Ertan Mahir KORKMAZ, Fariba MEHRKHOU, Nurper GÜZ, Naciye Sena ÇAĞATAY

Analysis of genetic variation in an important pest, Tuta absoluta, and its microbiota with a new bacterial endosymbiont

Tomato leaf miner is an aggressive and invasive pest that causes serious damage in tomato production, resulting in up to 100% yield losses during serious outbreaks. The management of tomato leaf miner with synthetic pesticides is difficult due to its leaf mining habit, short life span, high reproductive rates, and insecticide resistance problem. In this study, sequences of the mitochondrial cytochrome oxidase I (mtCOI) gene of Tuta absoluta specimens were analyzed and compared with the available COI sequence data members from GenBank. All the specimens of tomato leaf miner were clustered together in a single group with a high support value, suggesting the presence of a homogeneity in the T. absoluta specimens. Furthermore, 164 samples were analyzed in order to detect the prevalence of Arsenophonus, Cardinium, Hamiltonella, Pantoea, Spiroplasma,and Wolbachia infection in T. absoluta populations. PCR analysis revealed 100% prevalence of Wolbachia and Pantoea; however, no other symbiotic bacterial infections were observed in T. absoluta populations. Finally, Wolbachia wsp, Pantoea 16S ribosomal RNA genes, and mtDNA COI haplotypes were analyzed in order to estimate the mitochondrial effects of these endosymbionts on the population structure of tomato leaf miner. The findings of high genetic homogeneity among T. absoluta populations with high prevalence of Wolbachia and Pantoea infections seem to imply that both bacterial infections have less impact on the mtDNA variations.

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Ahmed MZ, Breinholt JW, Kawahara AY (2016). Evidence for common horizontal transmission of Wolbachia among butterflies and moths. BMC Evolutionary Biology 16 (1): 118. doi: 10.1186/s12862-016-0660-x
Baldo L, Hotopp JCD, Jolley KA, Bordenstein SR, Biber SA et al. (2006). Multilocus sequence typing system for the endosymbiont Wolbachiapipientis. Applied and Environmental Microbiology 72 (11): 7098-7110. doi: 10.1128/AEM.00731-06
Ballad JWO, Hatzidakis J, Karr TL, Kreitman M (1996). Reduced variation in Drosophila simulans mitochondrial DNA. Genetics 144 (4): 1519-1528.
Barati R, Hejazi MJ, Mohammadi SA (2018). Insecticide susceptibility in Tuta absoluta (Lepidoptera: Gelechiidae) and metabolic characterization of resistance to diazinon. Journal of Economic Entomology 111 (4): 1551-1557. doi: 10.1093/jee/toy134
Bennett GM, Moran NA (2015). Heritable symbiosis: the advantages and perils of an evolutionary rabbit hole. Proceedings of the National Academy of Sciences 112 (33): 10169-10176.doi: 10.1073/pnas.1421388112
Bettaibi A, Mezghani-Khemakhem M, Soltani Z, Makni H, Makni M (2016). Development of polymorphic microsatellite loci for the tomato leaf miner, Tuta absoluta (Lepidoptera: Gelechiidae) Journal of Genetics 93 (2): 110-112.
