Inverse resource allocation between vision and olfaction across the genus Drosophila

Ian W Keesey,Dario Riccardo Valenzano,Lydia Gruber,George F Obiero,Jürgen Rybak,Mohammed A Khallaf,Bruce A Barrett,Grit Kunert,Grant Bolton,Sofia Lavista-Llanos,Markus Knaden,Sarah Koerte,Bill S Hansson,Veit Grabe

doi:10.1038/s41467-019-09087-z

Abstract

Divergent populations across different environments are exposed to critical sensory information related to locating a host or mate, as well as avoiding predators and pathogens. These sensory signals generate evolutionary changes in neuroanatomy and behavior; however, few studies have investigated patterns of neural architecture that occur between sensory systems, or that occur within large groups of closely-related organisms. Here we examine 62 species within the genus Drosophila and describe an inverse resource allocation between vision and olfaction, which we consistently observe at the periphery, within the brain, as well as during larval development. This sensory variation was noted across the entire genus and appears to represent repeated, independent evolutionary events, where one sensory modality is consistently selected for at the expense of the other. Moreover, we provide evidence of a developmental genetic constraint through the sharing of a single larval structure, the eye-antennal imaginal disc. In addition, we examine the ecological implications of visual or olfactory bias, including the potential impact on host-navigation and courtship.

Highlights

Divergent populations across different environments are exposed to critical sensory information related to locating a host or mate, as well as avoiding predators and pathogens
The potential tradeoff seems to stem from a theoretically restricted resource allocation between the eye and antenna during larval development, which is linked to a single shared structure giving rise to both adult sensory systems (Fig. 5d–i). It remains to be seen whether this push–pull between the eye and antennal region of the imaginal disc is under similar genetic control in all non-melanogaster species; our study and a recent preprint[31] provide evidence that a simple mutation can mirror inverse variation in ommatidia and sensilla numbers for D. melanogaster, something which is consistent with our observations of repeated, independent evolutionary events across this genus of fly in regard to visual and olfactory divergence
In order to test this pseudogene argument, we examined the olfactory genes from many Drosophila species using previously published data on OR, GR, IR genes, and their associated pseudogenes across 14 members of Drosophilidae (Supplementary Figure 1J)[51], but we did not find any meaningful correlation between olfactory pseudogenes and eye size or visual enhancement

Summary

Introduction

Divergent populations across different environments are exposed to critical sensory information related to locating a host or mate, as well as avoiding predators and pathogens. The genus Drosophila provides between 1200 and 1500 individual species, with an ecology spanning nearly every imaginable environment and host choice, from deserts to forests, from islands to mountains, and across incredibly unique or specialized food resources, such as the gills of land crabs, protein sources within bat guano, or otherwise toxic fruits;[10,15,19,20,21] the potential to transform an already powerful model organism from a singular species into an entire genus is possible due to the recent advances in cellular and genetic tools for examining the complex neurological mechanisms of natural behavior in novel, non-model species. With the above-mentioned factors in mind, one of the goals of the present study is to encourage the expansion of the D. melanogaster model to become the Drosophila system, and thereby encompass a broader array of species within this genus for comparative, ecological research into what drives the evolution of the nervous system

Objectives

Methods

Results

Conclusion