Density-dependent Phase Polyphenism Research Articles

Modelling foraging competition between solitarious and gregarious organisms in increasingly heterogeneous environments

Density dependent phase polyphenism is the exhibiting of two or more distinct phenotypes from a single genotype depending on local population density. The most well known insect to exhibit this phenomenon is the locust, with whom the profound effect on behaviour leads to the classification of the two phases; solitarious, where locusts actively avoid other locusts, and gregarious, where locusts are strongly attracted to other locusts. It has been shown that food distributions at both small and large scales have an effect on the process of gregarisation. While gregarisation offers advantages, such as greater predator avoidance, the relationship between phase polyphenism and potential foraging benefits is still not fully understood.In this paper, we explore the effect of gregarisation on foraging within increasingly heterogeneous environments using a partial differential equation model. We first consider a single two dimensional simulation of a spatially heterogeneous environment to understand the mechanics of gregarious/solitarious foraging. We then look at the steady state foraging advantage (measured as the ratio of per-capita contact with food) in environments ranging from homogeneous to very spatially heterogeneous. Finally, we perform a parameter sensitivity analysis to find which model parameters have the greatest effect on foraging advantage. We find that during the aggregation stage, prior to the onset of marching (which we do not model here), in increasingly heterogeneous food environments it is better to be gregarious than solitarious. In addition, we find that this is intrinsic to the gregarious/solitarious behavioural dynamic as it occurs almost regardless of the model parameters. That is to say, it doesn’t matter how fast the organisms disperse or how strong their long range interactions as long as there is the solitarious/gregarious behaviour the gregarious foraging advantage will exist.

State of the Art Management of the Central American Locust Schistocerca piceifrons piceifrons (Walker, 1870)

The Central American locust (CAL), Schistocerca piceifrons piceifrons (Walker, 1870), is a transboundary pest that is distributed from Mexico to Panama. It is a true locust species characterized by density-dependent phase polyphenism. The ancient record of the CAL is found in the Popol Vuh, the Mayan sacred book, demonstrating how it has affected humans for millennia. In Mexico, the CAL have been declared a national threat to agriculture since 1824. Serious locust plagues occurred in 1882–1883 when swarms of 20 km2 in size invaded the Yucatán Peninsula and neighboring states in southern Mexico and, since then, management actions to suppress populations and economic damage have been implemented. A better understanding of the biology, ecology, and behavior of the CAL replaced a manual and mechanical collection of locust swarms, hopper bands, and egg pods with modern techniques such as the use of safer chemical products and environmentally friendly bioinsecticides. Presently, biomodels and GIS support the monitoring and forecasting of outbreaks. Currently, studies are conducted to investigate environmental factors that trigger locust gregarization, the evolution of phase polyphenism, and CAL bioactive compounds and nutritional contents, envisioning its potential use in biotechnological industries. Findings will be crucial to improve the management strategies of the CAL.

The role of the neuropeptide [His7]-corazonin on phase-related characteristics in the Central American locust

Density-dependent phase polyphenism in locusts is one of the most extreme forms of phenotypic plasticity. Locusts exist along the continuum between two density-dependent phenotypes that differ in nymphal coloration, behavior, morphology, physiology, and reproduction among others. Nymphs of the solitarious phase, found in low population densities, are usually green, relatively inactive, and avoid each other, while gregarious nymphs, found in high density, exhibit a very obvious yellow/orange background with black patterning, and are highly active and attracted to each other. The multifunctional neuropeptide [His7]-corazonin has been shown to strongly affect black coloration and several other phase-related characteristics in at least two locust species, even though no effect on phase-related behavioral traits has been found. In this study, we investigate the role of [His7]-corazonin in the Central American locust Schistocerca piceifrons (Walker), which evolved density-dependent phase polyphenism independently from the two previously studied locust species. After successfully knocking down the transcript encoding [His7]-corazonin (CRZ) using RNA interference, we show that such a knockdown influences both color and morphometrics in this species, but does not influence phase-related behavioral traits. Our results suggest that the role of [His7]-corazonin is conserved in different locust species. Finally, our study represents the first controlled study of behavioral solitarization in S. piceifrons.

