Quantitative Trait Loci and Antagonistic Associations for Two Developmentally Related Traits in the<i>Drosophila</i>Head

Norry, Fabian M.; Gómez, Federico H.

doi:10.1093/jisesa/iew115

Cited by 23 publications

(31 citation statements)

References 29 publications

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“…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.…”

Section: Introductionsupporting

confidence: 78%

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

Reis

Wiegleb

Julien

et al. 2020

Preprint

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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...

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Section: Introductionsupporting

confidence: 78%

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

Reis

Wiegleb

Julien

et al. 2020

Preprint

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“…The insect compound eye is composed of a crystalline array of small units, named facets or ommatidia. In insects, eye size depends both on the number and diameter of the ommatidia and is often negatively correlated with face and/or antenna size (Arif et al, 2013;Norry and Gomez, 2017;Posnien et al, 2012). In this study, we selected four Drosophila species, which presented a larger eye to head width ratio as compared to D. mel.…”

Section: Reciprocal Changes In the Sizes Of Visual And Non-visual Heamentioning

confidence: 99%

“…To understand the genetic basis of sensory trade-off in Drosophila, we exploited the fact such trade-offs have also been observed within single fly species (Arif et al, 2013;Cowley and Atchley, 1990;Norry and Gomez, 2017;Posnien et al, 2012). We found that two wild-type D.…”

Section: A Conserved Mechanism Of Sensory Trade-offsmentioning

confidence: 99%

Altering the temporal regulation of one transcription factor drives sensory trade-offs

Ramaekers

Weinberger

Claeys

et al. 2018

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Size trade-offs of visual versus olfactory organs is a pervasive feature of animal evolution. Comparing Drosophila species, we find that larger eyes correlate with smaller antennae, where olfactory organs reside, and narrower faces. We demonstrate that this tradeoff arises through differential subdivision of the head primordium into visual versus non-visual fields. Specification of the visual field requires a highly-conserved eye development gene called eyeless in flies and Pax6 in humans. We discover that changes in the temporal regulation of eyeless expression during development is a conserved mechanism for sensory trade-offs within and between Drosophila species. We identify a natural single nucleotide polymorphism in the cis-regulatory region of eyeless that is sufficient to alter its temporal regulation and eye size.Because Pax6 is a conserved regulator of sensory placode subdivision, we propose that alterations in the mutual repression between sensory territories is a conserved mechanism for sensory trade-offs in animals.Cellular and molecular mechanisms governing sensory development have been extensively studied in a variety of invertebrate (D. melanogaster, C. elegans) and vertebrate (mouse, chick, zebrafish) model organisms. These analyses have revealed that a common feature of sensory development is a shared developmental origin of most head sensory structures -such as eyes and noses -which derive from the subdivision of a single multipotent primordium. In vertebrates, most head sensory organs develop from a multipotent preplacodal ectoderm (Grocott et al., 2012;Singh and Groves, 2016). The olfactory and lens placodes derive from the subdivision of the anterior aspect of this common placode. Similarly, during Drosophila development, the ectodermal eye-antennal imaginal disc (EAD) gives rise to all external head structures, including the visual (compound eyes and ocelli) and olfactory (antennae and maxillary palps) sense organs, and the head cuticle. The subdivision of the EAD along the anterior-posterior axis forms the eye (posterior) and antennal (anterior) compartments, respectively. Each compartment is further subdivided into sensory organ versus head cuticle. Antagonistic relationships between gene regulatory networks (GRNs) and signaling pathways that promote different sensory identities regulate these processes (Grocott et al., 2012; Singh and Groves, 2016). For example, in vertebrates, the transcription factors (TFs) promoting olfactory and lens identity, Dlx5 and Pax6, are first co-expressed in the entire vertebrate anterior placode. Their expression domains segregate as the lens and olfactory territories become distinct. Ectopic expression of Dlx5 in the lens placode leads to the loss of Pax6 expression and of lens identity (Bhattacharyya et al., 2004). A similar mechanism subdivides the fruit fly EAD. At early developmental stages, TFs promoting eye fate, such as Pax6 homologs Eyeless (Ey) and Twin-of-Eyeless (Toy), and the SIX factor Sine oculis are ubiquitously co-expressed with TFs promotin...

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“…Additionally, a genome-wide association study in D. melanogaster found an association between variation at the kek1 locus and female inter-ocular distance but not eye size (VONESCH et al 2016). In contrast, analysis of D. melanogaster recombinant inbred lines suggested a common genetic basis for eye and head capsule variation (NORRY and GOMEZ 2017). Furthermore, a polymorphism in the 3 rd intron of eyeless (ey) has recently been shown to contribute to variation in eye size, caused by ommatidia number differences, and reciprocal changes in antennal size/inter-ocular distance between D.…”

mentioning

confidence: 98%

“…These effects were verified by introgressing these regions from D. mauritiana into D. simulans to generate flies with larger eyes or a shorter inter-ocular distance (POSNIEN et al 2012; ARIF et al 2013).Additionally, a genome-wide association study in D. melanogaster found an association between variation at the kek1 locus and female inter-ocular distance but not eye size (VONESCH et al 2016). In contrast, analysis of D. melanogaster recombinant inbred lines suggested a common genetic basis for eye and head capsule variation (NORRY and GOMEZ 2017). Furthermore, a polymorphism in the 3 rd intron of eyeless (ey) has recently been shown to contribute to variation in eye size, caused by ommatidia number differences, and reciprocal changes in antennal size/inter-ocular distance between D.melanogaster strains (RAMAEKERS et al 2019).Taken together, these studies suggest that different genetic mechanisms can cause 5 changes in ommatidia size and/or number, and consequently natural variation in the overall size of Drosophila compound eyes and the trade-off with inter-ocular distance.…”

mentioning

confidence: 99%

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

Gaspar

Arif

Sumner‐Rooney

et al. 2019

Preprint

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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...

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Quantitative Trait Loci and Antagonistic Associations for Two Developmentally Related Traits in theDrosophilaHead

Cited by 23 publications

References 29 publications

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

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

Altering the temporal regulation of one transcription factor drives sensory trade-offs

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

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