Behavioral and neuronal underpinnings of safety in numbers in fruit flies

Ferreira, Clara Howcroft; Moita, Marta A.

doi:10.1038/s41467-020-17856-4

Cited by 36 publications

(44 citation statements)

References 49 publications

(53 reference statements)

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“…Unlike the UAS and gal4 controls, females did not advance egg-laying in a group when T4 and T5 were blocked (Figure 4E), showing that T4 and T5 are necessary for group sensing. Lobula columnar (LC) neurons are an entry point for the circuit-level study of visual responses since it is the first layer where visual information about objects is decoded (Ferreira and Moita, 2020;Ribeiro et al, 2018;Wu et al, 2016). Having identified motion cues of group members as the leading source of the group effect on egg-laying, we investigated the role of visual projection neurons responsive to the movement of small objects like a flies: LC10 and LC11 (Ferreira and Moita, 2020;Keleş and Frye, 2017;Ribeiro et al, 2018;Wu et al, 2016).…”

Section: The Motion Detection Circuit Is Necessary For Egg-laying Advancementmentioning

confidence: 99%

“…Lobula columnar (LC) neurons are an entry point for the circuit-level study of visual responses since it is the first layer where visual information about objects is decoded (Ferreira and Moita, 2020;Ribeiro et al, 2018;Wu et al, 2016). Having identified motion cues of group members as the leading source of the group effect on egg-laying, we investigated the role of visual projection neurons responsive to the movement of small objects like a flies: LC10 and LC11 (Ferreira and Moita, 2020;Keleş and Frye, 2017;Ribeiro et al, 2018;Wu et al, 2016). LC neurons were silenced in females by expressing Kir2.1 and by testing the focal female for egg-laying latency alone or in groups with wild-type males.…”

Section: The Motion Detection Circuit Is Necessary For Egg-laying Advancementmentioning

confidence: 99%

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Social modulation of oogenesis and egg-laying inDrosophila melanogaster

Tiphaine

Kohlmeier

Etienne

et al. 2021

Preprint

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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.

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Section: The Motion Detection Circuit Is Necessary For Egg-laying Advancementmentioning

confidence: 99%

Section: The Motion Detection Circuit Is Necessary For Egg-laying Advancementmentioning

confidence: 99%

Social modulation of oogenesis and egg-laying inDrosophila melanogaster

Tiphaine

Kohlmeier

Etienne

et al. 2021

Preprint

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“…It is well known that the decision to freeze depends on several factors from the external and internal environment [23,24,[42][43][44][45]. In flies, we have shown that the animal's own behavioural state [11] and the social environment regulates threat-induced freezing [15]. Here, we show that two features of cardiac activity measured before threat, reversal rate and reversal variability, partially predict the amount of looming triggered freezing.…”

Section: Cardiac Activity As Modulator Of Freezingmentioning

confidence: 59%

“…Insects show a large repertoire of defensive behaviours, including freezing and fleeing responses, upon detection of a threat [11][12][13][14]. The fruit fly has become a very useful model to study the neuronal circuits of defensive behaviours, from the integration of cues of threat and surrounding context, to the selection and execution of the defensive responses [11,[14][15][16]. It has been previously postulated that threat induces a sustained change in the flies' internal state, akin to a primitive emotional state [17].…”

Section: Introductionmentioning

confidence: 99%

Threat induces changes in cardiac activity and metabolism negatively impacting survival in flies

Barrios

Farias

Moita

2020

Preprint

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Adjusting to a dynamic environment involves fast changes in the body’s internal state, characterized by coordinated alterations in brain activity, physiological and motor responses. Threat-induced defensive states are a classic example of coordinated adjustment of bodily responses, being cardiac regulation one of the best characterized in vertebrates. A great deal is known regarding the neural basis of invertebrate defensive behaviours, mainly in Drosophila melanogaster. However, whether physiological changes accompany these remains unknown. Here, we set out to describe the internal bodily state of fruit flies upon an inescapable threat and found cardiac acceleration during running and deceleration during freezing. In addition, we found that freezing leads to increased cardiac pumping from the abdomen towards the head-thorax, suggesting mobilization of energy resources. Concordantly, threat-triggered freezing reduces sugar levels in the hemolymph and renders flies less resistant to starvation. The cardiac responses observed during freezing were absent during spontaneous immobility, underscoring the active nature of freezing response. Finally, we show that baseline cardiac activity predicts the amount of freezing upon threat. This work reveals a remarkable similarity with the cardiac responses of vertebrates, suggesting an evolutionarily convergent defensive state in flies. Our findings are at odds with the widespread view that cardiac deceleration while freezing has first evolved in vertebrates and that it is energy sparing. Investigating the physiological changes coupled to defensive behaviours in the fruit fly has revealed that freezing is costly, yet accompanied by cardiac deceleration, and points to heart activity as a key modulator of defensive behaviours.

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“…As protection from predators by diluting the risk of being targeted (Hamilton, 1971; Vine, 1971) is one of the key benefits of sociality it is a logical consequence of social isolation to increase vigilance and respond to potentially threatening stimuli at a lower threshold (Hawkley and Cacioppo, 2010). For example, fruit flies display a graded decrease in freezing in response to threatening stimuli that is proportional to group size (Ferreira and Moita, 2020). Our results suggest that Pth2 might contribute to the regulation of appropriate vigilance states in vertebrates.…”

Section: Discussionmentioning

confidence: 99%

The neuropeptide Pth2 modulates social behavior and anxiety in zebrafish

Anneser

Gemmer

Eilers

et al. 2021

Preprint

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Animal behavior is strongly context-dependent and behavioral performance is often modulated by internal state. In particular, different social contexts can alter anxiety levels and modulate social behavior. The vertebrate-specific neuropeptide parathyroid hormone 2 (pth2) is directly regulated by the presence or absence of conspecifics in zebrafish. As its cognate receptor, the parathyroid hormone 2 receptor (pth2r), is widely expressed across the brain, we tested fish lacking the functional Pth2 peptide in several anxiety-related and social paradigms. Rodents lacking PTH2 display increased anxiety-related behavior. Here we show that the propensity to react to sudden stimuli with an escape response is increased in pth2-/- zebrafish, consistent with elevated anxiety. While overall social preference for conspecifics is maintained in pth2-/- fish until the early juvenile stage, we found that both social preference and shoaling are altered later in development. The data presented suggest that the neuropeptide Pth2 modulates several conserved behavioral features, and may thus enable the animal to react appropriately in different social contexts.

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Behavioral and neuronal underpinnings of safety in numbers in fruit flies

Cited by 36 publications

References 49 publications

Social modulation of oogenesis and egg-laying inDrosophila melanogaster

Social modulation of oogenesis and egg-laying inDrosophila melanogaster

Threat induces changes in cardiac activity and metabolism negatively impacting survival in flies

The neuropeptide Pth2 modulates social behavior and anxiety in zebrafish

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