Abstract

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.

Highlights

  • Locusts are grasshoppers belonging to the family Acrididae (Insecta: Orthoptera) that can form dense migrating swarms through an extreme form of density-dependent phenotypic plasticity, in which cryptically coloured, shy individuals can transform into conspicuously coloured, gregarious individuals in response to increases in population density[1,2,3]

  • Locust phase polyphenism is a collection of individual plastic reaction norms that all respond to changes in density[32]

  • Phylogeny and biogeography of Schistocerca. We used both maximum likelihood and Bayesian analyses to infer the phylogeny of Schistocerca, which resulted in identical topologies and recovered Schistocerca as a strong monophyletic group (Fig. 2)

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Summary

Introduction

Locusts are grasshoppers belonging to the family Acrididae (Insecta: Orthoptera) that can form dense migrating swarms through an extreme form of density-dependent phenotypic plasticity, in which cryptically coloured, shy individuals can transform into conspicuously coloured, gregarious individuals in response to increases in population density[1,2,3]. In nature, depending on local population density, locusts are polyphenic along the continuum between two extreme phenotypes, known as solitarious phase and gregarious phase[1, 3]. This syndrome of coordinated changes is known as locust phase polyphenism[1, 3, 8]. An explicitly phylogenetic study of phenotypic plasticity, that is, tracing the evolution of reaction norms based on a robust phylogenetic hypothesis, is extremely rare This is because obtaining an accurate phylogenetic hypothesis and quantifying reaction norms of multiple species in a clade are both challenging tasks. A phylogenetic approach in the study of phenotypic plasticity can provide a more accurate understanding regarding the polarity of the evolution of reaction norms[32, 38, 43]

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