Wolbachia affects mitochondrial population structure in two systems of closely related Palaearctic blue butterflies

. 2021 Feb 04 ; 11 (1) : 3019. [epub] 20210204

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33542272
Odkazy

PubMed 33542272
PubMed Central PMC7862691
DOI 10.1038/s41598-021-82433-8
PII: 10.1038/s41598-021-82433-8
Knihovny.cz E-zdroje

The bacterium Wolbachia infects many insect species and spreads by diverse vertical and horizontal means. As co-inherited organisms, these bacteria often cause problems in mitochondrial phylogeny inference. The phylogenetic relationships of many closely related Palaearctic blue butterflies (Lepidoptera: Lycaenidae: Polyommatinae) are ambiguous. We considered the patterns of Wolbachia infection and mitochondrial diversity in two systems: Aricia agestis/Aricia artaxerxes and the Pseudophilotes baton species complex. We sampled butterflies across their distribution ranges and sequenced one butterfly mitochondrial gene and two Wolbachia genes. Both butterfly systems had uninfected and infected populations, and harboured several Wolbachia strains. Wolbachia was highly prevalent in A. artaxerxes and the host's mitochondrial structure was shallow, in contrast to A. agestis. Similar bacterial alleles infected both Aricia species from nearby sites, pointing to a possible horizontal transfer. Mitochondrial history of the P. baton species complex mirrored its Wolbachia infection and not the taxonomical division. Pseudophilotes baton and P. vicrama formed a hybrid zone in Europe. Wolbachia could obscure mitochondrial history, but knowledge on the infection helps us to understand the observed patterns. Testing for Wolbachia should be routine in mitochondrial DNA studies.

Zobrazit více v PubMed

Jiggins FM. Male-killing Wolbachia and mitochondrial DNA: Selective sweeps, hybrid introgression and parasite population dynamics. Genetics. 2003;164:5–12. PubMed PMC

Poinsot D, Charlat S, Merçot H. On the mechanism of Wolbachia-induced cytoplasmic incompatibility: Confronting the models with the facts. BioEssays. 2003;25:259–265. doi: 10.1002/bies.10234. PubMed DOI

Werren JH, Baldo L, Clark ME. Wolbachia: Master manipulators of invertebrate biology. Nat. Rev. Microbiol. 2008;6:741–751. doi: 10.1038/nrmicro1969. PubMed DOI

Vavre F, Fleury F, Lepetit D, Fouillet P, Boulétreau M. Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol. Biol. Evol. 1999;16:1711–1723. doi: 10.1093/oxfordjournals.molbev.a026084. PubMed DOI

Sintupachee S, Milne JR, Poonchaisri S, Baimai V, Kittayapong P. Closely related Wolbachia strains within the pumpkin arthropod community and the potential for horizontal transmission via the plant. Microb. Ecol. 2006;51:294–301. doi: 10.1007/s00248-006-9036-x. PubMed DOI

Li S-J, et al. Plantmediated horizontal transmission of Wolbachia between whiteflies. ISME J. 2017;11:1019–1028. doi: 10.1038/ismej.2016.164. PubMed DOI PMC

Turelli M, Hoffmann AA. Rapid spread of an inherited incompatibility factor in California Drosophila. Nature. 1991;353:440. doi: 10.1038/353440a0. PubMed DOI

Oliveira DCSG, Raychoudhury R, Lavrov DV, Werren JH. Rapidly evolving mitochondrial genome and directional selection in mitochondrial genes in the parasitic wasp Nasonia (Hymenoptera: Pteromalidae) Mol. Biol. Evol. 2008;25:2167–2180. doi: 10.1093/molbev/msn159. PubMed DOI PMC

Raychoudhury R, et al. Phylogeography of Nasonia vitripennis (Hymenoptera) indicates a mitochondrial–Wolbachia sweep in North America. Heredity. 2010;104:318–326. doi: 10.1038/hdy.2009.160. PubMed DOI

Telschow A, Gadau J, Werren JH, Kobayashi Y. Genetic incompatibilities between mitochondria and nuclear genes: Effect on gene flow and speciation. Front. Genet. 2019;10:62. doi: 10.3389/fgene.2019.00062. PubMed DOI PMC

Kodandaramaiah U, Simonsen TJ, Bromilow S, Wahlberg N, Sperling F. Deceptive single-locus taxonomy and phylogeography: Wolbachia-associated divergence in mitochondrial DNA is not reflected in morphology and nuclear markers in a butterfly species. Ecol. Evol. 2013;3:5167–5176. doi: 10.1002/ece3.886. PubMed DOI PMC

