Male-killing Wolbachia and mitochondrial selective sweep in a migratory African insect

BMC Evolutionary Biology

Kenneth Wilson¹  Robert I Graham² 

[1] Lancaster Environment Centre, Lancaster University, Lancaster, LA1 4YQ, UK;School of Biological Sciences, Heydon-Laurence Building A08, University of Sydney, Sydney, NSW, 2006, Australia

关键词: Evolutionary genetics;    African armyworm;    Spodoptera exempta;    mtDNA;    COI;    Cytochrome Oxidase I;    Wolbachia;   

Others  :  1140165
DOI  :  10.1186/1471-2148-12-204

 received in 2012-05-15, accepted in 2012-10-09,  发布年份 2012

【 摘 要 】

Background

Numerous recent studies have shown that resident symbiotic microorganisms of insects play a fundamental role in host ecology and evolution. The lepidopteran pest, African armyworm (Spodoptera exempta), is a highly migratory and destructive species found throughout sub-Saharan Africa, that can experience eruptive outbreaks within the space of a single generation, making predicting population dynamics and pest control forecasting extremely difficult. Three strains of Wolbachia have recently been identified infecting this species in populations sampled from Tanzania. In this study, we examined the interaction between Wolbachia pipiensis infections and the co-inherited marker, mtDNA, within populations of armyworm, as a means to investigate the population biology and evolutionary history of Wolbachia and its host.

Results

A Wolbachia-infected isofemale line was established in the laboratory. Phenotypic studies confirmed the strain wExe1 as a male-killer. Partial sequencing of the mitochondrial COI gene from 164 individual field-collected armyworm of known infection status revealed 17 different haplotypes. There was a strong association between Wolbachia infection status and mtDNA haplotype, with a single dominant haplotype, haplo1 (90.2% prevalence), harbouring the endosymbiont. All three Wolbachia strains were associated with this haplotype. This indicates that Wolbachia may be driving a selective sweep on armyworm haplotype diversity. Despite very strong biological and molecular evidence that the samples represent a single species (including from nuclear 28S gene markers), the 17 haplotypes did not fall into a monophyletic clade within the Spodoptera genus; with six haplotypes (2 each from 3 geographically separate populations) differing by >11% in their nucleotide sequence to the other eleven.

Conclusions

This study suggests that three strains of Wolbachia may be driving a selective sweep on armyworm haplotype diversity, and that based on COI sequence data, S. exempta is not a monophyletic group within the Spodoptera genus. This has clear implications for the use of mtDNA as neutral genetic markers in insects, and also demonstrates the impact of Wolbachia infections on host evolutionary genetics.

