Octopamine and tyramine respectively regulate attractive and repulsive behavior in locust phase changes (original) (raw)
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Journal of insect behavior, 2001
Desert locusts [Schistocerca gregaria Forskål (Orthoptera, Acrididae)] change phase in response to population density: solitarious insects avoid one another, but when crowded they change to the gregarious phase and aggregate. The attraction/repulsion responses of gregarious and solitarious locusts maintain phase differences in locust populations. Despite considerable research, the cues for aggregation are poorly understood; moreover, the repulsion response of solitarious locusts has not previously been investigated. This study analyzes the role of visual and olfactory stimuli in triggering these different responses to conspecifics. Isolation-reared insects were repelled by both olfactory and visual stimuli from other locusts. Crowd-reared insects were attracted by the combination of olfactory and visual cues. In addition, olfactory stimuli affected other behaviors in both phases, and behavioral differences between isolationand crowd-reared locusts were clear even in the absence of conspecifics. The sensory and neurological mechanisms underlying these responses are not well understood and will form the basis for neurobiological investigations of locust phase.
Journal of Insect Physiology, 1999
Integration of behaviourally relevant odours at the central nervous level of 3rd instar nymphal desert locusts, Schistocerca gregaria, showed phase- and (developmental) stage-dependent characteristics which correlated with differences in the number of olfactory sensilla. Antennal lobe (AL) neurons of gregarious locusts generally responded more frequently and showed a higher sensitivity to the tested stimuli. However, AL neurons of solitary locusts responded significantly more frequently to phenylacetonitril, the major component of the adult aggregation pheromone. Pheromone-specific, plant-specific and pheromone-plant generalist neurons were found in both phases. The response spectra of pheromone-specific neurons correlated with the potential behavioural significance of attractant chemical cues in the environment. Neurons of both phases responded specifically to stage-specific aggregation-pheromone components and to other chemical cues that may be involved in the location of suitable roosting and foraging sites.
Critical role for protein kinase A in the acquisition of gregarious behavior in the desert locust
Proceedings of the National Academy of Sciences, 2012
The mechanisms that integrate genetic and environmental information to coordinate the expression of complex phenotypes are little understood. We investigated the role of two protein kinases (PKs) in the population density-dependent transition to gregarious behavior that underlies swarm formation in desert locusts: the foraging gene product, a cGMP-dependent PK (PKG) implicated in switching between alternative group-related behaviors in several animal species; and cAMP-dependent PK (PKA), a signal transduction protein with a preeminent role in different forms of learning. Solitarious locusts acquire key behavioral characters of the swarming gregarious phase within just 1 to 4 h of forced crowding. Injecting the PKA inhibitor KT5720 before crowding prevented this transition, whereas injecting KT5823, an inhibitor of PKG, did not. Neither drug altered the behavior of long-term gregarious locusts. RNAi against foraging effectively reduced its expression in the central nervous system, but this did not prevent gregarization upon crowding. By contrast, solitarious locusts with an RNAi-induced reduction in PKA catalytic subunit C1 expression behaved less gregariously after crowding, and RNAi against the inhibitory R1 subunit promoted more extensive gregarization following a brief crowding period. A central role of PKA is congruent with the recent discovery that serotonin mediates gregarization in locusts and with findings in vertebrates that similarly implicate PKA in the capacity to cope with adverse life events. Our results show that PKA has been coopted into effecting the wide-ranging transformation from solitarious to gregarious behavior, with PKAmediated behavioral plasticity resulting in an environmentally driven reorganization of a complex phenotype. phase change | phenotypic plasticity | Schistocerca gregaria H ow genetic information is integrated with environmental cues to control and coordinate complex phenotypes is a fundamental question in biology (1, 2). Environmental input can cause concerted changes in multiple traits to produce distinct phenotypic syndromes that are adaptive in particular conditions. Phase polyphenism in desert locusts (Schistocerca gregaria) is an extreme example. Locusts can reversibly transform between a solitarious phase and a gregarious phase that differ profoundly in morphology, physiology, and behavior (3-5). Solitarious locusts occur at low population densities and actively avoid conspecifics; they are cryptic in appearance and behavior; walk with a slow, creeping gait; and have restricted dietary preferences. The gregarious phase is characterized by increased activity and locomotion, an upright posture and gait, aposematic coloration, a broad dietary range, and, most critically, attraction to other locusts. Phase change is driven by huge changes in population density and is an adaptation to arid habitats where rains are infrequent and erratic. Transitory periods of verdure support rapid population growth, but after the rains cease, large numbers of solitarious locusts compete for dwindling patches of resources (6, 7). The resultant crowding causes a rapid transition to gregarious behavior by exposing solitarious locusts to specific sensory stimuli from conspecifics: repeated touch to the hind femur and the combination of visual and olfactory cues (8-10). Gre-garious behavior ensures further exposure to other locusts and thereby sets up a positive feedback loop that drives further phenotypic changes accruing over the locusts' lifetimes and even across generations. This behavior is also what makes locusts notorious pests, as highly mobile groups of gregarized locusts can further coalesce to escalate into enormous swarms that devastate crops and pastures.
