Stark, R., Grzelak, M. & Hadfield, J. RNA sequencing: The teenage years. Nat. Rev. Genet. https://doi.org/10.1038/s41576-019-0150-2 (2019).
Google Scholar
Gutzwiller, F. et al. Dynamics of Wolbachia pipientis gene expression across the Drosophila melanogaster life cycle. G3 Genes Genomes Genet. 5, 2843–2856 (2015).
Google Scholar
Bennuru, S. et al. Stage-specific transcriptome and proteome analyses of the filarial parasite Onchocerca volvulus and its Wolbachia endosymbiont. MBio 7, e02028-e2116 (2016).
Google Scholar
Baião, G. C., Schneider, D. I., Miller, W. J. & Klasson, L. The effect of Wolbachia on gene expression in Drosophila paulistorum and its implications for symbiont-induced host speciation. BMC Genom. 20, 465 (2019).
Google Scholar
Werren, J. H., Baldo, L. & Clark, M. E. Wolbachia: Master manipulators of invertebrate biology. Nat. Rev. Microbiol. 6, 741–751 (2008).
Google Scholar
Zug, R. & Hammerstein, P. Still a host of hosts for Wolbachia: Analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One 7, e38544 (2012).
Google Scholar
Sazama, E. J., Bosch, M. J., Shouldis, C. S., Ouellette, S. P. & Wesner, J. S. Incidence of Wolbachia in aquatic insects. Ecol. Evol. 7, 1165–1169 (2017).
Google Scholar
Detcharoen, M., Arthofer, W., Schlick-Steiner, B. C. & Steiner, F. M. Wolbachia megadiversity: 99% of these microorganismic manipulators unknown. FEMS Microbiol. Ecol. 95, fiz151 (2019).
Google Scholar
Hosokawa, T., Koga, R., Kikuchi, Y., Meng, X. Y. & Fukatsu, T. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc. Natl. Acad. Sci. U. S. A. 107, 769–774 (2010).
Google Scholar
Teixeira, L., Ferreira, Á. & Ashburner, M. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol. 6, 2753–2763 (2008).
Google Scholar
Hedges, L. M., Brownlie, J. C., O’Neill, S. L. & Johnson, K. N. Wolbachia and virus protection in insects. Science (80-). 322, 702–702 (2008).
Google Scholar
Osborne, S. E., Leong, Y. S., O’Neill, S. L. & Johnson, K. N. Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog. 5, e1000656 (2009).
Google Scholar
Cattel, J., Martinez, J., Jiggins, F., Mouton, L. & Gibert, P. Wolbachia-mediated protection against viruses in the invasive pest Drosophila suzukii. Insect Mol. Biol. 25, 595–603 (2016).
Google Scholar
Ranz, J. M., Castillo-Davis, C. I., Meiklejohn, C. D. & Hartl, D. L. Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science (80-). 300, 1742–1745 (2003).
Google Scholar
Herbert, R. I. & McGraw, E. A. The nature of the immune response in novel Wolbachia-host associations. Symbiosis 74, 225–236 (2018).
Google Scholar
Woodford, L. et al. Vector species-specific association between natural Wolbachia infections and avian malaria in black fly populations. Sci. Rep. 8, 4188 (2018).
Google Scholar
Huigens, M. E., De Almeida, R. P., Boons, P. A. H., Luck, R. F. & Stouthamer, R. Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc. R. Soc. B Biol. Sci. 271, 509–515 (2004).
Google Scholar
Detcharoen, M., Arthofer, W., Jiggins, F. M., Steiner, F. M. & Schlick-Steiner, B. C. Wolbachia affect behavior and possibly reproductive compatibility but not thermoresistance, fecundity, and morphology in a novel transinfected host, Drosophila nigrosparsa. Ecol. Evol. 10, 4457–4470 (2020).
Google Scholar
Woolfit, M. et al. Genomic evolution of the pathogenic Wolbachia strain, wMelPop. Genome Biol. Evol. 5, 2189–2204 (2013).
Google Scholar
Suh, E., Mercer, D. R., Fu, Y. & Dobson, S. L. Pathogenicity of life-shortening Wolbachia in Aedes albopictus after transfer from Drosophila melanogaster. Appl. Environ. Microbiol. 75, 7783–7788 (2009).