Migratory Take-Off Behaviour of the Mongolian Grasshopper Oedaleus asiaticus.

Oedaleus asiaticus is one of the dominant species of grasshoppers in the rangeland on the Mongolian plateau, and a serious pest, but its migratory behavior is poorly known. We investigated the take-off behavior of migratory O. asiaticus in field cages in the inner Mongolia region of northern China. The species shows a degree of density-dependent phase polyphenism, with high-density swarming populations characterized by a brown morph, while low-density populations are more likely to comprise a green morph. We found that only 12.4% of brown morphs engaged in migratory take-off, and 2.0% of green morphs. Migratory grasshoppers took off at dusk, especially in the half hour after sunset (20:00–20:30 h). Most emigrating individuals did not have any food in their digestive tract, and the females were mated but with immature ovaries. In contrast, non-emigrating individuals rarely had empty digestive tracts, and most females were mated and sexually mature. Therefore, it seems clear that individuals prepare for migration in the afternoon by eliminating food residue from the body, and migration is largely restricted to sexually immature stages (at least in females). Furthermore, it was found that weather conditions (particularly temperature and wind speed at 15:00 h) in the afternoon had a significant effect on take-off that evening, with O. asiaticus preferring to take off in warm, dry and calm weather. The findings of this study will contribute to a reliable basis for forecasting migratory movements of this pest.

Insect cytokine growth-blocking peptide may regulate density-dependent phase trait of cuticular melanization in the larval armyworm, Mythimna separata

Abstract Growth-blocking peptide (GBP) is a 25 amino acid insect cytokine found in lepidopteran insects that has diverse biological activities such as larval growth regulation, paralysis induction, cell proliferation and stimulation of immune cells. Density-dependent phase polyphenism is a phenomenon of phenotypic plasticity in which the expression of a variety of traits can be affected by local population density. In the present study, the armyworm Mythimna separata larvae with four rearing densities (1 larva/vial, 2 larvae/vial, 4 larvae/vial and 6 larvae/vial) were tested for cuticular melanization and body weight throughout the third-fifth instar, and the functional role of GBP in regulating the changes was investigated. The results indicated that when reared at high densities, the larvae exhibited less body weight and more degree of cuticular melanization than larvae reared at low densities. The gene expression of GBP in armyworm larvae showed an initial rise and then decline trend with increased rearing densities in the third to fifth instar. Compared with control, more degree of cuticular melanization was observed in GBP-injected larvae (500 ng/larva in volume 50 μL) than that in Ringer’s solution-injected counterparts. Furthermore, the gene expression level of dopa decarboxylase and prophenoloxidase increased significantly in GBP-injected fifth instar larvae from 6 h to 12 h after injection, suggesting the role of GBP in modulating density-dependent phase trait of armyworm cuticular melanization.

Geospatial Opinion on Unusual Locust Swarm Invasions during Amphan Cyclone

The desert locust, Schistocerca gregaria Forsk. (Orthoptera: Acrididae) is a peculiar insect that exhibits density-dependent phase polyphenism. Gregarious phase enables desert locust to form a large groups and mass migrations during which significant crop loss and food security issues may occur. Currently, the most recent upsurge of desert locust is prevailing across Eastern Africa and Southwestern Asia. Usually desert locusts are restricted to regions like semi-arid and arid regions. A super cyclonic storm, namely Amphan originated during May 2020, in the Bay of Bengal of North Indian Ocean has influenced numerous swarms to migrate from the Thar desert region to other parts of India. In this research, satellite data were used to investigate the reasons for this sudden swarm migration. The results that revealed the wind jets passing above the Thar desert region have integrated with the cyclogenesis of Amphan and led to the formation of conduits. The favorable conditions in the conduits include the open sky conditions, air temperature and fresh vegetation availability. Moreover, the wind settings in the conduits have enabled the swarm migrate to follow the downwind facing the sunrays during early mornings for an easy and successful take-off. It is observed that during the take-off session the wind speed at 850 hPa pressure level is mostly double than that of surface wind in both the conduits.

