Drosophila americana as a Model Species for Comparative Studies on the Molecular Basis of Phenotypic Variation

Fonseca, Nuno A.; Morales‐Hojas, Ramiro; Reis, Micael; Rocha, Hélder; Vieira, Cristina; Nolte, Viola; Schlötterer, Christian; Vieira, Jorge

doi:10.1093/gbe/evt037

Cited by 25 publications

(43 citation statements)

References 72 publications

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“…S7). Given the high levels of phenotypic and nucleotide variation characteristic of D. americana (Fonseca et al 2013), it is likely that the intermediate ancestral eye size represented the mean of a quantitative trait including smaller and bigger eyes. Thus, we assumed that the ancestral population of the virilis phylad was highly polymorphic for eye size, and both bigger and smaller eye size were selected for in specific lineages from a pool of standing genetic variation (Fig 5A).…”

Section: Resultsmentioning

confidence: 99%

“…The D. virilis and D. novamexicana strains were obtained from the Tucson stock center in 1995 and were kept in the laboratory since then. D. americana strains were established with single inseminated females collected from the wild in different locations of the USA (Omaha, Nebraska (O), 2008 and Saint Francisville (SF), Louisiana, 2010) (Reis et al 2011; Fonseca et al 2013; Reis et al 2015). All strains were kept at 25°C under 12h/12h light/dark cycles.…”

Section: Methodsmentioning

confidence: 99%

“…To test whether the presence of inversions was associated with differences in eye size (after accounting for body size) and head shape, we screened D. americana , D. novamexicana and D. virilis strains for the presence/absence of eight different inversions known to be fixed or polymorphic within the virilis phylad of Drosophila (Hsu 1952; Throckmorton 1982) and for which the breakpoint locations have been identified ( Xa , Xb , Xc (Muller A), 2a , 2b (Muller E), 4a (Muller B), 5a and 5b (Muller C), (Evans et al 2007; Fonseca et al 2012; Reis et al 2018)). Primers were developed for one breakpoint and its corresponding ancestral state for each of the eight inversions (File S2) based on the D. virilis (Clark et al 2007), D. americana (H5, W11, (Fonseca et al 2013) and SF12, (Reis et al 2018)), and D. novamexicana (15010-1031.00, (Reis et al 2018)) genome sequences to avoid polymorphism at the primer binding sites. Genomic DNA was extracted from pools of 20 females for each strain using a standard phenol:chloroform protocol, and the concentration was normalized based on concentration measurements using Nanodrop® prior to PCR amplification (File S2).…”

Section: Methodsmentioning

confidence: 99%

“…Species of the virilis phylad of Drosophila are diverging from D. melanogaster for at least 40 million years (Morales-Hojas and Vieira 2012; Russo et al 2013) and they have been extensively used in comparative genomics studies of important ecological traits, such as body color (Wittkopp et al 2009; Wittkopp et al 2011), cold resistance (Reis et al 2011), life span (Fonseca et al 2013) and developmental time (Reis et al 2014). D. virilis is a cosmopolitan species of Asian origin while D. americana and D. novamexicana are endemic to the USA (Throckmorton 1982) and constitute the americana complex.…”

Section: Introductionmentioning

confidence: 99%

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Multiple loci linked to inversions are associated with eye size variation in species of the Drosophila virilis phylad

Reis

Wiegleb

Julien

et al. 2020

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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: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Multiple loci linked to inversions are associated with eye size variation in species of the Drosophila virilis phylad

Reis

Wiegleb

Julien

et al. 2020

Preprint

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“…The virilis group of Drosophila provides a good model for analyzing the genetic basis of morphological differences among closely related species (Spicer 1991;Wittkopp et al 2010;Fonseca et al 2013). The virilis group contains two phylads, the montana phylad and the virilis phylad.…”

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A Single Gene Causes an Interspecific Difference in Pigmentation in Drosophila

