Microbiome composition is shaped by geography and population structure in the parasitic wasp Asobara japonica, but not in the presence of the endosymbiont Wolbachia.

environment microbe interaction geographical variation host microbiome interaction parasitoid wasp population structure reproductive mode

Journal

Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478

Informations de publication

Date de publication:
Dec 2023
Historique:
revised: 11 09 2022
received: 13 02 2022
accepted: 15 09 2022
medline: 27 11 2023
pubmed: 21 9 2022
entrez: 20 9 2022
Statut: ppublish

Résumé

The microbial community composition is crucial for diverse life-history traits in many organisms. However, we still lack a sufficient understanding of how the host microbiome is acquired and maintained, a pressing issue in times of global environmental change. Here we investigated to what extent host genotype, environmental conditions, and the endosymbiont Wolbachia influence the bacterial communities in the parasitic wasp Asobara japonica. We sampled multiple wasp populations across 10 locations in their natural distribution range in Japan and sequenced the host genome (whole genome sequencing) and microbiome (16S rRNA gene). We compared the host population structure and bacterial community composition of wasps that reproduce sexually and are uninfected with Wolbachia with wasps that reproduce asexually and carry Wolbachia. The bacterial communities in asexual wasps were highly similar due to a strong effect of Wolbachia rather than host genomic structure. In contrast, in sexual wasps, bacterial communities appear primarily shaped by a combination of population structure and environmental conditions. Our research highlights that multiple factors shape the bacterial communities of an organism and that the presence of a single endosymbiont can strongly alter their compositions. This information is crucial to understanding how organisms and their associated microbiome will react in the face of environmental change.

Identifiants

pubmed: 36125236
doi: 10.1111/mec.16699
doi:

Substances chimiques

RNA, Ribosomal, 16S 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

6644-6658

Informations de copyright

© 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

Références

Anderson, M. J., & Willis, T. J. (2003). Canonical analysis of principal coordinates: A useful method of constrained ordination for ecology. Ecology, 84, 511-525. https://doi.org/10.1890/0012-9658(2003)084[0511:CAOPCA]2.0.CO;2
Audsley, M. D., Ye, Y. H., & McGraw, E. A. (2017). The microbiome composition of Aedes aegypti is not critical for Wolbachia-mediated inhibition of dengue virus. PLoS Neglected Tropical Diseases, 11, e0005426. https://doi.org/10.1371/journal.pntd.0005426
Bhatia, G., Patterson, N., Sankararaman, S., & Price, A. L. (2013). Estimating and interpreting FST: The impact of rare variants. Genome Research, 23, 1514-1521. https://doi.org/10.1101/gr.154831.113
Bodawatta, K. H., Koane, B., Maiah, G., Sam, K., Poulsen, M., & Jønsson, K. A. (2021). Species-specific but not phylosymbiotic gut microbiomes of New Guinean passerine birds are shaped by diet and flight-associated gut modifications. Proceedings of the Royal Society B: Biological Sciences, 288, 20210446. https://doi.org/10.1098/rspb.2021.0446
Bouchon, D., Zimmer, M., & Dittmer, J. (2016). The terrestrial isopod microbiome: An all-in-one toolbox for animal-microbe interactions of ecological relevance. Frontiers in Microbiology, 7, 1472. https://doi.org/10.3389/fmicb.2016.01472
Brinker, P., Fontaine, M. C., Beukeboom, L. W., & Falcao Salles, J. (2019). Host, symbionts, and the microbiome: The missing tripartite interaction. Trends in Microbiology, 27, 480-488. https://doi.org/10.1016/j.tim.2019.02.002
Callahan, B. (2018). Silva taxonomic training data formatted for DADA2 (Silva version 132). Zendo. https://doi.org/10.5281/ZENODO.4587955
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13, 581-583. https://doi.org/10.1038/nmeth.3869
Chen, H., Rangasamy, M., Tan, S. Y., Wang, H., & Siegfried, B. D. (2010). Evaluation of five methods for total DNA extraction from western corn rootworm beetles. PLoS One, 5, e11963. https://doi.org/10.1371/journal.pone.0011963
Cohen, C., Toh, E., Munro, D., Dong, Q., & Hawlena, H. (2015). Similarities and seasonal variations in bacterial communities from the blood of rodents and from their flea vectors. ISME Journal, 9, 1662-1676. https://doi.org/10.1038/ismej.2014.255
Colman, D. R., Toolson, E. C., & Takacs-Vesbach, C. D. (2012). Do diet and taxonomy influence insect gut bacterial communities? Molecular Ecology, 21, 5124-5137. https://doi.org/10.1111/j.1365-294X.2012.05752.x
Conover, W. J., Johnson, M. E., & Johnson, M. M. (1981). A comparative study of tests for homogeneity of variances, with applications to the outer continental shelf bidding data. Technometrics, 23, 351-361. https://doi.org/10.1080/00401706.1981.10487680
Corbin, C., Heyworth, E. R., Ferrari, J., & Hurst, G. D. D. (2017). Heritable symbionts in a world of varying temperature. Heredity, 118, 10-20. https://doi.org/10.1038/hdy.2016.71
de Vries, E. J., Jacobs, G., Sabelis, M. W., Menken, S. B. J., & Breeuwer, J. A. J. (2004). Diet-dependent effects of gut bacteria on their insect host: The symbiosis of Erwinia sp. and western flower thrips. Proceedings of the Royal Society of London B: Biological Sciences, 271, 2171-2178. https://doi.org/10.1098/rspb.2004.2817
Dittmer, J., Beltran-Bech, S., Lesobre, J., Raimond, M., Johnson, M., & Bouchon, D. (2014). Host tissues as microhabitats for Wolbachia and quantitative insights into the bacterial community in terrestrial isopods. Molecular Ecology, 23, 2619-2635. https://doi.org/10.1111/mec.12760
Dittmer, J., & Bouchon, D. (2018). Feminizing Wolbachia influence microbiota composition in the terrestrial isopod Armadillidium vulgare. Scientific Reports, 8, 6998. https://doi.org/10.1038/s41598-018-25450-4
Duan, X. Z., Sun, J. T., Wang, L. T., Shu, X. H., Guo, Y., Keiichiro, M., Zhu, Y. X., Bing, X. L., Hoffmann, A. A., & Hong, X. Y. (2020). Recent infection by Wolbachia alters microbial communities in wild Laodelphax striatellus populations. Microbiome, 8, 104. https://doi.org/10.1186/s40168-020-00878-x