Google Scholar
McGraw, E. A., Merritt, D. J., Droller, J. N. & O’Neill, S. L. Wolbachia-mediated sperm modification is dependent on the host genotype in Drosophila. Proc. R. Soc. B Biol. Sci. 268, 2565–2570 (2001).
Google Scholar
Xie, J., Vilchez, I. & Mateos, M. Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS One 5, e12149 (2010).
Google Scholar
Hutchence, K. J., Fischer, B., Paterson, S. & Hurst, G. D. D. How do insects react to novel inherited symbionts? A microarray analysis of Drosophila melanogaster response to the presence of natural and introduced Spiroplasma. Mol. Ecol. 20, 950–958 (2011).
Google Scholar
O’Grady, P. M. & DeSalle, R. Phylogeny of the genus Drosophila. Genetics 209, 1–25 (2018).
Google Scholar
Kellermann, V., Van Heerwaarden, B., Sgrò, C. M. & Hoffmann, A. A. Fundamental evolutionary limits in ecological traits drive Drosophila species distributions. Science (80-). 325, 1244–1246 (2009).
Google Scholar
Bächli, G., Viljoen, F., Escher, S. A. & Saura, A. The Drosophilidae (Diptera) of Fennoscandia and Denmark (Brill, 2005).
Kinzner, M.-C. et al. Life-history traits and physiological limits of the alpine fly Drosophila nigrosparsa (Diptera: Drosophilidae): A comparative study. Ecol. Evol. 8, 2006–2020 (2018).
Google Scholar
Kinzner, M.-C. et al. Major range loss predicted from lack of heat adaptability in an alpine Drosophila species. Sci. Total Environ. 695, 133753 (2019).
Google Scholar
Kinzner, M.-C. et al. Oviposition substrate of the mountain fly Drosophila nigrosparsa (Diptera: Drosophilidae). PLoS One 11, e0165743 (2016).
Google Scholar
Cicconardi, F. et al. Chemosensory adaptations of the mountain fly Drosophila nigrosparsa (Insecta: Diptera) through genomics’ and structural biology’s lenses. Sci. Rep. 7, 43770 (2017).
Google Scholar
Tratter Kinzner, M. et al. Is temperature preference in the laboratory ecologically relevant for the field? The case of Drosophila nigrosparsa. Glob. Ecol. Conserv. 18, e00638 (2019).
Google Scholar
Arthofer, W. et al. Genomic resources notes accepted 1 August 2014–30 September 2014. Mol. Ecol. Resour. 15, 228–229 (2015).
Google Scholar
Cicconardi, F., Marcatili, P., Arthofer, W., Schlick-Steiner, B. C. & Steiner, F. M. Positive diversifying selection is a pervasive adaptive force throughout the Drosophila radiation. Mol. Phylogenet. Evol. 112, 230–243 (2017).
Google Scholar
Verspoor, R. L. & Haddrill, P. R. Genetic diversity, population structure and Wolbachia infection status in a worldwide sample of Drosophila melanogaster and D. simulans populations. PLoS One 6, e26318 (2011).
Google Scholar
Lints, F. A. Size in relation to development-time and egg-density in Drosophila melanogaster. Nature 197, 1128–1130 (1963).
Google Scholar
Clemson, A. S., Sgrò, C. M. & Telonis-Scott, M. Thermal plasticity in Drosophila melanogaster populations from eastern Australia: Quantitative traits to transcripts. J. Evol. Biol. 29, 2447–2463 (2016).
Google Scholar
Morozova, T. V., Anholt, R. H. & Mackay, T. F. Transcriptional response to alcohol exposure in Drosophila melanogaster. Genome Biol. 7, R95 (2006).
Google Scholar
Elya, C., Zhang, V., Ludington, W. B. & Eisen, M. B. Stable host gene expression in the gut of adult Drosophila melanogaster with different bacterial mono-associations. PLoS One 11, e0167357 (2016).
Google Scholar
Chrostek, E. et al. Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: A phenotypic and phylogenomic analysis. PLoS Genet. 9, e1003896 (2013).
Google Scholar
Zhang, B. et al. Comparative transcriptome analysis of chemosensory genes in two sister leaf beetles provides insights into chemosensory speciation. Insect Biochem. Mol. Biol. 79, 108–118 (2016).
