Pervasive Effects of <italic toggle="yes">Wolbachia</italic> on Host Temperature Preference

ABSTRACT Heritable symbionts can modify a range of ecologically important host traits, including behavior. About half of all insect species are infected with maternally transmitted Wolbachia, a bacterial endosymbiont known to alter host reproduction, nutrient acquisition, and virus susceptibility. H...

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Autores principales: Michael T. J. Hague, Chelsey N. Caldwell, Brandon S. Cooper
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:d7fe2b2a2e424970822be8e0f94062cb2021-11-15T16:19:08ZPervasive Effects of <italic toggle="yes">Wolbachia</italic> on Host Temperature Preference10.1128/mBio.01768-202150-7511https://doaj.org/article/d7fe2b2a2e424970822be8e0f94062cb2020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01768-20https://doaj.org/toc/2150-7511ABSTRACT Heritable symbionts can modify a range of ecologically important host traits, including behavior. About half of all insect species are infected with maternally transmitted Wolbachia, a bacterial endosymbiont known to alter host reproduction, nutrient acquisition, and virus susceptibility. Here, we broadly test the hypothesis that Wolbachia modifies host behavior by assessing the effects of eight different Wolbachia strains on the temperature preference of six Drosophila melanogaster subgroup species. Four of the seven host genotypes infected with A-group Wolbachia strains (wRi in Drosophila simulans, wHa in D. simulans, wSh in Drosophila sechellia, and wTei in Drosophila teissieri) prefer significantly cooler temperatures relative to uninfected genotypes. Contrastingly, when infected with divergent B-group wMau, Drosophila mauritiana prefers a warmer temperature. For most strains, changes to host temperature preference do not alter Wolbachia titer. However, males infected with wSh and wTei tend to experience an increase in titer when shifted to a cooler temperature for 24 h, suggesting that Wolbachia-induced changes to host behavior may promote bacterial replication. Our results indicate that Wolbachia modifications to host temperature preference are likely widespread, which has important implications for insect thermoregulation and physiology. Understanding the fitness consequences of these Wolbachia effects is crucial for predicting evolutionary outcomes of host-symbiont interactions, including how Wolbachia spreads to become common. IMPORTANCE Microbes infect a diversity of species, influencing the performance and fitness of their hosts. Maternally transmitted Wolbachia bacteria infect most insects and other arthropods, making these bacteria some of the most common endosymbionts in nature. Despite their global prevalence, it remains mostly unknown how Wolbachia influence host physiology and behavior to proliferate. We demonstrate pervasive effects of Wolbachia on Drosophila temperature preference. Most hosts infected with A-group Wolbachia prefer cooler temperatures, whereas the one host species infected with divergent B-group Wolbachia prefers warmer temperatures, relative to uninfected genotypes. Changes to host temperature preference generally do not alter Wolbachia abundance in host tissues, but for some A-group strains, adult males have increased Wolbachia titer when shifted to a cooler temperature. This suggests that Wolbachia-induced changes to host behavior may promote bacterial replication. Our results help elucidate the impact of endosymbionts on their hosts amid the global Wolbachia pandemic.Michael T. J. HagueChelsey N. CaldwellBrandon S. CooperAmerican Society for MicrobiologyarticleDrosophilahost-microbe interactionsymbiosisthermal adaptationthermoregulationwMelMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution DOAJ
collection DOAJ
language EN
topic Drosophila
host-microbe interaction
symbiosis
thermal adaptation
thermoregulation
wMel
Microbiology
QR1-502
spellingShingle Drosophila
host-microbe interaction
symbiosis
thermal adaptation
thermoregulation
wMel
Microbiology
QR1-502
Michael T. J. Hague
Chelsey N. Caldwell
Brandon S. Cooper
Pervasive Effects of <italic toggle="yes">Wolbachia</italic> on Host Temperature Preference
description ABSTRACT Heritable symbionts can modify a range of ecologically important host traits, including behavior. About half of all insect species are infected with maternally transmitted Wolbachia, a bacterial endosymbiont known to alter host reproduction, nutrient acquisition, and virus susceptibility. Here, we broadly test the hypothesis that Wolbachia modifies host behavior by assessing the effects of eight different Wolbachia strains on the temperature preference of six Drosophila melanogaster subgroup species. Four of the seven host genotypes infected with A-group Wolbachia strains (wRi in Drosophila simulans, wHa in D. simulans, wSh in Drosophila sechellia, and wTei in Drosophila teissieri) prefer significantly cooler temperatures relative to uninfected genotypes. Contrastingly, when infected with divergent B-group wMau, Drosophila mauritiana prefers a warmer temperature. For most strains, changes to host temperature preference do not alter Wolbachia titer. However, males infected with wSh and wTei tend to experience an increase in titer when shifted to a cooler temperature for 24 h, suggesting that Wolbachia-induced changes to host behavior may promote bacterial replication. Our results indicate that Wolbachia modifications to host temperature preference are likely widespread, which has important implications for insect thermoregulation and physiology. Understanding the fitness consequences of these Wolbachia effects is crucial for predicting evolutionary outcomes of host-symbiont interactions, including how Wolbachia spreads to become common. IMPORTANCE Microbes infect a diversity of species, influencing the performance and fitness of their hosts. Maternally transmitted Wolbachia bacteria infect most insects and other arthropods, making these bacteria some of the most common endosymbionts in nature. Despite their global prevalence, it remains mostly unknown how Wolbachia influence host physiology and behavior to proliferate. We demonstrate pervasive effects of Wolbachia on Drosophila temperature preference. Most hosts infected with A-group Wolbachia prefer cooler temperatures, whereas the one host species infected with divergent B-group Wolbachia prefers warmer temperatures, relative to uninfected genotypes. Changes to host temperature preference generally do not alter Wolbachia abundance in host tissues, but for some A-group strains, adult males have increased Wolbachia titer when shifted to a cooler temperature. This suggests that Wolbachia-induced changes to host behavior may promote bacterial replication. Our results help elucidate the impact of endosymbionts on their hosts amid the global Wolbachia pandemic.
format article
author Michael T. J. Hague
Chelsey N. Caldwell
Brandon S. Cooper
author_facet Michael T. J. Hague
Chelsey N. Caldwell
Brandon S. Cooper
author_sort Michael T. J. Hague
title Pervasive Effects of <italic toggle="yes">Wolbachia</italic> on Host Temperature Preference
title_short Pervasive Effects of <italic toggle="yes">Wolbachia</italic> on Host Temperature Preference
title_full Pervasive Effects of <italic toggle="yes">Wolbachia</italic> on Host Temperature Preference
title_fullStr Pervasive Effects of <italic toggle="yes">Wolbachia</italic> on Host Temperature Preference
title_full_unstemmed Pervasive Effects of <italic toggle="yes">Wolbachia</italic> on Host Temperature Preference
title_sort pervasive effects of <italic toggle="yes">wolbachia</italic> on host temperature preference
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/d7fe2b2a2e424970822be8e0f94062cb
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AT chelseyncaldwell pervasiveeffectsofitalictoggleyeswolbachiaitaliconhosttemperaturepreference
AT brandonscooper pervasiveeffectsofitalictoggleyeswolbachiaitaliconhosttemperaturepreference
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