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A Drosophila female pheromone elicits species-specific long-range attraction via an olfactory channel with dual specificity for sex and food.

ABSTRACT: BACKGROUND:Mate finding and recognition in animals evolves during niche adaptation and involves social signals and habitat cues. Drosophila melanogaster and related species are known to be attracted to fermenting fruit for feeding and egg-laying, which poses the question of whether species-specific fly odours contribute to long-range premating communication. RESULTS:We have discovered an olfactory channel in D. melanogaster with a dual affinity to sex and food odorants. Female flies release a pheromone, (Z)-4-undecenal (Z4-11Al), that elicits flight attraction in both sexes. Its biosynthetic precursor is the cuticular hydrocarbon (Z,Z)-7,11-heptacosadiene (7,11-HD), which is known to afford reproductive isolation between the sibling species D. melanogaster and D. simulans during courtship. Twin olfactory receptors, Or69aB and Or69aA, are tuned to Z4-11Al and food odorants, respectively. They are co-expressed in the same olfactory sensory neurons, and feed into a neural circuit mediating species-specific, long-range communication; however, the close relative D. simulans, which shares food resources with D. melanogaster, does not respond to Z4-11Al. CONCLUSION:The Or69aA and Or69aB isoforms have adopted dual olfactory traits. The underlying gene yields a collaboration between natural and sexual selection, which has the potential to drive speciation.

SUBMITTER: Lebreton S

PROVIDER: S-EPMC5622430 | biostudies-literature | 2017 Sep

REPOSITORIES: biostudies-literature

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A Drosophila female pheromone elicits species-specific long-range attraction via an olfactory channel with dual specificity for sex and food.

Lebreton Sebastien S Borrero-Echeverry Felipe F Gonzalez Francisco F Solum Marit M Wallin Erika A EA Hedenström Erik E Hansson Bill S BS Gustavsson Anna-Lena AL Bengtsson Marie M Birgersson Göran G Walker William B WB Dweck Hany K M HKM Becher Paul G PG Witzgall Peter P

BMC biology 20170929 1

<h4>Background</h4>Mate finding and recognition in animals evolves during niche adaptation and involves social signals and habitat cues. Drosophila melanogaster and related species are known to be attracted to fermenting fruit for feeding and egg-laying, which poses the question of whether species-specific fly odours contribute to long-range premating communication.<h4>Results</h4>We have discovered an olfactory channel in D. melanogaster with a dual affinity to sex and food odorants. Female fli ...[more]

PMID: 28962619

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Project description:BACKGROUND:Among invertebrates, specific pheromones elicit inherent (fixed) behavioural responses to coordinate social behaviours such as sexual recognition and attraction. By contrast, the much more complex social odours of mammals provide a broad range of information about the individual owner and stimulate individual-specific responses that are modulated by learning. How do mammals use such odours to coordinate important social interactions such as sexual attraction while allowing for individual-specific choice? We hypothesized that male mouse urine contains a specific pheromonal component that invokes inherent sexual attraction to the scent and which also stimulates female memory and conditions sexual attraction to the airborne odours of an individual scent owner associated with this pheromone. RESULTS:Using wild-stock house mice to ensure natural responses that generalize across individual genomes, we identify a single atypical male-specific major urinary protein (MUP) of mass 18893Da that invokes a female's inherent sexual attraction to male compared to female urinary scent. Attraction to this protein pheromone, which we named darcin, was as strong as the attraction to intact male urine. Importantly, contact with darcin also stimulated a strong learned attraction to the associated airborne urinary odour of an individual male, such that, subsequently, females were attracted to the airborne scent of that specific individual but not to that of other males. CONCLUSIONS:This involatile protein is a mammalian male sex pheromone that stimulates a flexible response to individual-specific odours through associative learning and memory, allowing female sexual attraction to be inherent but selective towards particular males. This 'darcin effect' offers a new system to investigate the neural basis of individual-specific memories in the brain and give new insights into the regulation of behaviour in complex social mammals.See associated Commentary http://www.biomedcentral.com/1741-7007/8/71.

Dataset Information

A Drosophila female pheromone elicits species-specific long-range attraction via an olfactory channel with dual specificity for sex and food.

Publications

A Drosophila female pheromone elicits species-specific long-range attraction via an olfactory channel with dual specificity for sex and food.

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