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W2984982009 abstract "Full text Figures and data Side by side Abstract eLife digest Introduction Results Discussion Materials and methods References Decision letter Author response Article and author information Metrics 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. https://doi.org/10.7554/eLife.07423.001 eLife digest Every animal must be able to adapt to threats and changes to their environment that could affect their survival. Some ‘social’ animals, such as honeybees and ants, go further than this, and also transmit information about a threat—and how to survive it—to other members of their species. This helpful behavior is now known to occur to some extent even in animals that have not been considered to be social, like the Drosophila species of fruit fly. Parasitoid wasps lay their eggs in the larvae and pupae of certain insect species. When the wasp eggs hatch, they feed on the host insect, eventually killing it. Drosophila fruit flies have evolved various behaviors to protect their offspring from these wasps. For example, female fruit flies reduce the number of eggs they lay when they are in the presence of a wasp. Kacsoh, Bozler et al. exposed female flies to wasps for a day. These flies produced fewer eggs than flies that were not exposed to wasps and continued to lay fewer eggs for 24 hours after the wasps were removed. Introducing these flies to ‘naive’ flies that had not encountered a wasp caused the naive flies to produce fewer eggs as well. After ruling out several possible ways that the wasp-exposed flies might ‘teach’ the naive flies to produce and lay fewer eggs, Kacsoh, Bozler et al. found that naive flies cannot learn this behavior when they are blind. In addition, exposed flies cannot instruct other flies of the threat if their wings are absent or deformed. These and other findings, therefore, suggest that information about the wasp threat is transmitted through visual cues that involve the wings. Kacsoh, Bozler et al. found that the flies must have certain brain circuits associated with memory and learning to be able to teach others and to reduce the numbers of eggs they lay after the wasp has been removed. This suggests that signals from this brain region must be continually sent out to alter the physiology of the developing eggs in order to maintain the lower rate of egg laying; understanding how flies use visual cues for communication and how the brain signals to the ovary remain key challenges for future work. https://doi.org/10.7554/eLife.07423.002 Introduction 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). This ability to adapt to environmental change is essential for survival, but can such an adaptive response occur in the absence of the direct experience? Well-defined examples of this phenomenon have been observed in what are considered ‘social’ organisms (Franks et al., 2002; Townsend et al., 2011). Yet, 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 now 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. The ability to learn from others influences the choices and behaviors of individuals and allows a group of individuals to share information about a changing environment. It is speculated that social information transmission involves either the ability to feel vicarious reward and punishment or other complex communication strategies to transmit an individual's experience to the community of conspecifics. The potential benefits of adaptive behavior, based on information acquired from others within the community, can give social learners a significant advantage over those that must directly explore and gather environmental information for themselves. Understanding how this information transfer occurs and what the underlying neurological and molecular mechanisms are is critical for a comprehensive view of adaptive behavior across a wide range of taxa. Many species considered as ‘social’ and ‘non-social’ communicate about the environment. Plants have been observed to alter their physiology in response to signaling from another plant (Baldwin and Schultz, 1983). An example of such communication involves salt stress, which has been shown to trigger the release of volatile organic compounds that induce salt resistance in neighboring plants that have yet to experience any salt stress (Lee and Seo, 2014). In animals, the process is speculated to be more complex: honeybees are able to fine tune signals directed at individuals within the hive that elicit highly specific behavioral changes in response to specific environmental cues (Wenner, 1962; Schneider and Lewis, 2004; Richard