Social modulation of oogenesis and egg-laying inDrosophila melanogaster

Abstract

Being part of a group facilitates cooperation between group members, but also creates competition for limited resources. This conundrum is problematic for gravid females who benefit from being in a group, but whose future offspring may struggle for access to nutrition in larger groups. Females should thus modulate their reproductive output depending on their social context. Although social-context dependent modulation of reproduction is documented in a broad range of species, its underlying mechanisms and functions are poorly understood. In the fruit fly Drosophila melanogaster, females actively attract conspecifics to lay eggs on the same resources, generating groups in which individuals may cooperate or compete. The tractability of the genetics of this species allows dissecting the mechanisms underlying physiological adaptation to their social context. Here, we show that females produce eggs increasingly faster as group size increases. By laying eggs faster in group than alone, females appear to reduce competition between offspring and increase their likelihood of survival. In addition, females in a group lay their eggs during the light phase of the day, while isolated females lay them during the night. We show that responses to the presence of others are determined by vision through the motion detection pathway and that flies from any sex, mating status or species can trigger these responses. The mechanisms of this modulation of egg-laying by group is connected to a lifting of the inhibition of light on oogenesis and egg-laying by stimulating hormonal pathways involving juvenile hormone. Because modulation of reproduction by social context is a hallmark of animals with higher levels of sociality, our findings represent a protosocial mechanism in a species considered solitary that may have been the target of selection for the evolution of more complex social systems.

Social cues of safety can override differences in threat level

“…Vertebrates use such social cues to procure food 3 for example using vision to assess where and how much others are eating 4 , to choose mates by copying the decisions of others 5 based for example on olfactory cues 6 , and to infer predation threat levels 7 for instance by auditory detection of escape 8 or freezing (active immobility response aimed at becoming inconspicuous) 9 . These types of social cue usage are also reported in invertebrates including in Drosophila melanogaster 10,11 , guiding aggregation on food [12][13][14][15] , reproduction related decisions in mating 16,17 and oviposition [18][19][20] , as well defensive responses 21 , many of which relying at least partially on vision.…”

Circadian control of a sex-specific behaviour in Drosophila

“…Likewise, the assessment of rhythmicity is more difficult than for locomotor activity because the variable studied (number of eggs) is discrete and usually small when recorded for periods of a few hours. Even though population-level experiments can partially overcome these difficulties, social interactions can influence the oviposition behavior of Drosophila females 16 , making the results much harder to interpret.…”

Social Cues of Safety Can Override Differences in Threat Level

“…Vertebrates use such social cues to procure food (Galef and Giraldeau, 2001), for example, using vision to assess where and how much others are eating (Coolen et al, 2005), to choose mates by copying the decisions of others (Kavaliers et al, 2017) based, for example, on olfactory cues (Galef and Laland, 2005), and to infer predation threat levels (Griffin, 2004), for instance, by auditory detection of escape (Murray et al, 2017) or freezing (active immobility response aimed at becoming inconspicuous) (Pereira et al, 2012). These types of social cue usage are also reported in invertebrates, including Drosophila melanogaster (Ferreira and Moita, 2019;Couzin-Fuchs and Ayali, 2021), guiding aggregation on food (Tinette et al, 2004;Dombrovski et al, 2017Dombrovski et al, , 2019Shultzaberger et al, 2018), reproduction-related decisions in mating (Mery et al, 2009;Danchin et al, 2018) and oviposition (Sarin and Dukas, 2009;Battesti et al, 2012;Bailly et al, 2021), as well as defensive responses (Ferreira and Moita, 2020), many of which rely at least partially on vision.…”