Socially-Responsive Gene Expression in Male<i>Drosophila melanogaster</i>Is Influenced by the Sex of the Interacting Partner

Ellis, Lisa L.; Carney, Ginger E.

doi:10.1534/genetics.110.122754

Cited by 43 publications

(41 citation statements)

References 72 publications

(95 reference statements)

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“…The aim was to capture a broad sweep across the phenotypic expression of responses to conspecific rivals. Based on previous research by us and others, we chose the 2 h time point to capture initial gene expression responses prior to the expression of any phenotypic responses, 26 h as the point at which we know males have passed a threshold of significant phenotypic responses to rivals, and 50 h to capture any longer-term changes at a point where the phenotypic responses appear to have ceased (Carney 2007;Bretman et al 2009Bretman et al , 2010Ellis and Carney 2011;Fedorka et al 2011). An additional, important justification for these three time points was the need to avoid strong interactions with circadian effects on gene expression (by sampling cohorts of flies for gene expression analysis at the same absolute time of day, i.e., after 2 h, then 24 h later at 26 h of exposure, and finally a further 24 h later at 50 h of exposure).…”

Section: Resultsmentioning

confidence: 99%

“…The prediction of observable transcriptional changes in response to the social and sexual environment is supported by previous research. For example, short-term (<20 min) exposure of males to females or other males can alter the transcription of spermatogenesis and odor perception genes (Carney 2007;Ellis and Carney 2011). Males exposed to other males for up to 72 h also show differential expression (DE) in two of three seminal fluid protein genes (but not in four testis genes) tested (Fedorka et al 2011).…”

Section: Introductionmentioning

confidence: 99%

“…The latter is crucial to resolve signatures of tissue-specific responses and avoid "swamping" of subtle signals (Chintapalli et al 2007). Our design to profile gene expression responses to rivals for 0-2 d offered the opportunity for comparisons with these previous studies (Carney 2007;Ellis and Carney 2011).…”

Section: Introductionmentioning

confidence: 99%

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Genomic responses to the socio-sexual environment in male Drosophila melanogaster exposed to conspecific rivals

Mohorianu

Bretman

Smith

et al. 2017

RNA

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Socio-sexual environments have profound effects on fitness. Local sex ratios can alter the threat of sexual competition, to which males respond via plasticity in reproductive behaviors and ejaculate composition. In Drosophila melanogaster, males detect the presence of conspecific, same-sex mating rivals prior to mating using multiple, redundant sensory cues. Males that respond to rivals gain significant fitness benefits by altering mating duration and ejaculate composition. Here we investigated the underlying genome-wide changes involved. We used RNA-seq to analyze male transcriptomic responses 2, 26, and 50 h after exposure to rivals, a time period that was previously identified as encompassing the major facets of male responses to rivals. The results showed a strong early activation of multiple sensory genes in the head-thorax (HT), prior to the expression of any phenotypic differences. This gene expression response was reduced by 26 h, at the time of maximum phenotypic change, and shut off by 50 h. In the abdomen (A), fewer genes changed in expression and gene expression responses appeared to increase over time. The results also suggested that different sets of functionally equivalent genes might be activated in different replicates. This could represent a mechanism by which robustness is conferred upon highly plastic traits. Overall, our study reveals that mRNA-seq can identify subtle genomic signatures characteristic of flexible behavioral phenotypes.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Genomic responses to the socio-sexual environment in male Drosophila melanogaster exposed to conspecific rivals

Mohorianu

Bretman

Smith

et al. 2017

RNA

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“…These slight variations in timelines were required to keep mouse and stickleback experiments consistent with previously published protocols (8,43,67,68). The protocol for honey bee was novel, so we followed the stickleback timeline because expression differences for IEGs and other socially responsive genes are generally best detected 30 min poststimulus (69,70). We sampled three individuals per treatment for mouse and stickleback and six groups per treatment for honey bees.…”

Section: Methodsmentioning

confidence: 99%

Neuromolecular responses to social challenge: Common mechanisms across mouse, stickleback fish, and honey bee

