Substantial changes in central nervous system neurotransmitters and neuromodulators accompany phase change in the locust

Rogers, Stephen M.; Matheson, Troy; Sasaki, Kohsuke; Kendrick, Keith M.; Simpson, Stephen J.; Burrows, Malcolm

doi:10.1242/jeb.01183

Cited by 123 publications

(108 citation statements)

References 78 publications

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“…Injecting KT5720 into long-term gregarious locusts did not cause them to behave solitariously, indicating that gregarious behavior, when it has been consolidated through prolonged crowding, does not depend on PKA activity. That newly acquired and fully consolidated gregarious behaviors are mechanistically distinct also tallies with the finding that 5-HT is elevated only transiently, during the first few hours of crowding (16), and therefore cannot maintain gregariousness in the longer term. Activation of PKA may thus provide the link between a transient 5-HT signal and a later phase of consolidation that entails changes in gene expression (11,13).…”

Section: Discussionsupporting

confidence: 61%

“…The discovery of a central role for the biogenic amine serotonin [5-hydroxytryptamine (5-HT)] in inducing behavioral gregarization (14) suggests parallels with mechanisms underlying classical forms of neuronal and behavioral plasticity (15). In solitarious locusts, gregarizing stimuli cause an increase in 5-HT in the thoracic ganglia, but with prolonged crowding, 5-HT decreases to lower than solitarious levels (16). This indicates that, after induction, gregariousness is maintained by other means, echoing the transient role of 5-HT in classical forms of learning.…”

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confidence: 99%

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Critical role for protein kinase A in the acquisition of gregarious behavior in the desert locust

Ott

Verlinden

Rogers

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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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...

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Section: Discussionsupporting

confidence: 61%

mentioning

confidence: 99%

Critical role for protein kinase A in the acquisition of gregarious behavior in the desert locust

Ott

Verlinden

Rogers

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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“…The desert locust Schistocerca gregaria shows a radical, but fully reversible, form of phenotypic plasticity (phase change) that involves changes in behavior, morphology physiology, neurochemistry and neuronal function (Uvarov, 1966(Uvarov, , 1977Simpson et al, 1999;Matheson et al, 2004;Rogers et al, 2004). Locusts generally occur at low population densities (Ͻ3/100 m 2 ) in the "solitarious phase."…”

Section: Introductionmentioning

confidence: 99%

Compensatory Plasticity at an Identified Synapse Tunes a Visuomotor Pathway

Rogers¹,

Krapp²,

Burrows³

et al. 2007

J. Neurosci.

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We characterized homeostatic plasticity at an identified sensory-motor synapse in an insect, which maintains constant levels of motor drive as locusts transform from their solitarious phase to their gregarious swarming phase. The same mechanism produces behaviorally relevant changes in response timing that can be understood in the context of an animal's altered behavioral state. For individual animals of either phase, different looming objects elicited different spiking responses in a visual looming detector interneuron, descending contralateral movement detector (DCMD), yet its synaptic drive to a leg motoneuron, fast extensor tibiae (FETi), always had the same maximum amplitude. Gregarious locust DCMDs produced more action potentials and had higher firing frequencies, but individual postsynaptic potentials (PSPs) elicited in FETi were half the amplitude of those in solitarious locusts. A model suggested that this alone could not explain the similarity in overall amplitude, and we show that facilitation increased the maximum compound PSP amplitude in gregarious animals. There was the same linear relationship between times of peak DCMD firing before collision and the size/velocity of looming objects in both phases. The DCMD-FETi synapse transformed this relationship nonlinearly, such that peak amplitudes of compound PSPs occurred disproportionately earlier for smaller/faster objects. Furthermore, the peak PSP amplitude occurred earlier in gregarious than in solitarious locusts, indicating a differential tuning. Homeostatic modulation of the amplitude, together with a nonlinear synaptic transformation of timing, acted together to tune the DCMD-FETi system so that swarming gregarious locusts respond earlier to small moving objects, such as conspecifics, than solitarious locusts.

