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Evolution of sensory organ morphology: genetic analysis of eye size evolution in Drosophila

Final Report Summary - ESED (Evolution of sensory organ morphology: genetic analysis of eye size evolution in Drosophila)

A central challenge in evolutionary developmental biology is to understand how the shape and size of organisms evolves. Meeting this challenge promises will allow a better understanding of complex biological processes such as developmental regulation, adaptation and speciation. In practice this requires identifying the genetic changes in developmental programs that facilitate the evolution of differences in size and shape, and morphological innovations, and investigating how these changes arise and spread in populations. The aim of this project was to characterise variation in the size, shape and function of compound eyes within and between populations and species of Drosophila, and to determine the precise genetic basis of these differences and how they impact developmental regulation to alter the structure of compound eyes. Insects have evolved a striking diversity of compound eye sizes and shapes. The number of ommatidia (facets) and their size are major determinants of the visual sensitivity and acuity of the eyes. Each ommatidium expresses various light sensitive Rhodopsin proteins that allow the discrimination of different wavelengths of light. It follows that variation in eye size, shape, and opsin composition is likely to directly influence the vision of insects.
We quantified variation in these three traits in D. melanogaster, D. simulans and D. mauritiana. We confirmed that D. mauritiana generally has larger eyes than the other species, which is mainly a result of larger ommatidia. In addition, intra- and inter-specific differences in eye size among D. simulans and D. melanogaster strains are mainly caused by variation in ommatidia number. We also found that an increase in eye size is associated with a reduction in the width of the face (i.e. the distance between the eyes) and vice versa. Furthermore we found variation in the frequency and distribution of ommatidium types among sexes strains and species. This was particularly evident in D. simulans Zom4, which exhibits a dorsal patch of pale and odd-coupled ommatidia. Our data shows that the size, shape and rhodopsin composition of the compound eyes varies considerably within and among Drosophila species and are part of coordinated morphological changes affecting other aspects of head capsule morphology.
We then mapped the genetic basis of eye size variation resulting from these differences in ommatidia size between D. mauritiana and D. simulans, and ommatidia number within D. simulans. We found a quantitative trait locus (QTL) that explained 38% of the parental difference in ommatidia size between D. mauritiana and D. simulans on the X chromosome, and a minor effect of chromosome II. However the causative region underlying the reciprocal difference in face width maps to chromosome III. Indeed, although we have found within species differences in ommatidia number also map to chromosome III, our study of the development of the eye antennal disc shows that differences in the size of the eye are present before differences in the size of the presumptive face tissue arise. This suggests that although there is a consistent developmental trade-off between eye and face cuticle fate, different loci are responsible for determining larger eyes and a narrower face, or smaller eyes and a wider face respectively.
To characterise the gene(s) responsible for these differences in eye size, we then carried out high resolution mapping of QTL on chromosome X using an introgression based in parallel with RNA-seq to identify positional and expression candidates in this region. Expression and functional analysis of these candidates suggest that changes in the expression of the gene orthodenticle (otd) underlies the difference in eye size between D. mauritiana and D. simulans. Therefore our work has identified a potential new role for otd in eye development and provided new insights into the genetic and developmental bases of evolutionary difference in the morphology of a complex sensory organ.