Characterization of the genetic architecture underlying eye size variation withinDrosophila melanogasterandDrosophila simulans

Abstract

1865 484191 Fax: +44 (0)1865 483242 Running title: Evolution of Drosophila eye size AbstractThe compound eyes of insects exhibit striking variation in size, reflecting adaptation to different lifestyles and habitats. However, the genetic and developmental bases of variation in insect eye size is poorly understood, which limits our understanding of how these important morphological differences evolve. To address this, we further explored natural variation in eye size within and between four species of the Drosophila melanogaster species subgroup. We found extensive variation in eye size among these species, and flies with larger eyes generally had a shorter inter-ocular distance and vice versa. We then carried out quantitative trait loci (QTL) mapping of intra-specific variation in eye size and inter-ocular distance in both D. melanogaster and D. simulans. This revealed that different genomic regions underlie variation in eye size and inter-ocular distance in both species, which we corroborated by introgression mapping in D. simulans. This suggests that although there is a trade-off between eye size and inter-ocular distance, variation in these two traits is likely to be caused by different genes and so can be genetically decoupled. Finally, although we detected QTL for intra-specific variation in eye size at similar positions in D. melanogaster and D. simulans, we observed differences in eye fate commitment between strains of these two species. This indicates that different developmental mechanisms and therefore, most likely, different genes contribute to eye size variation in these species. Taken together with the results of previous studies, our findings suggest that the gene regulatory network that specifies eye size has evolved at multiple genetic nodes to give rise to natural variation in this trait within and among species.2014; KEESEY et al. 2019;RAMAEKERS et al. 2019). Like other drosophilids and other dipterans, this variation in eye size is negatively correlated with face width (inter-ocular distance) and/or antennal size, suggesting trade-offs during the development of eyeantennal tissues that contribute to their final size (NORRY et al. 2000;DOMINGUEZ and CASARES 2005;SUKONTASON et al. 2008;POSNIEN et al. 2012;KEESEY et al. 2019;RAMAEKERS et al. 2019).Studying the genetic basis of eye size variation in Drosophila offers an excellent opportunity to better understand the regulation and evolution of the development of eyes and other tissues, and ultimately how these morphological changes can cause functional differences in vision. For example, strains of D. mauritiana have larger eyes than either D. melanogaster or D. simulans, caused mainly by differences in ommatidial diameter, which is wider in D. mauritiana (POSNIEN et al. 2012; ARIF et al. 2013). QTL mapping has shown that while the larger eyes of D. mauritiana is caused by an X-linked locus of large effect, the reciprocal shorter inter-ocular distance of this species is caused by non overlapping autosomal loci (POSNIEN et al. 2012; ARIF et al. 2013...

Multiple loci linked to inversions are associated with eye size variation in species of theDrosophila virilisphylad

“…Therefore, our comparative morphological and mapping data strongly suggest an independent evolution of eye size in different lineages. This observation is supported by similar data obtained for two species of the melanogaster group (Gaspar et al 2020).…”

“…Our shape analysis revealed that increased eye size was accompanied by a contraction of the interstitial head cuticle. A similar trade-off has been observed in other Drosophila species (Norry et al 2000; Posnien et al 2012; Arif et al 2013; Keesey et al 2019; Ramaekers et al 2019; Gaspar et al 2020) and it may be associated with different investment in visual or olfactory sensory perception (Keesey et al 2019; Ramaekers et al 2019). Indeed, it has been shown that a northern D. americana strain is more “visual” because it has significantly bigger eyes compared to the antennae, while D. virilis is a more “olfactory” species with smaller eyes and bigger antennae (Keesey et al 2019).…”

“…Quantitative genetics approaches have revealed multiple loci associated with variation in eye size between D. simulans and D. mauritiana supporting the complex genetic architecture of this trait (Arif et al 2013). Similar observations were made for intra-specific variation in D. melanogaster (Norry and Gomez 2017; Ramaekers et al 2019) and D. simulans (Gaspar et al 2020). However, Ramaekers et al (2019) have shown that a single mutation affecting the regulation of the eyeless/Pax6 gene can explain up to 50% of variation in eye size between two D. melanogaster strains.…”

“…Externally, this trade-off is often observed by extensive head shape variation if compound eye size increases at the expense of the cuticle between the eyes (i.e. interstitial head cuticle) (Norry et al 2000; Posnien et al 2012; Keesey et al 2019; Gaspar et al 2020). The compound eyes are the most noticeable sensory structures in the insect head and differences in eye size have been reported between species, as well as between populations of the same species across the Drosophila genus (Norry et al 2000; Hämmerle and Ferrús 2003; Posnien et al 2012; Arif et al 2013; Keesey et al 2019; Ramaekers et al 2019; Gaspar et al 2020).…”

“…interstitial head cuticle) (Norry et al 2000; Posnien et al 2012; Keesey et al 2019; Gaspar et al 2020). The compound eyes are the most noticeable sensory structures in the insect head and differences in eye size have been reported between species, as well as between populations of the same species across the Drosophila genus (Norry et al 2000; Hämmerle and Ferrús 2003; Posnien et al 2012; Arif et al 2013; Keesey et al 2019; Ramaekers et al 2019; Gaspar et al 2020). Interestingly, eye size can vary due to variation in facet size or due to changes in ommatidia number (Posnien et al 2012; Arif et al 2013; Hilbrant et al 2014; Gaspar et al 2020), suggesting that different functional needs influence final eye size.…”