Cooperative Behavior Emerges among Drosophila Larvae

Abstract

Spectacular examples of cooperative behavior emerge among a variety of animals and may serve critical roles in fitness [1, 2]. However, the rules governing such behavior have been difficult to elucidate [2]. Drosophila larvae are known to socially aggregate [3, 4] and use vision, mechanosensation, and gustation to recognize each other [5-8]. We describe here a model experimental system of cooperative behavior involving Drosophila larvae. While foraging in liquid food, larvae are observed to align themselves and coordinate their movements in order to drag a common air cavity and dig deeper. Large-scale cooperation is required to maintain contiguous air contact across the posterior breathing spiracles. On the basis of a directed genetic screen we find that vision plays a key role in cluster dynamics. Our experiments show that blind larvae form fewer clusters and dig less efficiently than wild-type and that socially isolated larvae behave as if they were blind. Furthermore, we observed that blind and socially isolated larvae do not integrate effectively into wild-type clusters. Behavioral data indicate that vision and social experience are required to coordinate precise movements between pairs of larvae, therefore increasing the degree of cooperativity within a cluster. Hence, we hypothesize that vision and social experience allow Drosophila larvae to assemble cooperative digging groups leading to more effective feeding and potential evasion of predators. Most importantly, these results indicate that control over membership of such a cooperative group can be regulated.

Kin recognition and co‐operative foraging in Drosophila melanogaster larvae

“…In Dombrovski et al. 's () study of group feeding, they observed that visually impaired transplanted larvae had trouble coordinating their movements with the other larvae within a cluster. They concluded that sight played an important role in coordinating contractile cycles and speculated that individuals of similar motor profiles would have an easier task of synchronizing their digging and feeding behaviours.…”

“…As time passes, the cumulative feeding of the growing larvae, the accumulation of their excreted waste products, the effects of secreted digestive enzymes and the continued microbiotic activity in the environment lead to a progressive loss of suitable forageable resources near the surface, a pattern that is also seen in laboratory‐raised populations (Ashburner, Golic, & Hawley, ; Gordon & Sang, ; Gregg, McCrate, Reveal, Hall, & Rypstra, ; Louis & de Polavieja, ; Sang, ). Additionally, these processes contribute to the increasing liquification of the upper layers of the environment, which prevents individuals from easily accessing any nutrients buried deeper down, due to the instability of air passages (Dombrovski et al., ). Faced with the risk of starvation, some larvae will engage in cannibalism, consuming conspecific larvae (Vijendravarma, Narasimha, & Kawecki, ) and/or eggs (Ahmad, Chaudhary, Afzal, & Tariq, , but see Narasimha et al., ).…”

“…Faced with the risk of starvation, some larvae will engage in cannibalism, consuming conspecific larvae (Vijendravarma, Narasimha, & Kawecki, ) and/or eggs (Ahmad, Chaudhary, Afzal, & Tariq, , but see Narasimha et al., ). However, an alternate strategy adopted by some third‐instar D. melanogaster larvae is to aggregate into foraging groups, wherein individuals, using both visual and mechanosensory cues, synchronize their digging behaviours (Dombrovski et al., ; Justice, Macedonia, Hamilton, & Condron, ; Wu et al., ). Together, the cluster of larvae is collectively able to dig a ‘well’ ( sensu Louis & de Polavieja, ) that allows access to the deeper, more nutritious, regions of their environment, whereas still allowing respiration (through their posterior breathing spiracles) via a common air cavity (Dombrovski et al., ).…”

“…A recent study by Dombrovski et al. () demonstrated that motion in clusters is highly co‐ordinated and is necessary for the formation of large, stable clusters. In their assays, individuals that were blind or socially isolated (during a critical period in which they acquire visual recognition of the movements of other larvae) did not integrate effectively into cluster groups, likely due to different motor profiles that impeded their ability to move in unison.…”

The role of the sugar receptor IR60b for Drosophila melanogaster: A hypothesis

“…More complete dose-response curves would be needed to address this point. We note that Drosophila larvae also use external digestion: they live in their food and engage in social digestion as they feed collectively (Gregg et al, 1990;Dombrovski et al, 2017) and actively regulate external digestion (Sakaguchi & Suzuki, 2013). Larvae express IR60b in their dorsal pharyngeal sensilla (Stewart et al, 2015).…”