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.
Highlights d Cool temperature reduces wMel Wolbachia oocyte abundance and maternal transmission d Thermal reductions are less severe for hosts and Wolbachia from a temperate climate d Temperature-dependent transmission can explain continentwide wMel frequency clines d A derived stop codon in WspB likely contributes to Wolbachia thermal sensitivity
1Heritable symbionts can modify a range of ecologically important host traits, including 2 behavior. About half of all insect species are infected with maternally transmitted Wolbachia, a 3 bacterial endosymbiont known to alter host reproduction, nutrient acquisition, and virus 4 susceptibility. Here, we broadly test the hypothesis that Wolbachia modify host behavior by 5 assessing the effects of eight different Wolbachia strains on the temperature preference of six 6Drosophila melanogaster-subgroup species. Four of the seven host genotypes infected with A-7 group Wolbachia strains (wRi in D. simulans, wHa in D. simulans, wSh in D. sechellia, and wTei 8 in D. teissieri) prefer significantly cooler temperatures relative to uninfected genotypes. 9Contrastingly, when infected with divergent B-group wMau, D. mauritiana prefer a warmer 10 temperature. For most strains, changes to host temperature preference do not alter Wolbachia 11 titer. However, males infected with wSh and wTei experience an increase in titer when shifted to 12 a cooler temperature for 24 hours, suggesting that Wolbachia-induced changes to host behavior 13 may promote bacterial replication and influence Wolbachia transmission rates. Modifications to 14 host temperature preference likely influence host thermoregulation, and understanding the fitness 15 consequences of these effects is crucial for predicting evolutionary outcomes of host-symbiont 16 interactions, including how Wolbachia spread to become common. 17 18
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