Drosophila Dating

 

 

 

In February, the month of love, we’ll take a brief look at the weird and wonderful courtship behaviour of one of the model organisms we annotate at UniProt, the amorous arthropod Drosophila melanogaster, and explore how studying their courtship song helps researchers understand the genetic and neural underpinnings of behaviour. The study of proteins from well characterised model organisms such as the fruit fly D.melanogaster (Drosophila protein annotation project) helps in understanding insect biology, allowing us to control their populations by manipulating processes such as reproduction, and also enables scientists to model human physiology and disease.

 

Communication, communication, communication.

How many times have you heard that the key to a successful relationship is communication? Well, no organism does it quite like the fruit fly Drosophila melanogaster.

As in many organisms, Drosophila sexual behaviour involves a complex communication of signals and responses between the mating pair. From identifying a potential mate to courtship, copulation and egg production, the male and female fruit fly continuously exchange visual, tactile, chemical, auditory and even genetic information to allow them to assess their potential mate and respond appropriately by adapting their behaviour, or stimulating the behaviour and physiology of their mate, to improve their chances of copulation and reproductive success.

 

Why do scientists study courtship behaviour in Drosophila?

Behaviour is the consequence of specific motor outputs produced by dedicated neural circuits, so any change in behaviour is the result of alterations in the structure or function of these neural circuits. Drosophila display a wide range of simple and complex behaviours including learning, memory, aggression, sleep and courtship. Examining these behaviours is of course of interest to entomologists studying insect behaviour. In addition, many of the genes and genetic pathways that control these behaviours are also found in mammals, meaning that Drosophila is a powerful genetic model organism in which to also research mechanisms of human neural disorders as well as the molecular, cellular and evolutionary basis of behaviour.

Drosophila courtship follows a series of innate and stereotyped behaviours which enable the fruit fly to evaluate their mate’s suitability, reproductive state, receptibility and fitness. Even wild-type Drosophila raised in solitude can correctly perform the mating ritual when introduced to a mate, demonstrating that the multimodal performance is innate and hardwired into the fly during development. This makes Drosophila courtship an ideal model for studying how regulatory genes establish neural circuits that drive behaviour, not only due to the extensive genetic and genomic resources available to Drosophila researchers but also because courtship behaviour is well documented and understood both within D.melanogaster and closely related species.

 

The love song of the flirtatious fly.

Drosophila is one of the many organisms which attracts their mate with song, and their courtship song is one of the most critical stages of the mating ritual. Once the male has identified a potential mate through visual and chemosensory cues, and assessed their desirability by tapping the partner’s abdomen, the male will begin following the female while extending and vibrating his wings to communicate his courtship song. The song consists of a humming sound called the sine song and a rhythmic patterned pulse song, which together increase female receptibility and reduce the time to copulation. Pulse songs are also species-specific, allowing females to recognise males of the same species. If his singing is deemed audible by the female, she will slow down and allow him to attempt copulation meaning that his ability to effectively communicate his melody can mean the difference between reproductive success or cruel rejection.

Detailed and extensive research has discovered that song manifestation and its proper species-specific motor patterning is under the control of two sex-determination genes, fruitless (fru) and doublesex (dsx) (P23023 and Q8IN81). These transcription factors are well known key regulators in the formation of the courtship neural circuits that control the male’s courtship song as well as many other stages of the Drosophila mating ritual. Both transcription factors undergo sex-specific splicing to produce male-specific and female-specific isoforms (dsx and fru isoforms in UniProt) that control both morphological and behavioural sexual dimorphisms, including mating behaviour. Studies turning these genes on or off in regions of the male or female Drosophila brain and looking at their effect on the mutant’s courtship song, have been able to identify specific motor neurons involved in song composition. For example, the fru-expressing P1 and pIP10 neurons initiate the courtship song while the descending pIP10 neuron also drives activity of thoracic motor neurons which shapes the song. In addition, dsx promotes male-specific expansion of dendritic arborizations of thoracic interneurons (TN1A neurons), which are required specifically for generation of the sine song. Studies using mutant females constitutively expressing male-specific isoforms of fru and/or dsx found that individually they are unable to specify the courtship song. Instead, both genes are required for complete song composition.