The puzzle of locust density-dependent phase polyphenism

Locust density-dependent phase polyphenism presents a quintessential example of environmentally induced plasticity. Almost a century of research has yielded ample knowledge regarding the multitude of ecological, physiological, and molecular phase-dependent characteristics. This short review highlights the considerable advances that have been made in our understanding of the locust's extreme plasticity and the highly complex nature of the phase phenomenon. Several challenges in locust research resulting from this unique complexity are also presented. It is concluded that the joint, interdisciplinary collaborative efforts, already underway, hold the promise of translating our ample knowledge into a complete solution to untangling the locust phase puzzle.

The Effect of Density-Dependent Phase on the Locust Gut Bacterial Composition.

The desert locust demonstrates density-dependent phase polyphenism: For extended periods it appears in a non-aggregating, non-migrating phenotype, known as the solitary phase. When circumstances change, solitary individuals may aggregate and transform to the gregarious phenotype, which have a strong propensity for generating large swarms. Previous reports have suggested a role for gut-bacteria derived volatiles in the swarming phenomenon, and suggested that locusts are capable of manipulating their gut microbiome according to their density-dependent phases. Here, we directly tested this hypothesis for the first time. Using locusts of both phases from well-controlled laboratory cultures as well as gregarious field-collected individuals; and high-throughput sequencing. We characterized the hindgut bacterial community composition in the two phases of the desert locust. Our findings demonstrate that laboratory-reared gregarious and solitary locusts maintain a stable core of Enterobacter. However, while different generations of gregarious locust experience shifts in their Enterobacter’s relative abundance; the solitary locusts maintain a stable gut microbiome, highly similar to that of the field-collected locusts. Tentative phase differences in wild populations’ microbiome may thus be an indirect effect of environmental or other factors that push the swarming individuals to homogenous gut bacteria. We therefore conclude that there are phase-related differences in the population dynamics of the locust hindgut bacterial composition, but there is no intrinsic density-dependent mechanism directly affecting the gut microbiome.

Identification of Odorant-Binding Proteins (OBPs) and Functional Analysis of Phase-Related OBPs in the Migratory Locust.

Olfactory plasticity, which is one of the major characteristics of density-dependent phase polyphenism, plays critical roles in the large-scale aggregation formation of Locusta migratoria. It is still unknown whether odorant-binding proteins (OBPs) are involved in phase-related olfactory plasticity of locusts, despite the confirmed involvement of several types of olfactory perception genes. In this study, we performed a large-scale search for OBPs and verified their expression patterns in the migratory locust. We identified 17 OBPs in the L. migratoria genome, of which 10 were novel, and we found their scattering distribution characteristics by mapping the genomic loci. Next, we revealed that these OBPs with close phylogenic relationships displayed similar tissue-specific expression profiles by a combined analysis of qRT-PCR and phylogenetic tree reconstruction. In all identified locust OBPs, seven OBPs showed differential mRNA expression levels in antenna tissue between gregarious and solitarious nymphs. Six of these seven OBPs displayed higher mRNA expression in the antennae of gregarious nymphs. The mRNA expression of LmigOBP2 and LmigOBP4 increased during gregarization and decreased during solitarization. RNAi experiments confirmed that only LmigOBP4 regulates the behavioral traits to affect gregarious behavior. These results demonstrated that OBPs also play important roles in the regulation of phase-related behavior of the locusts.

Molecular Characterization of a Lysozyme Gene and Its Altered Expression Profile in Crowded Beet Webworm (Loxostege sticticalis).

