Behavioral phase shift in nymphs of the desert locust, Schistocerca gregaria: Special attention to attraction/avoidance behaviors and the role of serotonin

Tanaka, Seiji; Nishide, Yudai

doi:10.1016/j.jinsphys.2012.10.018

Cited by 40 publications

(56 citation statements)

References 51 publications

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“…These observations establish serotonin as an important regulatory agent in phase transition, an effect that is probably mediated through protein kinase A signalling (Ott et al, 2012). We note that other researchers report no influence on attraction/avoidance behaviour by serotonin (Tanaka and Nishide, 2013) or on darkening of hatchlings (Maeno et al, 2011) in S. gregaria. However, in the latter experiments, serotonin was injected through the abdominal sternites in the thorax instead of directly into the thoracic ganglia, which could account for the difference in results.…”

Section: Reviewsupporting

confidence: 66%

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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Section: Reviewsupporting

confidence: 66%

Epigenetics and locust life phase transitions

Ernst

Hiel

Depuydt

et al. 2015

Journal of Experimental Biology

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“…Experimentally induced phase change can be assayed by measuring locomotion and, or how, it is used to express a preference or avoidance of conspecific animals (Hägele and Simpson, 2000; Tanaka and Nishide, 2013). Based on this we developed an experimental protocol in which animals were raised in a long-term crowded culture before being subjected as adults, in cohorts, to isolation in cages in which gregarising mechanical, olfactory, and visual cues were removed.…”

Section: Resultsmentioning

confidence: 99%

Dopaminergic modulation of phase reversal in desert locusts

Alessi

O’Connor

Aonuma

et al. 2014

Front. Behav. Neurosci.

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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.

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“…Although by design logistic regression analysis is robust to changes in single behaviours, it is theoretically possible for changes in one or a few behaviours to account for changes in P greg and that, rather than measuring a coherent change in overall phase state, the value is responding to successive changes in individual and non-linked behaviours. A recent paper by Tanaka and Nishide (2013) posits that the rapid onset of behavioural gregarization in just a few hours that has been consistently observed in studies by several groups since the 1950s is driven mostly or entirely by changes in activity rather than changes in the attraction/repulsion to other locusts. In other words, they argue that previous studies using logistic regression to quantify behavioural phase state may not have measured true behavioural gregarization that encompasses both activity and attraction to conspecifics.…”

Section: Introductionmentioning

confidence: 92%

“…In other words, they argue that previous studies using logistic regression to quantify behavioural phase state may not have measured true behavioural gregarization that encompasses both activity and attraction to conspecifics. Tanaka and Nishide (2013) also suggest that genuine behavioural gregarization is a much slower process taking days rather than hours, based on a metric that purely considers the proximity of a test locust to a group of stimulus locusts kept in a clear container as a measure of attraction. Further, Tanaka and Nishide (2013) go on to question the role of serotonin (Anstey et al, 2009; Ott et al, 2012) in initiating the expression of attraction-related behaviours as part of gregarization in S. gregaria .…”

Section: Introductionmentioning

confidence: 99%