et al., 2012). Even Drosophila are prone to social cues, altering their decision making based on the behavior of conspecifics (Mery et al., 2009; Sarin and Dukas, 2009; Battesti et al., 2012). It is clear that the once thought ‘fine line’ between social and non-social organisms is beginning to blur, and that social communication is actually much more fundamental to life than originally considered. In animals, this ability to transmit and process information about the environment has been termed ‘social learning’ (Gariepy et al., 2014; Gruter and Leadbeater, 2014). Learning can occur in a social context through olfactory cues, observation and instruction, or by imitation, and thus, is a mechanism for sharing information about a changing environment (Baldwin and Meldau, 2013; Cermakian et al., 2013). The potential benefits of adaptive behavior, based on information acquired from others within the community, can give social learners a significant advantage over those that must directly explore and gather environmental information for themselves. However, in general, the underlying molecular mechanisms of social learning are almost entirely mysterious and remain a terra incognita in terms of the strategies for communication, perception, neural plasticity, and the underlying physiological changes that cause changes in behavior. In this study, we use endoparasitoid wasps to explore social learning in the Drosophila model system with the aim of addressing some of these open questions. Endoparasitoid wasps are ubiquitous keystone species in many ecosystems around the world. These wasps prey on immature stages of other insects, using larva and pupa of certain species as hosts for their own offspring. Such wasps pose a serious threat to juvenile Drosophila, with infection rates as high as 90% in natural populations (Janssen et al., 1988; Driessen et al., 1990; Fleury et al., 2004). Adult Drosophila have evolved complex behavioral changes to protect their offspring from these predatory wasps, including altered food preference and reduced oviposition rates (Lefevre et al., 2012; Kacsoh et al., 2013). Adult Drosophila themselves are not infected by these wasps, thus, making the change in reproductive behavior beneficial only to an anticipated threat to their offspring and not a response to predation itself. A remarkable feature of this altered reproductive behavior is that female Drosophila never having seen this predator can nevertheless robustly and reproducibly respond to it, suggesting an innate recognition of this predator-threat. Here, we use this natural predator system to explore predator threat communication within Drosophila melanogaster and describe the specific learning, memory, and anatomical components necessary for this response. Our findings report the first example of social learning in Drosophila that can be delineated from simple mimicry, through the use of a natural predator. Exposure to the predatory wasp results in a distinct germ line-cell physiological apoptotic response in both flies having seen the wasp (direct experience) or flies having been paired with experienced individuals (social learning), which is clearly independent of mimicry. Furthermore, we address the genetic factors, neural circuits, and behavioral changes necessary for the transmission of this socially learned alteration in germ line physiology. Results Flies respond to wasps by decreasing oviposition and are able to confer this information to naive flies Drosophila melanogaster alters its egg-laying behavior after it encounters parasitoid wasps, which infect fly larvae. This behavioral change entails at least two different and quantifiable behavioral responses. First, if high-ethanol containing food is made available to adult Drosophila, then wasp-exposed females will actively prefer to lay eggs on ethanol-laden food (Kacsoh et al., 2013). Second, if ethanol-containing food is not an option, Drosophila females will depress their egg-laying frequency, presumably to allow for time to search and discover an egg-laying environment that is not wasp infested (Lefevre et al., 2012). Adult Drosophila are not infected by these wasps, thus, making the change in reproductive behavior beneficial only to an anticipated threat to their offspring. To address the question of whether changes in reproductive behavior could be transferred from exposed teacher flies to naive student conspecifics, we examined the underlying physiological, physical, and genetic components of the exposed teacher and naive student flies and asked if these mechanisms rely on learned reproductive behavior. Drosophila were exposed for 