Pervasive Effects of <i>Wolbachia</i> 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 <i>Wolbachia</i>, a bacterial endosymbiont known to alter host reproduction, nutrient acquisition, and virus susceptibility. Here, we broadly test the hypothesis that <i>Wolbachia</i> modifies host behavior by assessing the effects of eight different <i>Wolbachia</i> strains on the temperature preference of six <i>Drosophila melanogaster</i> subgroup species. Four of the seven host genotypes infected with A-group <i>Wolbachia</i> strains (<i>w</i>Ri in <i>Drosophila simulans</i>, <i>w</i>Ha in <i>D. simulans</i>, <i>w</i>Sh in <i>Drosophila sechellia</i>, and <i>w</i>Tei in <i>Drosophila teissieri</i>) prefer significantly cooler temperatures relative to uninfected genotypes. Contrastingly, when infected with divergent B-group <i>w</i>Mau, <i>Drosophila mauritiana</i> prefers a warmer temperature. For most strains, changes to host temperature preference do not alter <i>Wolbachia</i> titer. However, males infected with <i>w</i>Sh and <i>w</i>Tei tend to experience an increase in titer when shifted to a cooler temperature for 24 h, suggesting that <i>Wolbachia</i>-induced changes to host behavior may promote bacterial replication. Our results indicate that <i>Wolbachia</i> modifications to host temperature preference are likely widespread, which has important implications for insect thermoregulation and physiology. Understanding the fitness consequences of these <i>Wolbachia</i> effects is crucial for predicting evolutionary outcomes of host-symbiont interactions, including how <i>Wolbachia</i> spreads to become common.<b>IMPORTANCE</b> Microbes infect a diversity of species, influencing the performance and fitness of their hosts. Maternally transmitted <i>Wolbachia</i> 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 <i>Wolbachia</i> influence host physiology and behavior to proliferate. We demonstrate pervasive effects of <i>Wolbachia</i> on <i>Drosophila</i> temperature preference. Most hosts infected with A-group <i>Wolbachia</i> prefer cooler temperatures, whereas the one host species infected with divergent B-group <i>Wolbachia</i> prefers warmer temperatures, relative to uninfected genotypes. Changes to host temperature preference generally do not alter <i>Wolbachia</i> abundance in host tissues, but for some A-group strains, adult males have increased <i>Wolbachia</i> titer when shifted to a cooler temperature. This suggests that <i>Wolbachia</i>-induced changes to host behavior may promote bacterial replication. Our results help elucidate the impact of endosymbionts on their hosts amid the global <i>Wolbachia</i> pandemic.