From Molecules to Management: Mechanisms and Consequences of Locust Phase Polyphenism

Abstract

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.

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

“…Solitarious locusts moved much more hesitantly in both locomotor assays. This superficially resembles pre-291 vious reports that solitarious locusts walk more slowly than gregarious locusts in the Roessingh arena [16,31,32] , 292 but we find that the speed when walking ('walk bout speed') is very similar in the two phases -and in fact 293 is slightly lower in gregarious locusts.The discrepancy arises because previous studies scored 'walk speed' as 294 zero for locusts that did not walk [31] . This underestimates the walk speed of solitarious locusts because these 295 animals account for the majority of assays where walking did not occur.…”

“…The contrasting selection pressures of group-and lone-living are therefore expected to 14 lead to adaptive differences in the extent of behavioural variability [5] . 15 Reduction in either within-or between-individual variability of behaviour contributes to greater homo- 16 geneity of animal collectives [6] . Previous studies have largely focussed on changes in behavioural variability 17 as an instantaneously reactive process, when animals behave in one way when alone, but immediately adjust 18 their behaviour to be less variable when in the presence of conspecifics [2] .…”

“…111 Roessingh arena behavioural assay 112Experiments in the Roessingh arena used Leicester strain locusts. The Roessingh arena assay [19,21] was 113 originally developed for quantifying the behavioural phase state of individual locusts and has been used in 114 many subsequent studies in S. gregaria, Locusta migratoria and Chortoicetes terminifera (See Cullen et al, 115 2017 for review [16] ).…”

“…Here, we present robust evidence demonstrating that selective pressures have shaped intrinsic behavioural 33 variability in the desert locust Schistocerca gregaria. In this species, the same genotype can manifest in 34 two very distinct eco-phenotypes or phases, a lone-living 'solitarious' phase and a 'gregarious' phase that 35 forms large, dense groups [16] . Solitarious individuals show low levels of activity, have cryptic green or 36 beige colouration and avoid other locusts, whereas gregarious individuals are highly active, are attracted 37 to conspecifics, develop a striking aposematic yellow-and-black colouration, and can aggregate into swarms 38 containing billions of individuals [17] .…”

“…We have used the desert 256 locust, a species that manifests two extreme phenotypes with contrasting predation ecologies, to examine 257 the extent to which behavioural variability has evolved to be phenotypically plastic. Marked differences in 258 mean behavioural phenotypes between isolated and crowded individuals are the defining feature of locusts, 259 and a large body of work has documented that these differences outlast changes in the immediate social 260 environment [16] . Our present study provides a step change from all previous work by asking whether density-261 dependent polyphenism in the desert locust extends to differences in the variability of behaviour.…”