24 hr to wasps in cylindrical 7.5-cm long by 1.5-cm diameter tubes arrayed into fly condos of 24-tubes where each tube contained five female flies and one male fly, either with three female wasps (exposed) or with no wasps at all (unexposed) (Figure 1A, see methods and supporting information for details). After 24 hr, food plates were removed and embryos counted. Consistent with previous observations (Lefevre et al., 2012), exposed females reduced their oviposition rate significantly (average unexposed lay ∼65 ± 3.2 eggs; average exposed lay ∼13 ± 1.98 eggs) (Figure 1B). We observed this robust response in at least four different genetic backgrounds including Canton-S (CS), Oregon-R (OreR) (unexposed ∼57 ± 2.84 eggs compared to exposed 13 ± 1.88 eggs on average), w1118 (unexposed ∼25 ± 1.54 eggs compared to exposed ∼1 ± 0.53 egg on average), and transgenic flies carrying Histone H2AvD-GFP (His-GFP) (unexposed ∼108 ± 7.69 eggs compared to exposed 18 ± 1.97 eggs) (Clarkson and Saint, 1999). To test whether this decrease in egg laying can be transmitted from exposed flies to naive females, we exposed Canton-S flies to wasps for 24 hr, then removed the wasps and placed these pre-exposed flies in a new condo with three naive female flies expressing Histone-GFP (His-GFP) for an additional 24 hr (Figure 1A). The His-GFP line was ideal for discriminating mixed populations of non-green fluorescent protein (GFP) and GFP embryos since this histone is clearly visible by 70 min after oviposition (embryonic cell cycle 9) (Foe et al., 1993; Clarkson and Saint, 1999) (Figure 1—figure supplement 1A,B). Oviposition in exposed teacher females was significantly reduced during the 24-hr exposure to wasps (acute depression: 0–24 hr) (53 ± 3.35 compared to 14 ± 1.59 eggs) and this depression persisted for an additional 24-hr post wasp exposure (learned depression: 24–48 hr) (35 ± 2.44 compared to 19 ± 1.33 eggs), relative to age-matched, unexposed sibling controls (Figure 1C, Figure 1—figure supplement 1C). Quantification of total GFP and non-GFP embryos deposited during the 24–48 hr after initial teacher exposure to wasps demonstrated that naive His-GFP student flies had also decreased oviposition, relative to His-GFP siblings mixed with unexposed Canton-S flies (33 ± 2.34 compared to 6 ± 0.86 eggs) (Figure 1C, Figure 1—figure supplement 1C). In the reciprocal experiment, naive Canton-S student flies mixed with pre-exposed His-GFP teacher flies also exhibited a decrease in oviposition (46 ± 2.48 compared to 14 ± 1.34 eggs, see Supplementary files 6,7 for all raw egg numbers) (Figure 1—figure supplement 1D,E). Thus, naive female flies, never experiencing wasp exposure directly, reduced oviposition when encountering exposed flies. The decrease in oviposition of student flies is not due to an effect of the ratio of teacher to student flies. We tested a 1:1 ratio of 3 exposed female teachers to 3 naive female student flies. This elicited a similar reduction in oviposition (Figure 1—figure supplement 1F,G). Interestingly, when we tested a 1:1 ratio of 3 exposed males to 3 naive female student flies, we found no significant decrease in oviposition for students instructed by exposed males (Figure 1—figure supplement 1H,I). This suggests that, under these conditions, only females can transmit predator-response information. Males are neither necessary nor sufficient for the information transfer. Therefore, for all further experiments, we used a teaching cohort of 5 females and 1 male to 3 female students, unless otherwise noted. Figure 1 with 1 supplement see all Download asset Open asset Flies respond to wasps by decreasing oviposition and are able to confer this information to naive flies. (A) Standard exposure setup. (B and C) Percent of eggs laid normalized to unexposed. (B) Wild-type flies unexposed or exposed to wasps. (C) Canton-S teachers and His-GFP students. For (B) and (C), error bars represent standard error (n = 24 biological replicates) (**p < 1.0e-5). https://doi.org/10.7554/eLife.07423.003 Teacher-instructed student flies are unable to become teachers To test whether the decrease in oviposition can be transmitted from students to a new batch of naive flies, we removed Canton-S pre-exposed teacher females from student His-GFP expressing flies and placed the teacher-instructed student flies in a new chamber with 3 new, naive Canton-S flies (Figure 2A). In teacher-instructed student flies, reduced oviposition behavior persisted for 24 hr after they were separated from teacher flies, indicative of a persisting memory of social learning. Interestingly, we found that our teacher-instructed