Bozorov TA, Rasulov BA, Zhang D (2019). Characterization of the gut microbiota of invasive Agrilus mali Matsumara (Coleoptera: Buprestidae) using high-throughput sequencing: uncovering plant cell-wall degrading bacteria. Scientific Reports 9 (1): 1-12. doi:10.1038/s41598-019-41368-x
Braig HR, Zhou W, Dobson SL, O’Neill SL (1998). Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. Journal of Bacteriology 180: 2373-2378. doi: 10.1128/JB.180.9.2373- 2378.1998
Broderick NA, Raffa KF, Goodman RM, Handelsman J (2004). Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Applied and Environmental Microbiology 70 (1): 293-300. doi: 10.1128/AEM.70.1.293-300.2004
Carvalho GAS, Corrêa A, De Oliveria LO, Chediak M, Siqueira HÁ et al. (2018). Wolbachia strains, and lack of genetic diversity and parthenogenesis in Brazilian populations of Tuta absoluta (Lepidoptera: Gelechiidae). Journal of Applied Entomology 142 (9): 905-910. doi: 10.1111/jen.12531
Charlat S, Duplouy A, Hornett EA, Dyson EA, Davies N et al. (2009). The joint evolutionary histories of Wolbachia and mitochondria in Hypolimnas bolina. BMC Evolutionary Biology 9 (1): 64. doi: 10.1186/1471-2148-9-64
Chen J, Chia N, Kalari KR, Yao JZ, Novotna M et al. (2016). Multiple sclerosis patients have a distinct gut microbiota compared to healthy controls. Scientific Reports 6 (1): 1-10. doi:10.1038/ srep28484
Chiel E, Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Katzir N et al. (2007). Biotype-dependent secondary symbiont communities in sympatric populations of Bemisia tabaci. Bulletin of Entomological Research 97: 407-413. doi: 10.1017/ S0007485307005159
Choi, JY, Bubnell JE, Aquadro CF (2015). Population genomics of infectious and integrated Wolbachia pipientis genomes in Drosophila ananassae. Genome Biology and Evolution7 (8): 2362-2382. doi: 10.1093/gbe/evv158
Cifuentes D, Chynoweth R, Bielza P (2011). Genetic study of Mediterranean and South American populations of tomato leafminer Tuta absoluta (Povolny, 1994) (Lepidoptera: Gelechiidae) using ribosomal and mitochondrial markers. Pest Management Science 67 (9): 1155-1162. doi: 10.1002/ps.2166
Caparros‐Megido R, Haubruge E, Verheggen FJ (2012). First evidence of deuterotokous parthenogenesis in the tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae. Journal of Pest Science 85: 409-412. doi: 10.1007/s10340-012- 0458-6
Chevasco V, Elzinga JA, Viinikainen SM, Mappes J, Galarza JA (2012). Unexpected genetic variability in the parthenogenetic bag worm moth Dahlica fennicella (Lepidoptera: Psychidae) revealed by novel microsatellite markers.Conservation Genetics Resources 4 (1): 159-162. doi: 10.1007/s12686-011- 9498-0
Doyle JJJL, Doyle JL (1987). Genomic plant DNA preparation from fresh tissue-CTAB method. Phytochemical Bulletin19 (11): 11- 15.
Duman M, Guz N, Sertkaya E (2015) DNA barcoding of sunn pest adult parasitoids using cytochrome c oxidase subunit I (COI) Biochemical Systematics and Ecology 59: 70-77. doi: 10.1016/j. bse.2015.01.003
Đurić Z, Delić D, Hrnčić S, Radonjić S (2014). Distribution and molecular identification of Tuta absoluta (Meyrick, 1917) (Lepidoptera, Gelechiidae) populations in Bosnia and Herzegovina and Montenegro. Polish Journal of Entomology 83 (2): 121-129. doi: 10.2478/pjen-2014-0009
Duplouy A, Hornett EA (2018). Uncovering the hidden players in Lepidoptera biology: the heritable microbial endosymbionts. PeerJ 6: e4629.
EPPO (2005). Data sheets on quarantine pests: Tuta absoluta. In: EPPO Bulletin. Paris, France: EPPO.
Feldhaar H (2011). Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecological Entomology 36 (5): 533-543. doi: 10.1111/j.1365-2311.2011.01318.x
Flores LV, Gilardon E, Gardenal CN (2003). Genetic structure of populations of Tuta absoluta Meyrick (Lepidoptera: Gelechiidae). Journal of Basic and Applied Genetics 15 (2): 47-54.
