Exploring the abdominal microbiome of two Heliconius species in the Central Colombian Andes

Las comunidades microbianas del intestino tienen funciones importantes en la reproducción, digestión y protección contra patógenos de los insectos hospedadores. Dada la importancia de estas comunidades endosimbióticas para su anfitrión, la investigación sobre la diversidad y ecología de los microbio...

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Fecha de publicación:
2021
Institución:
Universidad del Rosario
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Repositorio EdocUR - U. Rosario
Idioma:
eng
OAI Identifier:
oai:repository.urosario.edu.co:10336/31623
Acceso en línea:
https://doi.org/10.48713/10336_31623
https://repository.urosario.edu.co/handle/10336/31623
Palabra clave:
Commensalibacter
Mariposas del género Heliconius
Microbioma
Wolbachia y Spiroplasma
Invertebrados
Heliconius butterflies
Microbiome
Commensalibacter
Wolbachia and Spiroplasma
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License
Atribución-NoComercial-CompartirIgual 2.5 Colombia
id EDOCUR2_568920464e7a8e801bc0768240232b02
oai_identifier_str oai:repository.urosario.edu.co:10336/31623
network_acronym_str EDOCUR2
network_name_str Repositorio EdocUR - U. Rosario
repository_id_str
dc.title.spa.fl_str_mv Exploring the abdominal microbiome of two Heliconius species in the Central Colombian Andes
dc.title.TranslatedTitle.spa.fl_str_mv Explorando el microbioma abdominal de dos especies de Heliconius en la cordillera central de Colombia
title Exploring the abdominal microbiome of two Heliconius species in the Central Colombian Andes
spellingShingle Exploring the abdominal microbiome of two Heliconius species in the Central Colombian Andes
Commensalibacter
Mariposas del género Heliconius
Microbioma
Wolbachia y Spiroplasma
Invertebrados
Heliconius butterflies
Microbiome
Commensalibacter
Wolbachia and Spiroplasma
title_short Exploring the abdominal microbiome of two Heliconius species in the Central Colombian Andes
title_full Exploring the abdominal microbiome of two Heliconius species in the Central Colombian Andes
title_fullStr Exploring the abdominal microbiome of two Heliconius species in the Central Colombian Andes
title_full_unstemmed Exploring the abdominal microbiome of two Heliconius species in the Central Colombian Andes
title_sort Exploring the abdominal microbiome of two Heliconius species in the Central Colombian Andes
dc.contributor.advisor.none.fl_str_mv Sanchez-Herrera, Melissa
Khazan, Emily
dc.contributor.none.fl_str_mv Brown, Anya
dc.subject.spa.fl_str_mv Commensalibacter
Mariposas del género Heliconius
Microbioma
Wolbachia y Spiroplasma
topic Commensalibacter
Mariposas del género Heliconius
Microbioma
Wolbachia y Spiroplasma
Invertebrados
Heliconius butterflies
Microbiome
Commensalibacter
Wolbachia and Spiroplasma
dc.subject.ddc.spa.fl_str_mv Invertebrados
dc.subject.keyword.spa.fl_str_mv Heliconius butterflies
Microbiome
Commensalibacter
Wolbachia and Spiroplasma
description Las comunidades microbianas del intestino tienen funciones importantes en la reproducción, digestión y protección contra patógenos de los insectos hospedadores. Dada la importancia de estas comunidades endosimbióticas para su anfitrión, la investigación sobre la diversidad y ecología de los microbiomas está recibiendo cada vez más atención. Quería probar la importancia de las especies hospedadoras y la geografía en la configuración de la composición del microbioma. Utilizando la región V4 del gen 16S, comparé las comunidades de microbiomas de dos especies de mariposas en dos ubicaciones geográficas. Usé 14 individuos de dos especies, Heliconius cydno y Heliconius clysonymus, capturadas en reservas forestales en Manizales, Caldas y Filandia, Quindío, en la Cordillera Central de los Andes colombianos. Los índices de diversidad alfa, incluidos Shannon e Inverse Simpson, demostraron similaridades en la diversidad taxonómica entre especies y sitios, pero con cambios en la abundancia entre las especies de mariposas. El análisis de coordenadas principales (PCoA) de las comunidades microbianas de individuos mostró que la variabilidad en los microbiomas se desacoplaba de la identidad y el sitio de las especies. Proteobacteria fue el filo más abundante en todas las muestras y Commensalibacter fue el género bacteriano más común. Además, encontramos la presencia de simbiontes intracelulares Spiroplasma y Wolbachia en nuestras muestras.