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“…Long-term solitarious locusts learn more quickly to associate an odour with an aversive food source, an effect that can be overridden by crowding, enabling locusts to adopt a different feeding strategy. Furthermore, brain functioning is affected by changes in the neurochemistry of the locust's nervous system upon phenotypic transformation (Anstey et al, 2009;Rogers et al, 2004;Verlinden et al, 2009). Solitarious locusts can switch to gregarious behaviour in only a few hours (Ellis, 1953; Ellis, 1962), whereas other changes, in colour, morphology and reproductive physiology, alter on a much slower time scale (Pener and Simpson, 2009;Pener and Yerushalmi, 1998;Roessingh et al, 1993;Simpson et al, 1999).…”

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confidence: 99%

Epigenetics and locust life phase transitions

Ernst

Hiel

Depuydt

et al. 2015

Journal of Experimental Biology

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Insects are one of the most successful classes on Earth, reflected in an enormous species richness and diversity. Arguably, this success is partly due to the high degree to which polyphenism, where one genotype gives rise to more than one phenotype, is exploited by many of its species. In social insects, for instance, larval diet influences the development into distinct castes; and locust polyphenism has tricked researchers for years into believing that the drastically different solitarious and gregarious phases might be different species. Solitarious locusts behave much as common grasshoppers. However, they are notorious for forming vast, devastating swarms upon crowding. These gregarious animals are shorter lived, less fecund and transmit their phase characteristics to their offspring. The behavioural gregarisation occurs within hours, yet the full display of gregarious characters takes several generations, as does the reversal to the solitarious phase. Hormones, neuropeptides and neurotransmitters influence some of the phase traits; however, none of the suggested mechanisms can account for all the observed differences, notably imprinting effects on longevity and fecundity. This is why, more recently, epigenetics has caught the interest of the polyphenism field. Accumulating evidence points towards a role for epigenetic regulation in locust phase polyphenism. This is corroborated in the economically important locust species Locusta migratoria and Schistocerca gregaria. Here, we review the key elements involved in phase transition in locusts and possible epigenetic regulation. We discuss the relative role of DNA methylation, histone modification and small RNA molecules, and suggest future research directions. KEY WORDS: Locust phase, Polyphenism, Locust swarming, Locusta migratoria, Schistocerca gregaria, Apis mellifera, Invertebrate, DNA methylation, Histone modification, Methylome IntroductionThe term epigenetics tends to take a variety of meanings (Haig, 2004;Jablonka and Lamb, 2002). In its narrow sense, it can be defined as 'meiotically and mitotically heritable changes in gene expression, not based on DNA sequence alterations ' (Riggs et al., 1996). In a broader sense, it can also be interpreted as 'modifications of chromosome structure ' (Bird, 2007). Independent of the interpretation, however, epigenetics did not receive much attention in insect research until recent years.The most prominent epigenetic mechanisms, namely (1) methylation of cytosine in DNA, (2) modifications of histone proteins and (3) nucleosome positioning and regulation by noncoding RNA, were only rarely the focus of the entomology field. This may have been due to the general low, often almost undetectable, levels of methylation in insects and other invertebrates REVIEW Functional Genomics and Proteomics Lab, KU Leuven, Naamsestraat 59, bus 2465, B-3000 Leuven, Belgium.*Author for correspondence (Liliane.Schoofs@bio.kuleuven.be) (Glastad et al., 2011), including the prime model organisms Drosophila melanogaster and Caenorhabdi...

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Substantial changes in central nervous system neurotransmitters and neuromodulators accompany phase change in the locust

Cited by 123 publications

References 78 publications

Critical role for protein kinase A in the acquisition of gregarious behavior in the desert locust

Critical role for protein kinase A in the acquisition of gregarious behavior in the desert locust

Compensatory Plasticity at an Identified Synapse Tunes a Visuomotor Pathway

Epigenetics and locust life phase transitions

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