Locusts are grasshoppers (Orthoptera: Acrididae) that are characterised by their capacity for extreme population density-dependent polyphenism, transforming between a cryptic solitarious phase that avoids other locusts, and a swarming gregarious phase that aggregates and undergoes collective migration. The two phases differ in many aspects of behaviour, physiology and ecology, making locusts a useful model through which to investigate the phenotypic interface of molecular processes and environmental cues. This review summarises recent progress in understanding the mechanisms and consequences of locust phase change, from differential gene expression and epigenetic regulation through to neuronal plasticity and altered behaviour. The impact of techniques such as RNA interference (RNAi), and the sequencing of the first locust genome is discussed, and we consider the evidence from comparative analyses between related locust species for the possible evolution of locust-like phenotypic plasticity. Collective movement, and new ways of measuring the behaviour of both migrating bands in the field and individuals in the laboratory, are analysed. We also examine the environmental factors that affect phase change, along with the wider impact of land use and management strategies that may unwittingly create environments conducive to outbreaks. Finally, we consider the human costs of locust swarming behaviour, and use combined social, economic and environmental approaches to suggest potential ways forward for locust monitoring and management.

Locusts are grasshoppers that can form dense migrating swarms through an extreme form of density-dependent phenotypic plasticity, known as locust phase polyphenism. We present a comprehensive phylogeny of the genus Schistocerca, which contains both non-swarming grasshoppers and swarming locusts. We find that the desert locust, S. gregaria, which is the only Old World representative of the genus, is the earliest diverging lineage. This suggests that the common ancestor of Schistocerca must have been a swarming locust that crossed the Atlantic Ocean from Africa to America approximately 6 million years ago, giving rise to the current diversity in the New World. This also implies that density-dependent phenotypic plasticity is an ancestral trait for the genus. Through ancestral character reconstruction of reaction norms, we show that colour plasticity has been largely retained in most species in the genus, but behavioural plasticity was lost and regained at least twice. Furthermore, we show that swarming species do not form a monophyletic group and non-swarming species that are closely related to locusts often express locust-like plastic reaction norms. Thus, we conclude that individual reaction norms have followed different evolutionary trajectories, which have led to the evolutionary transition between grasshoppers and locusts - and vice versa.

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.

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.