publishDate 2021
dc.date.accessioned.none.fl_str_mv 2021-06-16T20:04:59Z
dc.date.available.none.fl_str_mv 2021-06-16T20:04:59Z
dc.date.created.none.fl_str_mv 2021-05-28
dc.type.eng.fl_str_mv bachelorThesis
dc.type.coar.fl_str_mv http://purl.org/coar/resource_type/c_7a1f
dc.type.document.spa.fl_str_mv Trabajo de grado
dc.type.spa.spa.fl_str_mv Trabajo de grado
dc.identifier.doi.none.fl_str_mv https://doi.org/10.48713/10336_31623
dc.identifier.uri.none.fl_str_mv https://repository.urosario.edu.co/handle/10336/31623
url https://doi.org/10.48713/10336_31623
https://repository.urosario.edu.co/handle/10336/31623
dc.language.iso.spa.fl_str_mv eng
language eng
dc.rights.*.fl_str_mv Atribución-NoComercial-CompartirIgual 2.5 Colombia
dc.rights.coar.fl_str_mv http://purl.org/coar/access_right/c_abf2
dc.rights.acceso.spa.fl_str_mv Abierto (Texto Completo)
dc.rights.uri.none.fl_str_mv http://creativecommons.org/licenses/by-nc-sa/2.5/co/
rights_invalid_str_mv Atribución-NoComercial-CompartirIgual 2.5 Colombia
Abierto (Texto Completo)
http://creativecommons.org/licenses/by-nc-sa/2.5/co/
http://purl.org/coar/access_right/c_abf2
dc.format.extent.spa.fl_str_mv 41 pp.
dc.format.mimetype.none.fl_str_mv application/pdf
dc.publisher.spa.fl_str_mv Universidad del Rosario
dc.publisher.department.spa.fl_str_mv Facultad de Ciencias Naturales y Matemáticas
dc.publisher.program.spa.fl_str_mv Biología
institution Universidad del Rosario
dc.source.bibliographicCitation.spa.fl_str_mv Baxter, S. W., Papa, R., Chamberlain, N., Humphray, S. J., Joron, M., Morrison, C., ffrench-Constant, R. H., McMillan, W. O., & Jiggins, C. D. (2008). Convergent Evolution in the Genetic Basis of Müllerian Mimicry in Heliconius Butterflies. Genetics, 180(3), 1567-1577. https://doi.org/10.1534/genetics.107.082982
Chamberlain, N. L., Hill, R. I., Kapan, D. D., Gilbert, L. E., & Kronforst, M. R. (2009). Polymorphic Butterfly Reveals the Missing Link in Ecological Speciation. Science, 326(5954), 847-850. https://doi.org/10.1126/science.1179141
Chandler, J. A., Lang, J. M., Bhatnagar, S., Eisen, J. A., & Kopp, A. (2011). Bacterial Communities of Diverse Drosophila Species: Ecological Context of a Host–Microbe Model System. PLOS Genetics, 7(9), e1002272. https://doi.org/10.1371/journal.pgen.1002272
Crawford, J. E., Clarke, D. W., Criswell, V., Desnoyer, M., Cornel, D., Deegan, B., Gong, K., Hopkins, K. C., Howell, P., Hyde, J. S., Livni, J., Behling, C., Benza, R., Chen, W., Dobson, K. L., Eldershaw, C., Greeley, D., Han, Y., Hughes, B., … White, B. J. (2020). Efficient production of male Wolbachia -infected Aedes aegypti mosquitoes enables large-scale suppression of wild populations. Nature Biotechnology, 38(4), 482-492. https://doi.org/10.1038/s41587-020-0471-x
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(10), 2357-2368. https://doi.org/10.1111/1365-2435.13153
Fredensborg, B. L., Kálvalíð, I. F. í, Johannesen, T. B., Stensvold, C. R., Nielsen, H. V., & Kapel, C. M. O. (2020). Parasites modulate the gut-microbiome in insects: A proof-of-concept study. PLOS ONE, 15(1), e0227561. https://doi.org/10.1371/journal.pone.0227561
Gilbert, L. E. (1972). Pollen Feeding and Reproductive Biology of Heliconius Butterflies. Proceedings of the National Academy of Sciences, 69(6), 1403-1407. https://doi.org/10.1073/pnas.69.6.1403
Hammer, T. J., Dickerson, J. C., McMillan, W. O., & Fierer, N. (2020). Heliconius Butterflies Host Characteristic and Phylogenetically Structured Adult-Stage Microbiomes. Applied and Environmental Microbiology, 86(24), e02007-20, /aem/86/24/AEM.02007-20.atom. https://doi.org/10.1128/AEM.02007-20
