Skip to main content

Transovarial Transmission of Symbionts in Insects

  • Chapter
  • First Online:
Oocytes

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 63))

Abstract

Many insects, on account of their unbalanced diet, live in obligate symbiotic associations with microorganisms (bacteria or yeast-like symbionts), which provide them with substances missing in the food they consume. In the body of host insect, symbiotic microorganisms may occur intracellularly (e.g., in specialized cells of mesodermal origin termed bacteriocytes, in fat body cells, in midgut epithelium) or extracellularly (e.g., in hemolymph, in midgut lumen). As a rule, symbionts are vertically transmitted to the next generation. In most insects, symbiotic microorganisms are transferred from mother to offspring transovarially within female germ cells. The results of numerous ultrastructural and molecular studies on symbiotic systems in different groups of insects have shown that they have a large diversity of symbiotic microorganisms and different strategies of their transmission from one generation to the next. This chapter reviews the modes of transovarial transmission of symbionts between generations in insects.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Abt MC, Artis D (2009) The intestinal microbiota in health and disease: the influence of microbial products on immune cell homeostasis. Curr Opin Gastroenterol 25:496–502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baumann P (1998) Symbiotic associations involving microorganisms. A special issue devoted to some less well known symbiotic associations. BioScience 48:254–255

    Article  Google Scholar 

  • Baumann P (2005) Biology of bacteriocyte-associated endosymbionts of plant sup-sucking insects. Annu Rev Microbiol 59:155–189

    Article  CAS  PubMed  Google Scholar 

  • Baumann P, Baumann L, Lai CY, Rouhbakksh D, Moran NA, Clark MA (1995) Genetics, physiology and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu Rev Microbiol 49:55–94

    Article  CAS  PubMed  Google Scholar 

  • Biliński S (1998) Introductory remarks. Folia Histochem Cytobiol 3:143–145

    Google Scholar 

  • Braendle C, Miura T, Bickel R, Shingleton AW, Kambhampati S, Stern DL (2003) Developmental origin and evolution of bacteriocytes in the aphid – Buchnera symbiosis. PLoS Biol 1:70–76

    Article  CAS  Google Scholar 

  • Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8:218–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchner P (1955) Endosymbiosestudien an Schildläusen. III. Macrocerococcus und Puto zwei primitive Pseudococcinen. Z Morph Őkol Tiere 43:523–577

    Article  Google Scholar 

  • Buchner P (1965) Endosymbiosis of animals with plant microorganisms. Interscience Publishers, New York

    Google Scholar 

  • Büning J (1994) The insect ovary: ultrastructure, previtellogenic growth and evolution. Chapman and Hall, London

    Book  Google Scholar 

  • Burke GR, Normark BB, Favret C, Moran NA (2009) Evolution and diversity of facultative symbionts from the aphid subfamily Lachninae. Appl Environ Microbiol 75:5328–5335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng DJ, Hou RF (2001) Histological observations on transovarial transmission of a yeast-like symbiote in Nilaparvata lugens Stal (Homoptera, Delphacidae). Tissue Cell 33:273–279

    Article  CAS  PubMed  Google Scholar 

  • Cheung W, Purcell AH (1999) Invasion of bacteroids and BEV bacterium into oocytes of the leafhopper Euscelidius variegatus Kirschbaum (Homoptera: Cicadellidae): an electron microscopic study. Zool Stud 38:69–75

    Google Scholar 

  • Costa HS, Westcot DM, Ullman DE, Johnson MW (1993) Ultrastructure of the endosymbionts of the whitefly, Bemisia tabaci and Trialeurodes vaporariorum. Protoplasma 176:106–115

    Article  Google Scholar 

  • Dale C, Moran NA (2006) Molecular interactions between bacterial symbionts and their hosts. Cell 126:453–465

    Article  CAS  PubMed  Google Scholar 

  • Dasch AG, Weiss E, Chang KP (1984) Endosymbionts of insects. In: Krieg NR (ed) Bergey’s manual of systematic bacteriology, vol 1. Williams and Wilkins, Baltimore, pp 811–833