Ahmed-Braimah

Sweigart

2015

Genetics

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The genetic basis of species differences remains understudied. Studies in insects have contributed significantly to our understanding of morphological evolution. Pigmentation traits in particular have received a great deal of attention and several genes in the insect pigmentation pathway have been implicated in inter-and intraspecific differences. Nonetheless, much remains unknown about many of the genes in this pathway and their potential role in understudied taxa. Here we genetically analyze the puparium color difference between members of the virilis group of Drosophila. The puparium of Drosophila virilis is black, while those of D. americana, D. novamexicana, and D. lummei are brown. We used a series of backcross hybrid populations between D. americana and D. virilis to map the genomic interval responsible for the difference between this species pair. First, we show that the pupal case color difference is caused by a single Mendelizing factor, which we ultimately map to an 11-kb region on chromosome 5. The mapped interval includes only the first exon and regulatory region(s) of the dopamine N-acetyltransferase gene (Dat). This gene encodes an enzyme that is known to play a part in the insect pigmentation pathway. Second, we show that this gene is highly expressed at the onset of pupation in light brown taxa (D. americana and D. novamexicana) relative to D. virilis, but not in the dark brown D. lummei. Finally, we examine the role of Dat in adult pigmentation between D. americana (heavily melanized) and D. novamexicana (lightly melanized) and find no discernible effect of this gene in adults. Our results demonstrate that a single gene is entirely or almost entirely responsible for a morphological difference between species.KEYWORDS morphological evolution; pigmentation; genetics of species differences U NDERSTANDING the genetic basis of morphological differences between species is a central goal of evolutionary biology. A key question focuses on complexity: Do species differ by many genes of small effect or by a few genes of large effect (Haldane 1937)? The answer to this question has remained elusive; cases studied reveal examples of each scenario (Orr 2001). This is not surprising, however, as traits and species may differ in divergence rates and types of selection (or lack thereof). The question can best be stated as one of relative frequency: How often do major genes cause morphological differences between species (Orr 2001)?Insect pigmentation traits have received much attention from geneticists (Wittkopp et al. 2003a;True 2003;Wittkopp and Beldade 2009). These studies benefited from the fact that the pathway that determines insect cuticular pigment is both conserved and well understood (Wittkopp et al. 2002;Wittkopp et al. 2003a;Jeong et al. 2008;Williams et al. 2008;Werner et al. 2010). Several genes in the pigmentation pathway have been implicated in pigmentation differences between and within species, particularly in Drosophila (Wittkopp et al. 2003b;Takahashi et al. 2007;Jeong et al. 2008;T...

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Divergence and introgression among the virilis group of Drosophila

et al. 2022

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Speciation with gene flow is now widely regarded as common. However, the frequency of introgression between recently diverged species and the evolutionary consequences of gene flow are still poorly understood. The virilis group of Drosophila contains 12 species that are geographically widespread and show varying levels of prezygotic and postzygotic isolation. Here, we use de novo genome assemblies and whole-genome sequencing data to resolve phylogenetic relationships and describe patterns of introgression and divergence across the group. We suggest that the virilis group consists of three, rather than the traditional two, subgroups. Some genes undergoing rapid sequence divergence across the group were involved in chemical communication and desiccation tolerance, and may be related to the evolution of sexual isolation and adaptation. We found evidence of pervasive phylogenetic discordance caused by ancient introgression events between distant lineages within the group, and more recent gene flow between closely related species. When assessing patterns of genome-wide divergence in species pairs across the group, we found no consistent genomic evidence of a disproportionate role for the X chromosome as has been found in other systems. Our results show how ancient and recent introgressions confuse phylogenetic reconstruction, but may play an important role during early radiation of a group.

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Drosophila americana as a Model Species for Comparative Studies on the Molecular Basis of Phenotypic Variation

Cited by 25 publications

References 72 publications

Multiple loci linked to inversions are associated with eye size variation in species of the Drosophila virilis phylad

Multiple loci linked to inversions are associated with eye size variation in species of the Drosophila virilis phylad

A Single Gene Causes an Interspecific Difference in Pigmentation in Drosophila

Divergence and introgression among the virilis group of Drosophila

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