【 授权许可】

   
2012 Graham and Wilson; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Engelstaedter J, Hurst GDD: The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol S 2009, 40:127-149.
• [2]Oliver KM, Degnan PH, Burke GR, Moran NA: Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 2010, 55:247-266.
• [3]Zchori-Fein E, Perlman SJ, Kelly SE, Katzir N, MS H: Characterization of a ‘Bacteroidetes’ symbiont in Encarsia wasps (Hymenoptera: Aphelinidae): proposal of ‘Candidatus Cardinium hertigii’. Int J Syst Evol Micr 2004, 54:961-968.
• [4]Zchori-Fein E, Gottlieb Y, Kelly SE, Brown JK, Wilson JM, Karr TL, Hunter MS: A newly discovered bacterium associated with parthenogenesis and a change in host selection behaviour in parasitoid wasps. P Natl Acad Sci USA 2001, 98:12555-12560.
• [5]Hunter M, Perlman S, Kelly S: A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proc R Soc Lond B 2003, 270:2185-2190.
• [6]Scarborough CL, Ferrari J, Godfray HCJ: Aphid protected from pathogen by endosymbiont. Science 2005, 310:1781.
• [7]Haine ER: Symbiont-mediated protection. Proc R Soc Lond B 2008, 275(1633):353-361.
• [8]Vorburger C, Gehrer L, Rodriguez P: A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biol Lett 2010, 6:109-111.
• [9]Jaenike J, Brekke TD: Defensive endosymbionts: a cryptic trophic level in community ecology. Ecol Lett 2011, 14:150-155.
• [10]Jaenike J: Population genetics of beneficial heritable symbionts. Trends Ecol Evol 2012, 27:226-232.
• [11]Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg M, Bouletreau M: Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. P Natl Acad Sci USA 2001, 98:6247-6252.
• [12]Fenn K, Blaxter M: Are filarial nematode Wolbachia obligate mutualist symbionts? Trends Ecol Evol 2004, 19:163-166.
• [13]Werren JH, Windsor DM: Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc R Soc Lond B 2000, 267:1277-1285.
• [14]Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH: How many species are infected with Wolbachia? - a statistical analysis of current data. FEMS Microbiol Lett 2008, 281(2):215-220.
• [15]Werren JH, Baldo L, Clark ME: Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 2008, 6(10):741-751.
• [16]Vavre F, Charlat S: Making (good) use of Wolbachia: what the models say. Curr Opin Microbiol 2012, 15:263-268.
• [17]Perrot-Minnot M, Guo LR, Werren JH: Single and double infections with Wolbachia in the parasitic wasp Nasonia vitripennis: effects on compatibility. Genetics 1996, 143:961-972.
• [18]Werren J: Biology of Wolbachia. Ann Rev Entomol. 1997, 42:587-609.
• [19]Haag-Liautard C, Coffey N, Houle D, Lynch M, Charlesworth B, Keightley P: Direct Estimation of the Mitochondrial DNA Mutation Rate in Drosophila melanogaster. PLoS Biol 2008, 6:1706-1714.
• [20]Hurst GDD, Jiggins FM: Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc R Soc Lond B 2005, 272:1525-1534.
• [21]Charlat S, Duplouy A, Hornett EA, Dyson EA, Davies N, Roderick GK, Wedell N, Hurst GDD: The joint evolutionary histories of Wolbachia and mitochondria in Hypolimnas bolina. BMC Evol Biol 2009., 9(64)
• [22]Rodriguero MS, Lanteri AA, Confalonieri VA: Mito-nuclear genetic comparison in a Wolbachia infected weevil: insights on reproductive mode, infection age and evolutionary forces shaping genetic variation. BMC Evol Biol 2010, 4:340.
• [23]Xiao JH, Wang NX, Li YW, Murphy RW, Wan DG, Niu LM, Hu HY, Fu YG, Huang DW: Molecular approaches to identify cryptic species and polymorphic species within a complex community of fig wasps. PLoS One 2010, 29(5(11)):e15067.
• [24]Thierry M, Becker N, Hajri A, Reynaud B, Lett JM, Delatte H: Symbiont diversity and non-random hybridization among indigenous (Ms) and invasive (B) biotypes of Bemisia tabaci. Mol Ecol 2011, 20:2172-2187.
• [25]Yu MZ, Zhang KJ, Xue XF, Hong XY: Effects of Wolbachia on mtDNA variation and evolution in natural populations of Tetranychus urticae Koch. Insect Mol Biol 2011, 20:311-321.