    Google Scholar 

  • Dixon AFG (1985) Structure of aphid populations. Annu Rev Entomol 30:155–174

    Article  Google Scholar 

  • Douglas AE (1989) Mycetocyte symbiosis in insects. Biol Rev 64:409–434

    Article  CAS  PubMed  Google Scholar 

  • Douglas AE (1998) Nutritional interactions in insect – microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37

    Article  CAS  PubMed  Google Scholar 

  • Douglas AE (2009) The microbial dimension in insect nutritional ecology. Funct Ecol 23:38–47

    Article  Google Scholar 

  • Eberle MW, McLean DL (1982) Initiation and orientation of the symbiote migration in the human body louse Pediculus humanus L. J Insect Physiol 28:417–422

    Article  Google Scholar 

  • Eberle MW, McLean DL (1983) Observation on symbiote migration in human body lice with scanning and transmission electron microscopy. Can J Microbiol 29:755–762

    Article  CAS  PubMed  Google Scholar 

  • Fukatsu T, Hosokawa T (2002) Capsule-transmitted gut symbiotic bacterium of the Japanese common plataspid stinkbug, Megacopta punctatissima. Appl Environ Microbiol 68:389–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukatsu T, Ishikawa H (1992) A novel eukaryotic extracellular symbiont in an aphid, Astegopteryx styraci (Homoptera, Aphididae, Hormaphidinae). J Insect Physiol 38:765–773

    Article  Google Scholar 

  • Fukatsu T, Ishikawa H (1996) Phylogenetic position of yeast-like symbiont of Hamiltonaphis styraci (Homoptera, Aphididae) based on 18S rDNA sequence. Insect Biochem Mol Biol 26:383–388

    Article  CAS  PubMed  Google Scholar 

  • Fukatsu T, Nikoh N (1998) Two intracellular symbiotic bacteria from mulberry psyllid Anomoneura mori (Insecta, Homoptera). Appl Environ Microbiol 66:2748–2758

    Article  Google Scholar 

  • Fukatsu T, Nikoh N, Kawai R, Koga R (2000) The secondary endosymbiotic bacterium of the pea aphid, Acyrthosiphon pisum (Insecta: Homoptera). Appl Environ Microbiol 66:2748–2758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukatsu T, Koga R, Smith WA, Tanaka K, Nikoh N, Sasaki-Fukatsu K, Yoshizawa K, Dale C, Clayton DH (2007) Bacterial endosymbiont of the slender pigeon louse, Columbicola columbae, allied to endosymbionts of grain weevils and tsetse flies. Appl Environ Microbiol 73:6660–6668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gatehouse LN, Sutherland P, Forgie SA, Kaji R, Christeller JT (2011) Molecular and histological characterization of primary (Betaproteobacteria) and secondary (Gammaproteobacteria) endosymbionts of three mealybug species. Appl Environ Microbiol 78:1187–1197

    Article  PubMed  CAS  Google Scholar 

  • Gottlieb Y, Ghanim M, Gueguen G, Kontsedalov S, Vavre F, Fleury F, Zchori-Fein E (2008) Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies. FASEB J 22:2591–2599

    Article  CAS  PubMed  Google Scholar 

  • Hongoh Y, Ishikawa H (2000) Evolutionary studies on uricases of fungal endosymbionts of aphids and planthoppers. Mol Evol 51:265–277

    Google Scholar 

  • Hosokawa T, Kikuchi Y, Meng XY, Fukatsu T (2005) The making of symbiont capsule in the plataspid stinkbug Megacopta punctatissima. FEMS Microbiol Ecol 54:471–477

    Article  CAS  PubMed  Google Scholar 

  • Husnik F, McCutcheon JP (2016) Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis. PNAS 113:E5416–E5424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Husnik FN, Nikoh R, Koga R, Ross L, Duncan RP, Fujie M, Tanaka M, Satoh N, Bachtrog D, Wilson ACC, von Dohlen CD, Fukatsu T, McCutcheon JP (2013) Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153:1567–1578