Ritter S, et al. Wolbachia infections mimic cryptic speciation in two parasitic butterfly species, Phengaris teleius and P. nausithous (Lepidoptera: Lycaenidae) PLoS ONE. 2013;8:e78107. doi: 10.1371/journal.pone.0078107. PubMed DOI PMC

Whitworth TL, Dawson RD, Magalon H, Baudry E. DNA barcoding cannot reliably identify species of the blowfly genus Protocalliphora (Diptera: Calliphoridae) Proc. R. Soc. B Biol. Sci. 2007;274:1731–1739. doi: 10.1098/rspb.2007.0062. PubMed DOI PMC

Barton N, Bengtsson BO. The barrier to genetic exchange between hybridising populations. Heredity. 1986;57:357–376. doi: 10.1038/hdy.1986.135. PubMed DOI

Vavre F, Fleury F, Varaldi J, Fouillet P, Boulétreau M. Infection polymorphism and cytoplasmic incompatibility in Hymenoptera-Wolbachia associations. Heredity. 2002;88:361–365. doi: 10.1038/sj.hdy.6800063. PubMed DOI

Jaenike J, Dyer KA, Cornish C, Minhas MS. Asymmetrical reinforcement and Wolbachia infection in Drosophila. PLoS Biol. 2006;4:e325. doi: 10.1371/journal.pbio.0040325. PubMed DOI PMC

Telschow A, Flor M, Kobayashi Y, Hammerstein P, Werren JH. Wolbachia-induced unidirectional cytoplasmic incompatibility and speciation: Mainland-island model. PLoS ONE. 2007;2:e701. doi: 10.1371/journal.pone.0000701. PubMed DOI PMC

Flor M, Hammerstein P, Telschow A. Wolbachia-induced unidirectional cytoplasmic incompatibility and the stability of infection polymorphism in parapatric host populations. J. Evol. Biol. 2007;20:696–706. doi: 10.1111/j.1420-9101.2006.01252.x. PubMed DOI

Graham RI, Wilson K. Male-killing Wolbachia and mitochondrial selective sweep in a migratory African insect. BMC Evol. Biol. 2012;12:204. doi: 10.1186/1471-2148-12-204. PubMed DOI PMC

Ahmed MZ, Breinholt JW, Kawahara AY. Evidence for common horizontal transmission of Wolbachia among butterflies and moths. BMC Evol. Biol. 2016;16:118. doi: 10.1186/s12862-016-0660-x. PubMed DOI PMC

Salunkhe RC, Narkhede KP, Shouche YS. Distribution and evolutionary impact of Wolbachia on butterfly hosts. Indian J. Microbiol. 2014;54:249. doi: 10.1007/s12088-014-0448-x. PubMed DOI PMC

Talavera G, Lukhtanov VA, Pierce NE, Vila R. Establishing criteria for higher-level classification using molecular data: The systematics of Polyommatus blue butterflies (Lepidoptera, Lycaenidae) Cladistics. 2013;29:166–192. doi: 10.1111/j.1096-0031.2012.00421.x. PubMed DOI

Espeland M, et al. A Comprehensive and dated phylogenomic analysis of butterflies. Curr. Biol. 2018;28:770–778.e5. doi: 10.1016/j.cub.2018.01.061. PubMed DOI

Dincă V, Lee KM, Vila R, Mutanen M. The conundrum of species delimitation: A genomic perspective on a mitogenetically super-variable butterfly. Proc. R. Soc. B Biol. Sci. 2019;286:20191311. doi: 10.1098/rspb.2019.1311. PubMed DOI PMC

Gaunet A, et al. Two consecutive Wolbachia-mediated mitochondrial introgressions obscure taxonomy in Palearctic swallowtail butterflies (Lepidoptera, Papilionidae) Zool. Scr. 2019;48:507–519. doi: 10.1111/zsc.12355. DOI

Dinca V, Zakharov EV, Hebert PDN, Vila R. Complete DNA barcode reference library for a country’s butterfly fauna reveals high performance for temperate Europe. Proc. R. Soc. B Biol. Sci. 2011;278:347–355. doi: 10.1098/rspb.2010.1089. PubMed DOI PMC

Ugelvig LV, Vila R, Pierce NE, Nash DR. A phylogenetic revision of the Glaucopsyche section (Lepidoptera: Lycaenidae), with special focus on the Phengaris-Maculinea clade. Mol. Phylogenet. Evol. 2011;61:237–243. doi: 10.1016/j.ympev.2011.05.016. PubMed DOI

Sañudo-Restrepo CP, Dincă V, Talavera G, Vila R. Biogeography and systematics of Aricia butterflies (Lepidoptera, Lycaenidae) Mol. Phylogenet. Evol. 2013;66:369–379. doi: 10.1016/j.ympev.2012.10.010. PubMed DOI

