Variation In Bristle Number Research Articles

Interspecific variation in bristle number on forewings of tiny insects does not influence clap-and-fling aerodynamics.

Miniature insects must overcome significant viscous resistance in order to fly. They typically possess wings with long bristles on the fringes and use a clap-and-fling mechanism to augment lift. These unique solutions to the extreme conditions of flight at tiny sizes (<2 mm body length) suggest that natural selection has optimized wing design for better aerodynamic performance. However, species vary in wingspan, number of bristles (n) and bristle gap (G) to diameter (D) ratio (G/D). How this variation relates to body length (BL) and its effects on aerodynamics remain unknown. We measured forewing images of 38 species of thrips and 21 species of fairyflies. Our phylogenetic comparative analyses showed that n and wingspan scaled positively and similarly with BL across both groups, whereas G/D decreased with BL, with a sharper decline in thrips. We next measured aerodynamic forces and visualized flow on physical models of bristled wings performing clap-and-fling kinematics at a chord-based Reynolds number of 10 using a dynamically scaled robotic platform. We examined the effects of dimensional (G, D, wingspan) and non-dimensional (n, G/D) geometric variables on dimensionless lift and drag. We found that: (1) increasing G reduced drag more than decreasing D; (2) changing n had minimal impact on lift generation; and (3) varying G/D minimally affected aerodynamic forces. These aerodynamic results suggest little pressure to functionally optimize n and G/D. Combined with the scaling relationships between wing variables and BL, much wing variation in tiny flying insects might be best explained by underlying shared growth factors.

Variation and Evolution of Male Sex Combs in Drosophila: Nature of Selection Response and Theories of Genetic Variation for Sexual Traits

We investigated the genetic architecture of variation in male sex comb bristle number, a rapidly evolving secondary sexual character of Drosophila. Twenty-four generations of divergent artificial selection for sex comb bristle number in a heterogeneous population of Drosophila melanogaster resulted in a significant response that was more pronounced in the direction of low bristle numbers. We observed a strong positive correlated response to selection in the corresponding female transverse bristle row. The correlated response in male abdominal and sternopleural bristle numbers, on the other hand, did not follow the same pattern as sex comb bristle number differences between selection lines. Relaxation-of-selection experiments along with mate choice and fecundity assays using the selection lines developed demonstrated the action of stabilizing selection on sex comb bristle number. Our results show (1) substantial genetic variation underlying sex comb bristle number variation; (2) a weak relationship between the sex comb and developmentally related, non-sex bristle systems; and (3) that sexual selection may be a driving force in sex comb evolution, indicating the potential of sex combs to diversify rapidly during population differentiation and speciation. We discuss the implications of these results for theories of genetic variation in display and nondisplay male sex traits.

Divergent abdominal bristle patterns in two distantly related drosophilids: antero-posterior variations and sexual dimorphism in a modular trait

The number of neurosensory bristles on abdominal sternites of Drosophila is a most investigated trait for quantitative genetic studies. However, the developmental pattern expressed on successive segments in both sexes has remained so far a neglected field. We explored three aspects of this general problem with an isofemale line design: comparing two distantly related species, Drosophila melanogaster and Zaprionus indianus, investigating bristle number variation along the antero-posterior axis, and analysing the sexual dimorphism. Antero-posterior variations could be analysed from segment A2 to A7 in females, and A2-A5 in males. In D. melanogaster, males and females showed parallel changes with a consistently lower number in males. In Z. indianus females the number was quite stable along the abdomen, while in males an important antero-posterior increase was found. The sexual dimorphism was further analysed by considering the female-male correlation and the female/male ratio. The results suggest that sternite bristle number is determined by several developmental genetic systems. One is acting along the antero-posterior axis and may be associated to a gradient, since the genetic correlation decreases when more distant segments are compared. Another is acting in the same way on most segments of both sexes, since the female-male genetic correlation is similar between homologous and non-homologous segments. Finally, genes with specific sex effects are acting on A7 in females of both species, and on A5 in Z. indianus males. The overall architecture of female and male abdomen seems to be constrained by the development of reproductive organs. A large difference between species suggests, however, that the sexual dimorphism of abdominal bristle number is not evolutionarily constrained.

How Repeatable Are Associations Between Polymorphisms inachaete–scuteand Bristle Number Variation in Drosophila?

Currently, the relevance of common genetic variants--particularly those significantly associated with phenotypic variation in laboratory studies--to standing phenotypic variation in the wild is poorly understood. To address this, we quantified the relationship between achaete-scute complex (ASC) polymorphisms and Drosophila bristle number phenotypes in several new population samples. MC22 is a biallelic, nonrepetitive-length polymorphism 97 bp downstream of the scute transcript. It has been previously shown to be associated with sternopleural bristle number variation in both sexes in a set of isogenic lines. We replicated this association in a large cohort of wild-caught Drosophila melanogaster. We also detected a significant association at MC22 in an outbred population maintained under laboratory conditions for approximately 25 years, but the phenotypic effects in this sample were opposite from the direction estimated in the initial study. Finally, no significant associations were detected in a second large wild-caught cohort or in a set of 134 nearly isogenic lines. Our ability to repeat the initial association in wild samples suggests that it was not spurious. Nevertheless, inconsistent results from the other three panels suggest that the relationship between polymorphic genetic markers and loci contributing to continuous variation is not a simple one.

Phenotypic Variation and Natural Selection at Catsup, a Pleiotropic Quantitative Trait Gene in Drosophila

Quantitative traits are shaped by networks of pleiotropic genes . To understand the mechanisms that maintain genetic variation for quantitative traits in natural populations and to predict responses to artificial and natural selection, we must evaluate pleiotropic effects of underlying quantitative trait genes and define functional allelic variation at the level of quantitative trait nucleotides (QTNs). Catecholamines up (Catsup), which encodes a negative regulator of tyrosine hydroxylase , the rate-limiting step in the synthesis of the neurotransmitter dopamine, is a pleiotropic quantitative trait gene in Drosophila melanogaster. We used association mapping to determine whether the same or different QTNs at Catsup are associated with naturally occurring variation in multiple quantitative traits. We sequenced 169 Catsup alleles from a single population and detected 33 polymorphisms with little linkage disequilibrium (LD). Different molecular polymorphisms in Catsup are independently associated with variation in longevity, locomotor behavior, and sensory bristle number. Most of these polymorphisms are potentially functional variants in protein coding regions, have large effects, and are not common. Thus, Catsup is a pleiotropic quantitative trait gene, but individual QTNs do not have pleiotropic effects. Molecular population genetic analyses of Catsup sequences are consistent with balancing selection maintaining multiple functional polymorphisms.

The Effect of Polymorphisms in the Enhancer of split Gene Complex on Bristle Number Variation in a Large Wild-Caught Cohort of Drosophila melanogaster

The Enhancer of split complex [E(spl)-C] in Drosophila encompasses a variety of functional elements controlling bristle patterning and on the basis of prior work is a strong candidate for harboring alleles having subtle effects on bristle number variation. Here we extend earlier studies identifying associations between complex phenotypes and polymorphisms segregating among inbred laboratory lines of Drosophila and test the influence of E(spl)-C on bristle number variation in a natural cohort. We describe results from an association mapping study using 203 polymorphisms spread throughout the E(spl)-C genotyped in 2000 wild-caught Drosophila melanogaster. Despite power to detect associations accounting for as little as 2% of segregating variation for bristle number, and saturating the region with single-nucleotide polymorphisms (SNPs), we identified no single SNP marker showing a significant (additive over loci) effect after correcting for multiple tests. Using a newly developed test we conservatively identify six regions of the E(spl)-C in which the insertion of transposable elements as a class contributes to variation in bristle number, apparently in a sex- or trait-limited fashion. Finally, we carry out all possible 20,503 two-way tests for epistasis and identify a slight excess of marginally significant interactions, although none survive multiple-testing correction. It may not be straightforward to extend the results of laboratory-based association studies to natural populations.

