Conservation of the behavioral and transcriptional response to social experience among Drosophilids

Abstract

While social experience has been shown to significantly alter behaviors in a wide range of species, comparative studies that uniformly measure the impact of a single experience across multiple species have been lacking, limiting our understanding of how plastic traits evolve. To address this, we quantified variations in social feeding behaviors across 10 species of Drosophilids, tested the effect of altering rearing context on these behaviors (reared in groups or in isolation) and correlated observed behavioral shifts to accompanying transcriptional changes in the heads of these flies. We observed significant variability in the extent of aggressiveness, the utilization of social cues during food search, and social space preferences across species. The sensitivity of these behaviors to rearing experience also varied: socially naive flies were more aggressive than their socialized conspecifics in some species, and more reserved or identical in others. Despite these differences, the mechanism of socialization appeared to be conserved within the melanogaster subgroup as species could cross-socialize each other, and the transcriptional response to social exposure was significantly conserved. The expression levels of chemosensory-perception genes often varied between species and rearing conditions, supporting a growing body of evidence that behavioral evolution is driven by the differential regulation of this class of genes. The clear differences in behavioral responses to socialization observed in Drosophilids make this an ideal system for continued studies on the genetic basis and evolution of socialization and behavioral plasticity.

The genetic basis of variation in sexual aggression: Evolution versus social plasticity

“…Red asterisks indicate genes that we chose for follow-up candidate gene validation We identified a relatively large number of significant DE genes associated with diverged FC rate (Figure 2). This is in agreement of the growing body of literature showing that behavioural variation is associated with the DE of a large number of genes (Dierick & Greenspan, 2006;Gammie et al, 2007;Immonen et al, 2017;Shultzaberger et al, 2019), rather than a few genes with large effects. The vast majority of our observed differential gene expression effects appeared to be due to either the main effects of selection treatment or prior exposure to females, rather than the interaction of these effects with exposure to teneral females during the trial, or the main effect of exposure to teneral females.…”

Behavioral and environmental contributions to drosophilid social networks

“…Ultimately, the age, diet, and environment of each species was controlled in this study to ascertain the role of genetic differences toward social behavior. There is already evidence that a standard cornmeal diet has minimal effects on social behavior of different Drosophila species (42). Testing for gene-by-environment interactions across social behaviors of drosophilid species is an interesting future direction that can determine whether specific environmental factors, such as temperature and humidity, influence SINs.…”

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.…”