student His-GFP flies were not able to instruct new students, as the naive Canton-S females did not decrease oviposition (Figure 2B, Figure 2—figure supplement 1A). Figure 2 with 1 supplement see all Download asset Open asset Student flies cannot become teachers. (A) Standard exposure setup. (B) Teacher exposed primary student His-GFP flies paired with naive secondary student Canton-S flies. Error bars represent standard error (n = 24 biological replicates) (*p < 0.05, **p < 1.0e-5). https://doi.org/10.7554/eLife.07423.005 We postulated that perhaps information transfer could only occur once between wasp-exposed teachers and student flies, leading to the inability of students to further pass on information and become teachers. To test this, we removed the first cohort of student His-GFP expressing flies and placed the Canton-S pre-exposed teacher female flies in a new chamber with a second cohort of 3 new, naive Canton-S flies (Figure 3A). We found that oviposition depression in exposed teacher females was persistent for an additional 24-hr post wasp exposure (learned depression: 48–72 hr), relative to age-matched, unexposed, sibling controls (Figure 3B). Quantification of total GFP and non-GFP embryos deposited during the 48–72 hr after initial teacher exposure to wasps demonstrated that the second cohort of naive His-GFP student flies had also decreased oviposition, relative to His-GFP siblings mixed with unexposed Canton-S flies (Figure 3B). In the reciprocal experiment, a second cohort of naive Canton-S student flies mixed with pre-exposed His-GFP teacher flies also exhibited a decrease in oviposition (Figure 3C). Our results demonstrate that teachers can instruct multiple cohorts of students, thus, the inability of a student to become a teacher is not due to a limitation in amount a teacher can teach. Figure 3 Download asset Open asset Teacher flies can teach multiple batches of students. (A) Standard exposure setup for teachers teaching multiple batches of students. (B and C) Percent of eggs laid normalized to unexposed. (B) Canton-S flies unexposed or exposed to wasps and paired with primary and secondary His-GFP students. (C) His-GFP flies unexposed or exposed to wasps and paired with primary and secondary Canton-S students. For (B) and (C), error bars represent standard error (n = 24 biological replicates) (**p < 1.0e-5). https://doi.org/10.7554/eLife.07423.007 Wasp exposure induces stage-specific apoptosis in wasp-exposed teachers In order to better understand the physiological basis of how a predator-threat leads to changes in oviposition behavior, we examined the status of egg production in exposed female ovaries. Given that poor nutrition or other stressors can cause egg chambers in the ovaries to be eliminated by apoptosis at oogenesis checkpoints in region-2/3 of the germarium or stage 7/8 egg chambers (the mid-oogenesis checkpoint) (Drummond-Barbosa and Spradling, 2001; McCall, 2004), we hypothesized that the presence of parasitoid wasps could similarly reduce oviposition by triggering an oogenesis checkpoint, and thus, account for depressed oviposition. Therefore, we quantified stage-specific apoptosis in ovaries of exposed females. Dissection of ovaries from females having been exposed to wasps for 24 hr revealed a significant increase in the number of egg chambers exhibiting apoptosis relative to unexposed sibling control females (Supplementary file 1A,B). Interestingly, the majority of apoptosis was observed at the stage 7/8 egg chamber checkpoint, with almost no apoptosis in region 2/3, as visualized by DNA staining with 4', 6-diamidino-2-phenylindole (DAPI), suggesting that the pathway through which apoptosis was being triggered is fundamentally different from previously described apoptotic events (Drummond-Barbosa and Spradling, 2001; McCall, 2004) (Supplementary file 1A,B, Figure 4A–F). Canton-S and His-GFP fly ovaries were easily distinguishable when stained together, thus, making it possible to score apoptosis levels in ovaries of exposed and unexposed females under completely identical conditions (Figure 4—figure supplement 1A–D). Further confirmation that wasp exposure triggered a true apoptotic event is evidenced by the presence of characteristic DAPI-intense pychnotic nurse cell nuclei, by terminal deoxynucleotide transferase dUTP nick end labeling (TUNEL) stain that detects fragmented DNA (Figure 4G–J and Figure 4—figure supplement 1E,F), and activated caspase-3 staining (Figure 4—figure supplement 1G–J): All positive markers of the cell death process (McCall, 2004). We noted that both DAPI and TUNEL were readily detected in apoptotic stage 12/13 