Abstract
Behavioral adaptation to environmental threats and subsequent social transmission of adaptive behavior has evolutionary implications. In Drosophila, exposure to parasitoid wasps leads to a sharp decline in oviposition. We show that exposure to predator elicits both an acute and learned oviposition depression, mediated through the visual system. However, long-term persistence of oviposition depression after predator removal requires neuronal signaling functions, a functional mushroom body, and neurally driven apoptosis of oocytes through effector caspases. Strikingly, wasp-exposed flies (teachers) can transmit egg-retention behavior and trigger ovarian apoptosis in naive, unexposed flies (students). Acquisition and behavioral execution of this socially learned behavior by naive flies requires all of the factors needed for primary learning. The ability to teach does not require ovarian apoptosis. This work provides new insight into genetic and physiological mechanisms that underlie an ecologically relevant form of learning and mechanisms for its social transmission.
Highlights
All organisms must acquire and respond to information about their environment
We found that even in the presence of high-protein yeast food, exposed flies still depressed oviposition when compared to unexposed controls, in addition to having apoptosis induced at the egg chamber stage 7/8 checkpoint (Figure 5E–G, Figure 5—figure supplement 1M–T, Supplementary file 1E)
In cases when RU486 laden food was fed to flies containing the mushroom body (MB) Gene Switch and green fluorescent protein (GFP) nuclear localization signal construct, we find that 24 hr is sufficient to induce GFP signal localized to the MB, whereas food lacking RU486 does not induce GFP after 24 hr (Figure 15E–G, Figure 15—figure supplement 1E–G)
Summary
All organisms must acquire and respond to information about their environment. Some changes in the environment are predictable or periodic, like light/dark or seasonal cycles that result in organismal adaptation manifesting as physiological changes in order to optimize survival and fitness in the context of a changing environment (Baldwin and Meldau, 2013; Cermakian et al, 2013). Emerging studies are providing mounting evidence to suggest that the use of social cues extend far beyond the traditional notions of social animals: organisms once viewed as asocial in nature are known to have advanced forms of social communication (Gariepy et al, 2014). This social transmission of information can result in distinct behavioral changes, based on another individual’s set of experiences.
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