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa H (1989) Biochemical and molecular aspects of endosymbiosis in insects. Int Rev Cytol 116:1–45

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa H (2003) Insect symbiosis: an introduction. In: Bourtzis K, Miller TA (eds) Insect symbiosis. CRC Press, Boca Raton, pp 1–21

    Google Scholar 

  • Kikuchi Y (2009) Endosymbiotic bacteria in insects: their diversity and culturability. Microbes Environ 24:195–204

    Article  PubMed  Google Scholar 

  • Kikuchi Y, Fukatsu T (2003) Insect-bacterium mutualism without vertical transmission. In: Bourtzis K, Miller TA (eds) Insect symbiosis, vol 3. CRC Press, Boca Raton, pp 143–161

    Google Scholar 

  • Kikuchi Y, Hosokawa T, Fukatsu T (2007) Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl Environ Microbiol 73:4308–4316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kindlmann P, Dixon AFG (1989) Developmental constraints in the evolution of reproductive strategies: telescoping of generations in parthenogenetic aphids. Funct Ecol 3:531–537

    Article  Google Scholar 

  • Kobiałka M, Michalik A, Walczak M, Junkiert Ł, Szklarzewicz T (2015) Symbiotic microorganisms of the leafhopper Deltocephalus pulicaris (Fallén, 1806) (Insecta, Hemiptera, Cicadellidae: Deltocephalinae): Molecular characterization, ultrastructure and transovarial transmission. Pol J Entomol 84:289–304

    Google Scholar 

  • Kobiałka M, Michalik A, Walczak M, Junkiert Ł, Szklarzewicz T (2016) Sulcia symbiont of the leafhopper Macrosteles laevis (Ribaut, 1927) (Insecta, Hemiptera, Cicadellidae: Deltocephalinae) harbors Arsenophonus bacteria. Protoplasma 253:903–912

    Article  PubMed  Google Scholar 

  • Koga R, Tsuchida T, Fukatsu T (2003) Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc R Soc London B 270:2543–2550

    Article  Google Scholar 

  • Koga R, Meng X-Y, Tsuchida T, Fukatsu T (2012) Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte-embryo interface. PNAS 109:E1230–E1237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koga R, Bennett GM, Cryan JR, Moran NA (2013) Evolutionary replacement of symbionts in an ancient and diverse insect lineage. Environ Microbiol 15:2073–2081

    Article  PubMed  Google Scholar 

  • Kono M, Koga R, Shimada M, Fukatsu T (2008) Infection dynamics of coexisting β and γ-proteobacteria in the nested endosymbiotic system of mealybugs. Appl Environ Microbiol 74:4175–4184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kot M, Szklarzewicz T, Drohojowska J (2012) Ultrastructural studies on bacterial endosymbionts in psyllids (Insecta, Hemiptera: Psylloidea). Acta Biol Crac Ser Bot 54(Suppl 1):61

    Google Scholar 

  • Kot M, Michalik A, Szklarzewicz T (2014) Primary and secondary endosymbionts of psyllids (Insecta, Hemiptera: Psylloidea). Acta Biol Crac Ser Bot 56(Suppl 1):66

    Google Scholar 

  • Koteja J (1985) Essay on the prehistory of the scale insects (Homoptera, Coccinea). Ann Zool 38:461–503

    Google Scholar 

  • Koteja J, Pyka-Fosciak G, Vogelgesang M, Szklarzewicz T (2003) Structure of the ovary in Steingelia (Sternorrhyncha: Coccinea), and its phylogenetic implications. Arthropod Struct Dev 32:247–256

    Article  PubMed  Google Scholar 

  • Kuechler SM, Dettner K, Kehl S (2010) Molecular characterization and localization of the obligate endosymbiotic bacterium in the birch catkin bug Kleidocerys resedae (Heteroptera: Lygaeidae, Ischnorhynchinae). FEMS Microbiol Ecol 73:408–418

