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Sexual Differentiation in Dragonflies and Damselflies

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Spectrum of Sex

Abstract

As represented by gynandromorphs (sexually mosaic individuals), sexual differentiation in insects proceeds primarily cell autonomously depending on sex chromosomes. Insect sex determination systems, although dominated by male heterogamety, are highly diverse. Dragonflies and damselflies (the order Odonata) are the most ancestral winged insects and have male heterogametic sex determination systems. Some species (e.g., Crocothemis servilia) have intraspecific polymorphisms in their karyotypes, such as switching from X0 to neo-XY sex chromosome system by chromosome fusion. In dragonflies and damselflies, adults of many species exhibit sexual color dimorphism, color transition upon adult maturation, and intraspecific color polymorphisms within the same sex. Molecular mechanisms underlying sex determination and sexual differentiation in insects have been investigated extensively in the fruit fly Drosophila melanogaster, but recent studies have revealed that the upstream genes of insect sex determination cascade are highly diverse. Most insects have sex-specific isoforms for doublesex (dsx) gene, which is important for sexual differentiation, and dsx gene plays important roles in masculinization not only for males but also for androchrome females in the damselfly Ischnura senegalensis. In this review, current knowledge on sex determination and sexual differentiation of insects is summarized, with particular focus on the most ancestral winged insects, dragonflies and damselflies.

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References

  • Aryan A, Anderson MAE, Biedler JK, Qi Y, Overcash JM, Naumenko AN, Sharakhova MV, Mao C, Adelman ZN, Tu Z (2020) Nix alone is sufficient to convert female Aedes aegypti into fertile males and myo-sex is needed for male flight. Proc Natl Acad Sci U S A 117(30):17702–17709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bachtrog D, Mank JE, Peichel CL, Kirkpatrick M, Otto SP, Ashman TL, Hahn MW, Kitano J, Mayrose I, Ming R, Perrin N, Ross L, Valenzuela N, Vamosi JC, Tree of Sex Consortium (2014) Sex determination: why so many ways of doing it? PLoS Biol 12(7):e1001899

    Article  PubMed  PubMed Central  Google Scholar 

  • Bear A, Monteiro A (2013) Both cell-autonomous mechanisms and hormones contribute to sexual development in vertebrates and insects. BioEssays 35(8):725–732

    Article  PubMed  Google Scholar 

  • Bergerard J (1972) Environmental and physiological control of sex determination and differentiation. Annu Rev Entomol 17:57–74

    Article  Google Scholar 

  • Beye M, Hasselmann M, Fondrk MK, Page RE, Omholt SW (2003) The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114(4):419–429

    Article  CAS  PubMed  Google Scholar 

  • Blackmon H, Demuth JP (2015) Coleoptera karyotype database. Coleopts Bull 69:174–175

    Article  Google Scholar 

  • Blackmon H, Ross L, Bachtrog D (2017) Sex determination, sex chromosomes, and karyotype evolution in insects. J Hered 108(1):78–93

    Article  CAS  PubMed  Google Scholar 

  • Blow R, Willink B, Svensson EI (2021) A molecular phylogeny of forktail damselflies (genus Ischnura) reveals a dynamic macroevolutionary history of female colour polymorphisms. Mol Phylogenet Evol 160:107134

    Article  PubMed  Google Scholar 

  • Bybee S, Córdoba-Aguilar A, Duryea MC, Futahashi R, Hansson B, Lorenzo-Carballa MO, Schilder R, Stoks R, Suvorov A, Svensson EI, Swaegers J, Takahashi Y, Watts PC, Wellenreuther M (2016) Odonata (dragonflies and damselflies) as a bridge between ecology and evolutionary genomics. Front Zool 13:46

