Pervasive Effects of Wolbachia 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. 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.

Pervasive effects ofWolbachiaon host activity

“…Locomotion is a basic host activity underlying many ecologically important behaviors, including foraging, thermoregulation, and mate seeking. In combination with our recent work demonstrating pervasive effects of A- and B-group Wolbachia on host temperature preference [20], we posit that Wolbachia infections may often alter host behavior.…”

“…We reared flies at 25°C under a 12-h light: 12-h dark cycle (Percival model I-36LL) on a standard food diet [20]. Each day, we collected a batch of female and male virgins for one pair of uninfected and infected genotypes.…”

“…We used publicly available Wolbachia genome assemblies [20,42,43,59,69–71], and new Illumina sequencing, to generate a Bayesian phylogram [20] (see Supplemental Methods). Wolbachia effects on host activity were especially common for w Ri-like Wolbachia , so we used the phylogram to test whether Wolbachia effects on hosts exhibit phylogenetic signal.…”

Wolbachiain the spittlebugProsapia ignipectus:Variable infection frequencies, but no apparent effect on host reproductive isolation

“…Animals interact with microorganisms that influence their behavior, physiology, and fitness (Hurst and Jiggins, 2000;Brownlie et al, 2009;McFall-Ngai et al, 2013;Fredericksen et al, 2017;Gould et al, 2018;Hague, Caldwell and Cooper, 2020). These include associations between hosts and vertically transmitted endosymbionts that live inside their cells (McCutcheon, Boyd and Dale, 2019).…”

“…In contrast, Wolbachia that cause weak or no CI tend to occur at variable intermediate frequencies (Hoffmann, Clancy and Duncan, 1996;Hamm et al, 2014;Kriesner et al, 2016;Cooper et al, 2017;Meany et al, 2019). These include wMel-like Wolbachia frequencies that vary spatially in D. melanogaster and D. yakuba (Kriesner et al, 2016;Hague et al, 2020), and temporally in D. yakuba and D. santomea (Cooper et al, 2017;Hague, Caldwell and Cooper, 2020). In all but a few systems, limited sampling has left a gap in knowledge about whether Wolbachia frequency variation is common Hamm et al, 2014;Cattel et al, 2016;Schuler et al, 2016;Ross et al, 2020).…”