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

BMC Evolutionary Biology

Volumn 12, Issue 1, 2012, Pages 1-11

  Graham, Robert I ^a,b   Wilson, Kenneth ^a  

^a LANCASTER UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

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

Indexed keywords

HEXAPODA; SPODOPTERA; SPODOPTERA EXEMPTA; WOLBACHIA;

BACTERIAL PROTEIN; CYTOCHROME C OXIDASE; MITOCHONDRIAL DNA; RIBOSOME DNA; RNA 28S;

ANIMAL; ARTICLE; CELL NUCLEUS; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; FEMALE; GENETIC SELECTION; GENETICS; GEOGRAPHY; HOST PATHOGEN INTERACTION; MALE; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; POPULATION MIGRATION; SEASON; SEX DIFFERENCE; SPODOPTERA; SYMBIOSIS; TANZANIA; WOLBACHIA;

ANIMAL MIGRATION; ANIMALS; BACTERIAL PROTEINS; CELL NUCLEUS; DNA, MITOCHONDRIAL; DNA, RIBOSOMAL; ELECTRON TRANSPORT COMPLEX IV; EVOLUTION, MOLECULAR; FEMALE; GEOGRAPHY; HOST-PATHOGEN INTERACTIONS; MALE; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL, 28S; SEASONS; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA; SEX FACTORS; SPODOPTERA; SYMBIOSIS; TANZANIA; WOLBACHIA;

MLCS; MLOWN;

EID: 84991406625     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-12-204     Document Type: Article

References (74)

1. Engelstaedter J, Hurst GDD: The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol S. 2009, 40: 127-149. 10.1146/annurev.ecolsys.110308.120206.
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. 10.1146/annurev-ento-112408-085305.
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. 10.1099/ijs.0.02957-0.
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. 10.1073/pnas.221467498.
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. 10.1098/rspb.2003.2475.
6. Scarborough CL, Ferrari J, Godfray HCJ: Aphid protected from pathogen by endosymbiont. Science. 2005, 310: 1781-10.1126/science.1120180.
7. Haine ER: Symbiont-mediated protection. Proc R Soc Lond B. 2008, 275 (1633): 353-361. 10.1098/rspb.2007.1211.
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. 10.1098/rsbl.2009.0642.
9. Jaenike J, Brekke TD: Defensive endosymbionts: a cryptic trophic level in community ecology. Ecol Lett. 2011, 14: 150-155. 10.1111/j.1461-0248.2010.01564.x.
10. Jaenike J: Population genetics of beneficial heritable symbionts. Trends Ecol Evol. 2012, 27: 226-232. 10.1016/j.tree.2011.10.005.
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. 10.1073/pnas.101304298.
12. Fenn K, Blaxter M: Are filarial nematode Wolbachia obligate mutualist symbionts?. Trends Ecol Evol. 2004, 19: 163-166. 10.1016/j.tree.2004.01.002.
13. Werren JH, Windsor DM: Wolbachia infection frequencies in insects: evidence of a global equilibrium?. Proc R Soc Lond B. 2000, 267: 1277-1285. 10.1098/rspb.2000.1139.
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. 10.1111/j.1574-6968.2008.01110.x.
15. Werren JH, Baldo L, Clark ME: Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol. 2008, 6 (10): 741-751. 10.1038/nrmicro1969.
16. Vavre F, Charlat S: Making (good) use of Wolbachia: what the models say. Curr Opin Microbiol. 2012, 15: 263-268. 10.1016/j.mib.2012.03.005.
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. 10.1146/annurev.ento.42.1.587.
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. 10.1098/rspb.2005.3056.
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. 10.1111/j.1365-294X.2011.05087.x.
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. 10.1111/j.1365-2583.2010.01066.x.
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. 10.1534/genetics.104.027854.
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: 49-10.1186/1471-2148-9-49.
28. Shoemaker DD, Keller G, Ross KG: Effects of Wolbachia on mtDNA variation in two fire ant species. Mol Ecol. 2003, 12: 1757-1771. 10.1046/j.1365-294X.2003.01864.x.
29. Rose DJW, Dewhurst CF, Page WW: The African Armyworm Handbook. 2000, NRI, Chatham, UK, 2
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. 10.1111/j.1365-2311.1985.tb00727.x.
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. 10.1111/j.1461-0248.2012.01820.x.
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. 10.1038/sj.hdy.6800021.
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. 10.1093/oxfordjournals.molbev.a026084.
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. 10.1128/AEM.00731-06.
36. Haine ER, Pickup NJ, Cook JM: Horizontal transmission of Wolbachia in a Drosophila community. Ecol Entomol. 2005, 30 (4): 464-472. 10.1111/j.0307-6946.2005.00715.x.
37. Gehrer L, Vorburger C: Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol Lett. 2012, 8: 613-615. 10.1098/rsbl.2012.0144.
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. 10.1098/rspb.2011.2095.
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. 10.1111/j.1558-5646.2011.01485.x.
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. 10.1016/S0169-5347(02)02480-1.
41. Haselkorn T, Markow T, Moran N: Multiple introductions of the Spiroplasma bacterial endosymbiont into Drosophila. Mol Ecol. 2009, 18: 1294-1305. 10.1111/j.1365-294X.2009.04085.x.
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): e21831-10.1371/journal.pone.0021831.
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. 10.1016/j.jip.2011.10.003.
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. 10.1098/rspb.2003.2425.
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. 10.1098/rspb.2003.2604.
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. 10.1111/j.1471-8286.2004.00772.x.
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. 10.1111/j.1095-8312.1996.tb01446.x.
49. Hurst GDD, Jiggins FM, Robinson SJW: What causes inefficient transmission of male-killing Wolbachia in Drosophila?. Heredity. 2001, 87: 220-226. 10.1046/j.1365-2540.2001.00917.x.
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. 10.1098/rsbl.2005.0340.
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. 10.1073/pnas.94.20.10792.
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. 10.2108/zsj.20.153.
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. 10.1534/genetics.104.026716.
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. 10.1098/rsbl.2003.0025.
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: 86-10.1186/1471-2148-11-86.
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. 10.1098/ rspb.2011.1653.
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. 10.1002/ece3.268.
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. 10.1098/rspb.2007.0062.
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. 10.1111/j.1365-294X.2008.03988.x.
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. 10.2307/2408575.
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. 10.1016/j.meegid.2011.02.004.
64. Cotter S, Wilson K: Heritability of immune function in the caterpillar Spodoptera littoralis. Heredity. 2002, 88: 229-234. 10.1038/sj.hdy.6800031.
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. 10.1098/rspb.1998.0324.
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. 10.1038/sj.hdy.6800077.
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. 10.1093/nar/22.22.4673.
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. 10.1093/molbev/msr121.
73. Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009, 25: 1451-1452. 10.1093/bioinformatics/btp187.
74. Bandelt H, Forster P, Röhl A: Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999, 16: 37-48. 10.1093/oxfordjournals.molbev.a026036.