Duplouy, A., Dotson, B. R., Nishiguchi, M. K., & Cárdenas, C. A. (2021). Editorial: Symbiosis in a changing environment. Frontiers in Ecology and Evolution, 9, 536. https://doi.org/10.3389/fevo.2021.731892
Easson, C. G., Chaves-Fonnegra, A., Thacker, R. W., & Lopez, J.v. (2020). Host population genetics and biogeography structure the microbiome of the sponge Cliona delitrix. Ecology and Evolution, 10, 2007-2020. https://doi.org/10.1002/ece3.6033
Falony, G., Joossens, M., Vieira-Silva, S., Wang, J., Darzi, Y., Faust, K., Kurilshikov, A., Bonder, M. J., Valles-Colomer, M., Vandeputte, D., Tito, R. Y., Chaffron, S., Rymenans, L., Verspecht, C., de Sutter, L., Lima-Mendez, G., D'hoe, K., Jonckheere, K., Homola, D., … Raes, J. (2016). Population-level analysis of gut microbiome variation. Science, 352, 560-564. https://doi.org/10.1126/science.aad3503
Ferguson, L. v., Dhakal, P., Lebenzon, J. E., Heinrichs, D. E., Bucking, C., & Sinclair, B. J. (2018). Seasonal shifts in the insect gut microbiome are concurrent with changes in cold tolerance and immunity. Functional Ecology, 32, 2357-2368. https://doi.org/10.1111/1365-2435.13153
Fox, E. A., Wright, A. E., Fumagalli, M., & Vieira, F. G. (2019). ngsLD: Evaluating linkage disequilibrium using genotype likelihoods. Bioinformatics, 35, 3855-3856. https://doi.org/10.1093/bioinformatics/btz200
Fumagalli, M., Vieira, F. G., Korneliussen, T. S., Linderoth, T., Huerta-Sánchez, E., Albrechtsen, A., & Nielsen, R. (2013). Quantifying population genetic differentiation from next-generation sequencing data. Genetics, 195, 979-992. https://doi.org/10.1534/genetics.113.154740
Gao, C. H., Yu, G., & Cai, P. (2021). ggVennDiagram: An intuitive, easy-to-use, and highly customizable R package to generate venn diagram. Frontiers in Genetics, 12, 706907. https://doi.org/10.3389/fgene.2021.706907
Gatesoupe, F. J., Huelvan, C., le Bayon, N., le Delliou, H., Madec, L., Mouchel, O., Quazuguel, P., Mazurais, D., & Zambonino-Infante, J. L. (2016). The highly variable microbiota associated to intestinal mucosa correlates with growth and hypoxia resistance of sea bass, Dicentrarchus labrax, submitted to different nutritional histories. BMC Microbiology, 16, 1-13. https://doi.org/10.1186/S12866-016-0885-2
Goulet, T. L., & Goulet, D. (2021). Climate change leads to a reduction in symbiotic derived cnidarian biodiversity on coral reefs. Frontiers in Ecology and Evolution, 9, 636279. https://doi.org/10.3389/FEVO.2021.636279
Greenspan, S. E., Migliorini, G. H., Lyra, M. L., Pontes, M. R., Carvalho, T., Ribeiro, L. P., Moura-Campos, D., Haddad, C. F. B., Toledo, L. F., Romero, G. Q., & Becker, C. G. (2020). Warming drives ecological community changes linked to host-associated microbiome dysbiosis. Nature Climate Change, 10, 1057-1061. https://doi.org/10.1038/s41558-020-0899-5
Guerrieri, E., Giorgini, M., Cascone, P., Carpenito, S., & van Achterberg, C. (2016). Species diversity in the parasitoid genus asobara (Hymenoptera: Braconidae) from the native area of the fruit fly pest Drosophila suzukii (Diptera: Drosophilidae). PLoS One, 11, e0147382. https://doi.org/10.1371/journal.pone.0147382
Herren, C. M., & McMahon, K. D. (2018). Keystone taxa predict compositional change in microbial communities. Environmental Microbiology, 20, 2207-2217. https://doi.org/10.1111/1462-2920.14257
Hurst, G. D. D., Johnson, A. P., Schulenburg, J. H. G. v. d., & Fuyama, Y. (2000). Male-killing Wolbachia in Drosophila: A temperature-sensitive trait with a threshold bacterial density. Genetics, 156, 699-709. https://doi.org/10.1093/genetics/156.2.699
Jaenike, J. (2009). Coupled population dynamics of endosymbionts within and between hosts. Oikos, 118, 353-362. https://doi.org/10.1111/j.1600-0706.2008.17110.x
Jehrke, L., Stewart, F. A., Droste, A., & Beller, M. (2018). The impact of genome variation and diet on the metabolic phenotype and microbiome composition of Drosophila melanogaster. Scientific Reports, 8, 6215. https://doi.org/10.1038/s41598-018-24542-5
