Copulation Song inDrosophila: Do Females Sing to Change Male Ejaculate Allocation and Incite Postcopulatory Mate Choice?

Abstract

Drosophila males sing a courtship song to achieve copulations with females. Females were recently found to sing a distinct song during copulation, which depends on male seminal fluid transfer and delays female remating. Here, it is hypothesized that female copulation song is a signal directed at the copulating male and changes ejaculate allocation. This may alter female remating and sperm usage, and thereby affect postcopulatory mate choice. Mechanisms of how female copulation song is elicited, how males respond to copulation song, and how remating is modulated, are considered. The potential adaptive value of female signaling during copulation is discussed with reference to vertebrate copulation calls and their proposed function in eliciting mate guarding. Female copulation song may be widespread within the Drosophila genus. This newly discovered behavior opens many interesting avenues for future research, including investigation of how sexually dimorphic neuronal circuits mediate communication between nervous system and reproductive organs.

Non‐visual cues and indirect strategies that enable discrimination of asymmetric mates

“…Such direct pheromone transfers from bilaterally located dermal glands during mating are also known in some salamander species (Houck, 2009 ). Drosophila melanogaster females seem to assess seminal fluid transferred by males during mating (Figure 1f ) and if preferred, sing a copulation song by wing vibration in response, which in turn directly modulates male's ejaculate allocation in ways that prolong time to female remating (Kerwin & Philipsborn, 2020 ; Kerwin et al, 2020 ). Thus, copulation itself can provide multimodal cues that could reveal male asymmetry.…”

Flexibility of neural circuits regulating mating behaviors in mice and flies

“…Although more is known regarding the underlying circuitry in males, the neural basis of female mating behaviors is also beginning to emerge, and it has become evident that females take an active role in the mating process. Depending on her mating status, the female may exhibit active rejecting behaviors, changing her speed in response to the male song or extruding her ovipositor to signal her willingness to mate ( Rezával et al, 2012 ; Feng et al, 2014 ; Kerwin and von Philipsborn, 2020 ; Mezzera et al, 2020 ; Wang et al, 2020a ), and possibly even singing during copulation ( Kerwin et al, 2020 ), although the specific role of this song is currently unknown ( Kerwin and von Philipsborn, 2020 ). Recent advances in the fine automatic quantification of mating behaviors ( Pereira et al, 2020 ), and in tracing neural circuits at a synaptic level using EM-based connectomes ( Scheffer et al, 2020 ; Dorkenwald et al, 2022 ) are expected to accelerate the dissection of mating circuits in both sexes.…”

Inter-sexual multimodal communication during mating in wild geladas: the leading role of females

“…According to previous reports, EEC helps the male’s pelvic thrusting and prolongs sexual contact, thus improving the chances of ejaculation ( Dixson 2015 ; Palagi et al 2020 ; Zanoli et al 2021 ). As concerns the acoustic channel, several animal species, in particular primates, can emit rhythmic vocalizations before, during, or after copulations, the so-called “copulation calls” (e.g., insects: Drosophila sp., Kerwin and von Philipsborn 2020 ; amphibians: Rana blythii , Emerson 1992 ; Emerson and Boyd 1999 ; rodents: Rattus norvegicus , Thomas and Barfield 1985 ; mammals: Loxodonta africana , Poole et al 1988 ; Mirounga angustirostris , Cox and LeBoeuf 1977 ; New-World monkeys: Cebus apella , Carosi and Visalberghi 2002 ; Brachyteles arachnoides , Milton 1985 ; Old-World monkeys: Macaca sylvanus , Pfefferle et al 2008b ; Papio sp., Maestripieri and Rooney 2005; Miopithecus talapoin , Dixson et al 1975 ; great apes: Pan paniscus , Clay et al 2011 ; Pan troglodytes , Townsend et al 2011 ; Gorilla gorilla , Salmi et al 2013 ; see also Pradhan et al 2006 ; Dixson 2015 ; Pfefferle 2016 for reviews; humans: Homo sapiens , Dixson 2015 ; Hamilton and Arrowood 1978 ). Although both sexes can separately or concurrently call during mating ( Doyle et al 1967 ; Hamilton and Arrowood 1978 ; Townsend et al 2008 ; Salmi et al 2013 ), females are the sex that most likely emits copulation calls (e.g., C. apella , Carosi and Visalberghi 2002 ; B. arachnoides , Milton 1985 ; M. sylvanus , Pfefferle et al 2008b ; Papio sp., Maestripieri and Rooney 2005; M. talapoin , Dixson et al 1975 ; P. paniscus , Clay et al 2011 ; P. troglodytes , Townsend et al 2011 ; H. sapiens , Dixson 2015 ; Hamilton and Arrowood 1978 ).…”

“…Females from different non primate ( Drosophila sp. : Kerwin and von Philipsborn 2020 ; R. blythii : Emerson 1992 , Emerson and Boyd 1999 ) and primate species can emit vocalizations during male ejaculation (e.g., Old-World monkeys: Macaca fascicularis : Deputte and Goustard 1980 ; M. talapoin : Dixson et al 1975 ; Papio cynocephalus : O'Connell and Cowlishaw 1994 ; M. sylvanus : Todt et al 1995 ; African great apes: P. troglodytes : van Lawick-Goodall 1968 ; P. paniscus : Thompson-Handler et al 1984 ; reviewed in Maestripieri and Roney 2005 ; Dixson 2015 ; H. sapiens : Prokop 2021 ; Brewer and Hendrie 2011 ). Hence, the gelada end-copulation call may be a marker of completed copulation.…”