PLOS Genetics, 2020
Animals often exhibit dramatically behavioral plasticity depending on their internal physiological state, yet little is known about the underlying molecular mechanisms. The migratory locust, Locusta migratoria, provides an excellent model for addressing these questions because of their famous phase polyphenism involving remarkably behavioral plasticity between gregarious and solitarious phases. Here, we report that a major insect hormone, juvenile hormone, is involved in the regulation of this behavioral plasticity related to phase change by influencing the expression levels of olfactory-related genes in the migratory locust. We found that the treatment of juvenile hormone analog, methoprene, can significantly shift the olfactory responses of gregarious nymphs from attraction to repulsion to the volatiles released by gregarious nymphs. In contrast, the repulsion behavior of solitarious nymphs significantly decreased when they were treated with precocene or injected with double-stranded RNA of JHAMT, a juvenile hormone acid O-methyltransferase. Further, JH receptor Met or JH-response gene Kr-h1 knockdown phenocopied the JH-deprivation effects on olfactory behavior. RNA-seq analysis identified 122 differentially expressed genes in antennae after methoprene application on gregarious nymphs. Interestingly, several olfactory-related genes were especially enriched, including takeout (TO) and chemosensory protein (CSP) which have key roles in behavioral phase change of locusts. Furthermore, methoprene application and Met or Kr-h1 knockdown resulted in simultaneous changes of both TO1 and CSP3 expression to reverse pattern, which mediated the transition between repulsion and attraction responses to gregarious volatiles. Our results suggest the regulatory roles of a pleiotropic hormone in locust behavioral plasticity through modulating gene expression in the peripheral olfactory system.
A Multifunctional Role for Octopamine in Locust Flight
Annual Review of Entomology, 1993
KEY WORDS: octopaminergic modulation of behavior, flight energy metabolism, central and peripheral neurons, flight muscles, insect PERSPECTIVES AND OVERVIEW A complex cascade of neuronal, hormonal, muscular, and metabolic events leads to the initiation and maintenance of a behavioral act. Hormones are released to mobilize metabolic energy; muscle properties are altered to ensure the generation of the necessary force; neuronal circuits are activated to generate a specific locomotor pattern; and the neuronal circuit underlying respiration may also be altered to adapt the animal to increased oxygen consumption. All these events are part of a complex transition of the animal into a new behavioral state. A critical aspect of this transition is the need to alter these events at the appropriate time. This coordinating function may not only depend on neuronal interaction but may also be attributed to chemical substances that bias, at many levels, neuronal, hormonal, and muscular events towards the new functional state of the animal. For example, egg-laying by Aplysia spp. requires several peptides (38, 76) to elicit a complex of behaviors, including the cessation of locomotion, increase in heart and respiratory rate, egg laying, head waving, and mucous secretion. Similarly, serotonin controls 227
Physiological Entomology, 1999
Recordings from antennal olfactory receptor neurones in young adult Schistocerca gregaria Forskål (Orthoptera: Acrididae) showed that behaviourally important odours are detected by receptor neurones present in morphologically identifiable sensillum types. Both nymph-and adult-produced aggregation pheromones activate receptor neurones housed in sensilla basiconica. The receptor neurones in this sensillum type in solitary-reared locusts display a higher sensitivity to aggregation pheromones and to some other behaviourally relevant odours than the same type of neurones in gregarious locusts. Receptor neurones present in sensilla coeloconica respond to green leaf odours, organic acids, and nymphal odours but are inhibited by mature adult-produced aggregation pheromones. Receptor neurones housed in sensilla trichodea respond to a possible sex pheromone. No phase differences were found in the response of coeloconic-or trichoid-associated receptor neurones.
Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology, 1998
Physiological and morphological characteristics of antennal lobe neurons of solitary and gregarious ®fth-instar nymphs of the desert locust, Schistocerca gregaria, were studied using intracellular recording and staining techniques. Physiological characteristics of antennal lobe neurons of both locust phases responding to stage-dependent aggregation pheromones, egg-laying attractants, a putative sex pheromone and plant-associated volatiles are described. Antennal lobe neurons showed excitatory, inhibitory, combined excitatory and inhibitory and delayed responses. In addition, one neuron showing an initial inhibition followed by an excitation and inhibition response was found. Pheromone-speci®c-, plant-speci®c-and pheromone-plant-generalist neurons were found in both locust phases. Antennal lobe neurons displayed stage-and phase-dependent dierences in the processing of aggregation pheromone component input. Nymphal antennal lobe neurons showed stage-dependent response characteristics highly correlated with the preferential behavioural attraction to the nymphal aggregation pheromone. Phase-dependent differences were found in the response spectra and the sensitivity of the same neuron types. Neurons of solitary locusts responded signi®cantly more frequently to some of the tested components than neurons of gregarious locusts. Furthermore, antennal lobe neurons of solitary locusts showed a higher sensitivity to most of the tested compounds.