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Differential activation of serotonergic neurons during short- and long-term gregarization of desert locusts.

ABSTRACT: Serotonin is a neurochemical with evolutionarily conserved roles in orchestrating nervous system function and behavioural plasticity. A dramatic example is the rapid transformation of desert locusts from cryptic asocial animals into gregarious crop pests that occurs when drought forces them to accumulate on dwindling resources, triggering a profound alteration of behaviour within just a few hours. The onset of crowding induces a surge in serotonin within their thoracic ganglia that is sufficient and necessary to induce the switch from solitarious to gregarious behaviour. To identify the neurons responsible, we have analysed how acute exposure to three gregarizing stimuli--crowding, touching the hind legs or seeing and smelling other locusts--and prolonged group living affect the expression of serotonin in individual neurons in the thoracic ganglia. Quantitative analysis of cell body immunofluorescence revealed three classes of neurons with distinct expressional responses. All ganglia contained neurons that responded to multiple gregarizing stimuli with increased expression. A second class showed increased expression only in response to intense visual and olfactory stimuli from conspecifics. Prolonged group living affected a third and entirely different set of neurons, revealing a two-tiered role of the serotonergic system as both initiator and substrate of socially induced plasticity. This demonstrates the critical importance of ontogenetic time for understanding the function of serotonin in the reorganization of behaviour.

SUBMITTER: Rogers SM

PROVIDER: S-EPMC4298206 | biostudies-literature | 2015 Feb

REPOSITORIES: biostudies-literature

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Differential activation of serotonergic neurons during short- and long-term gregarization of desert locusts.

Rogers Stephen M SM Ott Swidbert R SR

Proceedings. Biological sciences 20150201 1800

Serotonin is a neurochemical with evolutionarily conserved roles in orchestrating nervous system function and behavioural plasticity. A dramatic example is the rapid transformation of desert locusts from cryptic asocial animals into gregarious crop pests that occurs when drought forces them to accumulate on dwindling resources, triggering a profound alteration of behaviour within just a few hours. The onset of crowding induces a surge in serotonin within their thoracic ganglia that is sufficient ...[more]

PMID: 25520357

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Project description:Desert locusts (Schistocerca gregaria) show an extreme form of phenotypic plasticity and can transform between a cryptic solitarious phase and a swarming gregarious phase. The two phases differ extensively in behavior, morphology and physiology but very little is known about the molecular basis of these differences. We used our recently generated Expressed Sequence Tag (EST) database derived from S. gregaria central nervous system (CNS) to design oligonucleotide microarrays and compare the expression of thousands of genes in the CNS of long-term gregarious and solitarious adult desert locusts. This identified 214 differentially expressed genes, of which 40% have been annotated to date. These include genes encoding proteins that are associated with CNS development and modeling, sensory perception, stress response and resistance, and fundamental cellular processes. Our microarray analysis has identified genes whose altered expression may enable locusts of either phase to deal with the different challenges they face. Genes for heat shock proteins and proteins which confer protection from infection were upregulated in gregarious locusts, which may allow them to respond to acute physiological challenges. By contrast the longer-lived solitarious locusts appear to be more strongly protected from the slowly accumulating effects of ageing by an upregulation of genes related to anti-oxidant systems, detoxification and anabolic renewal. Gregarious locusts also had a greater abundance of transcripts for proteins involved in sensory processing and in nervous system development and plasticity. Gregarious locusts live in a more complex sensory environment than solitarious locusts and may require a greater turnover of proteins involved in sensory transduction, and possibly greater neuronal plasticity. Two condition experiment: Solitarious central nervous system (CNS) vs gregarious CNS. 6 biological repeats per condition, balanced over 3 male and 3 females samples. The overall experimental design consisted of two identical repeats of an n+2 A-optimal design, organized per sex (n=6 per sex, 3 solitarious - 3 gregarious samples)

Project description:Phenotypic plasticity allows animals to modify their behavior, physiology, and morphology to adapt to environmental change. The global pest, the desert locust, shows two extreme phenotypes; a solitarious phase that is relatively harmless and a gregarious phase that forms swarms and causes extensive agricultural and economic damage. In the field, environmental conditions can drive isolated animals into crowded populations and previous studies have identified the biogenic amine serotonin as a key determinant of this transition. Here we take an integrated approach to investigate the neurochemical, physiological, and behavioral correlates defined by a laboratory based paradigm that mimics facets of swarm break down as gregarious locusts become isolated. Following isolation there was an increased propensity of locusts to avoid conspecifics, and show a reduced locomotion. Changes in choice behavior occurred within 1 h of isolation although isolation-related changes progressed with increased isolation time. Isolation was accompanied by changes in the levels of the biogenic amines dopamine, octopamine, and serotonin within the CNS within 1 h. Dopamine levels were higher in isolated animals and we focused on the role played by this transmitter in synaptic changes that may underpin solitarization. Dopamine reduced synaptic efficacy at a key central synapse between campaniform sensilla (CS) and a fast extensor tibiae motor neuron that is involved in limb movement. We also show that dopamine injection into the haemocoel was sufficient to induce solitarious-like behavior in otherwise gregarious locusts. Further, injection of a dopamine antagonist, fluphenazine, into isolated locusts induced gregarious-like behavior. This highlights that dopaminergic modulation plays an important role in the plasticity underpinning phase transition and sets a context to deepen the understanding of the complementary role that distinct neuromodulators play in polyphenism in locusts.

Dataset Information

Differential activation of serotonergic neurons during short- and long-term gregarization of desert locusts.

Publications

Differential activation of serotonergic neurons during short- and long-term gregarization of desert locusts.

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