Fujii Y, Kageyama D, Hoshizaki S, Ishikawa H, Sasaki T (2001). Transfection of Wolbachia in Lepidoptera: the feminizer of the adzuki bean borer Ostrinia scapulalis causes male killing in the Mediterranean flour moth Ephestia kuehniella. Biological Sciences Proceedings of the Royal Society of London 268 (1469): 855-859. doi: 10.1098/rspb.2001.1593
Graham RI, Wilson K (2012). Male-killing Wolbachia and mitochondrial selective sweep in a migratory African insect. BMC Evolutionary Biology 12 (1): 204. doi: 10.1186/1471- 2148-12-204
Glowska E, Dragun-Damian A, Dabert M, Gerth M (2015). New Wolbachia supergroups detected in quill mites (Acari: Syringophilidae). Infection, Genetics and Evolution 30: 140- 146. doi: 10.1016/j.meegid.2014.12.019
Guedes RNC, Roditakis E, Campos MR, Haddi K, Bielza P et al. (2019). Insecticide resistance in the tomato pinworm Tuta absoluta: patterns, spread, mechanisms, management and outlook. Journal of Pesticide Science 92: 1329-1342. doi: 10.1007/s10340-019-01086-9
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W et al. (2010). New algorithms and methods to estimate MaximumLikelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59 (3): 307-321. doi: 10.1093/sysbio/ syq010
Gurung K, Wertheim B, Falcao Salles J (2019). The microbiome of pest insects: it is not just bacteria. Entomologia Experimentalis et Applicata 167 (3): 156-170. doi: 10.1111/eea.12768
Guz, N, Kocak, E, Kilincer, N (2013). Molecular phylogeny of Trissolcus species (Hymenoptera: Scelionidae). Biochemical Systematics and Ecology 48: 85-91. doi: 10.1016/j. bse.2012.12.010
Guz N, Arshad M, Cagatay NS, Dageri A, Ullah MI (2020a). Detection of Wolbachia (Rickettsiales: Anaplasmataceae) and Candidatus Liberibacter asiaticus (Rhizobiales: Rhizobiaceae) associated with Diaphorina citri (Hemiptera: Liviidae)c from Citrus reticulata (Sapindales: Rutaceae) and alternate host, Cordia myxa (Boraginales: Boraginaceae). Journal of Economic Entomology. doi: 10.1007/s00284-020-01969-6
Guz N, Arshad M, Cagatay NS, Dageri A (2020b). High prevalence of Pantoea in Diaphorina citri (Hemiptera: Liviidae): vector of citrus huanglongbing disease. Current Microbiology. doi: 10.1007/s00284-020-01969-6
Guillemaud T, Blin A, Le Goff I, Desneux N, Reyes M et al. (2015). The tomato borer, Tuta absoluta, invading the Mediterranean Basin, originates from a single introduction from Central Chile. Scientific Reports 5: 8371. doi: 10.1038/srep08371
Hagenblad J, Hülskötter J, Acharya KP, Brunet J, Chabrerie O et al. (2015). Low genetic diversity despite multiple introductions of the invasive plant species Impatiens glandulifera in Europe. BMC Genetics 16 (1): 103. doi: 10.1186/s12863-015-0242-8
Hammer TJ, McMillan WO, Fierer N (2014). Metamorphosis of a butterfly-associated bacterial community. PLoS One 9 (1). doi: 10.1371/journal.pone.0086995
Hassan MN, Alzaidi S (2009). Tuta absoluta-A serious pest advancing in the Mediterranean region. Roll of pheromones in management strategies. International Pest Control 51 (2): 85-87.
Hawley DM, Hanley D, Dhondt AA, Lovette IJ (2006). Molecular evidence for a founder effect in invasive house finch (Carpodacus mexicanus) populations experiencing an emergent disease epidemic. Molecular Ecology 15: 263-275. doi: 10.1111/j.1365-294X.2005.02767.x
He C, Nan X, Zhang Z, Li M (2013).Composition and diversity analysis of the gut bacterial community of the Oriental armyworm, Mythimna separata, determined by cultureindependent and culture-dependent techniques. Journal of Insect Science 13 (1): 165. doi: 10.1673/031.013.16501
Hebert PD, Ratnasingham S, De Waard JR (2003). Barcoding animal life: cytochrome coxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London Series B 270: S96-S99. doi: 10.1098/rsbl.2003.0025
Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werrenn JH (2008). How many species are infected with Wolbachia?: a statistical analysis of current data. FEMS microbiology letters 281 (2): 215-220. doi: 10.1111/j.1574- 6968.2008.01110.x
Hiroki M, Kato Y, Kamito T, Miura K (2002).Feminization of genetic males by a symbiotic bacterium in a butterfly, Eurema hecabe (Lepidoptera: Pieridae). Naturwissenschaften 89 (4): 167-170. doi: 10.1007/s00114-002-0303-5
Hornett EA, Duplouy AM, Davies N, Roderick GK, Wedell N et al. (2008). You can’t keep a good parasite down: evolution of a male‐killer suppressor uncovers cytoplasmic incompatibility. Evolution: International Journal of Organic Evolution 62 (5): 1258-1263.