Rittschof

Bukhari

Sloofman

et al. 2014

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

141

196

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Certain complex phenotypes appear repeatedly across diverse species due to processes of evolutionary conservation and convergence. In some contexts like developmental body patterning, there is increased appreciation that common molecular mechanisms underlie common phenotypes; these molecular mechanisms include highly conserved genes and networks that may be modified by lineage-specific mutations. However, the existence of deeply conserved mechanisms for social behaviors has not yet been demonstrated. We used a comparative genomics approach to determine whether shared neuromolecular mechanisms could underlie behavioral response to territory intrusion across species spanning a broad phylogenetic range: house mouse (Mus musculus), stickleback fish (Gasterosteus aculeatus), and honey bee (Apis mellifera). Territory intrusion modulated similar brain functional processes in each species, including those associated with hormone-mediated signal transduction and neurodevelopment. Changes in chromosome organization and energy metabolism appear to be core, conserved processes involved in the response to territory intrusion. We also found that several homologous transcription factors that are typically associated with neural development were modulated across all three species, suggesting that shared neuronal effects may involve transcriptional cascades of evolutionarily conserved genes. Furthermore, immunohistochemical analyses of a subset of these transcription factors in mouse again implicated modulation of energy metabolism in the behavioral response. These results provide support for conserved genetic "toolkits" that are used in independent evolutions of the response to social challenge in diverse taxa.genetic hotspot | NF-κB signaling | brain metabolism | aggression S imilar phenotypes can have a shared molecular basis, even among distantly related species (1-3). This phenomenon has been observed for an array of traits, including morphological adaptations like coat color or wing patterning, rapid adaptations like drug resistance, and artificially selected phenological traits like flowering time (reviewed in ref. 2). Shared molecular mechanisms can arise convergently as a result of de novo mutations at genetic hotspots (2) or as a result of conservation. Both of these processes result in "genetic toolkits" or genes that are repeatedly used over evolutionary time to give rise to similar phenotypes (3). The phenomenon of genetic toolkits challenges fundamental notions about evolutionary convergence, conservation, and the origins of biodiversity.The role of genetic toolkits in shaping behavioral phenotypes is unclear (4, 5). Behaviors are typically polygenic (6) and they show great nuance and plasticity within a species, raising the possibility that cross-species similarities in behavior are superficial. Social behaviors in particular present a challenge to the genetic toolkit concept: these behaviors are critical to survival and reproductive success, but across species there is significant variation in the contexts for an...

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“…Consistent with this observation, one of the strongest LA cline outliers, egh, has been conclusively linked to strong effects on male courtship behavior using a variety of genetic techniques [79]. Additionally, gene knockouts of CG43759, another LA cline outlier locus, have strong effects on inter-male aggressive behavior [80], and may also contribute to behavioral differences between admixed individuals.…”

Section: Candidate Behavioral Reproductive Isolation Genesmentioning

confidence: 62%

A hidden Markov model approach for simultaneously estimating local ancestry and admixture time using next generation sequence data in samples of arbitrary ploidy

Corbett-Detig

Nielsen

2016

Preprint

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Admixture-the mixing of genomes from divergent populations-is increasingly appreciated as a central process in evolution. To characterize and quantify patterns of admixture across the genome, a number of methods have been developed for local ancestry inference. However, existing approaches have a number of shortcomings. First, all local ancestry inference methods require some prior assumption about the expected ancestry tract lengths. Second, existing methods generally require genotypes, which is not feasible to obtain for many nextgeneration sequencing projects. Third, many methods assume samples are diploid, however a wide variety of sequencing applications will fail to meet this assumption. To address these issues, we introduce a novel hidden Markov model for estimating local ancestry that models the read pileup data, rather than genotypes, is generalized to arbitrary ploidy, and can estimate the time since admixture during local ancestry inference. We demonstrate that our method can simultaneously estimate the time since admixture and local ancestry with good accuracy, and that it performs well on samples of high ploidy-i.e. 100 or more chromosomes. As this method is very general, we expect it will be useful for local ancestry inference in a wider variety of populations than what previously has been possible. We then applied our method to pooled sequencing data derived from populations of Drosophila melanogaster on an ancestry cline on the east coast of North America. We find that regions of local recombination rates are negatively correlated with the proportion of African ancestry, suggesting that selection against foreign ancestry is the least efficient in low recombination regions. Finally we show that clinal outlier loci are enriched for genes associated with gene regulatory functions, consistent with a role of regulatory evolution in ecological adaptation of admixed D. melanogaster populations. Our results illustrate the potential of local ancestry inference for elucidating fundamental evolutionary processes. Data Availability Statement:No novel data were produced for this work. Short read data analyzed in this work are all available through the NCBI short read trace archive under project accession number PRJNA256231.Funding: RCD was supported by a Chancellor's Postdoctoral Fellowship during this work. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Author SummaryWhen divergent populations hybridize, their offspring obtain portions of their genomes from each parent population. Although the average ancestry proportion in each descendant is equal to the proportion of ancestors from each of the ancestral populations, the contribution of each ancestry type is variable across the genome. Estimating local ancestry within admixed individuals is a fundamental goal for evolutionary genetics, and here we develop a method for doing this that circumvents many of the problems associated with existing methods. Briefly, our method c...

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Socially-Responsive Gene Expression in MaleDrosophila melanogasterIs Influenced by the Sex of the Interacting Partner

Cited by 43 publications

References 72 publications

Genomic responses to the socio-sexual environment in male Drosophila melanogaster exposed to conspecific rivals

Genomic responses to the socio-sexual environment in male Drosophila melanogaster exposed to conspecific rivals

Neuromolecular responses to social challenge: Common mechanisms across mouse, stickleback fish, and honey bee

A hidden Markov model approach for simultaneously estimating local ancestry and admixture time using next generation sequence data in samples of arbitrary ploidy

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