Ontogenetic expansion and regionalization of the triatomine compound eye supports flight-related vision

Abstract

Triatomines are the vectors of Chagas disease, one of the main endemic diseases from South to North America, now expanding to other continents. These hemimetabolous insects have been considered poorly visual animals. However, recent findings challenge this idea. Here, we used Rhodnius prolixus as a model species to comprehensively characterize triatomine compound eyes. We found that in the adult stage, eye size significantly exceeds the dimensions predicted by the nymphal eye growth rate. Moreover, while the compound eye grows symmetrically in its dorsal and ventral directions throughout the nymphal instars, in the adult, the eye undergoes greater ventral growth, resulting in a dorsoventrally asymmetrical eye. By studying a bright pseudopupil induced by fluorescence in natural mutant animals, we observed no major differences in sampling resolution between the last nymphal instar and the adult stage. However, the adult eye possesses significantly larger ommatidia, particularly in its ventral region, shifting the area of highest sensitivity from the equatorial region in the nymphal instars to the ventral region in the adult. A similar eye growth pattern was observed in Triatoma infestans and Panstrongylus megistus. The analysis of photographic records from 39 species across 10 genera indicates that an asymmetrical eye is the predominant eye pattern in adult triatomines. Notable exceptions in wingless adults of Mepraia spinolai, reveal a tight association between possessing a large asymmetrical eye and the presence of wings. This suggests that vision might support triatomine dispersal flights among other visual behaviors. Significance StatementKissing bugs are hematophagous insects known for being the vectors of Chagas disease, one of the main endemic diseases in the Americas. Vision was not considered a relevant sensory system in these insects. Here, we show that their eyes increase in size beyond expected by ontogeny and become asymmetrical when transitioning from the last nymphal instar to the adult stage. The eyes undergo a ventral expansion that shifts the region of greatest light sensitivity from the equatorial zone in nymphs to the ventral region in adults. We found this asymmetrical eye only in winged kissing bugs, suggesting that vision supports flight. This is relevant in ecological and epidemiological terms since kissing bugs disperse by flight for habitat colonization and host-seeking.