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Symbiont-Induced Sexual and Reproductive Manipulation in Insects

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Spectrum of Sex

Abstract

Some insect symbionts are known to manipulate the reproduction and sexual development of their hosts for their own benefit. To accomplish this, these selfish sex ratio distorters must disturb the host’s sex determination pathways. Recent progress in molecular biological and bioinformatic methods has enabled us to identify the symbiont effectors. In this chapter, we introduce the diversity of insect sex determination systems and dosage compensation systems, both of which are tightly associated with one another. Moreover, we describe highly tuned symbiont strategies for host sexual manipulation by that target the sex determination and/or dosage compensation machineries by taking advantage of their own factors.

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References

  • Beckmann JF, Ronau JA, Hochstrasser M (2017) A Wolbachia deubiquitylating enzyme induces cytoplasmic incompatibility. Nat Microbiol 2:17007

    Article  PubMed  PubMed Central  Google Scholar 

  • Berec L, Maxin D, Bernhauerova V (2016) Male-killing bacteria as agents of insect pest control. J Appl Ecol 53:1270–1279

    Article  CAS  Google Scholar 

  • Beye M, Hasselmann M, Fondrk MK et al (2003) The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114:419–429

    Article  CAS  PubMed  Google Scholar 

  • Bordenstein SR, Bordenstein SR (2016) Eukaryotic association module in phage WO genomes from Wolbachia. Nat Commun 7:13155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charlat S, Hornett EA, Fullard JH et al (2007) Extraordinary flux in sex ratio. Science 317:214

    Article  CAS  PubMed  Google Scholar 

  • Cheng B, Kuppanda N, Aldrich JC et al (2016) Male-killing Spiroplasma alters behavior of the dosage compensation complex during Drosophila melanogaster embryogenesis. Curr Biol 26:1339–1345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clough E, Jimenez E, Kim YA et al (2014) Sex- and tissue-specific functions of Drosophila doublesex transcription factor target genes. Dev Cell 31:761–773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Criscione F, Qi Y, Tu Z (2016) GUY1 confers complete female lethality and is a strong candidate for a male-determining factor in Anopheles stephensi. Elife 5:e19281

    Article  PubMed  PubMed Central  Google Scholar 

  • Dannowski J, Flor M, Telschow A et al (2009) The effect of sibmating on the infection dynamics of male-killing bacteria. Evolution 63:2525–2534

    Article  PubMed  Google Scholar 

  • Duarte EH, Carvalho A, López-Madrigal S et al (2021) Forward genetics in Wolbachia: regulation of Wolbachia proliferation by the amplification and deletion of an addictive genomic island. PLoS Genet 17:e1009612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ellison C, Bachtrog D (2019) Contingency in the convergent evolution of a regulatory network: dosage compensation in Drosophila. PLoS Biol 17:e3000094

    Article  PubMed  PubMed Central  Google Scholar 

  • Elnagdy S, Majerus MEN, Handley LJL (2011) The value of an egg: resource reallocation in ladybirds (Coleoptera: Coccinellidae) infected with male-killing bacteria. J Evol Biol 24:2164–2172

    Article  CAS  PubMed  Google Scholar 

  • Fujita R, Inoue MN, Takamatsu T et al (2021) Late male-killing viruses in Homona magnanima identified as Osugoroshi viruses, novel members of Partitiviridae. Front Microbiol 11:620623

    Article  PubMed  PubMed Central  Google Scholar 

  • Fukui T, Kawamoto M, Shoji K et al (2015) The endosymbiotic bacterium Wolbachia selectively kills male hosts by targeting the masculinizing gene. PLoS Pathog 11:e1005048

    Article  PubMed  PubMed Central  Google Scholar 

  • Fukui T, Kiuchi T, Shoji K et al (2018) In vivo masculinizing function of the Ostrinia furnacalis Masculinizer gene. Biochem Biophys Res Commun 503:1768–1772