More recently it was discovered that males aren’t the only crooners during mating. Wild-type females also produce their own song during copulation which directly affects male seminal fluid allocation. This copulation song is distinct from the male courtship song and requires specific ventral nerve cord neurons expressing only the female-specific isoform of dsx. Production of the copulation song by the female depends on transfer of seminal fluid components from the male accessory gland, while hearing the female copulation song increases the male’s reproductive success when challenged by competition, suggesting that her song can increase male ejaculate allocation.

 

Post-mating communication.

D.melanogaster, like most animals, continues to communicate even after copulation to improve reproductive success. Most post-mating behaviours occur in the Drosophila females as the result of male seminal proteins such as SP (P05623), Acp26Aa (P10333) and Acp36DE (Q9V3R1) which, once transferred to the female, modify the activity of distinct neuronal circuitries in the mated female to promote post-mating behavioural responses such as increased ovulation, enhanced egg laying, elevated feeding, activation of the immune system, reduced receptivity to additional courting males and reduced lifespan in multiple mated females.

 

So, in this month of love, why not follow the fruit fly’s example and continuously communicate your adoration to your sweetheart? Perhaps even court them with a soulful serenade - although if your singing ability isn’t quite to your partner’s liking, maybe leave it to the professionals and play their favourite mixtape.

 

References and additional reading

Anholt RRH, O'Grady P, Wolfner MF, Harbison ST. Evolution of Reproductive Behavior. Genetics. 2020 Jan;214(1):49-73. doi: 10.1534/genetics.119.302263. PMID: 31907301; PMCID: PMC6944409.

Hollis B, Koppik M, Wensing KU, Ruhmann H, Genzoni E, Erkosar B, Kawecki TJ, Fricke C, Keller L. Sexual conflict drives male manipulation of female postmating responses in Drosophila melanogaster. Proc Natl Acad Sci U S A. 2019 Apr 23;116(17):8437-8444. doi: 10.1073/pnas.1821386116. Epub 2019 Apr 8. PMID: 30962372; PMCID: PMC6486729.

Kerwin P, Yuan J, von Philipsborn AC. Female copulation song is modulated by seminal fluid. Nat Commun. 2020 Mar 18;11(1):1430. doi: 10.1038/s41467-020-15260-6. PMID: 32188855; PMCID: PMC7080721.

Pavlou HJ, Goodwin SF. Courtship behavior in Drosophila melanogaster: towards a 'courtship connectome'. Curr Opin Neurobiol. 2013 Feb;23(1):76-83. doi: 10.1016/j.conb.2012.09.002. Epub 2012 Sep 28. PMID: 23021897; PMCID: PMC3563961.

Rideout EJ, Billeter JC, Goodwin SF. The sex-determination genes fruitless and doublesex specify a neural substrate required for courtship song. Curr Biol. 2007 Sep 4;17(17):1473-8. doi: 10.1016/j.cub.2007.07.047. Epub 2007 Aug 23. PMID: 17716899; PMCID: PMC2583281.

Sato K, Tanaka R, Ishikawa Y, Yamamoto D. Behavioral Evolution of Drosophila: Unraveling the Circuit Basis. Genes (Basel). 2020 Feb 1;11(2):157. doi: 10.3390/genes11020157. PMID: 32024133; PMCID: PMC7074016.

Shirangi TR, Wong AM, Truman JW, Stern DL. Doublesex Regulates the Connectivity of a Neural Circuit Controlling Drosophila Male Courtship Song. Dev Cell. 2016 Jun 20;37(6):533-44. doi: 10.1016/j.devcel.2016.05.012 . PMID: 27326931.

von Philipsborn AC, Liu T, Yu JY, Masser C, Bidaye SS, Dickson BJ. Neuronal control of Drosophila courtship song. Neuron. 2011 Feb 10;69(3):509-22. doi: 10.1016/j.neuron.2011.01.011 . PMID: 21315261.