There is growing evidence that insects living in high-density populations exhibit an increase in immune function to counter a higher risk of disease. This phenomenon, known as density-dependent prophylaxis, has been experimentally tested in a number of insect species. Although density-dependent prophylaxis is especially prevalent in insects exhibiting density-dependent phase polyphenism, the molecular mechanism remains unclear. Our previous study demonstrated that the antibacterial activity of lysozyme is important for this process in the beet webworm Loxostege sticticalis. In this study, a lysozyme cDNA from L. sticticalis was cloned and characterized. The full-length cDNA is 1078 bp long and contains an open reading frame of 426 bp that encodes 142 amino acids. The deduced protein possesses structural characteristics of a typical c-type lysozyme and clusters with c-type lysozymes from other Lepidoptera. LsLysozyme was found to be expressed throughout all developmental stages, showing the highest level in pupae. LsLysozyme was also highly expressed in the midgut and fat body. Elevated LsLysozyme expression was observed in L. sticticalis larvae infected by Beauveria bassiana and in larvae reared under crowding conditions. In addition, the expression level of LsLysozyme in infected larvae reared at a density of 10 larvae per jar was significantly higher compared to those reared at a density of l or 30 larvae per jar. These results suggest that larval crowding affects the gene expression profile of this lysozyme. This study provides additional insight into the expression of an immune-associated lysozyme gene and helps us to better understand the immune response of L. sticticalis under crowding conditions.

Characteristics and expression patterns of histone-modifying enzyme systems in the migratory locust

The density-dependent phase polyphenism in locusts offers an excellent model to investigate the epigenetic regulatory mechanisms underlying phenotypic plasticity. In this study, we identified histone-modifying enzymes mediating histone post-translational modifications, which serve as a major regulatory mechanism of epigenetic processes, on the basis of the whole genome sequence of the migratory locust, Locusta migratoria. We confirmed the existence of various functional histone modifications in the locusts. Compared with other sequenced insect genomes, the locust genome contains a richer repertoire of histone-modifying enzymes. Several locust histone-modifying enzymes display vertebrate-like characteristics, such as the presence of a Sirt3-like gene and multiple alternative splicing of GCN5 gene. Most histone-modifying enzymes are highly expressed in the eggs or in the testis tissues of male adults. Several histone deacetylases and H3K4-specific methyltransferases exhibit differential expression patterns in brain tissues between solitarious and gregarious locusts. These results reveal the main characteristics of histone-modifying enzymes and provide important cues for understanding the epigenetic mechanisms underlying phase polyphenism in locusts.

Knockdown of the corazonin gene reveals its critical role in the control of gregarious characteristics in the desert locust

The two plague locusts, Schistocerca gregaria and Locusta migratoria, exhibit density-dependent phase polyphenism. Nymphs occurring at low population densities (solitarious forms) are uniformly colored and match their body color to the background color of their habitat, whereas those occurring at high population densities (gregarious) develop black patterns. An injection of the neuropeptide, corazonin (Crz) has been shown to induce black patterns in locusts and affect the classical morphometric ratio, F/C (F, hind femur length; C, maximum head width). We herein identified and cloned the CRZ genes from S. gregaria (SgCRZ) and L. migratoria. A comparative analysis of prepro-Crz sequences among insects showed that the functional peptide was well conserved; its conservation was limited to the peptide region. Silencing of the identified SgCRZ gene in gregarious S. gregaria nymphs markedly lightened their body color and shifted the adult F/C ratio toward the value typical of solitarious forms. In addition, knockdown of the gene in solitarious nymphs strongly inhibited darkening even after a transfer to crowded conditions; however, these individuals developed black patterns after being injected with the Crz as a rescue treatment. SgCRZ was constitutively expressed in the brains of S. gregaria during nymphal development in both phases. This gene was highly expressed not only in the brain in both phases, but also in the corpora allata in the gregarious phase. This conspicuous phase-dependent difference in SgCRZ gene expression may indicate a functional role in the control of phase polyphenism in this locust.

Hormonal Control of the Phase Polyphenism of the Desert Locust: A Review of Current Understanding

Locusts show density-dependent continuous phase polyphenism; they appear in two forms or phases, gregari- ous and solitary, and there is a continuous range of intermediates between the extreme phases. The endocrine control of phase polyphenism has been the most intensively studied in desert locusts, Schistocerca gregaria, Indeed, results of inves- tigations over the past 15 years, provide some of the most detailed information on the endocrine mechanisms that poten- tially regulate desert locust phase polyphenism. In addition, recent studies on the juvenile hormone titres, ecdysteroid ti- tres, the discovery of (His 7 )-corazonin as dark-colour-inducing neuropeptide (DCIN) and the involvement of serotonin pulse in the metathoracic ganglion that triggers behavioural gregarization in the desert locust have yielded not only a good progress in our understanding the endocrine control of phase polyphenism but also unexpected results which indicate that the endocrine control of desert locust phase polyphenism is more complex than envisioned by the classical model. This review gives an overview of the progress made to date in elucidating the hormonal control of the desert locust phase polyphenism. Moreover, this review will summarize these findings and present some questions that still need to be an- swered.