Hammer, T. J., McMillan, W. O., & Fierer, N. (2014). Metamorphosis of a Butterfly-Associated Bacterial Community. PLOS ONE, 9(1), e86995. https://doi.org/10.1371/journal.pone.0086995
Hansen, A. K., & Moran, N. A. (2014). The impact of microbial symbionts on host plant utilization by herbivorous insects. Molecular Ecology, 23(6), 1473-1496. https://doi.org/10.1111/mec.12421
Huff, R., Pereira, R. I., Pissetti, C., Araújo, A. M. de, d’Azevedo, P. A., Frazzon, J., & GuedesFrazzon, A. P. (2020). Antimicrobial resistance and genetic relationships of enterococci from siblings and non-siblings Heliconius erato phyllis caterpillars. PeerJ, 8, e8647. https://doi.org/10.7717/peerj.8647
Jari Oksanen, F. Guillaume Blanchet, Michael Friendly, Roeland Kindt, Pierre Legendre, Dan McGlinn, Peter R. Minchin, R.B. O'Hara, Gavin L. Simpson, Peter Solymos, M. Henry H. Stevens, Eduard Szoecs and Helene Wagner (2019). vegan: Community Ecology Package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan
Jiggins, F. M., Hurst, G. D. D., Jiggins, C. D., Schulenburg, J. H. G. v d, & Majerus, M. E. N. (2000). The butterfly Danaus chrysippus is infected by a male-killing Spiroplasma bacterium. Parasitology, 120(5), 439-446. https://doi.org/10.1017/S0031182099005867
Joron, M., Jiggins, C. D., Papanicolaou, A., & McMillan, W. O. (2006). Heliconius wing patterns: An evo-devo model for understanding phenotypic diversity. Heredity, 97(3), 157-167. https://doi.org/10.1038/sj.hdy.6800873
Kapan, D. D. (1998). Divergent natural selection and müllerian mimicry in polymorphic Heliconius cydno (Lepidoptera: Nymphalidae). https://doi.org/10.14288/1.0088808
Kim, B.-R., Shin, J., Guevarra, R. B., Lee, J. H., Kim, D. W., Seol, K.-H., Lee, J.-H., & Isaacson, H. B. K. and R. E. (2017). Deciphering Diversity Indices for a Better Understanding of Microbial Communities. 27(12), 2089-2093.
Kim, J. Y., Lee, J., Shin, N.-R., Yun, J.-H., Whon, T. W., Kim, M.-S., Jung, M.-J., Roh, S. W., Hyun, D.-W., & Bae, J.-W. (2013). Orbus sasakiae sp. Nov., a bacterium isolated from the gut of the butterfly Sasakia charonda, and emended description of the genus Orbus. International Journal of Systematic and Evolutionary Microbiology, 63(Pt_5), 1766-1770. https://doi.org/10.1099/ijs.0.041871-0
Kim, M., Cha, I.-T., Lee, K.-E., Lee, E.-Y., & Park, S.-J. (2020). Genomics Reveals the Metabolic Potential and Functions in the Redistribution of Dissolved Organic Matter in Marine Environments of the Genus Thalassotalea. Microorganisms, 8(9), 1412. https://doi.org/10.3390/microorganisms8091412
Krishnan, M., Bharathiraja, C., Pandiarajan, J., Prasanna, V. A., Rajendhran, J., & Gunasekaran, P. (2014). Insect gut microbiome – An unexploited reserve for biotechnological application. Asian Pacific Journal of Tropical Biomedicine, 4, S16-S21. https://doi.org/10.12980/APJTB.4.2014C95
Kronforst, M. R., & Papa, R. (2015). The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry. Genetics, 200(1), 1-19. https://doi.org/10.1534/genetics.114.172387
Leo Lahti, Sudarshan Shetty et al. (2017). Tools for microbiome analysis in R. Version 1.10.0. URL: http://microbiome.github.com/microbiome
Luna. (2021). Variación geográfica de la microbiota en cuatro especies del género Heliconius (Lepidoptera: Nymphalidae) en Colombia. https://repository.urosario.edu.co/handle/10336/30921?show=full
Majumder, R., Sutcliffe, B., Taylor, P. W., & Chapman, T. A. (2019). Next-Generation Sequencing reveals relationship between the larval microbiome and food substrate in the polyphagous Queensland fruit fly. Scientific Reports, 9(1), 14292. https://doi.org/10.1038/s41598-019-50602-5
McMurdie and Holmes (2013) phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS ONE. 8(4): e61217.
