The remarkable visual capacities of nocturnal insects: vision at the limits with small eyes and tiny brains

Abstract

Nocturnal insects have evolved remarkable visual capacities, despite small eyes and tiny brains. They can see colour, control flight and land, react to faint movements in their environment, navigate using dim celestial cues and find their way home after a long and tortuous foraging trip using learned visual landmarks. These impressive visual abilities occur at light levels when only a trickle of photons are being absorbed by each photoreceptor, begging the question of how the visual system nonetheless generates the reliable signals needed to steer behaviour. In this review, I attempt to provide an answer to this question. Part of the answer lies in their compound eyes, which maximize light capture. Part lies in the slow responses and high gains of their photoreceptors, which improve the reliability of visual signals. And a very large part lies in the spatial and temporal summation of these signals in the optic lobe, a strategy that substantially enhances contrast sensitivity in dim light and allows nocturnal insects to see a brighter world, albeit a slower and coarser one. What is abundantly clear, however, is that during their evolution insects have overcome several serious potential visual limitations, endowing them with truly extraordinary night vision.This article is part of the themed issue 'Vision in dim light'.

Rod nuclear architecture determines contrast transmission of the retina and behavioral sensitivity in mice

“…As an important determinant of fitness, animals evolved a wide range of visual adaptation to see in the dark (Nilsson, 2009;O'Carroll & Warrant, 2017;Thomas, Robison, & Johnsen, 2017;Warrant, 2017;Warrant & Nilsson, 2006). Nocturnal vision is known to rely on highly efficient light capture, both at the level of the lens and photoreceptor outer segments, and often 255 compromises spatio-temporal resolution by summation strategies of neuronal readout (Warrant, 1999;2017). Here we established nuclear inversion as a complementary strategy to maximize sensitivity under low light conditions.…”

Differential investment in brain regions for a diurnal and nocturnal lifestyle in Australian Myrmecia ants

“…This increase in optical sensitivity, though significant, is not sufficient to explain the visually guided behaviors of insects at low light levels (Warrant, ). Insects may thus engage in spatial and temporal integration of receptor signals to improve the visual signal‐to‐noise ratio at low light levels (Greiner, Ribi, & Warrant, ; Stöckl, O'Carroll, & Warrant, ; Warrant, ). Spatial summation is thought to occur in the first optic neuropil, the lamina, via extensive lateral branching of laminar monopolar cell dendrites into neighboring cartridges, which receive input from single ommatidia (Greiner, Ribi, Wcislo, & Warrant, ; Ribi, ; Stöckl, Ribi, & Warrant, ).…”

Antennal asymmetry is not associated with social behaviour in Australian Hymenoptera

“…For example, larger workers of the bumblebee Bombus terrestris have both longer antennae and a higher density of some types of antennal sensilla (Spaethe et al 2007). and some species of dim light-active Hymenoptera have both larger compound eye facet size and more ommatidia for their body size compared with their day-active counterparts (Greiner et al 2007; reviewed by Tierney et al 2017;Warrant 2017;Wcislo & Tierney 2009). The density of sensilla trichodea A is negatively correlated with body size in R. bituberculata.…”

“…obs.) and some species of dim light-active Hymenoptera have both larger compound eye facet size and more ommatidia for their body size compared with their day-active counterparts (Greiner et al 2007; reviewed by Tierney et al 2017;Warrant 2017;Wcislo & Tierney 2009). While trade-off theory predicts that increased investment in one life history trait is likely to come at the expense of decreased investment in another trait (Stearns 1989;Zera & Harshman 2001), there is no a priori reason to expect a trade-off between any particular pair of traits.…”