Solitary and Gregarious Locusts Differ in Circadian Rhythmicity of a Visual Output Neuron

Locusts demonstrate remarkable phenotypic plasticity driven by changes in population density. This density dependent phase polyphenism is associated with many physiological, behavioral, and morphological changes, including observations that cryptic solitarious (solitary-reared) individuals start to fly at dusk, whereas gregarious (crowd-reared) individuals are day-active. We have recorded for 24-36 h, from an identified visual output neuron, the descending contralateral movement detector (DCMD) of Schistocerca gregaria in solitarious and gregarious animals. DCMD signals impending collision and participates in flight avoidance maneuvers. The strength of DCMD's response to looming stimuli, characterized by the number of evoked spikes and peak firing rate, varies approximately sinusoidally with a period close to 24 h under constant light in solitarious locusts. In gregarious individuals the 24-h pattern is more complex, being modified by secondary ultradian rhythms. DCMD's strongest responses occur around expected dusk in solitarious locusts but up to 6 h earlier in gregarious locusts, matching the times of day at which locusts of each type are most active. We thus demonstrate a neuronal correlate of a temporal shift in behavior that is observed in gregarious locusts. Our ability to alter the nature of a circadian rhythm by manipulating the rearing density of locusts under identical light-dark cycles may provide important tools to investigate further the mechanisms underlying diurnal rhythmicity.

Metabolomic analysis reveals that carnitines are key regulatory metabolites in phase transition of the locusts

Phenotypic plasticity occurs prevalently and plays a vital role in adaptive evolution. However, the underlying molecular mechanisms responsible for the expression of alternate phenotypes remain unknown. Here, a density-dependent phase polyphenism of Locusta migratoria was used as the study model to identify key signaling molecules regulating the expression of phenotypic plasticity. Metabolomic analysis, using high-performance liquid chromatography and gas chromatography-mass spectrometry, showed that solitarious and gregarious locusts have distinct metabolic profiles in hemolymph. A total of 319 metabolites, many of which are involved in lipid metabolism, differed significantly in concentration between the phases. In addition, the time course of changes in the metabolic profiles of locust hemolymph that accompany phase transition was analyzed. Carnitine and its acyl derivatives, which are involved in the lipid β-oxidation process, were identified as key differential metabolites that display robust correlation with the time courses of phase transition. RNAi silencing of two key enzymes from the carnitine system, carnitine acetyltransferase and palmitoyltransferase, resulted in a behavioral transition from the gregarious to solitarious phase and the corresponding changes of metabolic profiles. In contrast, the injection of exogenous acetylcarnitine promoted the acquisition of gregarious behavior in solitarious locusts. These results suggest that carnitines mediate locust phase transition possibly through modulating lipid metabolism and influencing the nervous system of the locusts.

Density-Dependent Phase Polyphenism in Nonmodel Locusts: A Minireview

Although the specific mechanisms of locust phase transformation are wellunderstood for model locust species such as the desert locustSchistocerca gregariaand the migratory locustLocusta migratoria, the expressions of density-dependent phase polyphenism in other nonmodel locust species are not wellknown. The present paper is an attempt to review and synthesize what we know about these nonmodel locusts. Based on all available data, I find that locust phase polyphenism is expressed in many different ways in different locust species and identify a pattern that locust species often belong to large taxonomic groups which contain mostly nonswarming grasshopper species. Although locust phase polyphenism has evolved multiple times within Acrididae, I argue that its evolution should be studied from a phylogenetic perspective because I find similar density-dependent phenotypic plasticity among closely related species. Finally, I emphasize the importance of comparative analyses in understanding the evolution of locust phase and propose a phylogeny-based research framework.

