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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Beckmann JF, Ronau JA, Hochstrasser M (2017) A Wolbachia deubiquitylating enzyme induces cytoplasmic incompatibility. Nat Microbiol 2:17007
Berec L, Maxin D, Bernhauerova V (2016) Male-killing bacteria as agents of insect pest control. J Appl Ecol 53:1270–1279
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
Bordenstein SR, Bordenstein SR (2016) Eukaryotic association module in phage WO genomes from Wolbachia. Nat Commun 7:13155
Charlat S, Hornett EA, Fullard JH et al (2007) Extraordinary flux in sex ratio. Science 317:214
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
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
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
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
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
Ellison C, Bachtrog D (2019) Contingency in the convergent evolution of a regulatory network: dosage compensation in Drosophila. PLoS Biol 17:e3000094
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
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
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
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
Hall AB, Basu S, Jiang X et al (2015) A male-determining factor in the mosquito Aedes aegypti. Science 348:1268–1270
Harumoto T, Anbutsu H, Fukatsu T (2014) Male-killing Spiroplasma induces sex-specific cell death via host apoptotic pathway. PLoS Pathog 10:e1003956
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
Harumoto T, Lemaitre B (2018) Male-killing toxin in a bacterial symbiont of Drosophila. Nature 557:252–255
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
Hasimoto H (1933) The role of the W-chromosome in the sex determination of Bombyx mori. Jpn J Genet 8:245–247
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
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
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
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
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
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
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
Hopkins BR, Kopp A (2021) Evolution of sexual development and sexual dimorphism in insects. Curr Opin Genet Dev 69:129–139
Hornett EA, Charlat S, Duplouy AM et al (2006) Evolution of male-killer suppression in a natural population. PLoS Biol 4:e283
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
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
Hurst GDD, Frost CL (2015) Reproductive parasitism: maternally inherited symbionts in a biparental world. Cold Spring Harb Perspect Biol 7:a017699
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
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
Kageyama D, Yoshimura K, Sugimoto TN et al (2017b) Maternally transmitted non-bacterial male killer in Drosophila biauraria. Biol Lett 13:20170476
Katsuma S, Shoji K, Sugano Y et al (2019) Masc-induced dosage compensation in silkworm cultured cells. FEBS Open Bio 9:1573–1579
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
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
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
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
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
Krzywinska E, Dennison NJ, Lycett GJ et al (2016) A maleness gene in the malaria mosquito Anopheles gambiae. Science 353:67–69
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
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
LePage DP, Metcalf JA, Bordenstein SR et al (2017) Prophage WO genes recapitulate and enhance Wolbachia-induced cytoplasmic incompatibility. Nature 543:243–247
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
Lucchesi JC (1978) Gene dosage compensation and the evolution of sex chromosomes. Science 202:711–716
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
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
Miyahara Y (1984) Abnormal sex ratio in Ostrinia furnacalis Guenée (Lepidoptera: Pyralidae). Jap J Appl Ent Zool 28:131–136
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
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
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
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
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
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
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
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
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
Regassa LB, Gasparich GE (2006) Spiroplasmas: evolutionary relationships and biodiversity. Front Biosci 11:2983–3002
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
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
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
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
Starr DJ, Cline TW (2002) A host parasite interaction rescues Drosophila oogenesis defects. Nature 418:76–79
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
Stouthamer R, Breeuwert JA, Luck RF et al (1993) Molecular identification of microorganisms associated with parthenogenesis. Nature 361:66–68
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
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
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
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
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
Tanaka Y (1916) Genetic studies in the silkworm. J Coll Agric Sapporo 6:1–33
Tinsley MC, Majerus MEN (2006) A new male-killing parasitism: Spiroplasma bacteria infect the ladybird beetle Anisosticta novemdecimpunctata (Coleoptera: Coccinellidae). Parasitology 132:757–765
Veneti Z, Bentley JK, Koana T et al (2005) A functional dosage compensation complex required for male killing in Drosophila. Science 307:1461–1463
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
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
Watanabe K, Yukuhiro F, Matsuura Y et al (2014) Intrasperm vertical symbiont transmission. Proc Natl Acad Sci U S A 111:7433–7437
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
Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751
Whiting AR (1967) The biology of the parasitic Wasp Mormoniella vitripennis [=Nasonia brevicornis] (Walker). Q Rev Biol 42:333–406
Williamson DL, Poulson DF (1979) In: Whitcomb RF, Tully JG (eds) In the mycoplasmas, volume III: plant and insect mycoplasmas, pp 175–208
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
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
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
Download citation
DOI: https://doi.org/10.1007/978-981-19-5359-0_11
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-19-5358-3
Online ISBN: 978-981-19-5359-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)