Johnston, P. R., & Rolff, J. (2015). Host and symbiont jointly control gut microbiota during complete metamorphosis. PLoS Pathogens, 11(11), e1005246. https://doi.org/10.1371/journal.ppat.1005246
Kikuchi, Y., Tada, A., Musolin, D. L., Hari, N., Hosokawa, T., Fujisaki, K., & Fukatsu, T. (2016). Collapse of insect gut symbiosis under simulated climate change. MBio, 7(5), e01578-16. https://doi.org/10.1128/mBio.01578-16
Koch, H., & Schmid-Hempel, P. (2012). Gut microbiota instead of host genotype drive the specificity in the interaction of a natural host-parasite system. Ecology Letters, 15(10), 1095-1103. https://doi.org/10.1111/j.1461-0248.2012.01831.x
Kolasa, M., Ścibior, R., Mazur, M. A., Kubisz, D., Dudek, K., & Kajtoch, Ł. (2019). How hosts taxonomy, trophy, and endosymbionts shape microbiome diversity in beetles. Microbial Ecology, 78, 995-1013. https://doi.org/10.1007/s00248-019-01358-y
Kolodny, O., & Schulenburg, H. (2020). Microbiome-mediated plasticity directs host evolution along several distinct time scales. Philosophical Transactions of the Royal Society B, 375(1808), 20190589. https://doi.org/10.1098/RSTB.2019.0589
Korneliussen, T. S., Albrechtsen, A., & Nielsen, R. (2014). ANGSD: Analysis of next generation sequencing data. BMC Bioinformatics, 15, 356. https://doi.org/10.1186/s12859-014-0356-4
Kraaijeveld, K., Franco, P., Reumer, B. M., & van Alphen, J. J. M. (2009). Effects of parthenogenesis and geographic isolation on female sexual traits in a parasitoid wasp. Evolution, 63, 3085-3096. https://doi.org/10.1111/j.1558-5646.2009.00798.x
Kremer, N., Charif, D., Henri, H., Bataille, M., Prévost, G., Kraaijeveld, K., & Vavre, F. (2009). A new case of Wolbachia dependence in the genus Asobara: Evidence for parthenogenesis induction in Asobara japonica. Heredity, 103, 248-256. https://doi.org/10.1038/hdy.2009.63
Lapanje, A., Zrimec, A., Drobne, D., & Rupnik, M. (2010). Long-term Hg pollution-induced structural shifts of bacterial community in the terrestrial isopod (Porcellio scaber) gut. Environmental Pollution, 158, 3186-3193. https://doi.org/10.1016/j.envpol.2010.07.001
Lefort, V., Desper, R., & Gascuel, O. (2015). FastME 2.0: A comprehensive, accurate, and fast distance-based phylogeny inference program. Molecular Biology and Evolution, 32, 2798-2800. https://doi.org/10.1093/molbev/msv150
Lim, S. J., & Bordenstein, S. R. (2020). An introduction to phylosymbiosis. Proceedings of the Royal Society B: Biological Sciences, 287, 20192900. https://doi.org/10.1098/rspb.2019.2900
Love, M. I., Huber, W., & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550. https://doi.org/10.1186/s13059-014-0550-8
Ma, W. J., Pannebakker, B. A., Li, X., Geuverink, E., Anvar, S. Y., Veltsos, P., Schwander, T., van de Zande, L., & Beukeboom, L. W. (2021). A single QTL with large effect is associated with female functional virginity in an asexual parasitoid wasp. Molecular Ecology, 30, 1979-1992. https://doi.org/10.1111/mec.15863
Ma, W. J., Pannebakker, B. A., van de Zande, L., Schwander, T., Wertheim, B., & Beukeboom, L. W. (2015). Diploid males support a two-step mechanism of endosymbiont-induced thelytoky in a parasitoid wasp. BMC Evolutionary Biology, 15, 84. https://doi.org/10.1186/s12862-015-0370-9
Ma, W. J., & Schwander, T. (2017). Patterns and mechanisms in instances of endosymbiont-induced parthenogenesis. Journal of Evolutionary Biology, 30, 868-888. https://doi.org/10.1111/jeb.13069
McFall-Ngai, M., Hadfield, M. G., Bosch, T. C. G., Carey, H.v., Domazet-Lošo, T., Douglas, A. E., Dubilier, N., Eberl, G., Fukami, T., Gilbert, S. F., Hentschel, U., King, N., Kjelleberg, S., Knoll, A. H., Kremer, N., Mazmanian, S. K., Metcalf, J. L., Nealson, K., Pierce, N. E., … Wernegreen, J. J. (2013). Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences of the United States of America, 110, 3229-3236. https://doi.org/10.1073/pnas.1218525110
McMurdie, P. J., & Holmes, S. (2013). phyloseq: An R Package for reproducible interactive analysis and graphics of microbiome census data. PLoS One, 8, e61217. https://doi.org/10.1371/journal.pone.0061217