    CAS  Google Scholar 

  • Kuechler SM, Dettner K, Kehl S (2011) Characterization of an obligate intracellular bacterium in the midgut epithelium of the bulrush bug Chilacis typhae (Heteroptera, Lygaeidae, Artheneinae). Appl Environ Microbiol 77:2869–2876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuechler SM, Renz P, Dettner K, Kehl S (2012) Diversity of symbiotic organs and bacterial endosymbionts of lygaeoid bugs of the families Blissidae and Lygaeidae (Hemiptera: Heteroptera: Lygaeoidea). Appl Environ Microbiol 78:2648–2659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kupper M, Stigloher C, Feldhaar H, Gross R (2016) Distribution of the obligate endosymbiont Blochmannia floridanus and expression analysis of putative immune genes in ovaries of the carpenter ant Camponotus floridanus. Arthropod Struct Dev 45:475–487

    Article  PubMed  Google Scholar 

  • Lukasik P, Guo H, Van Asch M, Ferrari J, Godfray HCJ (2013) Protection against a fungal pathogen conferred by the aphid facultative endosymbionts Rickettsia and Spiroplasma is expressed in multiple host genotypes and species and is not influenced by co-infection with another symbiont. J Evol Biol 26:2654–2661

    Article  CAS  PubMed  Google Scholar 

  • Matsuura Y, Koga R, Nikoh N, Meng XY, Hanada S, Fukatsu T (2009) Huge symbiotic organs in giant scale insects of the genus Drosicha (Coccoidea: Monophlebidae) harbor flavobacterial and enterobacterial endosymbionts. Zoolog Sci 26:448–456

    Article  CAS  PubMed  Google Scholar 

  • Matsuura Y, Kikuchi Y, Hosokawa T, Koga R, Meng X-Y, Kamagata Y, Nikoh N, Fukatsu T (2012) Evolution of symbiotic organs and endosymbionts in lygaeid stinkbugs. ISME J 6:397–409

    Article  CAS  PubMed  Google Scholar 

  • McCutcheon JP, Moran NA (2007) Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. PNAS 104:19392–19397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCutcheon JP, von Dohlen CD (2011) An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr Biol 21:1366–1372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCutcheon JP, McDonald BR, Moran NA (2009) Convergent evolution of metabolic roles in bacterial co-symbionts of insects. PNAS 106:15394–15399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michalik A, Jankowska W, Szklarzewicz T (2009) Ultrastructure and transovarial transmission of endosymbiotic microorganisms in Conomelus anceps and Metcalfa pruinosa (Insecta, Hemiptera, Fulgoromorpha). Folia Biol (Kraków) 57:131–137

    Article  Google Scholar 

  • Michalik A, Gołas A, Kot M, Wieczorek K, Szklarzewicz T (2013) Endosymbiotic microorganisms in Adelges (Sacchiphantes) viridis (Insecta, Hemiptera, Adelgoidea: Adelgidae): molecular characterization, ultrastructure and transovarial transmission. Arthropod Struct Dev 42:531–538

    Article  PubMed  Google Scholar 

  • Michalik A, Szklarzewicz T, Jankowska W, Wieczorek K (2014a) Endosymbiotic microorganisms of aphids (Hemiptera: Sternorrhyncha: Aphidoidea): ultrastructure, distribution and transovarial transmission. Eur J Entomol 111:91–104

    Article  Google Scholar 

  • Michalik A, Jankowska W, Kot M, Gołas A, Szklarzewicz T (2014b) Symbiosis in the green leafhopper, Cicadella viridis (Hemiptera, Cicadellidae). Association in statu nascendi? Arthropod Struct Dev 43:579–587