nurse cells in both exposed and unexposed females at similar levels. Developmentally regulated cell death is normally expected to eliminate late-stage nurse cells in maturing oocytes, thus, serving as an internal control for the level of detected apoptosis in exposed and unexposed females (Supplementary file 1A,B). Similar to the reduced oviposition behavior observed, this physiologically triggered apoptosis specifically of stage 7/8 egg chambers persisted well beyond the period of initial wasp exposure (Figure 4A,B, Supplementary file 1C,D). Figure 4 with 1 supplement see all Download asset Open asset Stage-specific apoptosis observed in wasp-exposed teachers and teacher-exposed student flies. (A and B) Average percent of apoptotic events for stage 7/8 egg chambers. (A) Canton-S exposed and unexposed ovary apoptosis. (B) His-GFP exposed and unexposed ovary apoptosis. (C to D) Canton-S unexposed/exposed ovariole. (E to F) His-GFP unexposed/exposed ovariole. (G to H) Canton-S transferase dUTP nick end labeling (TUNEL) staining performed on exposed fly ovaries. (I to J) His-GFPTUNEL staining. For (A) and (B), error bars represent standard error (n = 3 biological replicates from which 12 ovaries were scored for each group) (*p < 0.05). Scale bars, 20 μm. https://doi.org/10.7554/eLife.07423.008 Flies continue to eat high-protein diet following wasp exposure but still depress oviposition We considered the possibility that exposure to wasps could change fly feeding behavior, and subsequent poor nutrition could trigger the mid-oogenesis checkpoint (Drummond-Barbosa and Spradling, 2001). We gave both exposed and unexposed flies a high-protein yeast food stained with red food dye to visualize food intake. We found that both wasp-exposed and unexposed flies exhibited a similar amount of high-protein yeast food intake even when given a choice to feed on normal food without yeast by visualizing the red dye in the fly abdomens (Figure 5A–D, Figure 5—figure supplement 1A–D). The red yeast paste was placed on instant Drosophila media, which turns blue upon contact with water, allowing us to visualize whether flies are preferring high (red)- or low (blue)- nutrient food (Figure 5—figure supplement 1E–L). 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). Thus, the mid-oogenesis apoptosis checkpoint triggered in exposed flies is not due to a poor nutrition intake. These data are indicative of a predator-induced neuroendocrine signaling pathway that impinges on a pathway specifically controlling mid-oogenesis specifically (stage 7/8 but not stage 2/3), and therefore, is likely different from the previously described poor nutrition oogenesis checkpoint. Figure 5 with 1 supplement see all Download asset Open asset Flies continue to eat high-protein diet following wasp exposure but still depress oviposition. Continued oviposition depression cannot be explained by a lack of nutrient intake that normally inactivates insulin signaling. The high-nutrient intake by exposed female flies suggests that an active insulin signaling pathway is inhibited or bypassed downstream of nutrient sensing. (A) Exposed and unexposed flies anesthetized immediately after 24-hr exposure period shows red food in abdomens. (B) Lateral view of unexposed fly. (C) Lateral view of exposed fly. (D) Percent of male and female flies with red food in abdomen, error bars are 95% confidence intervals. (E) Percent of eggs laid normalized to unexposed following 24-hr exposure period. All eggs on the food plate were counted, including eggs on the yeast paste. (F) Representative ovary dissected from unexposed fly. 36 total ovaries were dissected and examined across 3 replicates for each treatment. (G) Ovary dissected from exposed fly. Scale bar for (F) to (G) is 1.0 mm. (H) Average percent apoptosis in mid-oogenesis checkpoint for unexposed and exposed Canton S. For (D), (E), and (H), error bars represent standard error (n = 3 biological replicates. For (D), 100 female and 20 male flies were counted per replicate. For (E), 3 egg lay plates were counted per treatment. For (H), 3 biological replicates from which 12 ovaries were scored for each group) (*p < 0.05). https://doi.org/10.7554/eLife.07423.010 Naive student flies induce apoptosis when paired with wasp-exposed teachers To test whether triggering of the mid-oogenesis check point could be transmitted from experienced, wasp-exposed females to naive females, we mixed teacher and student flies as described above. Naive student flies mixed with exposed teachers showed apoptosis at the stage 7/8 checkpoint, as did their teachers (Supplementary file 1C,D,F,G, Figure 4A–B). Students