Meisner, J., & Albrechtsen, A. (2018). Inferring population structure and admixture proportions in low-depth NGS data. Genetics, 210, 719-731. https://doi.org/10.1534/genetics.118.301336
Menken, S. B. J. (1991). Does haplodiploidy explain reduced levels of genetic variability in hymenoptera? Proceedings of Experimental and Applied Entomology, 2, 172-178.
Metcalf, R. A., Marlin, J. C., & Whitt, G. S. (1975). Low levels of genetic heterozygosity in Hymenoptera. Nature, 257, 792-794. https://doi.org/10.1038/257792a0
Mitsui, H., van Achterberg, K., Nordlander, G., & Kimura, M. T. (2007). Geographical distributions and host associations of larval parasitoids of frugivorous Drosophilidae in Japan. Journal of Natural History, 41, 1731-1738. https://doi.org/10.1080/00222930701504797
Miyawaki, A. (1984). A Vegetation ~ Ecological View of the Japanese Archipelago*. Bulletin of the Institute of Environmental Science and Technology, 101, 85-101.
Moran, N. A., McCutcheon, J. P., & Nakabachi, A. (2008). Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics, 42, 165-190. https://doi.org/10.1146/annurev.genet.41.110306.130119
Nielsen, R., Korneliussen, T., Albrechtsen, A., Li, Y., & Wang, J. (2012). SNP calling, genotype calling, and sample allele frequency estimation from new-generation sequencing data. PLoS One, 7, e37558. https://doi.org/10.1371/journal.pone.0037558
Novakova, E., Woodhams, D. C., Rodríguez-Ruano, S. M., Brucker, R. M., Leff, J. W., Maharaj, A., Amir, A., Knight, R., & Scott, J. (2017). Mosquito microbiome dynamics, a background for prevalence and seasonality of West Nile virus. Frontiers in Microbiology, 8, 526. https://doi.org/10.3389/fmicb.2017.00526
Ochman, H., Worobey, M., Kuo, C. H., Ndjango, J. B. N., Peeters, M., Hahn, B. H., & Hugenholtz, P. (2010). Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biology, 8, e1000546. https://doi.org/10.1371/journal.pbio.1000546
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara R.B., Simpson G.L., Solymos P., & Stevens M. (2016). vegan: Community ecology package. R Package Version 2.3-5. Retrieved from https://cran.r-project.org/package=vegan
Packer, L., & Owen, R. (2001). Population genetic aspects of pollinator decline. Conservation Ecology, 5, 4. https://doi.org/10.5751/ES-00267-050104
Patterson, N., Price, A. L., & Reich, D. (2006). Population structure and eigenanalysis. PLoS Genetics, 2, e190. https://doi.org/10.1371/journal.pgen.0020190
Pita, L., Rix, L., Slaby, B. M., Franke, A., & Hentschel, U. (2018). The sponge holobiont in a changing ocean: From microbes to ecosystems. Microbiome, 6, 1-18. https://doi.org/10.1186/S40168-018-0428-1
Plottel, C. S., & Blaser, M. J. (2011). Microbiome and malignancy. Cell Host and Microbe, 10, 324-335. https://doi.org/10.1016/j.chom.2011.10.003
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., & Glöckner, F. O. (2013). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41, D590-D596. https://doi.org/10.1093/NAR/GKS1219
Ramalho, M. O., Bueno, O. C., Moreau, C. S., Oliveira Ramalho, M., Correa Bueno, O., & Saux Moreau, C. (2017). Species-specific signatures of the microbiome from Camponotus and Colobopsis ants across developmental stages. PLoS One, 12, e0187461. https://doi.org/10.1371/journal.pone.0187461
Rennison, D. J., Rudman, S. M., & Schluter, D. (2019). Parallel changes in gut microbiome composition and function during colonization, local adaptation and ecological speciation. Proceedings of the Royal Society B: Biological Sciences, 286, 20191911. https://doi.org/10.1098/rspb.2019.1911
Reynolds, J., Weir, B. S., & Cockerham, C. C. (1983). Estimation of the coancestry coefficient: Basis for a short-term genetic distance. Genetics, 105, 767-779. https://doi.org/10.1093/genetics/105.3.767
Ridley, E.v., Wong, A. C. N., Westmiller, S., & Douglas, A. E. (2012). Impact of the resident microbiota on the nutritional phenotype of Drosophila melanogaster. PLoS One, 7, e36765. https://doi.org/10.1371/journal.pone.0036765
