The eyes have it: dim-light activity is associated with the morphology of eyes but not antennae across insect orders

Abstract

The perception of cues and signals in visual, olfactory and auditory modalities underpins all animal interactions and provides crucial fitness-related information. Sensory organ morphology is under strong selection to optimize detection of salient cues and signals in a given signalling environment, the most well-studied example being selection on eye design in different photic environments. Many dim-light active species have larger compound eyes relative to body size, but little is known about differences in non-visual sensory organ morphology between diurnal and dim-light active insects. Here, we compare the micromorphology of the compound eyes (visual receptors) and antennae (olfactory and mechanical receptors) in representative pairs of day active and dim-light active species spanning multiple taxonomic orders of insects. We find that dim-light activity is associated with larger compound eye ommatidia and larger overall eye surface area across taxonomic orders but find no evidence that morphological adaptations that enhance the sensitivity of the eye in dim-light active insects are accompanied by morphological traits of the antennae that may increase sensitivity to olfactory, chemical or physical stimuli. This suggests that the ecology and natural history of species is a stronger driver of sensory organ morphology than is selection for complementary investment between sensory modalities.

Adaptive divergence in the eyes ofHeliconiusbutterflies likely contributes to pre- and post-mating isolation

“…Habitat-associated variation in eye morphology has been reported across taxa (e.g., insects: (Greiner, 2006); mammals: (Veilleux & Lewis, 2011); fish: (Lisney et al, 2020); snakes: (Liu et al, 2012); primates: (Kirk, 2004)), and this variation is generally interpreted as an adaptive response to the local sensory conditions. For example, visual perception in insects is affected by the total number of ommatidia and their size/density (Greiner, 2006; Land, 1997; Warrant, 2004), and nocturnal and crepuscular species often possess larger eyes and larger facets to enhance photon sensitivity in low-light environments (Freelance et al, 2021). However, most studies do not formally evaluate the role of selection, which is a key element to define adaptation (Gould & Vrba, 1982).…”

“…Variation in the total number of ommatidia, their size, and density directly affects visual perception and often correlates with temporal activity (Greiner, 2006;Land, 1997;Stöckl et al, 2017;Warrant, 2004). For example, nocturnal and crepuscular species often have larger eyes and larger facets to enhance photon sensitivity in light-poor environments, as observed across insect taxa (Freelance et al, 2021). Associations between the local environment and the visual systems of diurnal insects are less studied and often included only as a comparison to other nocturnal species (e.g., Frederiksen & Warrant, 4 2008).…”

Long‐term captivity is associated with changes to sensory organ morphology in a critically endangered insect

“…Elaborate sensory systems require considerable energetic resources to develop and maintain, due largely to the associated neural circuitry (Niven & Laughlin, 2008), and sensory organ morphology is optimised to detect salient signals and cues from the background noise in the signalling environment (Elgar et al., 2018; Endler, 1992). For example, insects living in environments characterised by low ambient light levels have larger compound eye ommatidia to enhance sensitivity to light (Freelance, Tierney, et al., 2021) while halictid bees that evolved from a social to solitary lifestyle, and thus no longer need to frequently detect diverse social odours, have a lower density of antennal sensilla (Wittwer et al., 2017). Captive breeding environments, typically characterised by ready access to suitable food sources, proximity of potential mates and an absence of predators, effectively simplify the sensory environment and thus may relax natural selection pressures on sensory morphology that would be present in the wild.…”

Complex allometric relationships and ecological factors shape the development and evolution of eye size in the modular visual system of spiders

“…Nocturnal spiders had significantly larger PMEs and minimum eye sizes than diurnal spiders. Greater eye aperture (pupil) diameter increases achievable contrast sensitivity, and many species that use vision in low-light environments exhibit larger eyes, including crustaceans (Howell et al, 2023), fish, insects (Freelance et al, 2021;Tierney et al, 2017;Warrant, 2008), geckos (Schmitz & Higham, 2018), frogs (Thomas et al, 2020), primates (Ross & Kirk, 2007), and birds (Brooke et al, 1999;Garamszegi et al, 2002;Hall & Ross, 2007;Liu et al, 2023). In spiders, the secondary eyes are well suited for low-light vision thanks to the reflective tapetum enabling improved photon capture and enhanced sensitivity, so the enlargement of the PMEs, as the only medially placed secondary eyes, is logical for species that rely on visual tasks at night.…”

“…One way to resolve this conflict is to make the eye larger: an eye with a wider aperture can collect more photons and support greater sensitivity, and a longer focal length can support greater spatial resolution (Caves et al, 2017(Caves et al, , 2018Land & Nilsson, 2012;Rutowski et al, 2009;Taylor et al, 2019). As a result, eye size can be a good indicator of both sensitivity and achievable resolution, and can provide insight to the relative importance of vision, particularly in dim light environments (Freelance et al, 2021;Land & Nilsson, 2012;Tierney et al, 2017). However, the potential benefits of larger eyes may not outweigh the required cost of investment, and the energetic budget allocated to the development of visual systems ultimately depends on this balance (Niven & Laughlin, 2008).…”