The evolutionary diversity of insect retinal mosaics: common design principles and emerging molecular logic

Abstract

Independent evolution has resulted in a vast diversity of eyes. Despite the lack of a common Bauplan or ancestral structure, similar developmental strategies are used. For instance, different classes of photoreceptor cells (PRs) are distributed stochastically and/or localized in different regions of the retina. Here we focus on recent progress made towards understanding the molecular principles behind patterning retinal mosaics of insects, one of the most diverse groups of animals adapted to life on land, in the air, under water, or on the water surface. Morphological, physiological, and behavioral studies from many species provide detailed descriptions of the vast variation in retinal design and function. By integrating this knowledge with recent progress in the characterization of insect Rhodopsins as well as insight from the model organism Drosophila melanogaster, we seek to identify the molecular logic behind the adaptation of retinal mosaics to an animal’s habitat and way of life.

Sexual dimorphism in the compound eye of Heliconius erato: a nymphalid butterfly with at least five spectral classes of photoreceptor

“…Ommatidia are expressed spatially in a stochastic manner, but the proportion of each type of ommatidium is consistent within each sex, as in other insects (Wernet et al, 2015). Intracellular recordings of H. erato photoreceptor cells between 300 and 700 nm are reported from 42 cells in Figs 4 and 5.…”

“…Heliconius erato ommatidia resemble those of other insects, with the LVF receptors R1 and R2 containing SW opsins, while the SVFs R3-8 contain a single opsin, LWRh (Wernet and Desplan, 2004;Hadjieconomou et al, 2011;Wernet et al, 2015). Heliconius erato compound eyes have at least five spectral types of photoreceptor and are sexually dimorphic, despite monomorphic wing patterns.…”

“…Butterfly ommatidia contain nine photoreceptor cells R1-R9, whose photosensitive membranes form a fused rhabdom ( Fig. 1A-C; Wernet et al, 2015). In the nomenclature used for butterflies, R1 and R2 cells are long visual fiber (LVF) photoreceptors, which lie on opposite sides of the rhabdom and typically express either UVRh or BRh mRNAs (encoding SW opsins; Fig.…”

Retinal perception and ecological significance of color vision in insects

“…Each shows a columnar organization resembling the array of ommatidia in the retina [22]. In most insects six of the eight to nine photoreceptors are predominantly involved in motion vision and synapse first in the lamina, while the remaining color-sensitive PRs project directly to the medulla [16,23,24], the largest and most complex optic neuropil. In the medulla, different connections of color sensitive photoreceptors allow comparisons of wavelengths detected by two or more photoreceptors from the same and/or different ommatidia [25].…”

Diversity in cell motility reveals the dynamic nature of the formation of zebrafish taste sensory organs

“…In contrast to other sensory organs with a specific number of cells (i.e. insect ommatidia; Wernet et al, 2015), the cellular organization of taste buds is variable within a single species; an adult mouse taste bud contains 50-100 cells of types I, II or III but their proportion varies among taste bud loci (i.e. Ohtubo and Yoshii, 2011).…”