Meyer, J. L., Castellanos-Gell, J., Aeby, G. S., Häse, C. C., Ushijima, B., & Paul, V. J. (2019). Microbial Community Shifts Associated With the Ongoing Stony Coral Tissue Loss Disease Outbreak on the Florida Reef Tract. Frontiers in Microbiology, 10. https://doi.org/10.3389/fmicb.2019.02244
Minard, G., Tikhonov, G., Ovaskainen, O., & Saastamoinen, M. (2019). The microbiome of the Melitaea cinxia butterfly shows marked variation but is only little explained by the traits of the butterfly or its host plant. Environmental Microbiology, 21(11), 4253-4269. https://doi.org/10.1111/1462-2920.14786
Morris, J., Navarro, N., Rastas, P., Rawlins, L. D., Sammy, J., Mallet, J., & Dasmahapatra, K. K. (2019). The genetic architecture of adaptation: Convergence and pleiotropy in Heliconius wing pattern evolution. Heredity, 123(2), 138-152. https://doi.org/10.1038/s41437-018-0180-0
Salunkhe, R. C., Narkhede, K. P., & Shouche, Y. S. (2014). Distribution and Evolutionary Impact of Wolbachia on Butterfly Hosts. Indian Journal of Microbiology, 54(3), 249-254. https://doi.org/10.1007/s12088-014-0448-x
Santos-Garcia, D., Mestre-Rincon, N., Zchori-Fein, E., & Morin, S. (2020). Inside out: Microbiota dynamics during host-plant adaptation of whiteflies. The ISME Journal, 14(3), 847-856. https://doi.org/10.1038/s41396-019-0576-8
Siozios, S., Moran, J., Chege, M., Hurst, G. D. D., & Paredes, J. C. (2019). Complete Reference Genome Assembly for Commensalibacter sp. Strain AMU001, an Acetic Acid Bacterium Isolated from the Gut of Honey Bees. Microbiology Resource Announcements, 8(1), e01459-18, e01459-18. https://doi.org/10.1128/MRA.01459-18
Tandon, K., Lu, C.-Y., Chiang, P.-W., Wada, N., Yang, S.-H., Chan, Y.-F., Chen, P.-Y., Chang, H.-Y., Chiou, Y.-J., Chou, M.-S., Chen, W.-M., & Tang, S.-L. (2020). Comparative genomics: Dominant coral-bacterium Endozoicomonas acroporae metabolizes dimethylsulfoniopropionate (DMSP). The ISME Journal, 14(5), 1290-1303. https://doi.org/10.1038/s41396-020-0610-x
Turner, J. R. G. (1968). Some new Heliconius pupae: Their taxonomic and evolutionary significance in relation to mimicry (Lepidoptera, Nymphalidae) *. Journal of Zoology, 155(3), 311-325. https://doi.org/10.1111/j.1469-7998.1968.tb03055.x
van Schooten, B., Godoy-Vitorino, F., McMillan, W. O., & Papa, R. (2018). Conserved microbiota among young Heliconius butterfly species. PeerJ, 6, e5502. https://doi.org/10.7717/peerj.5502
Walters, W., Hyde, E. R., Berg-Lyons, D., Ackermann, G., Humphrey, G., Parada, A., Gilbert, J. A., Jansson, J. K., Caporaso, J. G., Fuhrman, J. A., Apprill, A., & Knight, R. (2016). Improved Bacterial 16S rRNA Gene (V4 and V4-5) and Fungal Internal Transcribed Spacer Marker Gene Primers for Microbial Community Surveys. MSystems, 1(1), sys0029, e00009-15. https://doi.org/10.1128/mSystems.00009-15
Xie, J., Vilchez, I., & Mateos, M. (2010). Spiroplasma Bacteria Enhance Survival of Drosophila hydei Attacked by the Parasitic Wasp Leptopilina heterotoma. PLOS ONE, 5(8), e12149. https://doi.org/10.1371/journal.pone.0012149