• [26]Dyer K, Jaenike J: Evolutionarily stable infection by a male-killing endosymbiont in Drosophila innubila: molecular evidence from the host and parasite genomes. Genetics 2004, 168:1443-1455.
• [27]Delgado A, Cook J: Effects of a sex-ratio distorting endosymbiont on mtDNA variation in a global insect pest. BMC Evol Biol 2009, 9:49. BioMed Central Full Text
• [28]Shoemaker DD, Keller G, Ross KG: Effects of Wolbachia on mtDNA variation in two fire ant species. Mol Ecol 2003, 12:1757-1771.
• [29]Rose DJW, Dewhurst CF, Page WW: The African Armyworm Handbook. 2nd edition. NRI, Chatham, UK; 2000.
• [30]Rose DJW, Page WW, Dewhurst CF, Riley JR, Reynolds DT, Pedgley DE, Tucker MR: Down-wind migration of the African armyworm moth, Spodoptera exempta, studied by mark-and-capture and by radar. Ecol Entomol 1985, 10:299-313.
• [31]Graham RI, Grzywacz D, Mushobozi WL, Wilson K: Wolbachia in a major African crop pest increases susceptibility to viral disease rather than protects. Ecol Lett 2012, 15:993-1000.
• [32]Dyson EA, Kamath MK, Hurst GDD: Wolbachiainfection associated with all-female broods inHypolimnas bolina(Lepidoptera: Nymphalidae): evidence for horizontal transmission of a butterfly male killer. Heredity 2002, 88:166-171.
• [33]Jiggins FM, Hurst GDD, Schulenburg JHG, Majerus MEN: Two male-killing Wolbachia strains coexist in a population of the butterfly Acraea encedon. Heredity 2001, 86:161-166.
• [34]Vavre F, Fleury F, Lepetit D, Fouillet P, Bouletreau M: Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol Biol Evol 1999, 16:1711-1723.
• [35]Baldo L, Hotopp JCD, Jolley KA, Bordenstein SR, Biber SA, Choudhury RR, Hayashi C, Maiden MCJ, Tettelin H, Werren JH: Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microbiol 2006, 72(11):7098-7110.
• [36]Haine ER, Pickup NJ, Cook JM: Horizontal transmission of Wolbachia in a Drosophila community. Ecol Entomol 2005, 30(4):464-472.
• [37]Gehrer L, Vorburger C: Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol Lett 2012, 8:613-615.
• [38]Caspi-Fluger A, Inbar M, Mozes-Daube N, Katzir N, Portney V, Belausov E, Hunter M, Zchori-Fein E: Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proc R Soc Lond B 2012, 279:1791-1796.
• [39]Unckless RL, Jaenike J: Maintenance of a male-killing Wolbachia in Drosophilla innubila by male-killing dependent and male-killing independent mechanisms. Evolution 2012, 66(3):678-689.
• [40]Weeks AR, Reynolds KT, Hoffmann AA: Wolbachia endosymbionts associated with cytoplasmic incompatibility dynamics and host effects: What has (and has not) been demonstrated? Trends Ecol Evol 2002, 17:257-262.
• [41]Haselkorn T, Markow T, Moran N: Multiple introductions of the Spiroplasma bacterial endosymbiont into Drosophila. Mol Ecol 2009, 18:1294-1305.
• [42]Simon JC, Boutin S, Tsuchida T, Koga R, Le Gallic JF, Frantz A, Outreman Y, Fukatsu T: Facultative symbiont infections affect aphid reproduction. PLoS One 2011, 6(7):e21831.
• [43]Hutchence KJ, Padé R, Swift HL, Bennet D, Hurst GDD: Phenotype and transmission efficiency of artificial and natural male-killing Spiroplasma infections in Drosophila melanogaster. J Invertebr Pathol 2012, 109:243-247.
• [44]Weeks AR, Velten R, Stouthamer R: Incidence of a new sex-ratiodistorting endosymbiotic bacterium among arthropods. Proc R Soc Lond B 2003, 270:1857-1865.
• [45]Kageyama D, Traut W: Opposite sex-specific effects of Wolbachia and interference with the sex determination of its host Ostrinia scapulalis. Proc R Soc Lond B 2004, 271:251-258.
• [46]den Boer M: Isoenzymes and migration in the African armyworm Spodoptera exempta (Lepidoptera, Noctuidae). J Zool 1978, 185:539-553.
• [47]Ibrahim KM, Yassin Y, Elguzouli A: Polymerase chain reaction primers for polymorphic microsatellite loci in the African armyworm, Spodoptera exempta (Lepidoptera: Noctuidae). Mol Ecol Notes 2004, 4:653-655.
• [48]Johnstone RA, Hurst GDD: Maternally inherited male-killing microorganisms may confound interpretation of mitochondrial DNA variability. Biol J Linn Soc 1996, 58:453-470.