Todisco V, et al. Molecular phylogeny of the Palaearctic butterfly genus Pseudophilotes (Lepidoptera: Lycaenidae) with focus on the Sardinian endemic P. barbagiae. BMC Zool. 2018;3:4. doi: 10.1186/s40850-018-0032-7. DOI

Sucháčková Bartoňová A, Beneš J, Fric ZF, Konvička M. Genetic confirmation of Aricia artaxerxes (Fabricius, 1793) (Lepidoptera, Lycaenidae) in the Czech Republic, its conservation significance and biogeographic context. Nota Lepidopterol. 2019;42(2):163–176. doi: 10.3897/nl.42.38853. DOI

Kames, P. Die Aufklärung des Differenzierungsgrades und der Phylogenese der beiden Aricia-Arten agestis Den. et Schiff. und artaxerxes Fabr. (allous G.-Hb.) mit Hilfe von Eizuchten und Kreuzungsversuchen (Lep., Lycaenidae). Mitt. Entomol. Ges. Basel, N. F.26, 7–13, 29–64 (1976).

Korb S, Faltynek Fric Z, Bartonova A. On the status of Aricia cf. scythissa (Nekrutenko, 1985) (Lepidoptera: Lycaenidae) based on molecular investigations. Euroasian Entomol. J. 2015;14:237–240.

Wiemers M, Chazot N, Wheat CW, Schweiger O, Wahlberg N. A complete time-calibrated multi-gene phylogeny of the European butterflies. ZooKeys. 2020;938:97–124. doi: 10.3897/zookeys.938.50878. PubMed DOI PMC

Settele J, Steiner R, Reinhardt R, Feldmann R, Hermann G. Schmetterlinge: Die Tagfalter Deutschlands. Stuttgart: Ulmer Eugen Verlag; 2015.

Monteiro A, Pierce NE. Phylogeny of Bicyclus (Lepidoptera: Nymphalidae) inferred from COI, COII, and EF-1alpha gene sequences. Mol. Phylogenet. Evol. 2001;18:264–281. doi: 10.1006/mpev.2000.0872. PubMed DOI

Wahlberg N, Wheat CW. Genomic outposts serve the phylogenomic pioneers: Designing novel nuclear markers for genomic DNA extractions of lepidoptera. Syst. Biol. 2008;57:231–242. doi: 10.1080/10635150802033006. PubMed DOI

Braig HR, Zhou W, Dobson SL, O’Neill SL. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J. Bacteriol. 1998;180:2373–2378. doi: 10.1128/JB.180.9.2373-2378.1998. PubMed DOI PMC

Sahoo RK, et al. Evolution of Hypolimnas butterflies (Nymphalidae): Out-of-Africa origin and Wolbachia-mediated introgression. Mol. Phylogenet. Evol. 2018;123:50–58. doi: 10.1016/j.ympev.2018.02.001. PubMed DOI

Baldo L, et al. Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl. Environ. Microbiol. 2006;72:7098–7110. doi: 10.1128/AEM.00731-06. PubMed DOI PMC

Kearse M. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. doi: 10.1093/bioinformatics/bts199. PubMed DOI PMC

Kajtoch Ł, et al. Using host species traits to understand the Wolbachia infection distribution across terrestrial beetles. Sci. Rep. 2019;9:847. doi: 10.1038/s41598-018-38155-5. PubMed DOI PMC

Ratnasingham, S. & Hebert, P. D. N. bold: The Barcode of Life Data System (http://www.barcodinglife.org). Mol. Ecol. Notes7, 355–364 (2007). PubMed PMC

Clement M, Posada D, Crandall KA. TCS: A computer program to estimate gene genealogies. Mol. Ecol. 2000;9:1657–1659. doi: 10.1046/j.1365-294x.2000.01020.x. PubMed DOI

Leigh JW, Bryant D. POPART: Full-feature software for haplotype network construction. Methods Ecol. Evol. 2015;6:1110–1116. doi: 10.1111/2041-210X.12410. DOI

Cheng L, Connor TR, Sirén J, Aanensen DM, Corander J. Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Mol. Biol. Evol. 2013;30:1224–1228. doi: 10.1093/molbev/mst028. PubMed DOI PMC

Tonkin-Hill, G., Lees, J. A., Bentley, S. D., Frost, S. D. W. & Corander, J. RhierBAPS: An R implementation of the population clustering algorithm hierBAPS. Wellcome Open Res.3 (2018). PubMed PMC

R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/ (2019).

