2.22 for both; n = 65) by sacrificing temporal acuity (26.3 vs. 10.8Hz; n = 112) at the neural level. Therefore, smaller flies sacrifice contrast sensitivity to maintain spatial acuity optically, but recover contrast sensitivity, almost completely, by sacrificing temporal acuity neurally.