mixed with unexposed, ‘mock’ teachers did not show significant levels of increased apoptosis in the ovary (Supplementary file 1C,D,F,G, Figure 4A–B). Thus, in naive student flies, transmitted information from exposed teacher flies results in triggering a specific-apoptotic mid-oogenesis checkpoint in students that have learned from teachers' experience. These data indicate that teacher flies transmit instructive cues to student flies that student flies receive these cues and then process them in a manner that leads to apoptosis of egg precursor cells and reduced oviposition. Oviposition depression in teacher and student requires the caspase encoding genes Dcp-1 and drice, which are dispensable for teacher behavior One explanation for social learning could be that student flies instinctively mimic the behavior of more experienced teacher flies. Repeated episodes of imitative behavior could lead to a strengthening of neural circuits that underlie this behavior. We explored this idea by testing if wasp-exposed flies that are genetically unable to suppress oviposition efficiency are still able to successfully act as teacher flies. The Drosophila mid-oogenesis checkpoint is known to activate effector caspases Dcp-1 and drice (McCall, 2004). Additionally, the caspase-3 staining we performed on wasp-exposed teacher ovaries recognizes effector caspases Dcp-1 and drice (Figure 4—figure supplement 1G–J), leading us to hypothesize that these caspases are important in oviposition depression in teacher and student flies as a response to parasitoid wasps. By using a maternal α-Tubulin > Gal4 driver to express an RNA-hairpin targeting mRNA from each of these genes, we were able to reverse both the decrease in oviposition as well as the increase of stage 7/8 egg chamber apoptosis of wasp-exposed females, while RNAi depletion of these caspases had no effect on oviposition of unexposed females (Figure 6—figure supplement 2A,B). This provides further evidence that the stage 7/8 egg chamber apoptosis and corresponding oviposition decrease is a specific physiological checkpoint, similar to that previously described for poor nutritional intake (Figure 4A,B, Supplementary file 1H) (Drummond-Barbosa and Spradling, 2001). We considered the possibility that ovarian apoptosis could produce secondary signals important for conveying information to naive flies, which in turn triggers apoptosis in student ovaries. To test this, we used teacher flies that were incapable of triggering apoptosis because of RNAi depletion of Dcp-1 or drice, specifically in developing egg chambers. Strikingly, following wasp exposure, flies, depleted of germ line Dcp-1 or drice function, were still excellent teachers capable of cueing naive student flies to decrease their oviposition and induce apoptosis at the stage 7/8 mid-oogenesis checkpoint in the students' ovaries (Figure 6A,B, Figure 6—figure supplement 1 A-B and G, Supplementary file 1I,J). The finding that Dcp-1 and drice deficient females incapable of depressing oviposition can nevertheless convey critical cues to naive students demonstrates that the depressed oviposition response can be decoupled from the process required for teacher–student information transfer. Thus, information transfer in this context is not due to secondary effects of ovarian cell death. Interestingly, Dcp-1- and drice-deficient student females could not depress oviposition in response to exposed, wild-type teachers, suggesting that the same effector caspases activated in exposed teachers are also needed for oviposition depression in students (Figure 6C–D). Control, parental lines were found to behave as wild type as both teachers and students (Figure 6—figure supplement 1A–F). We tested two additional Dcp-1 (Dcp-12 and Dcp-13) (Etchegaray et al., 2012) mutant lines that displayed the same phenotype as the RNAi result (Figure 6E–F, Figure 6—figure supplement 1G,H). We conclude that the depressed oviposition in student flies cannot be from simple mimicry. Figure 6 with 2 supplements see all Download asset Open asset Socially transmitted oviposition depression in response to wasp exposure acts through the mid-oogenesis checkpoint. (A to F) Percent of eggs laid normalized to unexposed. (A and C) Drice RNAi-knockdown as teachers and students. (B and D) Dcp-1 RNAi-knockdown as teachers and students. (E to F) Dcp-12 as teachers and students." @default.
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W2984982009 title "Author response: Social communication of predator-induced changes in Drosophila behavior and germ line physiology" @default.
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