Rudman, S. M., Greenblum, S., Hughes, R. C., Rajpurohit, S., Kiratli, O., Lowder, D. B., Lemmon, S. G., Petrov, D. A., Chaston, J. M., & Schmidt, P. (2019). Microbiome composition shapes rapid genomic adaptation of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 116, 20025-20032. https://doi.org/10.1073/pnas.1907787116
Russell, J. A., & Moran, N. A. (2006). Costs and benefits of symbiont infection in aphids: Variation among symbionts and across temperatures. Proceedings of the Royal Society B: Biological Sciences, 273(1586), 603-610. https://doi.org/10.1098/rspb.2005.3348
Ryan, M. H. (2022). Rmisc: Ryan Miscellaneous. In (Version 1.5.1) https://cran.r-project.org/package=Rmisc
Schliep, K. P. (2011). phangorn: Phylogenetic analysis in R. Bioinformatics, 27, 592-593. https://doi.org/10.1093/bioinformatics/btq706
Schliep, K. P., Potts, A. J., Morrison, D. A., & Grimm, G. W. (2017). Intertwining phylogenetic trees and networks. Methods in Ecology and Evolution, 8, 1212-1220. https://doi.org/10.1111/2041-210X.12760
Schneider, M. v., Driessen, G., Beukeboom, L. W., Boll, R., van Eunen, K., Selzner, A., Talsma, J., & Lapchin, L. (2003). Gene flow between arrhenotokous and thelytokous populations of Venturia canescens (Hymenoptera). Heredity, 90, 260-267. https://doi.org/10.1038/sj.hdy.6800245
Shapiro, S. S., & Wilk, M. B. (1965). An analysis of variance test for normality (complete samples). Biometrika, 52(3-4), 591-611. https://doi.org/10.1093/biomet/52.3-4.591
Sharon, G., Segal, D., Ringo, J. M., Hefetz, A., Zilber-Rosenberg, I., & Rosenberg, E. (2010). Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 107, 20051-20056. https://doi.org/10.1073/pnas.1302980110
Shropshire, J. D., & Bordenstein, S. R. (2016). Speciation by symbiosis: The microbiome and behavior. MBio, 7, e01785-e01715. https://doi.org/10.1128/mBio.01785-15
Simhadri, R. K., Fast, E., Guo, R., Schultz, M. J., Vaisman, N., Ortiz, L., Bybee, J., Slatko, B. E., & Frydman, H. M. (2017). The gut commensal microbiome of Drosophila melanogaster is modified by the endosymbiont Wolbachia. MSphere, 2, e00287-e00217. https://doi.org/10.1128/mSphere.00287-17
Ssekagiri A. (2020). microbiomeSeq: Microbial community analysis in an environmental context R package version 0.1. http://www.github.com/umerijaz/microbiomeSeq
Stamatakis, A. (2014). RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312-1313. https://doi.org/10.1093/bioinformatics/btu033
Sumi, T., Miura, K., & Miyatake, T. (2017). Wolbachia density changes seasonally amongst populations of the pale grass blue butterfly, Zizeeria maha (Lepidoptera: Lycaenidae). PLoS One, 12, e0175373. https://doi.org/10.1371/journal.pone.0175373
Trevathan-Tackett, S. M., Sherman, C. D. H., Huggett, M. J., Campbell, A. H., Laverock, B., Hurtado-McCormick, V., Seymour, J. R., Firl, A., Messer, L. F., Ainsworth, T. D., Negandhi, K. L., Daffonchio, D., Egan, S., Engelen, A. H., Fusi, M., Thomas, T., Vann, L., Hernandez-Agreda, A., Gan, H. M., … Macreadie, P. I. (2019). A horizon scan of priorities for coastal marine microbiome research. Nature Ecology & Evolution, 3(11), 1509-1520. https://doi.org/10.1038/s41559-019-0999-7
Uren Webster, T. M., Rodriguez-Barreto, D., Castaldo, G., Gough, P., Consuegra, S., & Garcia de Leaniz, C. (2020). Environmental plasticity and colonisation history in the Atlantic salmon microbiome: A translocation experiment. Molecular Ecology, 29(5), 886-898. https://doi.org/10.1111/mec.15369
van Opijnen, T., & Breeuwer, J. A. (1999). High temperatures eliminate Wolbachia, a cytoplasmic incompatibility inducing endosymbiont, from the two-spotted spider mite. Experimental and Applied Acarology, 23, 871-881. https://doi.org/10.1023/A:1006363604916
van Veelen, H. P. J., Falcão Salles, J., Matson, K. D., van der Velde, M., & Tieleman, B. I. (2020). Microbial environment shapes immune function and cloacal microbiota dynamics in zebra finches Taeniopygia guttata. Animal Microbiome, 2(1), 1-17. https://doi.org/10.1186/s42523-020-00039-3
