Seasonal fluctuation in susceptibility to insecticides within natural populations of Drosophila melanogaster. Empirical observations of fitness costs of insecticide resistance.

AbstractInsecticide resistance is a paradigm of microevolution and insecticides are responsible for the strongest cases of recent selection in the genome of Drosophila melanogaster. Here we use a naïve population and a novel insecticide class to examine the ab initio genetic architecture of a potential selective response. Genome wide association studies of chlorantraniliprole susceptibility reveal variation in a gene of major effect, Stretchin Myosin light chain kinase (Strn-Mlck), which we validate with linkage mapping and transgenic manipulation of gene expression. We propose that allelic variation in Strn-Mlck alters sensitivity to the calcium depletion attributable to chlorantraniliprole’s mode of action. Genome-wide association studies also reveal a network of genes involved in neuromuscular biology. In contrast, phenotype to transcriptome associations identify differences in constitutive levels of multiple transcripts regulated by cnc, the homologue of mammalian Nrf2. This suggests that genetic variation acts in trans to regulate multiple metabolic enzymes in this pathway. The most outstanding association is with the transcription level of Cyp12d1 which is also affected in cis by copy number variation. Transgenic overexpression of Cyp12d1 reduces susceptibility to both chlorantraniliprole and the closely related insecticide cyantraniliprole. This systems genetics study reveals multiple allelic variants segregating at intermediate frequency in a population that is completely naïve to this new insecticide chemistry and it adumbrates a selective response among natural populations to these chemicals.SignificanceAround the world insecticides are being deregistered and banned, as their environmental costs are deemed too great or their efficacy against pest insects is reduced through the evolution of insecticide resistance. With the introduction of replacement insecticides comes the responsibility to assess the way new insecticides perturb various levels of biological systems; from insect physiology to ecosystems. We used a systems genetics approach to identify genetic variants affecting survivorship of Drosophila melanogaster exposed to chlorantraniliprole. The study population was completely naïve to this insecticide chemistry and yet we find associations with variants in neuromuscular genes and co-regulated detoxification genes. We predict that these variants will increase in populations of this ‘sentinel species’ as these insecticides are applied in the environment.

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Faculty Opinions recommendation of Identification of Mob2, a novel regulator of larval neuromuscular junction morphology, in natural populations of Drosophila melanogaster.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.718087215.793483743 ◽

2013 ◽

Author(s):

J Troy Littleton ◽

Kathryn Harris

Keyword(s):

Drosophila Melanogaster ◽

Neuromuscular Junction ◽

Natural Populations ◽

Larval Neuromuscular Junction

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Meiotic Drive in Natural Populations of Drosophila melanogaster. VI. A Preliminary Report on the Presence of Segregation-Distortion in a Baja California Population

The American Naturalist ◽

10.1086/282162 ◽

1961 ◽

Vol 95 (881) ◽

pp. 87-96 ◽

Cited By ~ 3

Author(s):

Elaine Johansen Mange

Keyword(s):

Drosophila Melanogaster ◽

Segregation Distortion ◽

Preliminary Report ◽

Baja California ◽

Natural Populations ◽

Meiotic Drive ◽

California Population

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Female Genotypes Affect Sperm Displacement in Drosophila

Genetics ◽

10.1093/genetics/149.3.1487 ◽

1998 ◽

Vol 149 (3) ◽

pp. 1487-1493 ◽

Cited By ~ 6

Author(s):

Andrew G Clark ◽

David J Begun

Keyword(s):