Librado P, Rozas J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–1452. doi: 10.1093/bioinformatics/btp187. PubMed DOI

Dellicour S, Mardulyn P. SPADS 1.0: A toolbox to perform spatial analyses on DNA sequence data sets. Mol. Ecol. Resour. 2014;14:647–651. doi: 10.1111/1755-0998.12200. PubMed DOI

Watson DF, Philip GM. A Refinement of inverse distance weighted interpolation. Geoprocessing. 1985;2:315–327.

Manni F, Guérard E, Heyer E. Geographic patterns of (genetic, morphologic, linguistic) variation: How barriers can be detected by using Monmonier’s algorithm. Hum. Biol. 2004;76:173–190. doi: 10.1353/hub.2004.0034. PubMed DOI

Suchard MA, et al. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 2018;4:016. doi: 10.1093/ve/vey016. PubMed DOI PMC

Posada D. jModelTest: Phylogenetic model averaging. Mol. Biol. Evol. 2008;25:1253–1256. doi: 10.1093/molbev/msn083. PubMed DOI

Rambaut, A., Suchard, M. A., Xie, D. & Drummond, A. J. Tracer v1.6.http://tree.bio.ed.ac.uk/software/tracer/. (2014).

Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–1574. doi: 10.1093/bioinformatics/btg180. PubMed DOI

Miller, M. A., Pfeiffer, W. & Schwartz, T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. in 2010 Gateway Computing Environments Workshop (GCE) 1–8 (2010).

Aagaard K, et al. Phylogenetic relationships in brown argus butterflies (Lepidoptera: Lycaenidae: Aricia) from northwestern Europe. Biol. J. Linn. Soc. 2002;75:27–37. doi: 10.1046/j.1095-8312.2002.00004.x. DOI

Hernández-Roldán JL, et al. Integrative analyses unveil speciation linked to host plant shift in Spialia butterflies. Mol. Ecol. 2016;25:4267–4284. doi: 10.1111/mec.13756. PubMed DOI

Jiang W, et al. Wolbachia infection status and genetic structure in natural populations of Polytremis nascens (Lepidoptera: Hesperiidae) Infect. Genet. Evol. 2014;27:202–211. doi: 10.1016/j.meegid.2014.07.026. PubMed DOI

Mallet J, Wynne IR, Thomas CD. Hybridisation and climate change: Brown argus butterflies in Britain (Polyommatus subgenus Aricia) Insect Conserv. Divers. 2011;4:192–199. doi: 10.1111/j.1752-4598.2010.00122.x. DOI

Gutzwiller F, Dedeine F, Kaiser W, Giron D, Lopez-Vaamonde C. Correlation between the green-island phenotype and Wolbachia infections during the evolutionary diversification of Gracillariidae leaf-mining moths. Ecol. Evol. 2015;5:4049–4062. doi: 10.1002/ece3.1580. PubMed DOI PMC

Mascarenhas RO, Prezotto LF, Perondini ALP, Marino CL, Selivon D. Wolbachia in guilds of Anastrepha fruit flies (Tephritidae) and parasitoid wasps (Braconidae) Genet. Mol. Biol. 2016;39:600–610. doi: 10.1590/1678-4685-gmb-2016-0075. PubMed DOI PMC

Sucháčková Bartoňová A, et al. Recently lost connectivity in the Western Palaearctic steppes: The case of a scarce specialist butterfly. Conserv. Genet. 2020;21:561–575. doi: 10.1007/s10592-020-01271-9. DOI

Schmitt T, Varga Z. Extra-Mediterranean refugia: The rule and not the exception? Front. Zool. 2012;9:1–12. doi: 10.1186/1742-9994-9-22. PubMed DOI PMC

de Lattin G. Grundriss der Zoogeographie. Jena: VEB Gustav Fischer Verlag; 1967.

Hewitt GM. Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. 1996;58:247–276. doi: 10.1006/bijl.1996.0035. DOI

Schmitt T. Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Front. Zool. 2007;4:11. doi: 10.1186/1742-9994-4-11. PubMed DOI PMC

Hampe A, Petit RJ. Conserving biodiversity under climate change: The rear edge matters. Ecol. Lett. 2005;8:461–467. doi: 10.1111/j.1461-0248.2005.00739.x. PubMed DOI

Heiser M, Dapporto L, Schmitt T. Coupling impoverishment analysis and partitioning of beta diversity allows a comprehensive description of Odonata biogeography in the Western Mediterranean. Org. Divers. Evol. 2014;14:203–214. doi: 10.1007/s13127-013-0161-3. DOI

Vodă R, et al. Historical and contemporary factors generate unique butterfly communities on islands. Sci. Rep. 2016;6:28828. doi: 10.1038/srep28828. PubMed DOI PMC

Scalercio S, et al. How long is 3 km for a butterfly? Ecological constraints and functional traits explain high mitochondrial genetic diversity between Sicily and the Italian Peninsula. J. Anim. Ecol. 2020;89:2013–2026. doi: 10.1111/1365-2656.13196. PubMed DOI

Descimon, H. & Mallet, J. Bad species. in Ecology and Evolution of European Butterflies (Oxford University Press, Oxford, 2009).

