Comparative analysis of phenotypic plasticity sheds light on the evolution and molecular underpinnings of locust phase polyphenism

Locusts exhibit one of nature’s most spectacular examples of complex phenotypic plasticity, in which changes in density cause solitary and cryptic individuals to transform into gregarious and conspicuous locusts forming large migrating swarms. We investigated how these coordinated alternative phenotypes might have evolved by studying the Central American locust and three closely related non-swarming grasshoppers in a comparative framework. By experimentally isolating and crowding during nymphal development, we induced density-dependent phenotypic plasticity and quantified the resulting behavioural, morphological, and molecular reaction norms. All four species exhibited clear plasticity, but the individual reaction norms varied among species and showed different magnitudes. Transcriptomic responses were species-specific, but density-responsive genes were functionally similar across species. There were modules of co-expressed genes that were highly correlated with plastic reaction norms, revealing a potential molecular basis of density-dependent phenotypic plasticity. These findings collectively highlight the importance of studying multiple reaction norms from a comparative perspective.

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.

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.

Plasticity of behavioural variability reflects conflicting selection in group-living and solitary desert locusts

Animals living in groups tend to express less variable behaviour than animals living alone. It is widely assumed that this difference reflects, at least in part, an adaptive response to contrasting selection pressures: group-living should favour the evolution of more uniform behaviour whereas lone-living should favour behaviour that is less predictable. Empirical evidence linking these contrasting selection pressures to intrinsic differences in behavioural variability is, however, largely lacking. The desert locust, Schistocerca gregaria, manifests in two very distinct eco-phenotypes, a lone-living cryptic “solitarious phase” and a swarming “gregarious phase” that aggregates into very large and dense groups. This “phase polyphenism” has evolved in response to contrasting selection pressures that change rapidly and unpredictably. Phase differences in mean behaviour are well-characterised, but no previous study has considered differences in variability. Here we used locust phase polyphenism to test the hypothesis that group living leads to the evolution of reduced intrinsic variability in behaviour. We measured two behaviours in both phenotypes: locomotor activity in the presence of conspecifics, and locomotor hesitation in approaching food when alone. We assayed each individual repeatedly and estimated variability relative to the mean in log-normal mixed-effects models that explicitly account for the means-variance dependency in the behavioural measures. Our results demonstrate that relative behavioural variability differs between the two phases in line with predictions from ecological theory: both within-individual and between-individual variability were lower in the group-living gregarious phenotype. This contrasts with previous studies on social niche construction in spiders and crickets, and highlights the importance of social ecology: in animals that form non-social collectives, such as locusts, reduced individual behavioural variability is key for coherent collective behaviour. The differences in variability persisted when gregarious locusts were tested in isolation and solitarious locusts were tested in groups, indicating that they arise not simply as flexible reactions to different social contexts, but are intrinsic to the individual animals of each phase. This “variance polyphenism” in locusts provides empirical evidence that evolutionary adaptation for group living has driven a reduction in within- and between-individual behavioural variability.

Density-Dependent Phenotypic Plasticity in the South American Locust, Schistocerca cancellata (Orthoptera: Acrididae)

Historically, the South American locust, Schistocerca cancellata (Serville, 1838), has been considered the most serious agricultural pest in Argentina. An outbreak of a magnitude not recorded since 1954 started in 2015 through 2017 in northern Argentina and neighboring Paraguay and Bolivia. Schistocerca cancellata is widely considered as a true locust, with pronounced locust phase polyphenism, although the expression of its phenotypic plasticity has never been quantitatively tested under different density conditions. In this study, we explicitly quantified density-dependent reaction norms in behavior, coloration, and morphology in last instar nymphs of S. cancellata under isolated and crowded conditions. We also quantified density-dependent plasticity in adults (size) and in some life history traits. Our results showed that crowded nymphs were significantly more active and more attracted to congeners than isolated nymphs, and developed a much higher percentage of black pattern color. We also found that density had strong effects on body size and there was a sex-dependent pattern in both nymphs and adults, revealing that differences in size between males and females were less pronounced in crowded locusts. We have recorded for the isolated nymphs the presence of about 50% more hairs in the hind femora than in crowded nymphs. Finally, the mean duration of each nymphal instar and adult stage was significantly longer in isolated individuals. We have found strong resemblance with the desert locust, S. gregaria (Forskål, 1775) in several traits, and we conclude that S. cancellata exhibits an extreme form of density-dependent phenotypic plasticity in behavior, coloration, morphology, and life history traits.