Drosophila Melanogaster ◽

Genetic Variation ◽

Natural Populations ◽

Isogenic Line ◽

Female Fitness ◽

Sperm Displacement ◽

Extensive Variation ◽

Polymorphic Genes ◽

Displacement Parameter ◽

Competitive Success

Abstract Differential success of sperm is likely to be an important component of fitness. Extensive variation among male genotypes in competitive success of sperm in multiply mated females has been documented for Drosophila melanogaster. However, virtually all previous studies considered the female to be a passive vessel. Nevertheless, under certain conditions female fitness could be determined by her role in mediating use of sperm from multiple males. Here we ask whether females differ among genotypes in their tendency to exhibit last-male precedence. Competition of sperm from two tester male genotypes (bwD and B3-09, a third-chromosome isogenic line from Beltsville, MD) was quantified by doubly mating female lines that had been rendered homozygous for X, second, or third chromosomes isolated from natural populations. The composite sperm displacement parameter, P2′, was highly heterogeneous among lines, whether or not viability effects were compensated, implying the presence of polymorphic genes affecting access of sperm to eggs. Genetic variation of this type is completely neutral in the absence of pleiotropy or interaction between variation in the two sexes.

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The Regulatory Properties of Autonomous Subtelomeric P Elements Are Sensitive to a Suppressor of variegation in Drosophila melanogaster

Genetics ◽

10.1093/genetics/143.4.1663 ◽

1996 ◽

Vol 143 (4) ◽

pp. 1663-1674 ◽

Cited By ~ 3

Author(s):

Stéphane Ronsseray ◽

Monique Lehmann ◽

Danielle Nouaud ◽

Dominique Anxolabéhère

Keyword(s):

Drosophila Melanogaster ◽

Genetic Recombination ◽

Natural Populations ◽

P Element ◽

Single Element ◽

Heterochromatin Protein 1 ◽

X Chromosomes ◽

P Elements ◽

Associated Sequences ◽

Regulatory Properties

Abstract Genetic recombination was used in Drosophila melanogaster to isolate P elements, inserted at the telomeres of X chromosomes (cytological site 1A) from natural populations, in a genetic background devoid of other P elements. We show that complete maternally inherited P repression in the germline (P cytotype) can be elicited by only two autonomous P elements at 1A and that a single element at this site has partial regulatory properties. The analysis of the surrounding chromosomal regions of the P elements at 1A shows that in all cases these elements are flanked by Telomeric Associated Sequences, tandemly repetitive noncoding sequences that have properties of heterochromatin. In addition, we show that the regulatory properties of P elements at 1A can be inhibited by some of the mutant alleles of the Su(var)205 gene and by a deficiency of this gene. However, the regulatory properties of reference P strains (Harwich and Texas 007) are not impaired by Su(var)205 mutations. Su(var)205 encodes Heterochromatin Protein 1 (HP1). These results suggest that the HP1 dosage effect on the P element properties is sitedependent and could involve the structure of the chromatin.

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GENETIC AND BIOCHEMICAL BASIS OF ENZYME ACTIVITY VARIATION IN NATURAL POPULATIONS. I. ALCOHOL DEHYDROGENASE IN DROSOPHILA MELANOGASTER

Genetics ◽

10.1093/genetics/89.2.371 ◽

1978 ◽

Vol 89 (2) ◽

pp. 371-388

Author(s):

John F McDonald ◽

Francisco J Ayala

Keyword(s):

Gene Regulation ◽

Drosophila Melanogaster ◽

Alcohol Dehydrogenase ◽

Natural Populations ◽

Difficult Problem ◽

Regulatory Genes ◽

Biochemical Basis ◽

Evolutionary Consequence ◽

The Third ◽

Adh Activity

ABSTRACT Recent studies by various authors suggest that variation in gene regulation may be common in nature, and might be of great evolutionary consequence; but the ascertainment of variation in gene regulation has proven to be a difficult problem. In this study, we explore this problem by measuring alcohol dehydrogenase (ADH) activity in Drosophila melanogaster strains homozygous for various combinations of given second and third chromosomes sampled from a natural population. The structural locus (Adh) coding for ADH is on the second chromosome. The results show that: (1) there are genes, other than Adh, that affect the levels of ADH activity; (2) at least some of these "regulatory" genes are located on the third chromosome, and thus are not adjacent to the Adh locus; (3) variation exists in natural populations for such regulatory genes; (4) the effect of these regulatory genes varies as they interact with different second chromosomes; (5) third chromosomes with high-activity genes are either partially or completely dominant over chromosomes with low-activity genes; (6) the effects of the regulatory genes are pervasive throughout development; and (7) the third chromosome genes regulate the levels of ADH activity by affecting the number of ADH molecules in the flies. The results are consistent with the view that the evolution of regulatory genes may play an important role in adaptation.