    Article  PubMed  PubMed Central  Google Scholar 

  • Bybee SM, Kalkman VJ, Erickson RJ, Frandsen PB, Breinholt JW, Suvorov A, Dijkstra KB, Cordero-Rivera A, Skevington JH, Abbott JC, Sanchez Herrera M, Lemmon AR, Moriarty Lemmon E, Ware JL (2021) Phylogeny and classification of Odonata using targeted genomics. Mol Phylogenet Evol 160:107115

    Article  PubMed  Google Scholar 

  • Casper A, Van Doren M (2006) The control of sexual identity in the Drosophila germline. Development 133(15):2783–2791

    Article  CAS  PubMed  Google Scholar 

  • Chauhan P, Swaegers J, Sánchez-Guillén RA, Svensson EI, Wellenreuther M, Hansson B (2021) Genome assembly, sex-biased gene expression and dosage compensation in the damselfly Ischnura elegans. Genomics 113(4):1828–1837

    Article  CAS  PubMed  Google Scholar 

  • Chauhan P, Wellenreuther M, Hansson B (2016) Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression. BMC Genomics 17(1):985

    Article  PubMed  PubMed Central  Google Scholar 

  • Corbet PS (1999) Dragonflies, behavior and ecology of odonata. Cornell University Press

    Google Scholar 

  • Córdoba-Aguilar A, Cordero-Rivera A (2005) Evolution and ecology of Calopterygidae (Zygoptera: Odonata): status of knowledge and research perspectives. Neotro Entomol 34(6):861–879

    Article  Google Scholar 

  • Das S (2016) Vertebrate hormones in insects: the role of estrogen in silkworm – a review. Turk J Zool 40:297–302

    Article  CAS  Google Scholar 

  • de la Filia AG, Bain SA, Ross L (2015) Haplodiploidy and the reproductive ecology of arthropods. Curr Opin Insect Sci 9:36–43

    Article  PubMed  Google Scholar 

  • De Loof A (2006) Ecdysteroids: the overlooked sex steroids of insects? Males: the black box. Insect Sci 13:325–338

    Article  Google Scholar 

  • Denlinger DL, Brueggemeier RW, Mechoulam R, Katlic N, Yocum LB, Yocum GD (1987) Estrogens and androgens in insects. In: Law JH (ed) Molecular entomology. Alan R. Liss, New York, NY, USA, pp 189–199

    Google Scholar 

  • Dübendorfer A, Hediger M, Burghardt G, Bopp D (2002) Musca domestica, a window on the evolution of sex-determining mechanisms in insects. Int J Dev Biol 46(1):75–79

    PubMed  Google Scholar 

  • Erickson JW, Quintero JJ (2007) Indirect effects of ploidy suggest X chromosome dose, not the X:A ratio, signals sex in Drosophila. PLoS Biol 5(12):e332

    Article  PubMed  PubMed Central  Google Scholar 

  • Fincke OM, Jödicke R, Paulson DR, Schultz TD (2005) The evolution and frequency of female color morphs in Holarctic Odonata: why are male-like females typically the minority? Int J Odonatol 8:183–212

    Article  Google Scholar 

  • Fukui T, Kiuchi T, Shoji K, Kawamoto M, Shimada T, Katsuma S (2018) In vivo masculinizing function of the Ostrinia furnacalis Masculinizer gene. Biochem Biophys Res Commun 503(3):1768–1772

    Article  CAS  PubMed  Google Scholar 

  • Futahashi R (2011) A revisional study of Japanese dragonflies based on DNA analysis. Tombo 53:59–66

    Google Scholar 

  • Futahashi R (2016) Color vision and color formation in dragonflies. Curr Opin Insect Sci 17:32–39

    Article  PubMed  Google Scholar 

  • Futahashi R (2017) Molecular mechanisms underlying color vision and color formation in dragonflies. In: Sekimura T, Nijhout HF (eds) Diversity and evolution of butterfly wing patterns: an integrative approach. Springer, Singapore, pp 303–321

    Chapter  Google Scholar 

  • Futahashi R (2020) Diversity of UV reflection patterns in Odonata. Front Ecol Evol 8:201

