Multiple Quantitative Trait Loci Influence the Shape of a Male-Specific Genital Structure in<i>Drosophila melanogaster</i>

Evolutionary innovation can allow a species access to a new ecological niche, potentially reducing competition with closely related species. While the vast majority of Drosophila flies feed on rotting fruit and other decaying matter, and are harmless to human activity, Drosophila suzukii, which has a morphologically modified ovipositor, is capable of colonizing live fruit that is still in the process of ripening, causing massive agricultural damage. Here, we conducted the first comparative analysis of this species and its close relatives, analysing both ovipositor structure and fruit susceptibility. We found that the ovipositor of the species most closely related to D. suzukii, Drosophila subpulchrella, has a similar number of enlarged, evolutionarily derived bristles, but a notably different overall shape. Like D. suzukii, D. subpulchrella flies are capable of puncturing the skin of raspberries and cherries, but we found no evidence that they could penetrate the thicker skin of two varieties of grapes. More distantly related species, one of which has previously been mistaken for D. suzukii, have blunt ovipositors with small bristles. While they did not penetrate fruit skin in any of the assays, they readily colonized fruit interiors where the skin was broken. Our results suggest that considering evolutionary context may be beneficial to the management of invasive species.

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“…In a manner analogous to a study of the posterior lobe of the male genitalia [18,19], a horizontal rspb.royalsocietypublishing.org Proc. R. Soc.…”

Section: (B) Morphological Analysis Of the Ovipositorsmentioning

confidence: 99%

The making of a pest: the evolution of a fruit-penetrating ovipositor inDrosophila suzukiiand related species

et al. 2014

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“…melanogaster using a cross between a pair of phenotypically different inbred strains [23]. Here we attempt to replicate these QTL using an independent mapping cross.…”

Section: Introductionmentioning

confidence: 99%

Mapping QTL Contributing to Variation in Posterior Lobe Morphology between Strains of Drosophila melanogaster

Hackett¹,

Wang²,

Smith³

et al. 2016

PLoS ONE

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Closely-related, and otherwise morphologically similar insect species frequently show striking divergence in the shape and/or size of male genital structures, a phenomenon thought to be driven by sexual selection. Comparative interspecific studies can help elucidate the evolutionary forces acting on genital structures to drive this rapid differentiation. However, genetic dissection of sexual trait divergence between species is frequently hampered by the difficulty generating interspecific recombinants. Intraspecific variation can be leveraged to investigate the genetics of rapidly-evolving sexual traits, and here we carry out a genetic analysis of variation in the posterior lobe within D. melanogaster. The lobe is a male-specific process emerging from the genital arch of D. melanogaster and three closely-related species, is essential for copulation, and shows radical divergence in form across species. There is also abundant variation within species in the shape and size of the lobe, and while this variation is considerably more subtle than that seen among species, it nonetheless provides the raw material for QTL mapping. We created an advanced intercross population from a pair of phenotypically-different inbred strains, and after phenotyping and genotyping-by-sequencing the recombinants, mapped several QTL contributing to various measures of lobe morphology. The additional generations of crossing over in our mapping population led to QTL intervals that are smaller than is typical for an F2 mapping design. The intervals we map overlap with a pair of lobe QTL we previously identified in an independent mapping cross, potentially suggesting a level of shared genetic control of trait variation. Our QTL additionally implicate a suite of genes that have been shown to contribute to the development of the posterior lobe. These loci are strong candidates to harbor naturally-segregating sites contributing to phenotypic variation within D. melanogaster, and may also be those contributing to divergence in lobe morphology between species.

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“…If genes that contribute to polymorphism within a species are generally also those that influence a trait difference between species, there should be significant overlap between mapped intra- and interspecific QTL intervals. Several previous studies have observed QTL overlap in both within and between species (Nuzhdin and Reiwitch, 2000; Fishman et al , 2002; Lexer et al , 2005; Hall et al , 2006; Wittkopp et al , 2009; McNeil et al , 2011; Groot et al , 2013), supporting the idea that interspecific differences are not fundamentally distinct from variation within species in many instances. However, at least one study failed to identify any overlap in the positions of QTLs mapped within and between species (Gleason and Ritchie, 2004).…”

Section: Discussionmentioning

confidence: 59%

Genetic dissection of intraspecific variation in a male-specific sexual trait in Drosophila melanogaster

2016

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An open question in evolutionary biology is the relationship between standing variation for a trait and the variation that leads to interspecific divergence. By identifying loci underlying phenotypic variation in intra- and interspecific crosses we can determine the extent to which polymorphism and divergence are controlled by the same genomic regions. Sexual traits provide abundant examples of morphological and behavioral diversity within and among species, and here we leverage variation in the Drosophila sex comb to address this question. The sex comb is an array of modified bristles or ‘teeth' present on the male forelegs of several Drosophilid species. Males use the comb to grasp females during copulation, and ablation experiments have shown that males lacking comb teeth typically fail to mate. We measured tooth number in >700 genotypes derived from a multiparental advanced-intercross population, mapping three moderate-effect loci contributing to trait heritability. Two quantitative trait loci (QTLs) coincide with previously identified intra- and interspecific sex comb QTL, but such overlap can be explained by chance alone, in part because of the broad swathes of the genome implicated by earlier, low-resolution QTL scans. Our mapped QTL regions encompass 70–124 genes, but do not include those genes known to be involved in developmental specification of the comb. Nonetheless, we identified plausible candidates within all QTL intervals, and used RNA interference to validate effects at four loci. Notably, TweedleS expression knockdown substantially reduces tooth number. The genes we highlight are strong candidates to harbor segregating, functional variants contributing to sex comb tooth number.

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Multiple Quantitative Trait Loci Influence the Shape of a Male-Specific Genital Structure inDrosophila melanogaster

Cited by 26 publications

References 62 publications

The making of a pest: the evolution of a fruit-penetrating ovipositor inDrosophila suzukiiand related species

The making of a pest: the evolution of a fruit-penetrating ovipositor inDrosophila suzukiiand related species

Mapping QTL Contributing to Variation in Posterior Lobe Morphology between Strains of Drosophila melanogaster

Genetic dissection of intraspecific variation in a male-specific sexual trait in Drosophila melanogaster

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