• [49]Hurst GDD, Jiggins FM, Robinson SJW: What causes inefficient transmission of male-killing Wolbachia in Drosophila? Heredity 2001, 87:220-226.
• [50]Kondo N, Shimada M, Fukatsu T: Infection density of Wolbachia endosymbiont affected by co-infection and host genotype. Biol Lett 2005, 1:488-491.
• [51]Min KT, Benzer S: Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. P Natl Acad Sci USA 1997, 94:10792-10796.
• [52]Ikeda T, Ishikawa H, Sasaki T: Regulation of Wolbachia density in the Mediterranean flour moth, Ephestia kuehniella, and the almond moth, Cadra cautella. Zool Sci 2003, 20:153-157.
• [53]Mouton L, Dedeine F, Henri H, Boulétreau M, Profizi N, Vavre F: Virulence, multiple infections and regulation of symbiotic population in the Wolbachia-Asobara tabida symbiosis. Genetics 2004, 168:181-189.
• [54]Hebert P, Ratnasingham S, de Waard J: Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond B 2003, 270:S96-S99.
• [55]Meusnier I, Singer GA, Landry JF, Hickey DA, Hebert PDN, Hajibabaei M: A universal DNA mini-barcode for biodiversity analysis. BMC Genomics 2008, 12:214.
• [56]Sun XJ, Xiao JH, Cook JM, Feng G, Huang DW: Comparisons of host mitochondrial, nuclear and endosymbiont bacterial genes reveal cryptic fig wasp species and the effects of Wolbachia on host mtDNA evolution and diversity. BMC Evol Biol 2011, 11:86. BioMed Central Full Text
• [57]Funk W, Caminer M, Ron S: High levels of cryptic species diversity uncovered in Amazonian frogs. Proc R Soc Lond B 2011, 279:1806-1814.
• [58]Nagoshi RN, Meagher RL, Hay-Roe M: Inferring the annual migration patterns of fall armyworm (Lepidoptera: Noctuidae) in the United States from mitochondrial haplotypes. Ecology and Evolution 2012, 2:1458-1467.
• [59]Whitworth TL, Dawson RD, Magalon H, Baudry E: DNA barcoding cannot reliably identify species of the blowfly genus Protocalliphora (Diptera: Calliphoridae). Proc R Soc Lond B 2007, 274:1731-1739.
• [60]Gompert Z, Forister M, Fordyce J, Nice C: Widespread mito-nuclear discordance with evidence for introgressive hybridization and selective sweeps in Lycaeides. Mol Ecol 2008, 17:5231-5244.
• [61]Solignac M, Monnerot M: Race formation, speciation, and introgression within Drosophila simulans, D. mauritiana, and D. sechellia inferred from mitochondrial DNA analysis. Evolution 1986, 40:531-539.
• [62]Jiggins FM: Male-killing Wolbachia and mitochondrial DNA. Selective sweeps, hybrid introgression and parasite population dynamics. Genetics 2003, 164:5-12.
• [63]Dsouli N, Delsuc F, Michaux J, De Stordeur E, Couloux A, Veuille M, Duvallet G: Phylogenetic analyses of mitochondrial and nuclear data in haematophagous flies support the paraphyly of the genus Stomoxys (Diptera: Muscidae). Infect Genet Evol 2011, 11:663-670.
• [64]Cotter S, Wilson K: Heritability of immune function in the caterpillar Spodoptera littoralis. Heredity 2002, 88:229-234.
• [65]Zhou WG, Rousset F, O'Neill S: Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc R Soc Lond B 1998, 265(1395):509-515.
• [66]Werren JH, Guo LR, Zhang W: Evolution and phylogeny of Wolbachia: reproductive parasites of Arthropods. Proc R Soc Lond B 1995, 251:55-63.
• [67]Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R: DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 1994, 3:294-299.
• [68]Kageyama D, Nishimura G, Hoshizaki S, Ishikawa Y: FeminizingWolbachiain an insect,Ostrinia furnacalis(Lepidoptera: Crambidae). Heredity 2002, 88:444-449.
• [69]Hall T: BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 1999, 41:95-98.
• [70]Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
• [71]Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680.
• [72]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum Parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
• [73]Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
• [74]Bandelt H, Forster P, Röhl A: Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999, 16:37-48.