Hurst GD, Jiggins FM (2005) Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proceedings of the Royal Society B: Biological Sciences 272 (1572): 1525-1534. doi: 10.1098/rspb.2005.3056
Ilinsky Y, Kosterin OE (2017). Molecular diversity of Wolbachia in Lepidoptera: prevalent allelic content and high recombination of MLST genes. Molecular Phylogenetics and Evolution 109: 164-179. doi: 10.1016/j.ympev.2016.12.034
Jiggins FM, Hurst GD, Schulenburg JHG, Majerus ME (2001). Two male-killing Wolbachia strains coexist within a population of the butterfly Acraea encedon. Heredity 86 (2): 161-166. doi: 10.1046/j.1365-2540.2001.00804.x
Kageyama D, Ohno S, Hoshizaki S, Ishikawa Y (2003). Sexual mosaics induced by tetracycline treatment in the Wolbachiainfected adzuki bean borer, Ostrinia scapulalis. Genome 46: 983-989. doi: 10.1139/G07-041
Kageyama D, Traut W (2004). Opposite sex-specific effects of Wolbachia and interference with the sex determination of its host Ostrinia scapulalis. Proceedings of the Royal Society B: Biological Sciences 271: 251-258. doi: 10.1098/rspb.2003.2604
Kanle Satishchandra N, Chakravarthy AK, Özgökçe MS, Atlihan R (2019). Population growth potential of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on tomato, potato, and eggplant. Journal of Applied Entomology 143 (5): 518-526. doi: 10.1111/ jen.12622
Karaağaç SU (2015). Enzyme activities and analysis of susceptibility levels in Turkish Tuta absoluta populations to chlorantraniliprole and metaflumizone insecticides. Phytoparasitica 43 (5): 693- 700. doi:10.1007/s12600-015-0476-z
Keeling MJ, Jiggins FM, Read JM (2003). The invasion and coexistence of competing Wolbachia strains. Heredity 91 (4): 382-388.
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28 (12): 1647-1649. doi: 10.1093/ bioinformatics/bts199
Kenyon LJ, Meulia T, Sabree ZL (2015).Habitat visualization and genomic analysis of “Candidatus Pantoea carbekii,” the primary symbiont of the brown marmorated stink bug. Genome Biology and Evolution 7 (2): 620-635. doi: 10.1093/gbe/evv006
Kinyanjui G, Khamis FM, Ombura FLO, Kenya EU, Ekesi S et al. (2019). Infestation levels and molecular identification based on mitochondrial COI Barcode region of five invasive gelechiidae pest species in Kenya. Journal of Economic Entomology 112 (2): 872-882. doi: 10.1093/jee/toy357
Kontsedalov S, Zchori-Fein E, Chiel E, Gottlieb Y, Inbar M et al. (2008). The presence of Rickettsia is associated with increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides. Pest Management Science 64: 789-792. doi: 10.1002/ps.1595
Korkmaz EM, Budak M, Başıbüyük HH (2011).Utilization of cytochrome oxidase I in Cephus pygmeus (L.) (Hymenoptera: Cephidae). Turkish Journal of Biology 35: 713-726. doi: 10.3906/biy-1003-65
Krenn HW (2010). Feeding mechanisms of adult Lepidoptera: structure, function, and evolution of the mouthparts. Annual Review of Entomology 55: 307-327. doi: 10.1146/annurevento-112408-085338
Krishnamurthy PK, Francis RA (2012). A critical review on the utility of DNA barcoding in biodiversity conservation. Biodiversity and Conservation 21 (8): 1901-1919. doi: 10.1007/s10531-012- 0306-2
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35 (6): 1547-1549. doi: 10.1093/molbev/msy096
Librado P, Rozas J (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451- 1452. doi: 10.1093/bioinformatics/btp187
Lindholm AK, Breden F, Alexander HJ, Chan WK, Thakurta SG et al. (2005).Invasion success and genetic diversity of introduced populations of guppies Poecilia reticulata in Australia. Molecular Ecology 14: 3671-3682. doi: 10.1111/j.1365- 294X.2005.02697.x
