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Official websites use. Share sensitive information only on official, secure websites. Cooper, University of Kentucky, United States. The use, distribution or reproduction in other forums is permitted, provided the original author s and the copyright owner s are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. The development of high-throughput behavioral assays, where numerous individual animals can be analyzed in various experimental conditions, has facilitated the study of animal personality. Previous research showed that isogenic Drosophila melanogaster flies exhibit striking individual non-heritable locomotor handedness. The variability of this trait, i. This suggests that the brain can dynamically regulate the extent of animal personality. It has been recently shown that predators can induce changes in prey phenotypes via lethal or non-lethal effects affecting the serotonergic signaling system. The results of this study demonstrate a negative association between the unpredictability of turning behavior of fruit flies and the hunting success of their predators. We also show that the neurotransmitter serotonin controls predator-induced changes in the turning variability of fruit flies, regulating the dynamic control of behavioral predictability. Keywords: Drosophila melanogaster , behavioral predictability, serotonin, survival under predation, turning behavior. Living organisms adapt to varying environmental conditions by attempting to modify their morphological, biochemical, and behavioral phenotypes Xue et al. Prey individuals respond to predator acoustic, visual, chemical, and other cues, which improve the chances of prey to escape predator attacks Lima, ; Preisser et al. When developing under predation risk, prey individuals often grow smaller, more agile, less palatable, or more cryptic, conferring fitness benefits associated with a modified phenotype Krams et al. Fruit flies Drosophila melanogaster raised during the larval stage together with jumping spiders had more nitrogen in their bodies and lower body lipid reserves, while they had a higher climbing speed in the negative geotaxis test than flies grown without spiders Krams et al. Moreover, fruit flies grown together with predators had significantly higher adult survival ability when exposed to predation than flies grown in a predator-free environment Krams et al. This shows that predator exposure in ontogeny may directly affect survival in adulthood. However, it is not always clear what changes in the neural and behavioral phenotypes facilitate the escape performance of fruit flies at risk of predation. Ambush predators remain concealed and motionless until the prey comes within ambush distance before pouncing. If the prey survives in the initial attack, the predator often does not pursue it Scharf et al. Fruit flies exhibit striking locomotor handedness during their exploratory behavior Buchanan et al. During exploratory walking in symmetrical environments, individual fruit flies exhibit significant bias in their left vs. This behavioral idiosyncrasy is present across different fly lines and genotypes. Moreover, the flies differing in neural state Buchanan et al. Specifically, the magnitude of turning bias variation is under the control of columnar neurons within the central complex, a brain region implicated in motor planning and execution of fruit fly behavior Buchanan et al. Turn bias variability has a complex genetic architecture involving many genes, particularly those involved in circuit development during pupation, including specifically teneurin-A Ayroles et al. Silencing the central complex columnar neurons or knocking down teneurin-A expression increased exploratory laterality in fruit fly turning behavior, with more extreme leftiness and rightiness, decreasing the predictability of turning choices across individuals. In the mathematical limit, a population with maximal turn bias unpredictability across individuals composed of equal parts extreme righties and extreme lefties would consist of animals with high within-individual predictability making exclusively right or left turns, respectively. But in experiments, examining microhabitat occupancy, a positive correlation was observed between population-level behavioral predictability and individual predictability Stamps et al. Neurotransmitters are known to control the predictability of behavior Maloney, The predictability of phototaxis in flies is under the control of the neurotransmitter serotonin 5-HT , and the lowest predictability of turning choices were found in white-eyed w mutants Kain et al. With respect to turn bias variability, both increasing and decreasing 5-HT with metabolic drugs had small effects of reducing turn bias variability, averaged across many genotypes de Bivort et al. Applying serotonin precursor increases variability in locomotor speed, and there is a bidirectional effect of altering serotonin levels on variability in higher-order left-right turn sequences de Bivort et al. All these effects are small, but they generally suggest a role for serotonin in decreasing locomotor predictability. It has been recently shown that predator-induced stress influences a number of 5-HT-associated behavioral and physiological effects in fruit flies grown together with spiders during larval development Krama et al. This implies that predators may influence the brain to dynamically regulate the predictability of the turning behavior of fruit flies to improve their survival under predation risk. In this study, we tested whether fruit flies reared with spiders exhibit lower predictability in their turning behavior in Y-mazes Buchanan et al. We also studied the survival of fruit flies grown with and without spiders. We hypothesized that predator presence during larval development might make the turning behavior of adult fruit flies less predictable and improve their survival. Individual-to-individual differences in experimental behavioral observations reflect persistent idiosyncrasies requiring large samples Sih et al. Small mazes arrayed in parallel allow the measurement of behavior of hundreds of individual flies simultaneously de Bivort et al. The wild type strain of D. This line of OR was inbred for 10 generations before behavioral experiments were collected. We used adult jumping spiders Phidippus apacheanus as predators to affect the development and behavior of fruit flies. The adult spiders were caught in Florida and delivered by the supplier phids. Developmental speed significantly affects body mass, elemental body composition, food uptake, and fat metabolism of D. This makes the flies with rapid, intermediate, and slow development different in their biochemical and morphological phenotype, which needs to be considered when planning research. To avoid the developmental speed-related confounding effects, we used only rapidly developing fruit flies in this study. We defined rapidly developing flies as individuals that eclose between 9. Rapidly growing fruit flies experience relatively low stress levels during ontogeny Krams et al. We isolated fruit flies using carbon dioxide anesthesia within 6—7 h after eclosion. Vials with Drosophila larvae were randomly divided into two groups: one that was exposed to spiders and one that was not. In the spider-treated group, a single P. The vials did not have stoppers, giving the spider free access to the developing flies as well as the fly media. Developing flies were also exposed to the odor of the spider throughout the container. Flies for behavioral and survival assays were removed the day after they eclosed, without anesthesia, and transferred to drug-treated vials as described below. We had two main experimental groups of D. The drug stock solutions were vortex-mixed and added to food powder. The flies were 5—7 days old at the moment of behavioral experiments. Honegger et al. Schematic of the turning assay A and the survival experiment B this figure was made using some sample images from BioRender. Since using variance as a phenotypic trait requires large sample sizes Caballero et al. We put flies into an array containing 95 individual Y-mazes consisting of three symmetrical arms each 12 mm long fabricated from laser-cut acrylic Figure 1A. Maze arrays were illuminated from below with a grid of white LEDs K, Knema below acrylic diffusers. We recorded the turning behavior of 3—6-day old flies, the standard age for measuring this behavior, for 2 h. Data from the small portion of individuals making fewer than 30 turns were discarded. Each fly was used only once. We estimated MAD for each experimental group. Upon eclosion, adult F1 flies were assayed on days 4—5. Thus, we had ten jars for each survival group 48 jars containing fruit flies for 12 h during daylight time Krams et al. We did not use carbon dioxide anesthesia to move fruit flies from their stock vials to survival jars. During survival tests, we placed one young c. The spiders had access to water in a polycarbonate dish and a fitted luffa sponge. The spiders were deprived of food for c. Each spider was used only once. To compare behavioral MADs across experimental groups, we used the permutation test. The data table of the proportion of right turns taken was shuffled, and the obtained MAD scores among randomized groups were compared to those of unshuffled data. The procedure was repeated 99, times, and P -values were calculated as the proportion of instances when the shuffled difference between group pairs was larger than the unshuffled difference. We performed a two-way ANOVA to assess the effect of development conditions and drugs added to the food on the subsequent survival of adult flies under predation risk. Turn bias proportion of right turns was compared between groups using Kruskal—Wallis Test by ranks. One Sample Wilcoxon Signed Rank Test was used to assess turn bias deviation from equal amount of right and left turns. We also compared the number of turns taken by fruit flies in the y-maze per minute using the Mann—Whitney U test. Data analyses were performed in the R environment version 4. P -values of multiple comparisons were adjusted using Benjamini—Hochberg procedure Benjamini and Hochberg, Turn bias variability MAD of fruit flies reared with and without spiders receiving different drug treatments. Proportion of right turns by each group was also not significantly different from 0. Turn bias of fruit flies reared with and without spiders and receiving different drug treatments during development. Thick lines indicate the median, and boxes indicate the 25th and 75th percentile. A dashed horizontal line indicates 0. Thick lines indicate the median, boxes show the Q1 and Q3 quartiles, and whiskers represent the upper and lower quartile, excluding outliers. Black dots represent outliers: data points more than 1. Flies reared with spiders made significantly fewer turns per unit time 2. Feeding 5-HTP to flies reared with spiders significantly increased the turn rate 3. The flies reared with predators were previously exposed to predation during the larval stage, while in the control group, the flies were raised without jumping spiders. Black dots represent outliers data points more than 1. Survival percentage of adult fruit flies during a h exposure to predation by jumping spiders. The flies reared with predators were exposed to predation during the larval stage; flies in the control group were raised without jumping spiders. The presence of predators is known to alter prey morphology McCollum and Leimberger, ; Hossie et al. In this study, we found that the turning choices of fruit flies grown with predators are less predictable than that of flies grown in a predator-free environment. We also show that flies raised with predators survived under predation by spiders significantly better than flies grown without predators. We also show with pharmacological experiments that the effects of predator-rearing on turning variability and survival of D. However, these serotonin-associated effects applied only for fruit flies grown with spiders. Unpredictable and erratic turning behavior in some animals makes them more challenging to attack Yager et al. Individual insects can exhibit substantial differences in escape behaviors, even in the absence of genetic variation Schuett et al. Our results suggest a link between less predictable turning behavior and better survival under predation risk by jumping spiders that are sit-and-wait predators. One explanation is that growing up with predators provides prey with signals that are not generated by transient contact with predators post-development. Perhaps the effect of these signals is mediated by serotonergic neuromodulation during prey development. Some previous work has shown that fruit flies reared in identical lab environments show broad diversity in their phototactic choices, variability which is under the control of 5-HT Kain et al. Notably, inhibiting 5-HT synthesis was associated with higher phototactic variability — here we observed that inhibiting 5-HT reduced the excess turn bias variability seen in flies reared with spiders. Geographic variation of fruit fly phototaxis was consistent with a negative relationship between 5-HT and variability of phototactic choices. Flies from northern climates grow on food relatively deficient in the metabolic precursors of serotonin and had lower predictability of phototactic choices Krams I. Thus, the association between 5-HT and behavioral predictability went in opposite directions in the present study and previous work examining phototaxis. These contradictory results suggest that the control of 5-HT over different behaviors may lead to different results, probably because different serotonin-responsive neuronal circuits are involved in different behaviors. To better understand the developmental, epigenetic and neurophysiological changes caused by direct predation and non-lethal predator presence, more study of behavior-specific neurobiological effects is required. Our results support the results by Pantoja et al. They found that zebrafish individuals show significant variation in acoustic startle responses. These responses are linked with the neurosecretion of dorsal raphe neurons Pantoja et al. It was shown that zebrafish individuals show a higher fraction of serotonergic dorsal raphe nucleus neurons active during predator attacks. Pantoja et al. Together, these results suggest the importance of serotonergic signaling in the CNS and its ontogenetic development in establishing a distribution of antipredator behaviors across individuals. The results of this study may have evolutionary implications. It is known that without phenotypic variation, there would be no evolution by natural selection. This suggests that asymmetries within the brain predispose the animal to go one way rather than the other and that neural activity influences the variation between animals Buchanan et al. However, explaining the proximate origins of changes in behavioral variability as a response to environmental challenges is not easy. Behavioral phenotypes emerge from many different levels of biological organization, including sensing of predators in the environment, adaptive gene expression, and even stochasticity in gene expression Raj et al. This study found that flies reared with spiders were less mobile than control flies. Our recent study shows that predator stress during larval development of Drosophila impairs carbohydrate metabolism by systemic inhibition of Akt protein kinase, which is a central regulator of glucose uptake Krama et al. This metabolic disorder is a likely cause of developing a diabetes-like biochemical and behavioral phenotype. An inability to metabolize glucose shifts the metabolism of fruit flies to triglyceride consumption, which decreases walking activity and might be a direct reason for the enhanced survival of fruit flies grown with spiders. Consistent with this idea, carbohydrate metabolism was found as one of the molecular functions most enriched in genes whose expression variation predicts variation in locomotor activity among individual isogenic flies Werkhoven et al. However, the mechanism causing the higher variability of the turning behavior in flies with a diabetes-like phenotype remains unknown. Antipredator behavior consists of a complex set of behavioral and physiological reactions and therefore likely involves neural pathways other than 5-HT. Omura et al. This suggests that future research on the neural regulation of antipredator responses in fruit flies should examine the effects of several neurotransmitters and their possible interactions. Experimental manipulations targeting more than one neuromodulator may be essential, as one neuromodulator can alter the efficacy of other neuromodulators Niederkofler et al. Finally, animals may respond to neuromodulators differentially based on their personalities Krams et al. The complex interactions of neuromodulators and their behavior-specific effects on predictability will make this a rich and challenging area of research. All authors contributed to the article and approved the submitted version. We thank Dr. We are thankful to Don Cadle from Phids. We thank Professors Christine R. Boake, Todd M. Freeberg, and Gordon M. Burghardt for their support during initial phases of this study and Professors Jae H. Bembenek kindly provided access to their lab facilities at Knoxville. We also thank Sudershana Nair and Kristers-Raivo Krams for their support at various stages of the study. This study was also supported by the Fulbright Program of the U. Department of State. SP was supported by a grant of the European Social Fund 8. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher. This section collects any data citations, data availability statements, or supplementary materials included in this article. As a library, NLM provides access to scientific literature. Front Behav Neurosci. Development under predation risk increases serotonin-signaling, variability of turning behavior and survival in adult fruit flies Drosophila melanogaster Tatjana Krama Tatjana Krama 1 Department of Biotechnology, Institute of Life Sciences and Technologies, Daugavpils University, Daugavpils, Latvia. Find articles by Tatjana Krama. Find articles by Ronalds Krams. Find articles by Tatjana Grigorjeva. Find articles by Giedrius Trakimas. Find articles by Sergejs Popovs. Find articles by Krists Zants. Find articles by Didzis Elferts. Find articles by Markus J Rantala. Find articles by Eriks Sledevskis. Find articles by Benjamin L de Bivort. Find articles by Indrikis A Krams. Krams, indrikis. Received Mar 18; Accepted May 9; Collection date This article has been corrected. 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