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      Pervasive Effects of Wolbachia on Host Temperature Preference

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          Abstract

          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.

          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.

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          Wolbachia: master manipulators of invertebrate biology.

          Wolbachia are common intracellular bacteria that are found in arthropods and nematodes. These alphaproteobacteria endosymbionts are transmitted vertically through host eggs and alter host biology in diverse ways, including the induction of reproductive manipulations, such as feminization, parthenogenesis, male killing and sperm-egg incompatibility. They can also move horizontally across species boundaries, resulting in a widespread and global distribution in diverse invertebrate hosts. Here, we review the basic biology of Wolbachia, with emphasis on recent advances in our understanding of these fascinating endosymbionts.
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            Climate change and evolutionary adaptation.

            Evolutionary adaptation can be rapid and potentially help species counter stressful conditions or realize ecological opportunities arising from climate change. The challenges are to understand when evolution will occur and to identify potential evolutionary winners as well as losers, such as species lacking adaptive capacity living near physiological limits. Evolutionary processes also need to be incorporated into management programmes designed to minimize biodiversity loss under rapid climate change. These challenges can be met through realistic models of evolutionary change linked to experimental data across a range of taxa.
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              Phylogenetic analysis and comparative data: a test and review of evidence.

              The question is often raised whether it is statistically necessary to control for phylogenetic associations in comparative studies. To investigate this question, we explore the use of a measure of phylogenetic correlation, lambda, introduced by Pagel (1999), that normally varies between 0 (phylogenetic independence) and 1 (species' traits covary in direct proportion to their shared evolutionary history). Simulations show lambda to be a statistically powerful index for measuring whether data exhibit phylogenetic dependence or not and whether it has low rates of Type I error. Moreover, lambda is robust to incomplete phylogenetic information, which demonstrates that even partial information on phylogeny will improve the accuracy of phylogenetic analyses. To assess whether traits generally show phylogenetic associations, we present a quantitative review of 26 published phylogenetic comparative data sets. The data sets include 103 traits and were chosen from the ecological literature in which debate about the need for phylogenetic correction has been most acute. Eighty-eight percent of data sets contained at least one character that displayed significant phylogenetic dependence, and 60% of characters overall (pooled across studies) showed significant evidence of phylogenetic association. In 16% of tests, phylogenetic correlation could be neither supported nor rejected. However, most of these equivocal results were found in small phylogenies and probably reflect a lack of power. We suggest that the parameter lambda be routinely estimated when analyzing comparative data, since it can also be used simultaneously to adjust the phylogenetic correction in a manner that is optimal for the data set, and we present an example of how this may be done.
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                Author and article information

                Contributors
                Role: Invited Editor
                Role: Editor
                Journal
                mBio
                mBio
                mbio
                mbio
                mBio
                mBio
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2150-7511
                6 October 2020
                Sep-Oct 2020
                : 11
                : 5
                : e01768-20
                Affiliations
                [a ]Division of Biological Sciences, University of Montana, Missoula, Montana, USA
                University of Kansas
                University of Pittsburgh
                Author notes
                Address correspondence to Michael T. J. Hague, michael.hague@ 123456mso.umt.edu .
                Author information
                https://orcid.org/0000-0003-0641-2420
                https://orcid.org/0000-0002-8269-7731
                Article
                mBio01768-20
                10.1128/mBio.01768-20
                7542361
                33024036
                976463c6-9b05-4274-b751-ff6b5120ff76
                Copyright © 2020 Hague et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 30 June 2020
                : 31 August 2020
                Page count
                supplementary-material: 10, Figures: 3, Tables: 1, Equations: 2, References: 148, Pages: 15, Words: 12382
                Funding
                Funded by: HHS | NIH | National Institute of General Medical Sciences (NIGMS), https://doi.org/10.13039/100000057;
                Award ID: R35GM124701
                Award Recipient :
                Categories
                Research Article
                Ecological and Evolutionary Science
                Custom metadata
                September/October 2020

                Life sciences
                drosophila,host-microbe interaction,symbiosis,thermal adaptation,thermoregulation,wmel
                Life sciences
                drosophila, host-microbe interaction, symbiosis, thermal adaptation, thermoregulation, wmel

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