Lietti MM, Botto E, Alzogaray RA (2005). Insecticide resistance in argentine populations of Tuta absoluta (Meyrick)(Lepidoptera: Gelechiidae). Neotropical Entomology 34 (1): 113-119. doi:10.1590/S1519-566X2005000100016
Lauzon CR, McCombs SD, Potter SE, Peabody NC (2009). Establishment and vertical passage of Enterobacter (Pantoea) agglomerans and Klebsiella pneumoniae through all life stages of the Mediterranean fruit fly (Diptera: Tephritidae). Annals of the Entomological Society of America102: 85-95. doi: 10.1603/008.102.0109
MacCollom GB, Lauzon CR, Sjogren RE, Meyer WL, Olday F (2009). Association and attraction of blueberry maggot fly Curran (Diptera: Tephritidae) to Pantoea (Enterobacter) agglomerans. Environmental Entomology 38 (1): 116-120. doi: 10.1603/022.038.0114
Mansour R, Brévault T, Chailleux A, Cherif A, Grissa-Lebdi K et al. (2018). Occurrence, biology, natural enemies and management of Tuta absoluta in Africa. Entomologia Generalis 38 (2): 83- 112. doi: 10.1127/entomologia/2018/0749
Moran NA, McCutcheon JP, Nakabachi A (2008).Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics 42: 165-190. doi: 10.1146/annurev. genet.41.110306.130119
Meyer CP (2003). Molecular systematics of cowries (Gastropoda: Cypraeidae) and diversification patterns in the tropics. Biological Journal of the Linnean Society 79 (3): 401-459. doi: 10.1046/j.1095-8312.2003.00197.x
Peakall ROD, Smouse PE (2006). GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6 (1): 288-295. doi: 10.1111/j.1471- 8286.2005.01155.x
Peakall R, Smouse PE (2012). GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 6 (1): 288-295.
Pereyra PC, Sánchez NE (2006). Effect of two solanaceous plants on developmental and population parameters of the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotropical Entomology 35 (5): 671-676. doi: 10.1590/S1519- 566X2006000500016
Pinto-Tomás AA, Sittenfeld A, Uribe-Lorío L, Chavarría F, Mora et al. (2011). Comparison of midgut bacterial diversity in tropical caterpillars (Lepidoptera: Saturniidae) fed on different diets. Environmental Entomology 40 (5): 1111-1122. doi: 10.1603/ EN11083
Richardson MF, Weinert LA, Welch JJ, Linheiro RS, Magwire MM et al. (2012). Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster. PLoS Genetics 8 (12). doi: 10.1371/journal.pgen.1003129
Robinson CJ, Schloss P, Ramos Y, Raffa K, Handelsman J (2010). Robustness of the bacterial community in the cabbage white butterfly larval midgut. Microbial Ecology 59 (2): 199-211. doi: 10.1007/s00248-009-9595-8
Russell JA, Funaro CF, Giraldo YM, Goldman-Huertas B, Suh D et al. (2012). A veritable menagerie of heritable bacteria from ants, butterflies, and beyond: broad molecular surveys and a systematic review. PLoS One 7 (12): e51027. doi: 10.1371/ journal.pone.0051027
Saccone C, Gissi C, Lanave C, Larizza A, Pesole G et al. (2000). Evolution of the mitochondrial genetic system: an overview. Gene 261 (1): 153-159. doi: 10.1016/S0378-1119(00)00484-4
Saidov N, Srinivasan R, Mavlyanova R, Qurbonov Z (2018). First report of invasive South American tomato leaf miner Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in Tajikistan. Florida Entomologist 101 (1): 147-149. doi: 10.1653/024.101.0129
Salunke BK, Salunkhe RC, Dhotre DP, Walujkar SA, Khandagale AB et al. (2012). Determination of Wolbachia diversity in butterflies from Western Ghats, India, by a multigene approach. Applied and Environmental Microbiology 78 (12): 4458-4467. doi: 10.1128/AEM.07298-11
Sasaki T, Kubo T, Ishikawa H (2002). Interspecific transfer of Wolbachia between two lepidopteran insects expressing cytoplasmic incompatibility: a Wolbachia variant naturally infecting Cadra cautella causes male killing in Ephestia kuehniella. Genetics 162 (3): 1313-1319.