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GENETIC LOAD IN NATURAL POPULATIONS: IS IT COMPATIBLE WITH THE HYPOTHESIS THAT MANY POLYMORPHISMS ARE MAINTAINED BY NATURAL SELECTION?

Genetics ◽

10.1093/genetics/77.3.569 ◽

1974 ◽

Vol 77 (3) ◽

pp. 569-589

Author(s):

Martin L Tracey ◽

Francisco J Ayala

Keyword(s):

Drosophila Melanogaster ◽

Natural Selection ◽

Natural Population ◽

Natural Populations ◽

Genetic Load ◽

Structural Genes ◽

Invertebrate Species ◽

Average Proportion ◽

Mean Fitness ◽

The Mean

ABSTRACT Recent studies of genetically controlled enzyme variation lead to an estimation that at least 30 to 60% of the structural genes are polymorphic in natural populations of many vertebrate and invertebrate species. Some authors have argued that a substantial proportion of these polymorphisms cannot be maintained by natural selection because this would result in an unbearable genetic load. If many polymorphisms are maintained by heterotic natural selection, individuals with much greater than average proportion of homozygous loci should have very low fitness. We have measured in Drosophila melanogaster the fitness of flies homozygous for a complete chromosome relative to normal wild flies. A total of 37 chromosomes from a natural population have been tested using 92 experimental populations. The mean fitness of homozygous flies is 0.12 for second chromosomes, and 0.13 for third chromosomes. These estimates are compatible with the hypothesis that many (more than one thousand) loci are maintained by heterotic selection in natural populations of D. melanogaster.

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Molecular Evolution of Duplicated Amylase Gene Regions in Drosophila melanogaster: Evidence of Positive Selection in the Coding Regions and Selective Constraints in the cis-Regulatory Regions

Genetics ◽

10.1093/genetics/157.2.667 ◽

2001 ◽

Vol 157 (2) ◽

pp. 667-677

Author(s):

Hitoshi Araki ◽

Nobuyuki Inomata ◽

Tsuneyuki Yamazaki

Keyword(s):

Drosophila Melanogaster ◽

Molecular Evolution ◽

Positive Selection ◽

Natural Populations ◽

Sliding Window ◽

Selective Constraint ◽

Proximal Region ◽

Coding Regions ◽

Asian Populations ◽

Flanking Region

Abstract In this study, we randomly sampled Drosophila melanogaster from Japanese and Kenyan natural populations. We sequenced duplicated (proximal and distal) Amy gene regions to test whether the patterns of polymorphism were consistent with neutral molecular evolution. Fst between the two geographically distant populations, estimated from Amy gene regions, was 0.084, smaller than reported values for other loci, comparing African and Asian populations. Furthermore, little genetic differentiation was found at a microsatellite locus (DROYANETSB) in these samples (Gst′=−0.018). The results of several tests (Tajima's, Fu and Li's, and Wall's tests) were not significantly different from neutrality. However, a significantly higher level of fixed replacement substitutions was detected by a modified McDonald and Kreitman test for both populations. This indicates that positive selection occurred during or immediately after the speciation of D. melanogaster. Sliding-window analysis showed that the proximal region 1, a part of the proximal 5′ flanking region, was conserved between D. melanogaster and its sibling species, D. simulans. An HKA test was significant when the proximal region 1 was compared with the 5′ flanking region of Alcohol dehydrogenase (Adh), indicating a severe selective constraint on the Amy proximal region 1. These results suggest that natural selection has played an important role in the molecular evolution of Amy gene regions in D. melanogaster.

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