    Article  CAS  PubMed  Google Scholar 

  • Hall AB, Basu S, Jiang X et al (2015) A male-determining factor in the mosquito Aedes aegypti. Science 348:1268–1270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harumoto T, Anbutsu H, Fukatsu T (2014) Male-killing Spiroplasma induces sex-specific cell death via host apoptotic pathway. PLoS Pathog 10:e1003956

    Article  PubMed  PubMed Central  Google Scholar 

  • Harumoto T, Anbutsu H, Lemaitre B et al (2016) Male-killing symbiont damages host's dosage-compensated sex chromosome to induce embryonic apoptosis. Nat Commun 7:12781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harumoto T, Lemaitre B (2018) Male-killing toxin in a bacterial symbiont of Drosophila. Nature 557:252–255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harvey-Samuel T, Norman VC, Carter R et al (2020) Identification and characterization of a Masculinizer homologue in the diamondback moth, Plutella xylostella. Insect Mol Biol 29:231–240

    Article  CAS  PubMed  Google Scholar 

  • Hasimoto H (1933) The role of the W-chromosome in the sex determination of Bombyx mori. Jpn J Genet 8:245–247

    Google Scholar 

  • Hasselmann M, Beye M (2004) Signatures of selection among sex-determining alleles of the honey bee. Proc Natl Acad Sci U S A 101:4888–4893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasselmann M, Gempe T, Schiøtt M et al (2008) Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees. Nature 454:519–522

    Article  CAS  PubMed  Google Scholar 

  • Hayashi M, Nomura M, Kageyama D (2018) Rapid comeback of males: evolution of male-killer suppression in a green lacewing population. Proc Biol Sci 285:20180369

    PubMed  PubMed Central  Google Scholar 

  • Hilgenboecker K, Hammerstein P, Schlattmann P et al (2008) How many species are infected with Wolbachia?--A statistical analysis of current data. FEMS Microbiol Lett 281:215–220

    Google Scholar 

  • Hiroki M, Kato Y, Kamito T et al (2002) Feminization of genetic males by a symbiotic bacterium in a butterfly, Eurema hecabe (Lepidoptera: Pieridae). Naturwissenschaften 89:167–170

    Article  CAS  PubMed  Google Scholar 

  • Hiroki M, Tagami Y, Miura K et al (2004) Multiple infection with Wolbachia inducing different reproductive manipulations in the butterfly Eurema hecabe. Proc Biol Sci 271:1751–1755

    Article  PubMed  PubMed Central  Google Scholar 

  • Hirota K, Matsuda-Imai N, Kiuchi T et al (2021) Characterization of nuclear localization signal in Ostrinia furnacalis Masculinizer protein. Arch Insect Biochem Physiol 106:e21768

    Article  CAS  PubMed  Google Scholar 

  • Hopkins BR, Kopp A (2021) Evolution of sexual development and sexual dimorphism in insects. Curr Opin Genet Dev 69:129–139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hornett EA, Charlat S, Duplouy AM et al (2006) Evolution of male-killer suppression in a natural population. PLoS Biol 4:e283

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoshino M, Nakanishi K, Nakai M et al (2008) Gross morphology and histopathology of male-killing strain larvae in the oriental tea tortrix Homona magnanima (Lepidoptera: Tortricidae). Appl Entomol Zool 43:119–125

    Article  Google Scholar 

  • Hurst GDD, Graf von der Schulenburg JH, Majerus TM et al (1999) Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. Insect Mol Biol 8:133–139

    Article  CAS  PubMed  Google Scholar 

  • Hurst GDD, Frost CL (2015) Reproductive parasitism: maternally inherited symbionts in a biparental world. Cold Spring Harb Perspect Biol 7:a017699

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiggins FM, Hurst GD, Jiggins CD et al (2000) The butterfly Danaus chrysippus is infected by a male-killing Spiroplasma bacterium. Parasitology 120:439–446

    Article  PubMed  Google Scholar 

  • Kageyama D, Ohno M, Sasaki T et al (2017a) Feminizing Wolbachia endosymbiont disrupts maternal sex chromosome inheritance in a butterfly species. Evol Lett 1:232–244