Schuler H, Köppler K, Daxböck‐Horvath S, Rasool B, Krumböck S et al. (2016). The hitchhiker’s guide to Europe: the infection dynamics of an ongoing Wolbachiainvasion and mitochondrial selective sweep in Rhagoletis cerasi. Molecular Ecology 25 (7): 1595-1609. doi: 10.1111/mec.13571
Schuler H, Egan SP, Hood GR, Busbee RW, Driscoe AL et al. (2018). Diversity and distribution of Wolbachia in relation to geography, host plant affiliation and life cycle of a heterogonic gall wasp. BMC Evolutionary Biology 18 (1): 37. doi: 10.1186/ s12862-018-1151-z
Sevim A, Sevim E, Demirci M, Sandallı C (2016). The internal bacterial diversity of stored product pests. Annals of Microbiology 66 (2): 749-764. doi: 10.1007/s13213-015-1155-5
Shashank PR, Twinkle S, Chandrashekar K, Meshram NM, Suroshe SS et al. (2018). Genetic homogeneity in South American tomato pinworm, Tuta absoluta: a new invasive pest to oriental region. 3Biotech 8 (8): 350. doi: 10.1007/s13205-018-1374-0
Solignac M, Vautrin D, Rousset F (1994). Widespread occurrence of the proteobacteria Wolbachia and partial cytoplasmic incompatibility in Drosophila melanogaster. Comptes rendus de l’Académie des sciences. Série 3, Sciences de la vie 317: 461- 470.
Siqueira HÁA, Guedes RNC, Picanço MC (2000). Insecticide resistance in populations of Tuta absoluta (Lepidoptera: Gelechiidae). Agricultural and Forest Entomology 2 (2): 147- 153. doi: 10.1046/j.1461-9563.2000.00062.x
Staudacher H, Kaltenpoth M, Breeuwer JA, Menken SB, Heckel DG et al. (2016). Variability of bacterial communities in the moth Heliothis virescens indicates transient association with the host. PLoS One 11 (5). doi: 10.1371/journal.pone.0154514
Stouthamer R, Breeuwer JA, Hurst GD (1999).Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annual Review of Microbiology 53 (1): 71-102. doi: 10.1146/annurev. micro.53.1.71
Škaljac M, Kostanjšek R, Žanić K (2012). The presence of Wolbachia in Tuta absoluta (Lepidoptera: Gelechiidae) populations from coastal Croatia and Montenegro. African Entomology 20 (1): 191-194. doi: 10.4001/003.020.0125
Tagami Y, Miura K (2004). Distribution and prevalence of Wolbachia in Japanese populations of Lepidoptera. Insect Molecular Biology 13 (4): 359-364. doi: 10.1111/j.0962-1075.2004.00492.x
Tang X, Freitak D, Vogel H, Ping L, Shao Y et al. (2012). Complexity and variability of gut commensal microbiota in polyphagous lepidopteran larvae. PLoS One 7 (7): e36978. doi: 10.1371/ journal.pone.0036978
Tabuloc CA, Lewald KM, Conner WR, Lee Y et al. (2019). Sequencing of Tuta absoluta genome to develop SNP genotyping assays for species identification. Journal of Pest Science 92 (4): 1397- 1407. doi: 10.1007/s10340-019-01116-6
Telschow A, Gadau J, Werren JH, Kobayashi Y (2019).Genetic incompatibilities between mitochondria and nuclear genes: effect on gene flow and speciation. Frontiers Genetics 10: 62. doi: 10.3389/fgene.2019.00062
Thao M, Baumann P (2004). Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Applied and Environmental Microbiology 70: 3401-3406. doi: 10.1128/AEM.70.6.3401-3406.2004
Tsuchida T, Koga R, Shibao H, Matsumoto T, Fukatsu T (2002). Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Molecular Ecology 11: 2123-2135. doi: 10.1046/j.1365-294X.2002.01606.x
Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000). Reduced genetic variation and the success of an invasive species. Proceedings of the National Academy of Sciences 97: 5948-5953. doi: 10.1073/ pnas.100110397
Turelli M, Hoffmannand AA, McKechnie SW (1992). Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations. Genetics, 132 (3): 713-723.