Drosophilabristles and the nature of quantitative genetic variation

Numbers of Drosophila sensory bristles present an ideal model system to elucidate the genetic basis of variation for quantitative traits. Here, we review recent evidence that the genetic architecture of variation for bristle numbers is surprisingly complex. A substantial fraction of the Drosophila genome affects bristle number, indicating pervasive pleiotropy of genes that affect quantitative traits. Further, a large number of loci, often with sex- and environment-specific effects that are also conditional on background genotype, affect natural variation in bristle number. Despite this complexity, an understanding of the molecular basis of natural variation in bristle number is emerging from linkage disequilibrium mapping studies of individual candidate genes that affect the development of sensory bristles. We show that there is naturally segregating genetic variance for environmental plasticity of abdominal and sternopleural bristle number. For abdominal bristle number this variance can be attributed in part to an abnormal abdomen-like phenotype that resembles the phenotype of mutants defective in catecholamine biosynthesis. Dopa decarboxylase (Ddc) encodes the enzyme that catalyses the final step in the synthesis of dopamine, a major Drosophila catecholamine and neurotransmitter. We found that molecular polymorphisms at Ddc are indeed associated with variation in environmental plasticity of abdominal bristle number.

Identifying Signatures of Selection at the Enhancer of split Neurogenic Gene Complex in Drosophila

The Enhancer of split gene complex (E(spl)-C) is one of the more highly annotated gene regions in Drosophila, and the 12 genes within the complex help determine the spacing and patterning of adult bristles. Any E(spl)-C coding, transcribed, or cis-regulatory regions experiencing nonneutral evolution are strong candidates to harbor polymorphisms contributing to naturally occurring variation in bristle number. We confirm that the E(spl)-C is strongly conserved and show that 74% of regulatory elements previously identified in D. melanogaster are conserved in D. pseudoobscura. Regulatory elements in enhancer regions show lower nucleotide diversity and more rare polymorphisms compared with adjacent nonregulatory DNA, suggesting they are under purifying selection, and these effects are particularly pronounced when considering only conserved regulatory elements. The ratio of polymorphism to divergence was significantly different between binding sites and nonbinding sites for transcription factors within enhancer regions, suggesting the action of some form of selection. Too few polymorphisms in regions of the 3' UTR harboring regulatory motifs prevents adequate comparison of diversity and the polymorphism frequency spectrum between 3' UTR motif and nonmotif sequence. We identified at least two broad regions of the gene complex showing strong population subdivision among four populations, which is suggestive of local adaptation or background selection. Finally, two regions of the E(spl)-C exhibit low nucleotide diversity, a high level of rare polymorphisms, and an increase in linkage disequilibrium, which together suggest the action of positive selection. Notably, the gene m2 shows a significant deviation from neutrality by the McDonald-Kreitman test and resides in one of the two regions putatively experiencing a selective sweep. All sites in regions apparently visible to various selective forces are candidates for future work to determine their phenotypic effects.

A potential regulatory polymorphism upstream of hairy is not associated with bristle number variation in wild-caught Drosophila.

To extend results from laboratory genetic mapping experiments to natural populations it is necessary to estimate the phenotypic effects attributable to laboratory-identified genetic factors in nature. We retested a polymorphism found to be strongly associated with an increase of 0.35 sternopleural bristles in laboratory strains in two large samples of wild-caught Drosophila melanogaster. Despite >90% power to detect effects as low as 0.27 bristles (<1% of the total variation in bristle number) we did not replicate the association in nature. Potential explanations for this result are explored.

Hairy: A quantitative trait locus for drosophila sensory bristle number.

