Sexually Dimorphic Regulation of Behavioral States by Dopamine in Caenorhabditis elegans

Abstract

Sex differences in behavior allow animals to effectively mate and reproduce. However, the mechanism by which biological sex regulates behavioral states, which underlie the regulation of sex-shared behaviors, such as locomotion, is largely unknown. In this study, we studied sex differences in the behavioral states of Caenorhabditis elegans and found that males spend less time in a low locomotor activity state than hermaphrodites and that dopamine generates this sex difference. In males, dopamine reduces the low activity state by acting in the same pathway as polycystic kidney disease-related genes that function in male-specific neurons. In hermaphrodites, dopamine increases the low activity state by suppression of octopamine signaling in the sex-shared SIA neurons, which have reduced responsiveness to octopamine in males. Furthermore, dopamine promotes exploration both inside and outside of bacterial lawn (the food source) in males and suppresses it in hermaphrodites. These results demonstrate that sexually dimorphic signaling allows the same neuromodulator to promote adaptive behavior for each sex.

Sperm regulates locomotor activity ofC. eleganshermaphrodites

“…We recorded the behavior of individually placed animals and determined the average speed and average angular speed of 10-second intervals. Consistent with previous studies [11,12,14], wildtype hermaphrodite animals exhibited low speed and high angular speed. High angular speed indicates frequent turning of animals.…”

“…The position of the animals within the bacterial lawn was obtained using a custom-written code in Python and the average speed and angular speed were determined. To analyze behavioral states, the average speed and angular speed of 10-sec intervals were determined and plotted [11]. Data points located above a predefined line were classified as roaming and those below were categorized as dwelling, similarly as described in a previously study [12].…”

Regulation and modulation of biogenic amine neurotransmission in Drosophila and Caenorhabditis elegans

“…Ordinary sinusoidal movements of the worm and several essential life processes including egg-laying and locomotion have been shown to be coordinated by DA ( Cermak et al, 2020 ). Further, the neurotransmitter is responsible for increased movement in males while searching for mates; as well as repression in hermaphrodites which rely on self-fertilization ( Suo et al, 2019 ). A key study on DA receptors delineated an antagonistic relationship in the regulation of locomotion between the D2-like receptor, DOP-3, and the D1-like receptor, DOP-1, such that a knockout of the former led to locomotion impairments that were reversed by a knockout of the latter.…”

Neuromodulators: an essential part of survival

“…DA is synthesized in eight neurons (ADEL/R, CEPDL/R, CEPVL/R, and PDEL/R) in hermaphrodites and in six additional neurons (R5AL/R, R7AL/R, R9AL/R) in males by the tyrosine hydroxylase CAT-2, which catalyzes the rate-limiting step in dopamine synthesis (Lints & Emmons, 1999;Sulston, Dew, & Brenner, 1975). As in other animals, C. elegans DA plays key roles in coordinating motor programs with the reward system during foraging, feeding, and egg laying (Ardiel et al, 2016;Bettinger & McIntire, 2004;Chase & Koelle, 2007;Cermak et al, 2020;Qin & Wheeler, 2007;Rivard et al, 2010;Sanyal et al, 2004;Sawin, Ranganathan, & Horvitz, 2000;Suo et al, 2019). DA is released upon sensing food (Oranth et al, 2018) to initiate the slowing of movement in the presence of food (Sawin et al, 2000).…”