Google Scholar
Gazara, R. K. et al. De novo transcriptome sequencing and comparative analysis of midgut tissues of four non-model insects pertaining to Hemiptera, Coleoptera, Diptera and Lepidoptera. Gene 627, 85–93 (2017).
Google Scholar
Braig, H. R., Zhou, W., Dobson, S. L. & O’Neill, S. L. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J. Bacteriol. 180, 2373–2378 (1998).
Google Scholar
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
Google Scholar
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419 (2017).
Google Scholar
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020), https://www.R-project.org.
Soneson, C., Love, M. I. & Robinson, M. D. Differential analyses for RNA-seq: Transcript-level estimates improve gene-level inferences. F1000Research 4, 1521 (2016).
Google Scholar
Thurmond, J. et al. FlyBase 2.0: The next generation. Nucleic Acids Res. 47, D759–D765 (2019).
Google Scholar
Hardcastle, T. J. & Kelly, K. A. BaySeq: Empirical Bayesian methods for identifying differential expression in sequence count data. BMC Bioinform. 11, 422 (2010).
Google Scholar
Huang, D. W., Sherman, B. T. & Lempicki, R. A. Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1–13 (2009).
Google Scholar
Gaujoux, R. & Seoighe, C. A flexible R package for nonnegative matrix factorization. BMC Bioinform. 11, 367 (2010).
Google Scholar
Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.5-6. (2019) https://cran.r-project.org/web/packages/vegan/.
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
Google Scholar
Wickham, H. ggplot2. Wiley Interdiscip. Rev. Comput. Stat. 3, 180–185 (2011).
Wittkopp, P. J. Variable gene expression in eukaryotes: A network perspective. J. Exp. Biol. 210, 1567–1575 (2007).
Google Scholar
Lin, Y., Chen, Z.-X., Oliver, B. & Harbison, S. T. Microenvironmental gene expression plasticity among individual Drosophila melanogaster. G3 Genes Genomes Genet. 6, 4197–4210 (2016).
Google Scholar
Kristensen, T. N., Sørensen, P., Pedersen, K. S., Kruhøffer, M. & Loeschcke, V. Inbreeding by environmental interactions affect gene expression in Drosophila melanogaster. Genetics 173, 1329–1336 (2006).
Google Scholar
Dunning, L. T., Dennis, A. B., Sinclair, B. J., Newcomb, R. D. & Buckley, T. R. Divergent transcriptional responses to low temperature among populations of alpine and lowland species of New Zealand stick insects (Micrarchus). Mol. Ecol. 23, 2712–2726 (2014).
Google Scholar
Lambert, A. J. & Brand, M. D. Reactive oxygen species production by mitochondria. In Mitochondrial DNA. Methods in Molecular Biology (ed. Stuart, J. A.) vol. 554 165–181 (Humana Press, 2009).
Kurz, M. et al. Structural and functional characterization of the oxidoreductase α-DsbA1 from Wolbachia pipientis. Antioxidants Redox Signal. 11, 1485–1500 (2009).
Google Scholar
Zug, R. & Hammerstein, P. Wolbachia and the insect immune system: What reactive oxygen species can tell us about the mechanisms of Wolbachia-host interactions. Front. Microbiol. 6, 1201 (2015).
Google Scholar
Ratzka, C., Gross, R. & Feldhaar, H. Endosymbiont tolerance and control within insect hosts. Insects 3, 553–572 (2012).
Google Scholar
Pan, X. et al. Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti. Proc. Natl. Acad. Sci. U. S. A. 109, E23-31 (2012).
Google Scholar
Brennan, L. J., Haukedal, J. A., Earle, J. C., Keddie, B. & Harris, H. L. Disruption of redox homeostasis leads to oxidative DNA damage in spermatocytes of Wolbachia-infected Drosophila simulans. Insect Mol. Biol. 21, 510–520 (2012).
Google Scholar
Blagrove, M. S. C., Arias-Goeta, C., Failloux, A.-B. & Sinkins, S. P. Wolbachia strain wMel induces cytoplasmic incompatibility and blocks dengue transmission in Aedes albopictus. Proc. Natl. Acad. Sci. 109, 255–260 (2012).
