Odorant Receptor Polymorphisms and Natural Variation in Olfactory Behavior in <i>Drosophila melanogaster</i>

Rollmann, Stephanie M.; Wang, Ping; Date, Priya; West, Steven A.; Mackay, Trudy F. C.; Anholt, Robert R. H.

doi:10.1534/genetics.110.119446

Cited by 44 publications

(47 citation statements)

References 62 publications

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“…In a previous study on D. mojavensis, host-specific behavioural responses were observed to a mixture of host plant volatiles and not recapitulated with single compounds alone [25]. Moreover, in D. melanogaster variation in behavioural responses to single compounds are associated with polymorphisms in several receptors [47,48]. Therefore, it is likely that multiple receptors play a role in host preference behaviour in this system.…”

Section: Discussionmentioning

confidence: 85%

Population differences in olfaction accompany host shift in Drosophila mojavensis

et al. 2016

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Evolutionary shifts in plant -herbivore interactions provide a model for understanding the link among the evolution of behaviour, ecological specialization and incipient speciation. Drosophila mojavensis uses different host cacti across its range, and volatile chemicals emitted by the host are the primary cue for host plant identification. In this study, we show that changes in host plant use between distinct D. mojavensis populations are accompanied by changes in the olfactory system. Specifically, we observe differences in olfactory receptor neuron specificity and sensitivity, as well as changes in sensillar subtype abundance, between populations. Additionally, RNA-seq analyses reveal differential gene expression between populations for members of the odorant receptor gene family. Hence, alterations in host preference are associated with changes in development, regulation and function at the olfactory periphery.

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Section: Discussionmentioning

confidence: 85%

Population differences in olfaction accompany host shift in Drosophila mojavensis

et al. 2016

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“…Before the availability of complete genome sequences for the DGRP lines, association studies for olfactory behavior focused on a few Or and Obp genes (26)(27)(28)(29). Here, we identified SNPs associated with variation in olfactory behavioral response to benzaldehyde across the entire genome using three different GWA analyses.…”

Section: Discussionmentioning

confidence: 99%

Analysis of natural variation reveals neurogenetic networks forDrosophilaolfactory behavior

Swarup

Huang

Mackay

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

104

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Understanding the relationship between genetic variation and phenotypic variation for quantitative traits is necessary for predicting responses to natural and artificial selection and disease risk in human populations, but is challenging because of large sample sizes required to detect and validate loci with small effects. Here, we used the inbred, sequenced, wild-derived lines of the Drosophila melanogaster Genetic Reference Panel (DGRP) to perform three complementary genome-wide association (GWA) studies for natural variation in olfactory behavior. The first GWA focused on single nucleotide polymorphisms (SNPs) associated with mean differences in olfactory behavior in the DGRP, the second was an extreme quantitative trait locus GWA on an outbred advanced intercross population derived from extreme DGRP lines, and the third was for SNPs affecting the variance among DGRP lines. No individual SNP in any analysis was associated with variation in olfactory behavior by using a strict threshold accounting for multiple tests, and no SNP overlapped among the analyses. However, combining the top SNPs from all three analyses revealed a statistically enriched network of genes involved in cellular signaling and neural development. We used mutational and gene expression analyses to validate both candidate genes and network connectivity at a high rate. The lack of replication between the GWA analyses, small marginal SNP effects, and convergence on common cellular networks were likely attributable to epistasis. These results suggest that fully understanding the genotype-phenotype relationship requires a paradigm shift from a focus on single SNPs to pathway associations.genetic architecture | chemosensation | behavioral genetics U nderstanding the rules by which variation in primary DNA sequence impacts variation for quantitative traits in natural populations is critical for predicting responses to natural and artificial selection and disease risk in human populations. The emerging picture from large genome-wide association (GWA) studies in human populations is that many common variants with individually small marginal (additive) effects affect diseases and quantitative traits, of which only a small fraction can be replicated across populations (1, 2). Although it is possible that effects of common single nucleotide polymorphisms (SNPs) underestimate the true effects because causal variants are not common or not SNPs, and lack of replication is due to differences in allele frequency and pattern of linkage disequilibrium (LD) (1, 2), it is also possible that small additive effects and lack of replication are due to underlying epistatic interactions (3, 4).Extremely large samples are required to determine individual significance of rare alleles and epistatic interactions. One approach to gaining biological insight from GWA studies in the absence of statistical significance of individual SNPs is functional evaluation of genes harboring the top SNPs regardless of individual significance. A second approach is to consider the genes w...

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“…The combinatorial coding of odorants through the activation of multiple receptors and ORNs is supported by an analysis of three Ors in adult Drosophila (107). Polymorphisms in all three of these genes were associated with variation in behavioral response to benzaldehyde.…”

Section: Mechanisms Of Insect Olfactionmentioning

confidence: 92%

Insect olfaction from model systems to disease control

Carey

Carlson

2011

Proc. Natl. Acad. Sci. U.S.A.

191

172

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Great progress has been made in the field of insect olfaction in recent years. Receptors, neurons, and circuits have been defined in considerable detail, and the mechanisms by which they detect, encode, and process sensory stimuli are being unraveled. We provide a guide to recent progress in the field, with special attention to advances made in the genetic model organism Drosophila. We highlight key questions that merit additional investigation. We then present our view of how recent advances may be applied to the control of diseasecarrying insects such as mosquitoes, which transmit disease to hundreds of millions of people each year. We suggest how progress in defining the basic mechanisms of insect olfaction may lead to means of disrupting host-seeking and other olfactory behaviors, thereby reducing the transmission of deadly diseases.olfactory coding | odorant receptor | olfactory circuits | vector biology | pheromone T he insect olfactory system has emerged as a prominent model in neuroscience. Investigation of its organization and function has revealed surprising answers to fundamental questions of how an animal detects, encodes, and processes sensory stimuli. The olfactory system is also of immense importance in the natural world, where it mediates attraction of insects to humans and thus underlies the transmission of disease to hundreds of millions of people each year.Remarkable progress has been made over the past decade in elucidating mechanisms of insect olfaction, in many cases facilitated by the genetic tractability of the model organism Drosophila melanogaster. Here, we consider recent advances in the understanding of insect olfactory receptors, neurons, and circuits made in Drosophila and other insect species. We present our view that this emerging body of knowledge poises the field to make major contributions to the control of insect pests and vectors of disease, and we highlight strategies for olfactory-based vector control. We offer our perspective on the most critical challenges to fulfilling this technological promise and to solving the scientific problem of how olfactory input is translated into behavioral output.

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Odorant Receptor Polymorphisms and Natural Variation in Olfactory Behavior in Drosophila melanogaster

Cited by 44 publications

References 62 publications

Population differences in olfaction accompany host shift in Drosophila mojavensis

Population differences in olfaction accompany host shift in Drosophila mojavensis

Analysis of natural variation reveals neurogenetic networks forDrosophilaolfactory behavior

Insect olfaction from model systems to disease control

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