    Article  Google Scholar 

  • Futahashi R, Kawahara-Miki R, Kinoshita M, Yoshitake K, Yajima S, Arikawa K, Fukatsu T (2015) Extraordinary diversity of visual opsin genes in dragonflies. Proc Natl Acad Sci U S A 112(11):E1247–E1256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Futahashi R, Kurita R, Mano H, Fukatsu T (2012) Redox alters yellow dragonflies into red. Proc Natl Acad Sci U S A 109(31):12626–12631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Futahashi R, Osanai-Futahashi M (2021) Pigments in insects. In: Hashimoto H, Goda M, Futahashi R, Kelsh R, Akiyama T (eds) Pigments, pigment cells, and pigment patterns. Springer, Singapore, pp 3–43

    Chapter  Google Scholar 

  • Futahashi R, Yamahama Y, Kawaguchi M, Mori N, Ishii D, Okude G, Hirai Y, Kawahara-Miki R, Yoshitake K, Yajima S, Hariyama T, Fukatsu T (2019) Molecular basis of wax-based color change and UV reflection in dragonflies. eLife 8:e43045

    Article  PubMed  PubMed Central  Google Scholar 

  • Gardner A, Ross L (2011) The evolution of hermaphroditism by an infectious male-derived cell lineage: an inclusive-fitness analysis. Am Nat 178:191–201

    Article  PubMed  Google Scholar 

  • Gempe T, Beye M (2010) Function and evolution of sex determination mechanisms, genes and pathways in insects. BioEssays 33(1):52–60

    Article  Google Scholar 

  • Gempe T, Hasselmann M, Schiøtt M, Hause G, Otte M, Beye M (2009) Sex determination in honeybees: two separate mechanisms induce and maintain the female pathway. PLoS Biol 7(10):e1000222

    Article  PubMed  PubMed Central  Google Scholar 

  • Gotoh H, Miyakawa H, Ishikawa A, Ishikawa Y, Sugime Y, Emlen DJ, Lavine LC, Miura T (2014) Developmental link between sex and nutrition; doublesex regulates sex-specific mandible growth via juvenile hormone signaling in stag beetles. PLoS Genet 10(1):e1004098

    Article  PubMed  PubMed Central  Google Scholar 

  • Gotoh H, Zinna RA, Warren I, DeNieu M, Niimi T, Dworkin I, Emlen DJ, Miura T, Lavine LC (2016) Identification and functional analyses of sex determination genes in the sexually dimorphic stag beetle Cyclommatus metallifer. BMC Genomics 17:250

    Article  PubMed  PubMed Central  Google Scholar 

  • Hall AB, Basu S, Jiang X, Qi Y, Timoshevskiy VA, Biedler JK, Sharakhova MV, Elahi R, Anderson MA, Chen XG, Sharakhov IV, Adelman ZN, Tu Z (2015) A male-determining factor in the mosquito Aedes aegypti. Science 348(6240):1268–1270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harvey-Samuel T, Norman VC, Carter R, Lovett E, Alphey L (2020) Identification and characterization of a Masculinizer homologue in the diamondback moth Plutella xylostella. Insect Mol Biol 29(2):231–240

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto 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, Gempe T, Schiøtt M, Nunes-Silva CG, Otte M, Beye M (2008) Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees. Nature 454(7203):519–522

    Article  CAS  PubMed  Google Scholar 

  • Hediger M, Henggeler C, Meier N, Perez R, Saccone G, Bopp D (2010) Molecular characterization of the key switch F provides a basis for understanding the rapid divergence of the sex-determining pathway in the housefly. Genetics 184(1):155–170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higashi K, Kayano H (1993) The distribution of distinct karyomorphs of Crocothemis servilia Drury (Anisoptera, Libellulidae) in Kyushu and the south-western islands of Japan. Japanese J Entomol 61:1–10