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spelling Brown, Anyawill be generated::orcid::0000-0002-0436-1458600Sanchez-Herrera, Melissa35199256600Khazan, Emilyd50b2019-6f15-46f7-b46b-785d0a81d499600Salazar-Sastoque, Maria PaulaBiólogoFull timef5f167fb-0766-42c6-86f4-1a7e8e462fda6002021-06-16T20:04:59Z2021-06-16T20:04:59Z2021-05-28Las comunidades microbianas del intestino tienen funciones importantes en la reproducción, digestión y protección contra patógenos de los insectos hospedadores. Dada la importancia de estas comunidades endosimbióticas para su anfitrión, la investigación sobre la diversidad y ecología de los microbiomas está recibiendo cada vez más atención. Quería probar la importancia de las especies hospedadoras y la geografía en la configuración de la composición del microbioma. Utilizando la región V4 del gen 16S, comparé las comunidades de microbiomas de dos especies de mariposas en dos ubicaciones geográficas. Usé 14 individuos de dos especies, Heliconius cydno y Heliconius clysonymus, capturadas en reservas forestales en Manizales, Caldas y Filandia, Quindío, en la Cordillera Central de los Andes colombianos. Los índices de diversidad alfa, incluidos Shannon e Inverse Simpson, demostraron similaridades en la diversidad taxonómica entre especies y sitios, pero con cambios en la abundancia entre las especies de mariposas. El análisis de coordenadas principales (PCoA) de las comunidades microbianas de individuos mostró que la variabilidad en los microbiomas se desacoplaba de la identidad y el sitio de las especies. Proteobacteria fue el filo más abundante en todas las muestras y Commensalibacter fue el género bacteriano más común. Además, encontramos la presencia de simbiontes intracelulares Spiroplasma y Wolbachia en nuestras muestras.Gut microbial communities have important roles in reproduction, digestion, and pathogen protection of their insect hosts. Given the importance of these endosymbiotic communities to their host, research on the diversity and ecology of microbiomes is receiving increasing attention. I wanted to test the relative importance of host species and geography in shaping microbiome composition. Using the V4 region of the 16S gene, we compared microbiome communities of two species of butterflies across two geographic locations. I used 14 individuals from two species, Heliconius cydno and Heliconius clysonymus, from forest reserves in Manizales, Caldas and Filandia, Quindío, in the Central Range of the Colombian Andes. Alpha diversity indices, including Shannon and Inverse Simpson, demonstrated similar amounts of taxonomic diversity across species and sites but with changes in abundance between butterfly species. Principal Coordinate Analysis (PCoA) of the microbial communities of individuals showed that the variability in microbiomes was decoupled from species identity and site. Proteobacteria was the most abundant phylum across all samples and Commensalibacter was the most common bacterial genus. In addition, we found the presence of intracellular symbiont Spiroplasma and Wolbachia in our samples.41 pp.application/pdfhttps://doi.org/10.48713/10336_31623 https://repository.urosario.edu.co/handle/10336/31623engUniversidad del RosarioFacultad de Ciencias Naturales y MatemáticasBiologíaAtribución-NoComercial-CompartirIgual 2.5 ColombiaAbierto (Texto Completo)EL AUTOR, manifiesta que la obra objeto de la presente autorización es original y la realizó sin violar o usurpar derechos de autor de terceros, por lo tanto la obra es de exclusiva autoría y tiene la titularidad sobre la