Drosophila melanogaster males respond differently at the behavioural and genome‐wide levels to Drosophila melanogaster and Drosophila simulans females

Abstract

Drosophila melanogaster are found in sympatry with Drosophila simulans, and matings between the species produce nonfertile hybrid offspring at low frequency. Evolutionary theory predicts that females choose mates, so males should alter their behaviour in response to female cues. We show that D. melanogaster males quickly decrease courtship towards D. simulans females. Courtship levels are reduced within 5 min of exposure to a heterospecific female, and overall courtship is significantly lower than courtship towards conspecific females. To understand changes at the molecular level during mate choice, we performed microarray analysis on D. melanogaster males that courted heterospecific D. simulans females and found nine genes have altered expression compared with controls. In contrast, males that court conspecific females alter expression of at least 35 loci. The changes elicited by conspecific courtship likely modulate nervous system function to reinforce positive conspecific signals and dampen the response to heterospecific signals.

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

“…Changes in male gene expression during social interactions with females or males: Within 5 min of male-to-female social interactions, whole-animal transcript profiles are altered in courting males, and there is a differential response to conspecific compared to heterospecific females (Carney 2007;Ellis and Carney 2009). Next, we focused solely on male-head gene expression in response to courtship since the head contains the brain as well as other tissues and sensory organs that impact behavioral and physiological responses to sensory inputs.…”

“…In songbirds, 33 genes are regulated by singing behavior, including loci involved in signal transduction and synaptic signaling (Wada et al 2006), and a variety of social environments and stimuli impact honeybee brain gene expression (Grozinger et al 2003;Whitfield et al 2003Whitfield et al , 2006Sen Sarma et al 2009). Similarly, male Drosophila melanogaster show rapid changes in transcript levels due to social interactions with females (Carney 2007;Ellis and Carney 2009). However, we do not know if these are specific responses to females or more general responses to interacting with a second individual.…”

“…Adding to the complexity of this process are the effects from the organism's genetics and environment, including social interactions, on behavior, brain morphology, and gene expression (Siegel and Hall 1979;Levine et al 2002;Shen et al 2004;Stewart and McLean 2004;Burmeister et al 2005;Kozorovitskiy et al 2006;Yurkovic et al 2006;Carney 2007;Technau 2007;Ellis and Carney 2009).…”

“…In males, interacting with a second individual causes rapid expression-level changes detectable in whole animals (Carney 2007;Ellis and Carney 2009). These rapid responses are likely mediated by signaling in the nervous system, sensory organs, and other tissues that affect neural physiology.…”

Transcriptional profiling of adult Drosophila antennae by high-throughput sequencing

“…A previous study found that when male flies of D. melanogaster encountered female flies from the closely related species, D. simulans, their courtship behavior significantly dropped within 5 min (Ellis and Carney 2009). In addition, expression levels of nine genes were significantly altered, mostly down-regulated, in males.…”