Dynamic, mating-induced gene expression changes in female head and brain tissues of Drosophila melanogaster

Dalton, Justin E.; Kacheria, Tanvi S; Knott, Simon; Lebo, Matthew S.; Nishitani, Allison M.; Sanders, Laura E.; Stirling, Emma J; Winbush, Ari; Arbeitman, Michelle N.

doi:10.1186/1471-2164-11-541

Cited by 62 publications

(82 citation statements)

References 59 publications

(120 reference statements)

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“…As with previous studies (Lawniczak and Begun 2004;McGraw et al 2004McGraw et al , 2008Mack et al 2006;Kocher et al 2008;Dalton et al 2010;Smith et al 2013) there is substantial difference in expression between virgin and mated flies. We observed 3048 exons from 1610 genes exhibiting differential expression at a false discovery rate of 0.05 (Benjamini and Hochberg 1995).…”

Section: Resultssupporting

confidence: 64%

“…Metabolic changes are found throughout the whole body (McGraw et al 2004(McGraw et al , 2008 as well as specific changes in the female head fat body (Dalton et al 2010), including effects on nutritional state postmating.…”

mentioning

confidence: 99%

“…Following mating in Drosophila melanogaster the fly experiences changes in metabolism (McGraw et al 2004(McGraw et al , 2008Dalton et al 2010), immune defense (reviewed by Lawniczak and Begun 2004;Peng et al 2005;Lawniczak et al 2007;Morrow and Innocenti 2012), life span (Chapman et al 1995), detoxification products (McGraw et al 2004), and gene expression (Smith et al 2013;Zhou et al 2014). Metabolic changes are found throughout the whole body (McGraw et al 2004(McGraw et al , 2008 as well as specific changes in the female head fat body (Dalton et al 2010), including effects on nutritional state postmating.…”

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confidence: 99%

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Buffering of Genetic Regulatory Networks inDrosophila melanogaster

et al. 2016

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Regulatory variation in gene expression can be described by cis-and trans-genetic components. Here we used RNA-seq data from a population panel of Drosophila melanogaster test crosses to compare allelic imbalance (AI) in female head tissue between mated and virgin flies, an environmental change known to affect transcription. Indeed, 3048 exons (1610 genes) are differentially expressed in this study. A Bayesian model for AI, with an intersection test, controls type I error. There are 200 genes with AI exclusively in mated or virgin flies, indicating an environmental component of expression regulation. On average 34% of genes within a cross and 54% of all genes show evidence for genetic regulation of transcription. Nearly all differentially regulated genes are affected in cis, with an average of 63% of expression variation explained by the cis-effects. Trans-effects explain 8% of the variance in AI on average and the interaction between cis and trans explains an average of 11% of the total variance in AI. In both environments cis-and trans-effects are compensatory in their overall effect, with a negative association between cis-and trans-effects in 85% of the exons examined. We hypothesize that the gene expression level perturbed by cis-regulatory mutations is compensated through trans-regulatory mechanisms, e. g., trans and cis by trans-factors buffering cis-mutations. In addition, when AI is detected in both environments, cis-mated, cis-virgin, and trans-mated-trans-virgin estimates are highly concordant with 99% of all exons positively correlated with a median correlation of 0.83 for cis and 0.95 for trans. We conclude that the gene regulatory networks (GRNs) are robust and that trans-buffering explains robustness.

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Section: Resultssupporting

confidence: 64%

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confidence: 99%

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confidence: 99%

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Buffering of Genetic Regulatory Networks inDrosophila melanogaster

et al. 2016

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“…Less is known about the responses to mating in males, although they are predicted to primarily involve the replenishment of sperm and seminal fluid storage (Sirot, Buehner, Fiumera, & Wolfner, 2009). Several studies using Drosophila melanogaster have aimed to uncover the gene products that respond to mating, although these studies have examined males and females separately (Dalton et al., 2010; Ellis & Carney, 2010; Innocenti & Morrow, 2009; Lawniczak & Begun, 2004). …”

Section: Introductionmentioning

confidence: 99%

Dietary choices are influenced by genotype, mating status, and sex in Drosophila melanogaster

Camus

Huang

Reuter

et al. 2018

Ecology and Evolution

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Mating causes many changes in physiology, behavior, and gene expression in a wide range of organisms. These changes are predicted to be sex specific, influenced by the divergent reproductive roles of the sexes. In female insects, mating is associated with an increase in egg production which requires high levels of nutritional input with direct consequences for the physiological needs of individual females. Consequently, females alter their nutritional acquisition in line with the physiological demands imposed by mating. Although much is known about the female mating‐induced nutritional response, far less is known about changes in males. In addition, it is unknown whether variation between genotypes translates into variation in dietary behavioral responses. Here we examine mating‐induced shifts in male and female dietary preferences across genotypes of Drosophila melanogaster. We find sex‐ and genotype‐specific effects on both the quantity and quality of the chosen diet. These results contribute to our understanding of sex‐specific metabolism and reveal genotypic variation that influences responses to physiological demands.

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“…Particularly well studied are the functions and fitness effects of seminal fluid proteins (Sfps) in males [2,18], which cause a substantial reprogramming of female behaviour and physiology [2]. The genomewide profiles of gene expression changes in response to courtship and mating [12,13,16,17] and to the receipt of Sfps [12,15,19] have been investigated. Here, we aimed to capture an in-depth genomic profile of gene expression changes resulting from the transfer of a single Sfp with striking fitness effects [20 -26], the sex peptide (SP).…”

Section: Introductionmentioning

confidence: 99%

Sex peptide of Drosophila melanogaster males is a global regulator of reproductive processes in females

et al. 2012

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Seminal fluid proteins (Sfps) alter female behaviour and physiology and can mediate sexual conflict. In Drosophila melanogaster, a single Sfp, the sex peptide (SP), triggers remarkable post-mating responses in females, including altered fecundity, feeding, immunity and sexual receptivity. These effects can favour the evolutionary interests of males while generating costs in females. We tested the hypothesis that SP is an upstream master-regulator able to induce diverse phenotypes through efficient induction of widespread transcriptional changes in females. We profiled mRNA responses to SP in adult female abdomen (Abd) and headþthorax (HT) tissues using microarrays at 3 and 6 h following mating. SP elicited a rich, subtle signature of temporally and spatially controlled mRNAs. There were significant alterations to genes linked to egg development, early embryogenesis, immunity, nutrient sensing, behaviour and, unexpectedly, phototransduction. There was substantially more variation in the direction of differential expression across time points in the HT versus Abd. The results support the idea that SP is an important regulator of gene expression in females. The expression of many genes in one sex can therefore be under the influence of a regulator expressed in the other. This could influence the extent of sexual conflict both within and between loci.

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Dynamic, mating-induced gene expression changes in female head and brain tissues of Drosophila melanogaster

Cited by 62 publications

References 59 publications

Buffering of Genetic Regulatory Networks inDrosophila melanogaster

Buffering of Genetic Regulatory Networks inDrosophila melanogaster

Dietary choices are influenced by genotype, mating status, and sex in Drosophila melanogaster

Sex peptide of Drosophila melanogaster males is a global regulator of reproductive processes in females

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