    Article  PubMed  PubMed Central  Google Scholar 

  • Kageyama D, Yoshimura K, Sugimoto TN et al (2017b) Maternally transmitted non-bacterial male killer in Drosophila biauraria. Biol Lett 13:20170476

    Article  PubMed  PubMed Central  Google Scholar 

  • Katsuma S, Shoji K, Sugano Y et al (2019) Masc-induced dosage compensation in silkworm cultured cells. FEBS Open Bio 9:1573–1579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawaoka S, Minami K, Katsuma S et al (2008) Developmentally synchronized expression of two Bombyx mori Piwi subfamily genes, SIWI and BmAGO3 in germ-line cells. Biochem Biophys Res Commun 367:755–760

    Article  CAS  PubMed  Google Scholar 

  • Kern P, Cook JM, Kageyama D et al (2015) Double trouble: combined action of meiotic drive and Wolbachia feminization in Eurema butterflies. Biol Lett 11:20150095

    Article  PubMed  PubMed Central  Google Scholar 

  • Kiuchi T, Koga H, Kawamoto M et al (2014) A single female-specific piRNA is the primary determiner of sex in the silkworm. Nature 509:633–636

    Article  CAS  PubMed  Google Scholar 

  • Kiuchi T, Sugano Y, Shimada T et al (2019) Two CCCH-type zinc finger domains in the Masc protein are dispensable for masculinization and dosage compensation in Bombyx mori. Insect Biochem Mol Biol 104:30–38

    Article  CAS  PubMed  Google Scholar 

  • Koop JL, Zeh DW, Bonilla MM et al (2009) Reproductive compensation favours male-killing Wolbachia in a live bearing host. Proc Biol Sci 276:4021–4028

    CAS  PubMed  PubMed Central  Google Scholar 

  • Krzywinska E, Dennison NJ, Lycett GJ et al (2016) A maleness gene in the malaria mosquito Anopheles gambiae. Science 353:67–69

    Article  CAS  PubMed  Google Scholar 

  • Lechner S, Ferretti L, Schöning C et al (2013) Nucleotide variability at its limit? Insights into the number and evolutionary dynamics of the sex-determining specificities of the honey bee Apis mellifera. Mol Biol Evol 31:272–287

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee J, Kiuchi T, Kawamoto M et al (2015) Identification and functional analysis of a Masculinizer orthologue in Trilocha varians (Lepidoptera: Bombycidae). Insect Mol Biol 24:561–569

    Article  CAS  PubMed  Google Scholar 

  • LePage DP, Metcalf JA, Bordenstein SR et al (2017) Prophage WO genes recapitulate and enhance Wolbachia-induced cytoplasmic incompatibility. Nature 543:243–247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu P, Jin B, Li X et al (2020) Nix is a male-determining factor in the Asian tiger mosquito Aedes albopictus. Insect Biochem Mol Biol 118:103311

    Article  CAS  PubMed  Google Scholar 

  • Lucchesi JC (1978) Gene dosage compensation and the evolution of sex chromosomes. Science 202:711–716

    Article  CAS  PubMed  Google Scholar 

  • Majerus TM, Graf von der Schulenburg JH, Majerus ME et al (1999) Molecular identification of a male-killing agent in the ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Insect Mol Biol 8:551–555

    Article  CAS  PubMed  Google Scholar 

  • Meccariello A, Salvemini M, Primo P et al (2019) Maleness-on-the-Y (MoY) orchestrates male sex determination in major agricultural fruit fly pests. Science 365:1457–1460

    Article  CAS  PubMed  Google Scholar 

  • Miyahara Y (1984) Abnormal sex ratio in Ostrinia furnacalis Guenée (Lepidoptera: Pyralidae). Jap J Appl Ent Zool 28:131–136

    Article  Google Scholar 

  • Morimoto S, Nakai M, Ono A et al (2001) Late male-killing phenomenon found in a Japanese population of the oriental tea tortrix, Homona magnanima (Lepidoptera: Tortricidae). Heredity 87:435–440