    Article  PubMed  Google Scholar 

  • Michalik K, Szklarzewicz T, Kalandyk-Kołodziejczyk M, Jankowska W, Michalik A (2016) Bacteria belonging to the genus Burkholderia are obligatory symbionts of the eriococcids Acanthococcus aceris Signoret, 1875 and Gossyparia spuria (Modeer, 1778) (Insecta, Hemiptera, Coccoidea). Arthropod Struct Dev 45:265–272

    Article  PubMed  Google Scholar 

  • Miura T, Braendle C, Shingleton A, Sisk G, Kambhampati S, Stern DL (2003) A comparison of parthenogenetic and sexual embryogenesis of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). J Exp Zool 295B:59–81

    Article  Google Scholar 

  • Montllor CB, Maxmen A, Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27:189–195

    Article  Google Scholar 

  • Moran NA (1992) The evolution of aphid life cycles. Annu Rev Entomol 37:321–348

    Article  Google Scholar 

  • Moran NA, Baumann P (2000) Bacterial endosymbionts in animals. Curr Opin Microbiol 3:270–275

    Article  CAS  PubMed  Google Scholar 

  • Moran NA, Telang A (1998) Bacteriocyte-associated symbionts of insects: a variety of insect groups harbor ancient prokaryotic endosymbionts. BioScience 48:295–304

    Article  Google Scholar 

  • Niżnik S, Szklarzewicz T (2007) Structure and development of hermaphroditic gonad in Icerya purchasi (Insecta, Hemiptera, Coccinea: Monophlebidae). Zool Polon 52:71–90

    Google Scholar 

  • Nováková E, Hypša V, Klein J, Foottit RG, von Dohlen CD, Moran NA (2013) Reconstructing the phylogeny of aphids (Hemiptera: Aphididae) using DNA of the obligate symbiont Buchnera aphidicola. Mol Phylogenet Evol 68:42–54

    Article  PubMed  Google Scholar 

  • Oliver KM, Russel JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. PNAS 100:1803–1807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliver KM, Moran NA, Hunter MS (2006) Cost and benefits of a superinfection of facultative symbionts in aphids. Proc R Soc B 273:1273–1280

    Article  PubMed  PubMed Central  Google Scholar 

  • Oliver KM, Degnan PH, Burke GR, Moran NA (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55:247–266

    Article  CAS  PubMed  Google Scholar 

  • Pyka-Fosciak G, Szklarzewicz T (2008) Germ cell cluster formation and ovariole structure in viviparous and oviparous generations of the aphid Stomaphis quercus. Int J Dev Biol 52:259–265

    Article  PubMed  Google Scholar 

  • Ramirez-Puebla ST, Rosenblueth M, Chavez-Moreno CK, Catanho Pereira de Lyra MC, Tecante A, Martinez-Romero A (2010) Molecular phylogeny of the genus Dactylopius (Hemiptera: Dactylopiidae) and identification of the symbiotic bacteria. Environ Entomol 39:1178–1183

    Article  CAS  PubMed  Google Scholar 

  • Ries E (1931) Die Symbiose der Läuse und Federlinge. Z Morphol Őkol Tiere 20:233–367

    Article  Google Scholar 

  • Sacchi L, Grigolo A, Mazzini M, Bigliardi E, Baccetti B, Laudani U (1988) Symbionts in the oocytes of Blattella germanica L. (Dictyoptera: Blattellidae): their mode of transmission. Int J Insect Morphol Embryol 17:437–446

    Article  Google Scholar 

  • Sacchi L, Nalepa CA, Lenz M, Bandi C, Corona S, Grigolo A, Bigliardi E (2000) Transovarial transmission of symbiotic bacteria in Mastotermes darwiniensis (Isoptera: Mastotermitidae): ultrastructural aspects and phylogenetic implications. Ann Entomol Soc Am 93:1308–1313

    Google Scholar 

  • Sacchi L, Genchi M, Clementi E, Bigliardi E, Avanzatti AM, Pajoroi M, Negri I, Marzorati M, Gonella E, Alma A, Daffonchio D, Bandi C (2008) Multiple symbiosis in the leafhopper Scaphoideus titanus (Hemiptera: Cicadellidae): details of transovarial transmission of Cardinium sp. and yeast-like endosymbionts. Tissue Cell 40:231–242