Habel JC, Schmitt T, Müller P. The fourth paradigm pattern of post-glacial range expansion of European terrestrial species: The phylogeography of the Marbled White butterfly (Satyrinae, Lepidoptera) J. Biogeogr. 2005;32:1489–1497. doi: 10.1111/j.1365-2699.2005.01273.x. DOI

Varga Z. Das Prinzip der areal-analytischen Methode in der Zoogeographie und die Faunenelement-Einteilung der europäischen Tagschmetterlinge (Lepidoptera: Diurna) Acta Biol. Debrecina. 1977;14:223–285.

Schmitt T, Zimmermann M. To hybridize or not to hybridize: What separates two genetic lineages of the Chalk-hill Blue Polyommatus coridon (Lycaenidae, Lepidoptera) along their secondary contact zone throughout eastern Central Europe? J. Zool. Syst. Evol. Res. 2012;50:106–115. doi: 10.1111/j.1439-0469.2011.00644.x. DOI

Janoušek V, et al. Genome-wide architecture of reproductive isolation in a naturally occurring hybrid zone between Musmusculus musculus and M. m. domesticus. Mol. Ecol. 2012;21:3032–3047. doi: 10.1111/j.1365-294X.2012.05583.x. PubMed DOI PMC

Nürnberger B, Lohse K, Fijarczyk A, Szymura JM, Blaxter ML. Para-allopatry in hybridizing fire-bellied toads (Bombinabombina and B. variegata): Inference from transcriptome-wide coalescence analyses. Evolution. 2016;70:1803–1818. doi: 10.1111/evo.12978. PubMed DOI PMC

Vitali F, Schmitt T. Ecological patterns strongly impact the biogeography of western Palaearctic longhorn beetles (Coleoptera: Cerambycoidea) Org. Divers. Evol. 2017;17:163–180. doi: 10.1007/s13127-016-0290-6. DOI

Narita S, Nomura M, Kato Y, Fukatsu T. Genetic structure of sibling butterfly species affected by Wolbachia infection sweep: Evolutionary and biogeographical implications. Mol. Ecol. 2006;15:1095–1108. doi: 10.1111/j.1365-294X.2006.02857.x. PubMed DOI

Kageyama S, et al. Feminizing Wolbachia endosymbiont disrupts maternal sex chromosome inheritance in a butterfly species. Evol. Lett. 2017;1:232–244. doi: 10.1002/evl3.28. PubMed DOI PMC

Nosil P, Harmon LJ, Seehausen O. Ecological explanations for (incomplete) speciation. Trends Ecol. Evol. (Amst.) 2009;24:145–156. doi: 10.1016/j.tree.2008.10.011. PubMed DOI

Talavera G, Lukhtanov VA, Rieppel L, Pierce NE, Vila R. In the shadow of phylogenetic uncertainty: The recent diversification of Lysandra butterflies through chromosomal change. Mol. Phylogenet. Evol. 2013;69:469–478. doi: 10.1016/j.ympev.2013.08.004. PubMed DOI

Kühne G, Kosuch J, Hochkirch A, Schmitt T. Extra-Mediterranean glacial refugia in a Mediterranean faunal element: The phylogeography of the chalk-hill blue Polyommatus coridon (Lepidoptera, Lycaenidae) Sci. Rep. 2017;7:srep43533. doi: 10.1038/srep43533. DOI

Wiemers M, Keller A, Wolf M. ITS2 secondary structure improves phylogeny estimation in a radiation of blue butterflies of the subgenus Agrodiaetus (Lepidoptera: Lycaenidae: Polyommatus) BMC Evol. Biol. 2009;9:300. doi: 10.1186/1471-2148-9-300. PubMed DOI PMC

Duron O, Hurst GD. Arthropods and inherited bacteria: From counting the symbionts to understanding how symbionts count. BMC Biol. 2013;11:45. doi: 10.1186/1741-7007-11-45. PubMed DOI PMC

Bailly-Bechet M, et al. How long does Wolbachia remain on board? Mol. Biol. Evol. 2017;34:1183–1193. doi: 10.1093/molbev/msx073. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...