Serotoninergic Modulation of Phototactic Variability Underpins a Bet-Hedging Strategy in Drosophila melanogaster

Abstract

When organisms’ environmental conditions vary unpredictably in time, it can be advantageous for individuals to hedge their phenotypic bets. It has been shown that a bet-hedging strategy possibly underlies the high inter-individual diversity of phototactic choice in Drosophila melanogaster. This study shows that fruit flies from a population living in a boreal and relatively unpredictable climate have more variable variable phototactic biases than fruit flies from a more stable tropical climate, consistent with bet-hedging theory. We experimentally show that phototactic variability of D. melanogaster is regulated by the neurotransmitter serotonin (5-HT), which acts as a suppressor of the variability of phototactic choices. When fed 5-HT precursor, boreal flies exhibited lower variability, and they were insensitive to 5-HT inhibitor. The opposite pattern was seen in the tropical flies. Thus, the reduction of 5-HT in fruit flies’ brains may be the mechanistic basis of an adaptive bet-hedging strategy in a less predictable boreal climate.

Neuromodulation and Individuality

“…The degree to which individuals within an isogenic population show divergent preferences is strongly influenced by genetics, as shown by studies showing differing amounts of individuality between isogenic populations with different genetic backgrounds ( Ayroles et al, 2015 ; Bruijning et al, 2020 ), demonstrating that intra-genotypic variability is under evolutionary control. This is supported by observed differences in population variability that match theoretical predictions of environments where variability provides a fitness advantage ( Akhund-Zade et al, 2020 ; Krams et al, 2021 ). One key proposed mechanism for the regulation of individuality is neuromodulation.…”

Precise Quantification of Behavioral Individuality From 80 Million Decisions Across 183,000 Flies

“…This two-dimensional distribution had two conspicuous features: an uncorrelated mode containing the vast majority of the flies, and a smaller mode exhibiting a negative linear relationship between turn switchiness and number of turns. The flies in this second mode were nearly all reared on potato flake media [which was sometimes supplemented with drugs targeting the neurotransmitter serotonin; Dierick and Greenspan (2007) , Kain et al (2012) , and Krams et al (2021) ]. Of these flies, approximately 296 flies were reared on media including the serotonin inhibitor aMW, 429 were reared on the serotonin precursor 5-HTP, and 942 were reared on control media.…”

“…Neuromodulation may have a special role in the control of behavioral variability ( Maloney, 2021 ), e.g., phototaxis ( Kain et al, 2012 ; Krams et al, 2021 ) and olfactory preference ( Honegger et al, 2020 ). We conducted experiments to see if serotonin modulation controls variability of locomotor behaviors in the Y-maze.…”

Variation and Variability in Drosophila Grooming Behavior

“…The fate of the passenger pigeons, hunted to death while flocking together, illustrates the dangers of behavioral homogeneity ( Murray et al, 2017 ). The degree of variability in behavior can be selected for as a bet-hedging strategy against unstable environmental conditions ( Kain et al, 2015 ; Krams et al, 2021 ). Genetic factors contribute to variability in fly visual, olfactory, and locomotor behaviors ( Ayroles et al, 2015 ; Honegger et al, 2019 ; Linneweber et al, 2020 ).…”