Advances in medicine, agriculture, and an understanding of evolution depend on resolving the genetic architecture of quantitative traits, which is challenging since variation for complex traits is caused by multiple interacting quantitative trait loci (QTL) with small and conditional effects. Here, we show that the key developmental gene, hairy (h), is a QTL for Drosophila sternopleural bristle number, a model quantitative trait. Near-isoallelic lines (NIL) for the h gene region exhibited significant variation in bristle number and failed to complement a hairy mutation. Sequencing 10 h alleles from a single population revealed 330 polymorphic sites in approximately 10 kb. Genotypes for 25 of these and 14 additional sites in the flanking regions were determined for the 57 NIL and associated with variation in bristle number in four genetic backgrounds. A highly significant association was found for a complicated insertion/deletion polymorphism upstream of the transcription start site. This polymorphism, present in 17.5% of the h alleles, was associated with an increase of 0.5 bristle and accounted for 31% of the genetic variance in bristle number in the NIL.

Association of single-nucleotide polymorphisms at the Delta locus with genotype by environment interaction for sensory bristle number in drosophila Melanogaster.

The nature of forces maintaining variation for quantitative traits can only be assessed at the level of individual genes affecting variation in the traits. Identification of single-nucleotide polymorphisms (SNPs) associated with variation in Drosophila sensory bristle number at the Delta (Dl) locus provides us with the opportunity to test a model for the maintenance of variation in bristle number by genotype by environment interaction (GEI). Under this model, genetic variation is maintained at a locus under stabilizing selection if phenotypic values of heterozygotes are more stable than homozygotes across a range of environments, and the mean allelic effect is much smaller than the standard deviation of allelic effects across environments. Homozygotes and heterozygotes for two SNPs at Dl, one affecting sternopleural and the other abdominal bristle number, were reared in five different environments. There was significant GEI for both bristle traits. Neither condition of the model was satisfied for Dl SNPs exhibiting GEI for sternopleural bristle number. Heterozygotes for the abdominal bristle number SNPs were indeed the most stable genotype for two of the three environment pairs exhibiting GEI, but the mean genotypic effect was greater than the standard deviation of effects across environments. Therefore, this mechanism of GEI seems unlikely to be responsible for maintaining the common bristle number polymorphisms at Dl.

Both naturally occurring insertions of transposable elements and intermediate frequency polymorphisms at the achaete-scute complex are associated with variation in bristle number in Drosophila melanogaster.

A restriction enzyme survey of a 110-kb region including the achaete scute complex (ASC) examined 14 polymorphic molecular markers in a sample of 56 naturally occurring chromosomes. Large insertions as a class were associated with a reduction in both sternopleural and abdominal bristle number, supporting deleterious mutation-selection equilibrium models for the maintenance of quantitative genetic variation. Two polymorphic sites were independently associated with variation in bristle number measured in two genetic backgrounds as assessed by a permutation test. A 6-bp deletion near sc alpha is associated with sternopleural bristle number variation in both sexes and a 3.4-kb insertion between sc beta and sc gamma is associated with abdominal bristle number variation in females. Under an additive genetic model, the small deletion polymorphism near sc alpha accounts for 25% of the total X chromosome genetic variation in sternopleural bristle number, and the 3.4 kb insertion accounts for 22% of the total X chromosome variation in female abdominal bristle number. The observation of common polymorphisms associated with variation in bristle number is more parsimoniously explained by models that incorporate balancing selection or assume variants affecting bristle number are neutral, than mutation-selection equilibrium models.

Linkage disequilibrium mapping of molecular polymorphisms at the scabrous locus associated with naturally occurring variation in bristle number in Drosophila melanogaster.

We evaluated the hypothesis that the Drosophila melanogaster second chromosome gene scabrous (sca), a candidate sensory bristle number quantitative trait locus (QTL), contributes to naturally occurring variation in bristle number. Variation in abdominal and sternopleural bristle number was quantified for wild-derived sca alleles in seven genetic backgrounds: as homozygous second chromosomes (C2) in an isogenic background, homozygous lines in which approximately 20 cM including the sca locus had been introgressed into the isogenic background (sca BC), as C2 and sca BC heterozygotes and hemizygotes against a P element insertional sca allele and a P-induced sca deficiency in the same isogenic background, and as sca BC heterozygotes against the wild-type sca allele of isogenic strain. Molecular restriction map variation was determined for a 45 kb region including the sca locus, and single-stranded conformational polymorphism (SSCP) was examined for the third intron and parts of the third and fourth exons. Associations between each of the 27 molecular polymorphisms and bristle number were evaluated within each genotype and on the first principal component score determined from all seven genotypes, separately for each sex and bristle trait. Permutation tests were used to assess the empirical significance thresholds, accounting for multiple, correlated tests, and correlated markers. Three sites in regulatory regions were associated with female-specific variation in abdominal bristle number, one of which was an SSCP site in the region of the gene associated with regulation of sca in embryonic abdominal segments.

