Sex and Caste-Specific Variation in Compound Eye Morphology of Five Honeybee Species

Abstract

Ranging from dwarfs to giants, the species of honeybees show remarkable differences in body size that have placed evolutionary constrains on the size of sensory organs and the brain. Colonies comprise three adult phenotypes, drones and two female castes, the reproductive queen and sterile workers. The phenotypes differ with respect to tasks and thus selection pressures which additionally constrain the shape of sensory systems. In a first step to explore the variability and interaction between species size-limitations and sex and caste-specific selection pressures in sensory and neural structures in honeybees, we compared eye size, ommatidia number and distribution of facet lens diameters in drones, queens and workers of five species (Apis andreniformis, A. florea, A. dorsata, A. mellifera, A. cerana). In these species, male and female eyes show a consistent sex-specific organization with respect to eye size and regional specialization of facet diameters. Drones possess distinctly enlarged eyes with large dorsal facets. Aside from these general patterns, we found signs of unique adaptations in eyes of A. florea and A. dorsata drones. In both species, drone eyes are disproportionately enlarged. In A. dorsata the increased eye size results from enlarged facets, a likely adaptation to crepuscular mating flights. In contrast, the relative enlargement of A. florea drone eyes results from an increase in ommatidia number, suggesting strong selection for high spatial resolution. Comparison of eye morphology and published mating flight times indicates a correlation between overall light sensitivity and species-specific mating flight times. The correlation suggests an important role of ambient light intensities in the regulation of species-specific mating flight times and the evolution of the visual system. Our study further deepens insights into visual adaptations within the genus Apis and opens up future perspectives for research to better understand the timing mechanisms and sensory physiology of mating related signals.

Visual acuity of the honey bee retina and the limits for feature detection

“…This region, where we observed smaller Δρ values, is one also associated with a higher sampling density of ommatidia typical of flying insects20. In honey bees, evidence for such an acute zone comes from optical estimates of smaller inter-ommatidial angles that sample this part of the scene1621, correspondingly larger ommatidial facets22, and through behavioural evidence for regional differences in visual performance13. The optical data suggests that bees have inter-ommatidial angles (Δϕ) of 2.1° (horizontally) and 0.9° (vertically) in this eye region21, although it has been argued that geometric distortions of the underlying photoreceptor mosaic lead to an average around 1.7° in both dimensions16, a value more consistent with behavioural estimates for grating resolution23.…”

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

“…While most of the dorsal retina of the honeybee drone contains this specialized DA drone subtype, it remains unclear whether expression of UV- and Blue receptors in the ventral retina leads to stochastically distributed ommatidial subtypes [83], like in the case of the worker bee (Figure 4J). In conclusion, the drone eye differs greatly from the worker bee both molecularly, as well as in size, shape, and ommatidia number [84]. Although drones do not participate in pollenating flights that require precise navigation, their eye also contains DRA ommatidia [85,86].…”

Visual Adaptations for Mate Detection in the Male Carpenter Bee Xylocopa tenuiscapa

“…[16]), and (d) eye size that may be larger in males to aid in the visual location of females (e.g. [17,18]).…”

“…Bright zones are similar to acute zones, but sacrifice spatial resolution in favour of even higher sensitivity by allowing larger inter-ommatidial angles, thus maximising contrast sensitivity for small targets, especially in dimmer light [30, 31]. Male-specific acute zones have been studied extensively in flies [21, 29, 32] and in drones of the European honey bee Apis mellifera [17, 26, 33], but have more recently also been described for Asian honey bees [18] and several species of bumble bees [15]. In A .…”