Abstract

The desert locust demonstrates density-dependent phase polyphenism: For extended periods it appears in a non-aggregating, non-migrating phenotype, known as the solitary phase. When circumstances change, solitary individuals may aggregate and transform to the gregarious phenotype, which have a strong propensity for generating large swarms. Previous reports have suggested a role for gut-bacteria derived volatiles in the swarming phenomenon, and suggested that locusts are capable of manipulating their gut microbiome according to their density-dependent phases. Here, we directly tested this hypothesis for the first time. Using locusts of both phases from well-controlled laboratory cultures as well as gregarious field-collected individuals; and high-throughput sequencing. We characterized the hindgut bacterial community composition in the two phases of the desert locust. Our findings demonstrate that laboratory-reared gregarious and solitary locusts maintain a stable core of Enterobacter. However, while different generations of gregarious locust experience shifts in their Enterobacter’s relative abundance; the solitary locusts maintain a stable gut microbiome, highly similar to that of the field-collected locusts. Tentative phase differences in wild populations’ microbiome may thus be an indirect effect of environmental or other factors that push the swarming individuals to homogenous gut bacteria. We therefore conclude that there are phase-related differences in the population dynamics of the locust hindgut bacterial composition, but there is no intrinsic density-dependent mechanism directly affecting the gut microbiome.

Highlights

  • Insect–bacteria symbiotic interaction is a common phenomenon, described in several insect orders (Moran and Baumann, 2000; Oliver et al, 2010; Bennett and Moran, 2013; Salem et al, 2015)

  • Desert locust swarms originating in Africa can reach the Middle East, India, and southern Europe (Pener and Simpson, 2009; Cullen et al, 2017; Food and Agriculture Organization [FAO], 2017), destroying cultivated fields and local vegetation, with a devastating impact on farmers’ livelihood (Food and Agriculture Organization [FAO], 2017)

  • Using denaturing gradient gel electrophoresis (DGGE) and 16S rRNA sequence analysis, those authors observed that the solitary individuals harbored a simpler hindgut bacterial community in comparison with their gregarious conspecifics

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Summary

INTRODUCTION

Insect–bacteria symbiotic interaction is a common phenomenon, described in several insect orders (Moran and Baumann, 2000; Oliver et al, 2010; Bennett and Moran, 2013; Salem et al, 2015). A healthy diverse hindgut bacterial community contributes to the locust’s resistance to pathogens by way of colonizationresistance and phenolic compound secretion (Dillon and Charnley, 1995, 2002) Some of these bacteria-derived phenolic volatile molecules (Phenol and Guaiacol) were found to be electrophysiologically active compounds that function as aggregating agents (reviewed in Pener and Simpson, 2009), suggesting a bacterial role in swarm gregariousness preservation (Dillon et al, 2000, 2002). Using DGGE and 16S rRNA sequence analysis, those authors observed that the solitary individuals harbored a simpler hindgut bacterial community in comparison with their gregarious conspecifics They suggested that these phase-dependent bacterial diversity-related differences may act to augment the gregarious superior pathogen resistance, as found by Wilson et al (2002). Any differentially expressed bacteria could have the potential to impact locust phase-related behavior and physiology, and potentially be harnessed to the efforts of controlling locust outbreaks

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