    Article  CAS  PubMed  Google Scholar 

  • Scarborough CL, Ferrari J, Godfray HCJ (2005) Aphid protected from pathogen by endosymbiont. Science 310:1781

    Article  CAS  PubMed  Google Scholar 

  • Schneider G (1940) Beitrage zur Kenntnis der symbiontischen Einrichtungen der Heteropteren. Z Morphol Őkol Tiere 36:565–644

    Google Scholar 

  • Spaulding AW, von Dohlen CD (1998) Phylogenetic characterization and molecular evolution of bacterial endosymbionts in psyllids (Hemiptera, Sternorrhyncha). Mol Biol Evol 15:1506–1513

    Article  CAS  PubMed  Google Scholar 

  • Swiatoniowska M, Ogorzalek A, Golas A, Michalik A, Szklarzewicz T (2013) Ultrastructure, distribution and transovarial transmission of symbiotic microorganisms in Nysius ericae and Nithecus jacobaeae (Heteroptera: Lygaeidae: Orsillinae). Protoplasma 250:325–332

    Article  PubMed  Google Scholar 

  • Szklarzewicz T, Moskal A (2001) Ultrastructure, distribution, and transmission of endosymbionts in the whitefly Aleurochiton aceris Modeer (Insecta, Hemiptera, Aleyrodinea). Protoplasma 218:45–53

    Article  CAS  PubMed  Google Scholar 

  • Szklarzewicz T, Kędra K, Niżnik S (2006) Ultrastructure and transovarial transmission of endosymbiotic microorganisms in Palaeococcus fuscipennis (Burmeister) (Insecta, Hemiptera, Coccinea: Monophlebidae). Folia Biol (Kraków) 54:69–74

    Article  Google Scholar 

  • Szklarzewicz T, Jankowska W, Łukasiewicz K, Szymańska B (2007) Structure of the ovaries and oogenesis in Cixius nervosus (Cixiidae), Javesella pellucida and Conomelus anceps (Delphacidae) (Insecta, Hemiptera, Fulgoromorpha). Arthropod Struct Dev 36:199–207

    Article  PubMed  Google Scholar 

  • Szklarzewicz T, Michalik A, Czaja A, Szydłowska S (2010) Germ cell cluster formation and ovariole structure in Puto albicans and Crypticerya morrilli (Hemiptera: Coccinea). Phylogenetic implications. Eur J Entomol 107:589–595

    Article  Google Scholar 

  • Szklarzewicz T, Kalandyk-Kolodziejczyk M, Kot M, Michalik A (2013) Ovary structure and transovarial transmission of endosymbiotic microorganisms in Marchalina hellenica (Insecta, Hemiptera, Coccomorpha: Marchalinidae). Acta Zool (Stockholm) 94:184–192

    Article  Google Scholar 

  • Szklarzewicz T, Michalik A, Kalandyk-Kołodziejczyk M, Kobiałka M, Simon E (2014) Ovary of Matsucoccus pini (Insecta, Hemiptera, Coccinea: Matsucoccidae). Morphology, ultrastructure and phylogenetic implications. Microsc Res Tech 77:327–334

    Article  PubMed  Google Scholar 

  • Szklarzewicz T, Grzywacz B, Szwedo J, Michalik A (2016) Bacterial symbionts of the leafhopper Evacanthus interruptus (Linnaeus, 1758) (Insecta, Hemiptera, Cicadellidae: Evacanthinae). Protoplasma 253:379–391

    Article  PubMed  Google Scholar 

  • Szklarzewicz T, Kalandyk-Kołodziejczyk K, Michalik K, Jankowska W, Michalik A (2017) Symbiotic microorganisms in Puto superbus (Leonardi, 1907) (Insecta, Hemiptera, Coccomorpha: Putoidae). Protoplasma. doi:10.1007/s00709-017-1135-7

