Drinking water is innately rewarding to thirsty animals. In addition, the consumed value can be assigned to behavioral actions and predictive sensory cues by associative learning. Here we show that thirst converts water avoidance into water-seeking in naïve Drosophila. Thirst also permits flies to learn olfactory cues paired with water reward. Water learning requires water taste and <40 water-responsive dopaminergic neurons that innervate a restricted zone of the mushroom body γ lobe. These water learning neurons are different from those that are critical to convey the reinforcing effects of sugar. Naïve water-seeking behavior in thirsty flies does not require water taste but relies on another subset of water-responsive dopaminergic neurons that target the mushroom body β′ lobe. Furthermore, these naïve water-approach neurons are not required for learned water-seeking. Our results therefore demonstrate that naïve and learned water-seeking, and water learning, utilize separable neural circuitry in the brain of thirsty flies.
Queens and workers of eusocial Hymenoptera are considered homologous to the reproductive and brood care phases of an ancestral subsocial life cycle. However, the molecular mechanisms underlying the evolution of reproductive division of labor remain obscure. Using a brain transcriptomics screen, we identified a single gene, (), which is always up-regulated in ant reproductives, likely because they are better nourished than their nonreproductive nestmates. In clonal raider ants (), larval signals inhibit adult reproduction by suppressing , thus producing a colony reproductive cycle reminiscent of ancestral subsociality. However, increasing ILP2 peptide levels overrides larval suppression, thereby breaking the colony cycle and inducing a stable division of labor. These findings suggest a simple model for the origin of ant eusociality via nutritionally determined reproductive asymmetries potentially amplified by larval signals.
The effects of heterogeneity in group composition remain a major hurdle to our understanding of collective behavior across disciplines. In social insects, division of labor (DOL) is an emergent, colony-level trait thought to depend on colony composition. Theoretically, behavioral response threshold models have most commonly been employed to investigate the impact of heterogeneity on DOL. However, empirical studies that systematically test their predictions are lacking because they require control over colony composition and the ability to monitor individual behavior in groups, both of which are challenging. Here, we employ automated behavioral tracking in 120 colonies of the clonal raider ant with unparalleled control over genetic, morphological, and demographic composition. We find that each of these sources of variation in colony composition generates a distinct pattern of behavioral organization, ranging from the amplification to the dampening of inherent behavioral differences in heterogeneous colonies. Furthermore, larvae modulate interactions between adults, exacerbating the apparent complexity. Models based on threshold variation alone only partially recapitulate these empirical patterns. However, by incorporating the potential for variability in task efficiency among adults and task demand among larvae, we account for all the observed phenomena. Our findings highlight the significance of previously overlooked parameters pertaining to both larvae and workers, allow the formulation of theoretical predictions for increasing colony complexity, and suggest new avenues of empirical study.
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