van Veelen, H. P. J., Falcao Salles, J., & Tieleman, B. I. (2017). Multi-level comparisons of cloacal, skin, feather and nest-associated microbiota suggest considerable influence of horizontal acquisition on the microbiota assembly of sympatric woodlarks and skylarks. Microbiome, 5(1), 156. https://doi.org/10.1186/S40168-017-0371-6
Vastra, M., Salvin, P., & Roos, C. (2016). MIC of carbon steel in Amazonian environment: Electrochemical, biological and surface analyses. International Biodeterioration & Biodegradation, 112, 98-107. https://doi.org/10.1016/J.IBIOD.2016.05.004
Vercken, E., Fontaine, M. C., Gladieux, P., Hood, M. E., Jonot, O., & Giraud, T. (2010). Glacial refugia in pathogens: European genetic structure of anther smut pathogens on Silene latifolia and Silene dioica. PLoS Pathogens, 6, e1001229. https://doi.org/10.1371/journal.ppat.1001229
Vieira, F. G., Fumagalli, M., Albrechtsen, A., & Nielsen, R. (2013). Estimating inbreeding coefficients from NGS data: Impact on genotype calling and allele frequency estimation. Genome Research, 23, 1852-1861. https://doi.org/10.1101/gr.157388.113
Vieira, F. G., Lassalle, F., Korneliussen, T. S., & Fumagalli, M. (2016). Improving the estimation of genetic distances from Next-Generation Sequencing data. Biological Journal of the Linnean Society, 117, 139-149. https://doi.org/10.1111/bij.12511
Wachi, N., Gau, J. J., Fujie, S., Fukano, K., & Maeto, K. (2021). Genomic population structure of sympatric sexual and asexual populations in a parasitic wasp, Meteorus pulchricornis (Hymenoptera: Braconidae), inferred from six hundred single-nucleotide polymorphism loci. Molecular Ecology, 30, 1612-1623. https://doi.org/10.1111/mec.15834
Wang, G. H., Dittmer, J., Douglas, B., Huang, L., & Brucker, R. M. (2021). Coadaptation between host genome and microbiome under long-term xenobiotic-induced selection. Science Advances, 7, eabd4473. https://doi.org/10.1126/sciadv.abd4473
Wickham, H. (2016). ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York.
Wong, A. C.-N., Dobson, A. J., & Douglas, A. E. (2014). Gut microbiota dictates the metabolic response of Drosophila to diet. Journal of Experimental Biology, 217, 1894-1901. https://doi.org/10.1242/jeb.101725RESEARCH
Ye, Y. H., Seleznev, A., Flores, H. A., Woolfit, M., & McGraw, E. A. (2017). Gut microbiota in Drosophila melanogaster interacts with Wolbachia but does not contribute to Wolbachia-mediated antiviral protection. Journal of Invertebrate Pathology, 143, 18-25. https://doi.org/10.1016/j.jip.2016.11.011
Yu, G., Lam, T. T.-Y., Zhu, H., & Guan, Y. (2018). Two methods for mapping and visualizing associated data on phylogeny using ggtree. Molecular Biology and Evolution, 35, 3041-3043.
Yun, J.-H., Roh, S. W., Whon, T. W., Jung, M.-J., Kim, M.-S., Park, D.-S., Yoon, C., Nam, Y. D., Kim, Y. J., Choi, J. H., Kim, J. Y., Shin, N. R., Kim, S. H., Lee, W. J., & Bae, J. W. (2014). Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Applied and Environmental Microbiology, 80, 5254-5264. https://doi.org/10.1128/aem.01226-14
Zug, R., & Hammerstein, P. (2012). Still a host of hosts for Wolbachia: Analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One, 7(6), e38544. https://doi.org/10.1371/journal.pone.0038544

Auteurs

Pina Brinker (P)

Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, Groningen, The Netherlands.

Fangying Chen (F)

Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, Groningen, The Netherlands.

Yacine Ben Chehida (YB)

Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, Groningen, The Netherlands.
Department of Animal and Plant Sciences, The University of Sheffield, Sheffield, UK.
Department of Biology, University of York, York, UK.

Leo W Beukeboom (LW)

Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, Groningen, The Netherlands.

Michael C Fontaine (MC)

Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, Groningen, The Netherlands.
MIVEGEC, Univ. Montpellier, CNRS, IRD, Montpellier, France.
Centre de Recherche en Écologie et Évolution de la Santé (CREES), Montpellier, France.

Joana Falcao Salles (JF)

Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, Groningen, The Netherlands.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH