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

Abstract

35The size and shape of organs is tightly controlled to achieve optimal function. Natural 36 morphological variations often represent functional adaptations to an ever-changing 37 environment. For instance, variation in head morphology is pervasive in insects and the 38 underlying molecular basis is starting to be revealed in the Drosophila genus for species of the 39 melanogaster group. However, it remains unclear whether similar diversifications are governed 40 by similar or different molecular mechanisms over longer timescales. To address this issue, we 41 used species of the virilis phylad because they have been diverging from D. melanogaster for 42 at least 40 million years. Our comprehensive morphological survey revealed remarkable 43 differences in eye size and head shape among these species with D. novamexicana having the 44 smallest eyes and southern D. americana populations having the largest eyes. We show that 45 the genetic architecture underlying eye size variation is complex with multiple associated 46 genetic variants located on most chromosomes. Our genome wide association study (GWAS) 47 strongly suggests that some of the putative causative variants are associated with the presence 48 of inversions. Indeed, northern populations of D. americana share derived inversions with D. 49 novamexicana and they show smaller eyes compared to southern ones. Intriguingly, we 50 observed a significant enrichment of genes involved in eye development on the 4 th chromosome 51 after intersecting chromosomal regions associated with phenotypic differences with those 52 showing high differentiation among D. americana populations. We propose that variants 53 associated with chromosomal inversions contribute to both intra-and inter-specific variation 54 in eye size among species of the virilis phylad.55 56 Quantitative genetics approaches have revealed multiple loci associated with variation 83 in eye size between D. simulans and D. mauritiana supporting the complex genetic architecture 84 of this trait (Arif et al. 2013). Similar observations were made for intra-specific variation in D. 85 melanogaster (Norry and Gomez 2017; Ramaekers et al. 2019) and D. simulans (Gaspar et al. 86 2020). However, Ramaekers et al. (2019) have shown that a single mutation affecting the 87 regulation of the eyeless/Pax6 gene can explain up to 50% of variation in eye size between two 88 D. melanogaster strains. Although, the genetic architecture underlying eye size variation is 89 starting to be revealed for species of the melanogaster group, it remains unclear whether similar 90 independent morphological diversifications identified in Drosophila (Norry et al. 2000; Keesey 91 et al. 2019) share the same molecular basis over longer timescales. 92 Chromosomal inversions are an interesting genetic variant because suppression of 93 recombination is thought to maintain linkage of favorable alleles which are protected from 94 immigrant alleles carrying variants which decrease fitness (Kirkpatrick and Barton 2006; 95 Kirkpatrick 2010). Therefore...

Heterochrony inorthodenticleexpression is associated with ommatidial size variation betweenDrosophilaspecies

“…Our work provides new insights into ommatidia size regulation and the evolution of eye size. Together with evidence from other studies showing that changes in the timing of ey expression contributes to differences in ommatidia number in Drosophila (Ramaekers et al, 2019), we now have a better understand the genetic and developmental mechanisms that underlie the large diversity in Drosophila eye size (Arif et al, 2013; Buchberger et al, 2021; Gaspar et al, 2020; Hilbrant et al, 2014; Keesey et al, 2019; Norry and Gomez, 2017; Posnien et al, 2012; Ramaekers et al, 2019; Reis et al, 2020). Moreover, this evidence suggests that changes in the temporal expression of upstream TFs is a widespread mechanism responsible for morphological evolution.…”

“…For example, killer flies, Coenosia sp., have evolved wider, flattened, anterior ommatidia to maximise contrast sensitivity and acuity as an adaptation to hunting (Gonzalez-Bellido et al, 2011). A number of studies have also found extensive variation in eye size within and between closely related species of Drosophila , caused by differences in ommatidia number and/or ommatidia area (Arif et al, 2013; Buchberger et al, 2021; Gaspar et al, 2020; Hilbrant et al, 2014; Keesey et al, 2019; Norry and Gomez, 2017; Posnien et al, 2012; Ramaekers et al, 2019; Reis et al, 2020). Despite the pervasive variation in eye morphology and detailed knowledge about eye development in Drosophila (Casares and Almudi, 2016; Casares and McGregor, 2021; Kumar, 2018), little is known about the genetic and developmental bases for variation in eye size even among Drosophila species with a few exceptions (e.g.…”

Divergence and introgression among the virilis group of Drosophila

“…But there has been extensive introgression between the X chromosomes of D. borealis and D. lacicola . Additionally, our data does not allow us to characterise or describe inversions despite their prevalence in the virilis group and their potential contribution to patterns of genomic divergence and speciation (Reis et al 2018, 2020).…”

“…Additionally, our data does not allow us to characterise or describe inversions despite their prevalence in the virilis group and their potential contribution to patterns of genomic divergence and speciation (Reis et al 2018(Reis et al , 2020 As with previous studies, we also observed a positive correlation between admixture proportion and absolute divergence across species pairs and genomic regions (Supplementary figure 6) (Stankowski et al 2019;Duranton et al 2020). In European lineages of sea bass, archaic genomic tracts were shown to contribute to excess absolute divergence and windows with high admixture proportions were also predicted to be involved in reproductive isolation (Duranton et al 2020).…”

Divergence and introgression among the virilis group of Drosophila

“…Additionally, our data do not allow us to characterize or describe inversions despite their prevalence in the virilis group (Reis et al. 2018, 2020).…”