Abstract

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.

Highlights

  • 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

  • In S. gregaria, crowd-reared nymphs are typically attracted towards conspecifics and are highly active, whereas those reared in isolation walk less and avoid other ­locusts[47,48]

  • We predicted that piceifrons, a known locust for which behaviour had never been quantified in a standardised manner, would show distinct and characteristic behavioural plasticity similar to that of S. gregaria, while the behavioural plasticity in the non-swarming species would be reduced or even absent

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Summary

Introduction

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. Changes in local population density cause shy ‘solitarious’ locusts that initially avoid each other, to transform into ‘gregarious’ individuals that form large migrating s­ warms[20] This phenomenon influences all aspects of a locust’s life, with phenotypic changes in behaviour, colouration, morphology, reproductive and developmental biology, physiology and e­ cology[15,16,17,19,20,21,22,23,24]. Locusts have not been prominently featured in the phenotypic plasticity literature, despite some previous attempts to place them as an exemplary system for studying the evolution of phenotypic ­plasticity[18]

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