    Article  CAS  PubMed  Google Scholar 

  • Nakanishi K, Hoshino M, Nakai M et al (2008) Novel RNA sequences associated with late male killing in Homona magnanima. Proc Biol Sci 275:1249–1254

    CAS  PubMed  PubMed Central  Google Scholar 

  • Narita S, Kageyama D, Nomura M et al (2007) Unexpected mechanism of symbiont-induced reversal of insect sex: feminizing Wolbachia continuously acts on the butterfly Eurema hecabe during larval development. Appl Environ Microbiol 73:4332–4341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oishi K (1971) Spirochaete-mediated abnormal sex-ratio (SR) condition in Drosophila: a second virus associated with spirochaetes and its use in the study of the SR condition. Genet Res 18:45–56

    Article  CAS  PubMed  Google Scholar 

  • Ote M, Ueyama M, Yamamoto D (2016) Wolbachia protein TomO targets nanos mRNA and restores germ stem cells in Drosophila Sex-lethal mutants. Curr Biol 26:2223–2232

    Article  CAS  PubMed  Google Scholar 

  • Ote M, Yamamoto D (2018) Enhancing Nanos expression via the bacterial TomO protein is a conserved strategy used by the symbiont Wolbachia to fuel germ stem cell maintenance in infected Drosophila females. Arch Insect Biochem Physiol 98:e21471

    Article  PubMed  Google Scholar 

  • Perlmutter JI, Bordenstein SR, Unckless RL et al (2019) The phage gene wmk is a candidate for male killing by a bacterial endosymbiont. PLoS Pathog 15:e1007936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Penalva LO, Sanchez L (2003) RNA binding protein Sex-lethal (Sxl) and control of Drosophila sex determination and dosage compensation. Microbiol Mol Biol Rev 67:343–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi Y, Wu Y, Saunders R et al (2019) Guy1, a Y-linked embryonic signal, regulates dosage compensation in Anopheles stephensi by increasing X gene expression. eLife 8:e43570

    Article  PubMed  PubMed Central  Google Scholar 

  • Regassa LB, Gasparich GE (2006) Spiroplasmas: evolutionary relationships and biodiversity. Front Biosci 11:2983–3002

    Article  CAS  PubMed  Google Scholar 

  • Reynolds KT, Hoffmann AA (2002) Male age, host effects and the weak expression or non-expression of cytoplasmic incompatibility in Drosophila strains infected by maternally transmitted Wolbachia. Genet Res 80:79–87

    Article  PubMed  Google Scholar 

  • Sakai H, Sumitani M, Chikami Y et al (2016) Transgenic expression of the piRNA-resistant Masculinizer gene induces female-specific lethality and partial female-to-male sex reversal in the silkworm, Bombyx mori. PLoS Genet 12:e1006203

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 162:1313–1319

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharma A, Heinze SD, Wu Y et al (2017) Male sex in houseflies is determined by Mdmd, a paralog of the generic splice factor gene CWC22. Science 356:642–645

    Article  CAS  PubMed  Google Scholar 

  • Starr DJ, Cline TW (2002) A host parasite interaction rescues Drosophila oogenesis defects. Nature 418:76–79

    Article  CAS  PubMed  Google Scholar 

  • Stouthamer R, Luck RF, Hamilton WD (1990) Antibiotics cause parthenogenetic Trichogramma (Hymenoptera/Trichogrammatidae) to revert to sex. Proc Natl Acad Sci U S A 87:2424–2427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stouthamer R, Breeuwert JA, Luck RF et al (1993) Molecular identification of microorganisms associated with parthenogenesis. Nature 361:66–68

    Article  CAS  PubMed  Google Scholar 

  • Sugano Y, Kokusho R, Ueda M et al (2016) Identification of a bipartite nuclear localization signal in the silkworm Masc protein. FEBS Lett 590:2256–2261

    Article  CAS  PubMed  Google Scholar 

  • Sugimoto TN, Ishikawa Y (2012) A male-killing Wolbachia carries a feminizing factor and is associated with degradation of the sex-determining system of its host. Biol Lett 8:412–415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki MG, Funaguma S, Kanda T et al (2003) Analysis of the biological functions of a doublesex homologue in Bombyx mori. Dev Genes Evol 213:345–354