  • Takiya DM, Tran P, Dietrich CH, Moran NA (2006) Co-cladogenesis spanning three phyla: leafhoppers (Insecta: Hemiptera: Cicadellidae) and their dual bacterial symbionts. Mol Ecol 15:4175–4191

    Article  CAS  PubMed  Google Scholar 

  • Thao ML, Moran NA, Abbot P, Bernnan EB, Burckhardt DH, Baumann P (2000a) Cospeciation of psyllids and their prokaryotic endosymbionts. Appl Environ Microbiol 66:2898–2905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thao ML, Clark MA, Baumann L, Brennan EB, Moran NA, Baumann P (2000b) Secondary endosymbionts of psyllids have been acquired multiple times. Curr Microbiol 41:300–304

    Article  CAS  PubMed  Google Scholar 

  • Thao ML, Gullan PJ, Baumann P (2002) Secondary (γ-proteobacteria) endosymbionts infect the primary (β-proteobacteria) endosymbionts of mealybugs multiple times and coevolve with their host. Appl Environ Microbiol 68:3190–3197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toenshoff ER, Gruber D, Horn M (2012) Co-evolution and symbiont replacement shaped the symbiosis between adelgids (Hemiptera: Adelgidae) and their bacterial symbionts. Environ Microbiol 14:1284–1295

    Google Scholar 

  • Tremblay E (1977) Advances in endosymbiont studies in Coccoidea. VA Polytech Inst State Univ Res Div Bull 127:23–33

    Google Scholar 

  • von Dohlen CD, Kohler S, Alsop ST, McManus WR (2001) Mealybug β-proteobacterial endosymbionts contain γ-proteobacterial symbionts. Nature 412:433–435

    Article  Google Scholar 

  • Vorburger C, Gehrer L, Rodriguez P (2010) A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biol Lett 6:109–111

    Article  PubMed  Google Scholar 

  • Wegierek P, Michalik A, Wieczorek K, Kanturski M, Kobiałka M, Śliwa K, Szklarzewicz T (2017) Buchnera aphidicola of the birch blister aphid, Hamamelistes betulinus (Horváth, 1896) (Insecta, Hemiptera, Aphididae: Hormaphidinae): molecular characterization, transmission between generations and its geographic significance. Acta Zool (Stockholm). doi:10.1111/azo.12186

  • Wilkinson TL, Ishikawa H (2001) On the functional significance of symbiotic microorganisms in the Homoptera: a comparative study of Acyrthosiphon pisum and Nilaparvata lugens. Physiol Entom 26:86–93

    Article  Google Scholar 

  • Wilkinson TL, Fukatsu T, Ishikawa H (2003) Transmission of symbiotic bacteria Buchnera to parthenogenetic embryos in the aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). Arthropod Struct Dev 32:241–245

    Article  CAS  PubMed  Google Scholar 

  • Wojciechowski W, Depa Ł, Kanturski M, Wegierek P, Wieczorek K (2015) An annotated checklist of the Aphids (Hemiptera: Aphidomorpha) of Poland. Pol J Entomol 84:383–420

    Google Scholar 

  • Wu D, Daugherty SC, Van Aken SE, Pai GH, Watkins KL, Khouri H (2006) Metabolic complementarity and genomics of the dual symbiosis of sharpshooters. PLoS Biol 4:e188

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Żelazowska M, Biliński SM (1999) Distribution and transmission of endosymbiotic microorganisms in the oocytes of the pig louse, Haematopinus suis (L.) (Insecta: Phthiraptera). Protoplasma 209:207–213

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Teresa Szklarzewicz .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Szklarzewicz, T., Michalik, A. (2017). Transovarial Transmission of Symbionts in Insects. In: Kloc, M. (eds) Oocytes. Results and Problems in Cell Differentiation, vol 63. Springer, Cham. https://doi.org/10.1007/978-3-319-60855-6_3

Download citation

Publish with us

Policies and ethics