Genetic and developmental analysis of differences in eye and face morphology between Drosophila simulans and Drosophila mauritiana

Saad Arif,Christian Schlötterer,Corinna Hopfen,Kentaro Tanaka,Philipp Mitteroecker,Alistair P Mcgregor,Maria D S Nunes,Nico Posnien,Isabel Almudi,Maarten Hilbrant,Linta Kuncheria

doi:10.1111/ede.12027

Abstract

Eye and head morphology vary considerably among insects and even between closely related species of Drosophila. Species of the D. melanogaster subgroup, and other Drosophila species, exhibit a negative correlation between eye size and face width (FW); for example, D. mauritiana generally has bigger eyes composed of larger ommatidia and conversely a narrower face than its sibling species. To better understand the evolution of eye and head morphology, we investigated the genetic and developmental basis of differences in eye size and FW between male D. mauritiana and D. simulans. QTL mapping of eye size and FW showed that the major loci responsible for the interspecific variation in these traits are localized to different genomic regions. Introgression of the largest effect QTL underlying the difference in eye size resulted in flies with larger eyes but no significant difference in FW. Moreover, introgression of a QTL region on the third chromosome that contributes to the FW difference between these species affected FW, but not eye size. We also observed that this difference in FW is detectable earlier in the development of the eye-antennal disc than the difference in the size of the retinal field. Our results suggest that different loci that act at different developmental stages underlie changes in eye size and FW. Therefore, while there is a negative correlation between these traits in Drosophila, we show genetically that they also have the potential to evolve independently and this may help to explain the evolution of these traits in other insects.

Highlights

Understanding the evolution of morphology remains a central goal of evolutionary biology
Our results suggest that different loci that act at different developmental stages underlie changes in eye size and face width (FW)
While there is a negative correlation between these traits in Drosophila, we show genetically that they have the potential to evolve independently and this may help to explain the evolution of these traits in other insects

Summary

Introduction

Understanding the evolution of morphology remains a central goal of evolutionary biology. While great progress has been made in understanding the precise genetic and developmental basis of variation in some traits, including trichome, bristle, and pigmentation patterns in Drosophila, and pelvic armor in sticklebacks (e.g., Hoekstra et al 2006; McGregor et al 2007; Rebeiz et al 2009; Chan et al 2010), less is known about the changes underlying the evolution of differences in organ shape and size (True et al 1997; Pavlicev et al 2008; Matta and Bitner‐ Mathe 2010) This is in part because organ shape and size are often composites of multiple traits with coordinated development, which can potentially influence each other during development and even evolution (Lande 1980; Smith et al 1985; Brakefield 2006). The size of the eyes, for example, will influence the overall width of the head, and because eye size is determined by the number, size, and shape of ommatidia, variation in eye size can potentially be caused by changes in a number of developmental programs and many loci across the genome

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