misma.http://creativecommons.org/licenses/by-nc-sa/2.5/co/http://purl.org/coar/access_right/c_abf2Baxter, S. W., Papa, R., Chamberlain, N., Humphray, S. J., Joron, M., Morrison, C., ffrench-Constant, R. H., McMillan, W. O., & Jiggins, C. D. (2008). Convergent Evolution in the Genetic Basis of Müllerian Mimicry in Heliconius Butterflies. Genetics, 180(3), 1567-1577. https://doi.org/10.1534/genetics.107.082982Chamberlain, N. L., Hill, R. I., Kapan, D. D., Gilbert, L. E., & Kronforst, M. R. (2009). Polymorphic Butterfly Reveals the Missing Link in Ecological Speciation. Science, 326(5954), 847-850. https://doi.org/10.1126/science.1179141Chandler, J. A., Lang, J. M., Bhatnagar, S., Eisen, J. A., & Kopp, A. (2011). Bacterial Communities of Diverse Drosophila Species: Ecological Context of a Host–Microbe Model System. PLOS Genetics, 7(9), e1002272. https://doi.org/10.1371/journal.pgen.1002272Crawford, J. E., Clarke, D. W., Criswell, V., Desnoyer, M., Cornel, D., Deegan, B., Gong, K., Hopkins, K. C., Howell, P., Hyde, J. S., Livni, J., Behling, C., Benza, R., Chen, W., Dobson, K. L., Eldershaw, C., Greeley, D., Han, Y., Hughes, B., … White, B. J. (2020). Efficient production of male Wolbachia -infected Aedes aegypti mosquitoes enables large-scale suppression of wild populations. Nature Biotechnology, 38(4), 482-492. https://doi.org/10.1038/s41587-020-0471-xFerguson, 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(10), 2357-2368. https://doi.org/10.1111/1365-2435.13153Fredensborg, B. L., Kálvalíð, I. F. í, Johannesen, T. B., Stensvold, C. R., Nielsen, H. V., & Kapel, C. M. O. (2020). Parasites modulate the gut-microbiome in insects: A proof-of-concept study. PLOS ONE, 15(1), e0227561. https://doi.org/10.1371/journal.pone.0227561Gilbert, L. E. (1972). Pollen Feeding and Reproductive Biology of Heliconius Butterflies. Proceedings of the National Academy of Sciences, 69(6), 1403-1407. https://doi.org/10.1073/pnas.69.6.1403Hammer, T. J., Dickerson, J. C., McMillan, W. O., & Fierer, N. (2020). Heliconius Butterflies Host Characteristic and Phylogenetically Structured Adult-Stage Microbiomes. Applied and Environmental Microbiology, 86(24), e02007-20, /aem/86/24/AEM.02007-20.atom. https://doi.org/10.1128/AEM.02007-20Hammer, T. J., McMillan, W. O., & Fierer, N. (2014). Metamorphosis of a Butterfly-Associated Bacterial Community. PLOS ONE, 9(1), e86995. https://doi.org/10.1371/journal.pone.0086995Hansen, A. K., & Moran, N. A. (2014). The impact of microbial symbionts on host plant utilization by herbivorous insects. Molecular Ecology, 23(6), 1473-1496. https://doi.org/10.1111/mec.12421Huff, R., Pereira, R. I., Pissetti, C., Araújo, A. M. de, d’Azevedo, P. A., Frazzon, J., & GuedesFrazzon, A. P. (2020). Antimicrobial resistance and genetic relationships of enterococci from siblings and non-siblings Heliconius erato phyllis caterpillars. PeerJ, 8, e8647. https://doi.org/10.7717/peerj.8647Jari Oksanen, F. 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K., Caporaso, J. G., Fuhrman, J. A., Apprill, A., & Knight, R. (2016). Improved Bacterial 16S rRNA Gene (V4 and V4-5) and Fungal Internal Transcribed Spacer Marker Gene Primers for Microbial Community Surveys. MSystems, 1(1), sys0029, e00009-15. https://doi.org/10.1128/mSystems.00009-15Xie, J., Vilchez, I., & Mateos, M. (2010). Spiroplasma Bacteria Enhance Survival of Drosophila hydei Attacked by the Parasitic Wasp Leptopilina heterotoma. 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