Development under predation risk increases serotonin-signaling, variability of turning behavior and survival in adult fruit flies Drosophila melanogaster

Tatjana Krama; Māris Munkevics; Ronalds Krams; Tatjana Grigorjeva; Giedrius Trakimas; Priit Jõers; Sergejs Popovs; Krists Zants; Didzis Elferts; Markus J Rantala; Eriks Sledevskis; Jorge Contreras-Garduño; Benjamin L de Bivort; Indrikis A Krams

doi:10.3389/fnbeh.2023.1189301

Development under predation risk increases serotonin-signaling, variability of turning behavior and survival in adult fruit flies Drosophila melanogaster

Front Behav Neurosci. 2023 May 25:17:1189301. doi: 10.3389/fnbeh.2023.1189301. eCollection 2023.

Authors

Tatjana Krama^{1

2}, Māris Munkevics^{1

3}, Ronalds Krams^{1

2}, Tatjana Grigorjeva¹, Giedrius Trakimas^{1

4}, Priit Jõers⁵, Sergejs Popovs¹, Krists Zants³, Didzis Elferts⁶, Markus J Rantala⁷, Eriks Sledevskis⁸, Jorge Contreras-Garduño^{9

10}, Benjamin L de Bivort¹¹, Indrikis A Krams^{3

12

13

14}

Affiliations

¹ Department of Biotechnology, Institute of Life Sciences and Technologies, Daugavpils University, Daugavpils, Latvia.
² Chair of Plant Health, Estonian University of Life Sciences, Tartu, Estonia.
³ Department of Zoology and Animal Ecology, Faculty of Biology, University of Latvia, Riga, Latvia.
⁴ Institute of Biosciences, Vilnius University, Vilnius, Lithuania.
⁵ Institute of Molecular and Cell Biology, University of Tartu, Tartu, Estonia.
⁶ Department of Botany and Ecology, Faculty of Biology, University of Latvia, Riga, Latvia.
⁷ Department of Biology, Turku Brain and Mind Center, University of Turku, Turku, Finland.
⁸ Department of Technology, Institute of Life Sciences and Technologies, Daugavpils University, Daugavpils, Latvia.
⁹ Escuela Nacional de Estudios Superiores, Universidad Nacional Autónoma de México, Morelia, Mexico.
¹⁰ Institute for Evolution and Biodiversity, University of Münster, Münster, Germany.
¹¹ Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, United States.
¹² Latvian Biomedical Research and Study Centre, Riga, Latvia.
¹³ Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia.
¹⁴ Department of Psychology, University of Tennessee, Knoxville, Knoxville, TN, United States.

Abstract

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.e., the predictability of left-right turn biases, varies across genotypes and under the influence of neural activity in specific circuits. 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. In this study, we tested whether fruit flies grown with predators exhibit higher variability/lower predictability in their turning behavior and higher survival than those grown with no predators in their environment. We confirmed these predictions and found that both effects were blocked when flies were fed an inhibitor (αMW) of serotonin synthesis. 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.

Grants and funding

This study was provided by the Latvian Council of Science to IK and TK (grants lzp-2020/2-0271, lzp-2021/1-0277, and lzp-2022/1-0348), the Estonian Research Council (Eesti Teadusagentuur; grant PUT1223). This study was also supported by the Fulbright Program of the U.S. Department of State. GT was supported by the Vilnius University Science Promotion Fund grant (MSF-JM-1/2021). BB was supported by a Sloan Research Fellowship, a Klingenstein-Simons Fellowship Award, a Smith Family Odyssey Award, a Harvard/MIT Basic Neuroscience Grant, and a National Science Foundation grant no. IOS-1557913. SP was supported by a grant of the European Social Fund (8.2.2.0/20/I/003).