Many species are able to share information about their environment by communicating through auditory, visual, and olfactory cues. In Drosophila melanogaster, exposure to parasitoid wasps leads to a decline in egg laying, and exposed females communicate this threat to naïve flies, which also depress egg laying. We find that species across the genus Drosophila respond to wasps by egg laying reduction, activate cleaved caspase in oocytes, and communicate the presence of wasps to naïve individuals. Communication within a species and between closely related species is efficient, while more distantly related species exhibit partial communication. Remarkably, partial communication between some species is enhanced after a cohabitation period that requires exchange of visual and olfactory signals. This interspecies “dialect learning” requires neuronal cAMP signaling in the mushroom body, suggesting neuronal plasticity facilitates dialect learning and memory. These observations establish Drosophila as genetic models for interspecies social communication and evolution of dialects.

In this study, we find that many different Drosophila species never having been exposed to parasitoid wasps can trigger caspase activation in the ovary and depress egg-laying when placed next to flies that had visual experience with wasps. Interestingly, when teacher flies of one species are placed with a student of a different species, communication exists, to varying degrees, which seems dependent on evolutionary relatedness. Cohabitation of two species that can partially communicate can learn each other’s “dialect”, yielding effective interspecies communication. There are various inputs involved in dialect learning, including the presence of visual and olfactory cues and memory functions, including genes implicated in social learning defects in murine models, such as PTEN. The neuroplasticity of adult Drosophila allows for learning of dialects, but the specific dialect learned is dependent on social interactions exclusive to a communal environmental context, which provides both visual and olfactory inputs. We find flies can communicate with one another about an anticipated danger, which is suggestive of a fly “language.” The presence of a neurologically plastic system, allowing for social learning, can subsequently lead to a dramatic physiological response, requiring active learning and memory formation through integration of multiple inputs.

Although modes of intra- and interspecies communication are likely to be genetically limited, there is also value in learning to interpret signals from variable, local environments that may provide immediate survival benefits. How do genetically constrained neurological features and variable environmental factors interact to produce context-dependent, meaningful information? Under which environmental factors would information sharing between different species occur and be beneficial? In this study, we sought to begin to address these questions in the Drosophila model system by using a pan-Drosophila predator known to elicit social communication [ 17 , 47 ]. D. melanogaster presented with parasitoid wasps have multiple behavioral responses, including a reduction in oviposition (egg laying) through an increase in ovarian apoptosis [ 17 , 48 – 51 ]. After removal of the wasp, a wasp-exposed “teacher” fly can instruct a naïve “student” fly about the presence of the wasp threat through the exclusive use of visual cues, such that students now reduce their own oviposition by triggering ovarian apoptosis. Using this fly-fly social communication paradigm we asked (1) whether social communication is conserved among other Drosophila species, (2) if Drosophilids engage in interspecies communication, and (3) what environmental and genetic factors are required for interspecies communication.

Drosophila melanogaster and other Drosophila species have provided insights into mechanisms of learning, memory, and complex behaviors[ 36 , 37 ]. However, these behaviors and phenotypes have been studied almost exclusively in domesticated D. melanogaster lab monocultures, while D. melanogaster wild populations are surrounded by a broad range of predators, microbes, and other Drosophilids, highlighting a communal component of the organism’s life cycle[ 38 ]. This raises the possibility of behavioral phenomenon that have yet to be discovered and analyzed in domesticated lab monocultures[ 39 – 41 ]. Given the vast range of environmental inputs on a wild Drosophilid, a fly must be able to discern important information from extraneous inputs, while interacting with conspecifics and a variety of other species [ 42 – 46 ].

Chemical cues can serve as intra- and interspecies signals, such as fox and guinea pig urine affecting not only conspecific behavior, but also the behavior of other animals[ 18 – 20 ]. Sound can also be used, such as in bats and bottlenose dolphins, which are able to distinguish members of the community through the use of echolocation pitch recognition[ 21 , 22 ]. Plants have a vast arsenal of responses to pathogens[ 23 ], including communicating a threat to neighboring plants through the use of volatile organic compounds[ 24 ]. Plant interspecies[ 25 – 31 ] and intraspecies[ 32 – 34 ] communication occurs both in laboratory settings and in the wild[ 30 , 35 ].

It is proposed that a myriad of environmental cues, both social and non-social, are critical to animal development in determining the ability to convey and receive specific types of information. However, there are many outstanding questions as a result of this proposition: What cues are important? When are these cues important? How can environmental cues interact with genetically determined developmental programs? Although social communication is most extensively documented in more derived species such as mammals and birds, insects can also display a broad range of behavioral tasks. Bees are known to be able to learn from non-natural sources in order to obtain a reward through social learning. Such information can be passed on to naïve, student bees through the use of visual cues[ 14 , 15 ]. Insect social learning extends to the genetic model system of Drosophila, where student, observer flies learn from a trained, teacher-fly, using visual cues. This has been shown in communication involving food sources and predator threats[ 16 , 17 ].

The ability to interpret environmental information is a phenomenon found throughout all life forms. From bacteria to plants and to mammals, communication occurs within as well as between species. In some cases, information that is being shared can be highly specific, such as in the case of honeybees communicating instructions on where to find nectar[ 1 – 3 ]. In other cases, opportunistic bystanders can also benefit from general information. For example, predator alarm calls generated as a warning are observed, where multiple species participate in repeating the alarm throughout the community[ 4 – 8 ]. In all cases, the information that is shared can be dependent on local environmental cues and experiences and the manner in which information is communicated is strongly influenced by past experiences of each individual. For example, birds, which live in geographically distinct populations, manifest unique song variants or regional dialects that can last for decades, but these animals are nevertheless still able to communicate with others of their species[ 9 – 11 ]. Because dialects are learned and therefore influenced[ 12 ] by specific local environmental differences, it suggests that both social and non-social experiences can have dramatic effects on cognitive development[ 13 ].

Results