Van Meer MMM, Witteveldt J, Stouthamer R (1999). Phylogeny of the arthropod endosymbiont Wolbachia based on the wsp gene. Insect Molecular Biology 8 (3): 399-408. doi: 10.1046/j.1365- 2583.1999.83129.x
Voirol LRP, Frago E, Kaltenpoth M, Hilker M, Fatouros NE (2018). Bacterial symbionts in Lepidoptera: their diversity, transmission, and impact on the host. Frontiers Microbiology 9: 1-14. doi: 10.3389/fmicb.2018.00556
Walterson AM, Stavrinides J (2015). Pantoea: insights into a highly versatile and diverse genus within the Enterobacteriaceae. FEMS Microbiology Reviews 39 (6): 968-984. doi: 10.1093/ femsre/fuv027
Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ (2015). The incidence of bacterial endosymbionts in terrestrial arthropods. Proceedings of the Royal Society B: Biological Sciences 282 (1807). doi: 10.1098/rspb.2015.0249
Werren JH, O’Neill SL (1997). The evolution of heritable symbionts. Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. New York, NY, USA: Oxford University Press, pp. 1-41.
Werren JH (1997). Biology of Wolbachia. Annual Review of Entomology 42 (1): 587-609.
Werren JH, Zhang W, Guo LR (1995). Evaluation of Wolbachia: reproductive parasites of arthropods. Proceedings of the Royal Society B: Biological Sciences 261 (1360).
Weeks AR, Velten R, Stouthhamer R (2003). Incidence of a new sexratio-distorting endosymbiotic bacterium among arthropods. Proceedings of the Royal Society B: Biological Sciences 270: 1857-1865. doi: 10.1098/rspb.2003.2425
Xia X, Gurr GM, Vasseur L, Zheng D, Zhong H et al. (2017). Metagenomic sequencing of diamondback moth gut microbiome unveils key holobiont adaptations for herbivory. Frontiers Microbiology 8: 663. doi: 10.3389/fmicb.2017.00663
Yalcin M, Mermer S, Kozaci LD, Turgut C (2015). Insecticide resistance in two populations of Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae) from Turkey. Turkish Journal of Entomology 39 (2): 137-145. doi: 10.16970/ted.63047
Yatkin G, Guz N (2018). The use of DNA barcoding in entomology. Yüzüncü Yıl University Journal of Agricultural Sciences 28 (1): 126-134. doi: 10.29133/yyutbd.350146
Yun JH, Roh SW, Whon TW, Jung MJ, Kim MS et al. (2014). Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Applied Environmental Microbiology 80 (17): 5254-5264. doi: 10.1128/ AEM.01226-14
Yükselbaba U, Göçmen H (2016). Determination of genetic variation of tomato leafminer [Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae)] populations from west Mediterreanean region of Turkey based on mitochondrial cytochrome oxidase I (mtCOI). Mediterranean Agricultural Sciences 29 (1): 5-7.
Zibaee I (2016). The expression profile of detoxifying enzyme of tomato leaf miner, Tuta absoluta Meyrik (Lepidoptera: Gelechiidae) to chlorpyrifos. Arthropods 5 (2): 77.