The Genetic Architecture of Selection Response: Inferences From Fine-Scale Mapping of Bristle Number Quantitative Trait Loci in Drosophila melanogaster

Quantitative trait loci (QTL) affecting responses and correlated responses to selection for abdominal and sternopleural bristle number have been mapped with high resolution to the X and third chromosomes. Advanced intercross recombinant isogenic chromosomes were constructed from high and low selection lines in an unselected inbred background, and QTL were detected using composite interval mapping and high density transposable element marker maps. We mapped a total of 26 bristle number QTL with large effects, which were in or immediately adjacent to intervals previously inferred to contain bristle number QTL on these chromosomes. The QTL contributing to response to selection for high bristle number were not the same as those contributing to response to selection for low bristle number, suggesting that distributions of allelic effects per locus may be asymmetrical. Correlated responses were more often attributable to loose linkage than pleiotropy or close linkage. Bristle number QTL mapping to the same locations have been inferred in studies with different parental strains. Of the 26 QTL, 20 mapped to locations consistent with candidate genes affecting peripheral nervous system development and/or bristle number. This facilitates determining the molecular basis of quantitative variation and allele frequencies by associating molecular variation at the candidate genes with phenotypic variation in bristle number in samples of alleles from nature.

Two sites in the Delta gene region contribute to naturally occurring variation in bristle number in Drosophila melanogaster.

A restriction enzyme survey of a 57-kb region including the gene Delta uncovered 53 polymorphic molecular markers in a sample of 55 naturally occurring chromosomes. A permutation test, which assesses the significance of the molecular marker with the largest effect on bristle variation in four genetic backgrounds relative to permuted data-sets, found two sites that were independently associated with variation in bristle number. A common site in the second intron of Delta affected only sternopleural bristle number, and another common site in the fifth intron affected only abdominal bristle number in females. Under an additive genetic model, the polymorphism in the second intron may account for 12% of the total genetic variation in sternopleural bristle number due to third chromosomes, and the site in the fifth intron may account for 6% of the total variation in female abdominal bristle number due to the third chromosomes. These results suggest the following: (1) models that incorporate balancing selection are more consistent with observations than deleterious mutation-selection equilibrium models, (2) mapped quantitative trait loci of large effect may not represent a single variable site at a genetic locus, and (3) linkage disequilibrium can be used as a tool for understanding the molecular basis of quantitative variation.

Genetic interactions between naturally occurring alleles at quantitative trait loci and mutant alleles at candidate loci affecting bristle number in Drosophila melanogaster.

Previously, we mapped quantitative trait loci (QTL) affecting response to short-term selection for abdominal bristle number to seven suggestive regions that contain loci involved in bristle development and/or that have adult bristle number mutant phenotypes, and are thus candidates for bristle number QTL in natural populations. To test the hypothesis that the factors contributing to selection response genetically interact with these candidate loci, high and low chromosomes from selection lines were crossed to chromosomes containing wild-type or mutant alleles at the candidate loci, and the numbers of bristles were recorded in trans heterozygotes. Quantitative failure to complement, detected as a significant selection line*cross effect by analysis of variance, can be interpreted as evidence for allelism or epistasis between the factors on selected chromosomes and the candidate loci. Mutations at some candidate loci (bb, emc, h, Dl, Hairless) showed strong interactions with selected chromosomes, whereas others interacted weakly (ASC, abd, Scr) or not at all (N, mab, E(spl)). These results support the hypothesis that some candidate loci, initially identified through mutations of large effect on bristle number, either harbor or are close members in the same genetic pathway as variants that contribute to standing variation in bristle number.