Behavioural phase change in the Australian plague locust, Chortoicetes terminifera, is triggered by tactile stimulation of the antennae

Density-dependent phase polyphenism is a defining characteristic of the paraphyletic group of acridid grasshoppers known as locusts. The cues and mechanisms associated with crowding that induce behavioural gregarization are best understood in the desert locust, Schistocerca gregaria, and involve a combination of sensory inputs from the head (visual and olfactory) and mechanostimulation of the hind legs, acting via a transient increase in serotonin in the thoracic ganglia. Since behavioural gregarization has apparently arisen independently multiple times within the Acrididae, the important question arises as to whether the same mechanisms have been recruited each time. Here we explored the roles of visual, olfactory and tactile stimulation in the induction of behavioural gregarization in the Australian plague locust, Chortoicetes terminifera. We show that the primary gregarizing input is tactile stimulation of the antennae, with no evidence for an effect of visual and olfactory stimulation or tactile stimulation of the hind legs. Our results show that convergent behavioural responses to crowding have evolved employing different sites of sensory input in the Australian plague locust and the desert locust.

Memoirs of a locust: Density-dependent behavioral change as a model for learning and memory

A locust outbreak is a stupendous natural phenomenon that remains in the memory of whoever has been lucky (or unlucky) enough to witness it. Recent years have provided novel and important insights into the neurobiology of locust swarming. However, the central nervous system processes that accompany and perhaps even lie at the basis of locust phase transformation are still far from being fully understood. Our current work deals with the memory of a locust outbreak from a new perspective: that of the individual locust. We take locust density-dependent phase transformation – a unique example of extreme behavioral plasticity, and place it within the context of the accepted scheme of learning and memory. We confirm that a short time period of exposure to a small crowd of locusts is sufficient to induce a significant behavioral change in a previously solitary locust. Our results suggest that part of the behavioral change is due to long-term habituation of evasive and escape responses. We further demonstrate that the memory of a crowding event lasts for at least 24 h, and that this memory is sensitive to a protein synthesis blocker. These findings add much to our understanding of locust density-dependent phase polyphenism. Furthermore, they offer a novel and tractable model for the study of learning and memory-related processes in a very distinctive behavioral context.

Behavioural phase polyphenism in the Australian plague locust ( Chortoicetes terminifera )

Swarming and the expression of phase polyphenism are defining characteristics of locust species. Increases in local population density mediate morphological, physiological and behavioural changes within individuals, which correlate with mass marching of juveniles in migratory bands and flying swarms of adults. The Australian plague locust (Chortoicetes terminifera) regularly forms migratory bands and swarms, but is claimed not to express phase polyphenism and has accordingly been used to argue against a central role for phase change in locust swarming. We demonstrate that juvenile C. terminifera express extreme density-dependent behavioural phase polyphenism. Isolated-reared juveniles are sedentary and repelled by conspecifics, whereas crowd-reared individuals are highly active and are attracted to conspecifics. In contrast to other major locust species, however, behavioural phase change does not accumulate across generations, but shifts completely within an individual's lifetime in response to a change in population density.

Do outbreaks affect genetic population structure? A worldwide survey inLocusta migratoria, a pest plagued by microsatellite null alleles

An understanding of the role of factors intrinsic to a species' life history in structuring contemporary genetic variation is a fundamental, but understudied, aspect of evolutionary biology. Here, we assessed the influence of the propensity to outbreak in shaping worldwide genetic variation in Locusta migratoria, a cosmopolitan pest well known for its expression of density-dependent phase polyphenism. We scored 14 microsatellites in nine subspecies from 25 populations distributed over most of the species' range in regions that vary in the historical frequency and extent of their outbreaks. We rejected the hypothesis that L. migratoria consists of two genetically distinct clusters adapted to habitats either rarely (nonoutbreaking) or cyclically (outbreaking) favourable to increases in population density. We also invalidated the current subspecific taxonomic classification based on morphometrics. Bayesian inferences indicated evidence of a homogenizing effect of outbreaks on L. migratoria population structure. Geographical and ecological barriers to gene flow in conjunction with historical events can also explain the observed patterns. By systematically assessing the effects of null alleles using computer simulations, we also provide a template for the analysis of microsatellite data sets characterized by a high prevalence of null alleles.