Google Scholar
Andrews, E. S., Crain, P. R., Fu, Y., Howe, D. K. & Dobson, S. L. Reactive oxygen species production and Brugia pahangi survivorship in Aedes polynesiensis with artificial Wolbachia infection types. PLoS Pathog. 8, e1003075 (2012).
Google Scholar
Oliveira, M. F. et al. Haem detoxification by an insect. Nature 400, 517–518 (1999).
Google Scholar
Paiva-Silva, G. O. et al. A heme-degradation pathway in a blood-sucking insect. Proc. Natl. Acad. Sci. U. S. A. 103, 8030–8035 (2006).
Google Scholar
Levi, S. & Rovida, E. The role of iron in mitochondrial function. Biochim. Biophys. Acta Gen. Subj. 1790, 629–636 (2009).
Google Scholar
Kremer, N. et al. Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathog. 5, e1000630 (2009).
Google Scholar
Kremer, N. et al. Influence of Wolbachia on host gene expression in an obligatory symbiosis. BMC Microbiol. 12, S7 (2012).
Google Scholar
Peng, Y., Nielsen, J. E., Cunningham, J. P. & McGraw, E. A. Wolbachia infection alters olfactory-cued locomotion in Drosophila spp. Appl. Environ. Microbiol. 74, 3943–3948 (2008).
Google Scholar
Peng, Y. & Wang, Y. Infection of Wolbachia may improve the olfactory response of Drosophila. Chin. Sci. Bull. 54, 1369–1375 (2009).
Fattouh, N., Cazevieille, C. & Landmann, F. Wolbachia endosymbionts subvert the endoplasmic reticulum to acquire host membranes without triggering ER stress. PLoS Negl. Trop. Dis. 13, e0007218 (2019).
Google Scholar
Chagas-Moutinho, V. A., Silva, R., de Souza, W. & Motta, M. C. Identification and ultrastructural characterization of the Wolbachia symbiont in Litomosoides chagasfilhoi. Parasit. Vectors 8, 74 (2015).
Google Scholar
Serbus, L. R., Casper-Lindley, C., Landmann, F. & Sullivan, W. The genetics and cell biology of Wolbachia-host interactions. Annu. Rev. Genet. 42, 683–707 (2008).
Google Scholar
Ping, Y. et al. Linking Aβ42-induced hyperexcitability to neurodegeneration, learning and motor deficits, and a shorter lifespan in an Alzheimer’s model. PLoS Genet. 11, e1005025 (2015).
Google Scholar
Ping, Y. et al. Shal/Kv4 channels are required for maintaining excitability during repetitive firing and normal locomotion in Drosophila. PLoS One 6, e16043 (2011).
Google Scholar
Ping, Y. & Tsunoda, S. Inactivity-induced increase in nAChRs upregulates Shal K+ channels to stabilize synaptic potentials. Nat. Neurosci. 15, 90–97 (2012).
Google Scholar
Kim, W. J., Jan, L. Y. & Jan, Y. N. A PDF/NPF neuropeptide signaling circuitry of male Drosophila melanogaster controls rival-induced prolonged mating. Neuron 80, 1190–1205 (2013).
Google Scholar
King, A. N. et al. A peptidergic circuit links the circadian clock to locomotor activity. Curr. Biol. 27, 1915-1927.e5 (2017).
Google Scholar
Kim, Y. J., Žitňan, D., Galizia, C. G., Cho, K. H. & Adams, M. E. A command chemical triggers an innate behavior by sequential activation of multiple peptidergic ensembles. Curr. Biol. 16, 1395–1407 (2006).
Google Scholar
Rapaport, F. et al. Comprehensive evaluation of differential gene expression analysis methods for RNA-seq data. Genome Biol. 14, 3158 (2013).
Google Scholar
Kvam, V. M., Liu, P. & Si, Y. A comparison of statistical methods for detecting differentially expressed genes from RNA-seq data. Am. J. Bot. 99, 248–256 (2012).
Google Scholar
Guo, Y., Li, C. I., Ye, F. & Shyr, Y. Evaluation of read count based RNAseq analysis methods. BMC Genom. 14, S2 (2013).
Google Scholar
Source: Ecology - nature.com