Naturally occurring variation in bristle number and DNA polymorphisms at the scabrous locus of Drosophila melanogaster.

The association between quantitative genetic variation in bristle number and molecular variation at a candidate neurogenic locus, scabrous, was examined in Drosophila melanogaster. Approximately 32 percent of the genetic variation in abdominal bristle number (21 percent for sternopleural bristle number) among 47 second chromosomes from a natural population was correlated with DNA sequence polymorphisms at this locus. Several polymorphic sites associated with large phenotypic effects occurred at intermediate frequency. Quantitative genetic variation in natural populations caused by alleles that have large effects at a few loci and that segregate at intermediate frequencies conflicts with the classical infinitesimal model of the genetic basis of quantitative variation.

Molecular and phenotypic variation in the achaete-scute region of Drosophila melanogaster

Variation in quantitative characters underlies much adaptive evolution and provides the basis for selective improvement of domestic species, yet the genetic nature of quantitative variation is poorly understood. Many loci affecting quantitative traits have been identified by the segregation of mutant alleles with major qualitative effects. These alleles may represent an extreme of a continuum of allelic effects, and most quantitative variation could result from the segregation of alleles with subtle effects at loci identified by alleles with major effects. The achaete-scute complex in Drosophila melanogaster plays a central part in bristle development and has been characterized at the molecular level. The hypothesis that naturally occurring quantitative variation in bristle number could be associated with wild-type alleles of achaete-scute was tested by correlating phenotypic variation in bristle number with molecular variation in restriction maps in this region among chromosomes extracted from natural populations. DNA insertion variation in the achaete-scute region was found to be strongly associated with variation in bristle number.

Temperature-sensitive mutations in Drosophila melanogaster: XIII. Temperature-sensitive periods of the lethal and morphological phenotypes of selected combinations of notch-locus mutations

Temperature-shift experiments were performed on five Notch-locus genotypes with temperature-sensitive phenotypes. The results show that temperature-sensitive periods (TSPs) for lethality may occur at any developmental stage: (1) N g11 N g11 ; Dp 51 b7 having a short embryonic TSP for lethality, (2) Ax 16172 N −40 having a second-instar TSP for lethality, and (3) N −103 fa no with a long, possibly polyphasic, TSP, beginning in the embryonic stage and ending in the pupal stage. On the other hand, TSPs for adult morphological phenotypes appear to be restricted to the third larval instar: (1) Ax 16172 N −40 having third-instar TSPs for wing vein gapping and ocellar bristle loss, and (2) N −103 spl having third-instar TSPs for eye facet disarray, wing notching, bristle number variation, and fusion of tarsal segments. The significance of these results is discussed in terms of the role of the Notch locus in development.

Selection for a threshold character inDrosophilaII. Homeostatic behaviour on relaxation of selection

This paper is concerned with three related aspects of the behaviour of populations under artificial selection for increased scutellar bristle number: (i) the pattern of response on the probit scale; (ii) the homeostatic behaviour of the selection lines on relaxation of artificial selection; and (iii) correlated responses in generation interval, reproductive capacity and competitive ability. The study was designed so that linkage would be a comparatively unimportant factor in promoting correlated responses to selection, and the effects of genetic sampling from generation to generation were also reduced to a low level.Progress from the base mean of 4·05 bristles in females to a level of almost 8 bristles has been shown to involve two distinct phases with realized heritabilities of 0·34 and 0·10 respectively, the zone of transition corresponding closely to the position of the 6/7 threshold on the underlying scale. In addition to an apparent average reduction of about 25% in the additive genetic standard deviation in phase II by comparison with phase I, the loss in response due to the opposition of natural selection has been shown to reach a maximum near the zone of separation of the two phases.The pattern of behaviour of the populations under artificial and natural selection has suggested the presence in the base population of genes of large effect on both bristle number and reproductive fitness. There is also evidence of additional genetic variation in bristle number which is effectively neutral with respect to fitness. Continued selection for increased scutellar bristle number in large populations has been shown to reduce mean competitive ability by more than 80%.