    Article  CAS  PubMed  Google Scholar 

  • Suzuki MG, Funaguma S, Kanda T et al (2005) Role of the male BmDSX protein in the sexual differentiation of Bombyx mori. Evol Dev 7:58–68

    Article  CAS  PubMed  Google Scholar 

  • Tabata J, Hattori Y, Sakamoto H et al (2011) Male killing and incomplete inheritance of a novel Spiroplasma in the moth Ostrinia zaguliaevi. Microb Ecol 61:254–263

    Article  PubMed  Google Scholar 

  • Tanaka Y (1916) Genetic studies in the silkworm. J Coll Agric Sapporo 6:1–33

    Google Scholar 

  • Tinsley MC, Majerus MEN (2006) A new male-killing parasitism: Spiroplasma bacteria infect the ladybird beetle Anisosticta novemdecimpunctata (Coleoptera: Coccinellidae). Parasitology 132:757–765

    Article  CAS  PubMed  Google Scholar 

  • Veneti Z, Bentley JK, Koana T et al (2005) A functional dosage compensation complex required for male killing in Drosophila. Science 307:1461–1463

    Article  CAS  PubMed  Google Scholar 

  • Visser S, Voleníková A, Nguyen P et al (2021) A conserved role of the duplicated Masculinizer gene in sex determination of the Mediterranean flour moth, Ephestia kuehniella. PLoS Genet 17:e1009420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang YH, Chen XE, Yang Y et al (2019) The Masc gene product controls masculinization in the black cutworm, Agrotis ipsilon. Insect Sci 26:1037–1044

    Article  CAS  PubMed  Google Scholar 

  • Watanabe K, Yukuhiro F, Matsuura Y et al (2014) Intrasperm vertical symbiont transmission. Proc Natl Acad Sci U S A 111:7433–7437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watanabe M, Kageyama D, Miura K (2013) Transfer of a parthenogenesis-inducing Wolbachia endosymbiont derived from Trichogramma dendrolimi into Trichogramma evanescens. J Invertebr Pathol 112:83–87

    Article  PubMed  Google Scholar 

  • Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751

    Article  CAS  PubMed  Google Scholar 

  • Whiting AR (1967) The biology of the parasitic Wasp Mormoniella vitripennis [=Nasonia brevicornis] (Walker). Q Rev Biol 42:333–406

    Article  Google Scholar 

  • Williamson DL, Poulson DF (1979) In: Whitcomb RF, Tully JG (eds) In the mycoplasmas, volume III: plant and insect mycoplasmas, pp 175–208

    Google Scholar 

  • Xu J, Chen S, Zeng B et al (2017a) Bombyx mori P-element somatic inhibitor (BmPSI) is a key auxiliary factor for silkworm male sex determination. PLoS Genet 13:e1006576

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu J, Zhan S, Chen S et al (2017b) Sexually dimorphic traits in the silkworm, Bombyx mori, are regulated by doublesex. Insect Biochem Mol Biol 80:42–51

    Article  CAS  PubMed  Google Scholar 

  • Zou Y, Geuverink E, Beukeboom LW et al (2020) A chimeric gene paternally instructs female sex determination in the haplodiploid wasp Nasonia. Science 370:1115–1118

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Takahiro Fukui and Fumiko Ishizuna for TEM sample preparation and data acquisition. This work was supported by Grants-in-Aid for Scientific Research on Innovative Areas “Spectrum of the Sex: a continuity of phenotypes between female and male” (17H06431) to S.K.

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Correspondence to Susumu Katsuma .

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Katsuma, S., Hirota, K., Muro, T. (2022). Symbiont-Induced Sexual and Reproductive Manipulation in Insects. In: Tanaka, M., Tachibana, M. (eds) Spectrum of Sex. Springer, Singapore. https://doi.org/10.1007/978-981-19-5359-0_11

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