    Google Scholar 

  • Higashi K, Lee CE, Kayano H, Kayano A (2001) Korea strait delimiting distribution of distinct karyomorphs of Crocothemis servilia (Drury) (Anisoptera: Libellulidae). Odonatologica 30(3):265–270

    Google Scholar 

  • Hodson CN, Hamilton PT, Dilworth D, Nelson CJ, Curtis CI, Perlman SJ (2017) Paternal genome elimination in Liposcelis booklice (Insecta: Psocodea). Genetics 206(2):1091–1100

    Article  CAS  PubMed  PubMed Central  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 

  • Ito Y, Harigai A, Nakata M, Hosoya T, Araya K, Oba Y, Ito A, Ohde T, Yaginuma T, Niimi T (2013) The role of doublesex in the evolution of exaggerated horns in the Japanese rhinoceros beetle. EMBO Rep 14(6):561–567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katatani N (1987) On the chromosomes of dragonflies, 1. Synopsis on the studies in some Japanese dragonflies. Aeschna 20:21–31

    Google Scholar 

  • Kato Y, Kobayashi K, Oda S, Tatarazako N, Watanabe H, Iguchi T (2010) Sequence divergence and expression of a transformer gene in the branchiopod crustacean, Daphnia magna. Genomics 95(3):160–165

    Article  CAS  PubMed  Google Scholar 

  • Kato Y, Kobayashi K, Watanabe H, Iguchi T (2011) Environmental sex determination in the branchiopod crustacean Daphnia magna: deep conservation of a Doublesex gene in the sex-determining pathway. PLoS Genet 7(3):e1001345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keller Valsecchi CI, Marois E, Basilicata MF, Georgiev P, Akhtar A (2021) Distinct mechanisms mediate X chromosome dosage compensation in Anopheles and Drosophila. Life Sci Alliance 4(9):e202000996

    Article  PubMed  PubMed Central  Google Scholar 

  • Kiauta B (1967) Considerations on the evolution of the chromosome complement in Odonata. Genetica 38(4):430–446

    Article  Google Scholar 

  • Kiauta B (1969a) Sex chromosomes and sex determining mechanisms in Odonata, with a review of the cytological conditions in the family Gomphidae, and reference to the karyotypic evolution in the order. Genetica 40(2):127–157

    Article  CAS  PubMed  Google Scholar 

  • Kiauta B (1969b) Autosomal fragmentations and fusions in Odonata and their evolutionary implications. Genetica 40(2):158–180

    Article  CAS  PubMed  Google Scholar 

  • Kiauta B (1972) Synopsis on the main cytotaxonomic data in the order Odonata. Odonatologica 1(2):73–102

    Google Scholar 

  • Kiauta B (1983) The status of the Japanese Crocothemis servilia (Drury) as revealed by karyotypic morphology (Anisoptera: Libellulidae). Odonatologica 12:381–388

    Google Scholar 

  • Kiauta B, Kiauta M (1982) List of species, with chromosome numbers and preliminary notes on the karyotypes of the Odonata, collected in May, 1979 and August, 1980 by the members of the Kansai Research Group of Odonatology, and examined by B. and M. Kiauta. Report for the Kansai Research Group of Odonatology, Osaka. Mimeographed. 8pp. Soc. Int. Odonatol., Utrecht

    Google Scholar 

  • Kiuchi T, Koga H, Kawamoto M, Shoji K, Sakai H, Arai Y, Ishihara G, Kawaoka S, Sugano S, Shimada T, Suzuki Y, Suzuki MG, Katsuma S (2014) A single female-specific piRNA is the primary determiner of sex in the silkworm. Nature 509(7502):633–636

    Article  CAS  PubMed  Google Scholar 

  • Krzywinska E, Dennison NJ, Lycett GJ, Krzywinski J (2016) A maleness gene in the malaria mosquito Anopheles gambiae. Science 353(6294):67–69

    Article  CAS  PubMed  Google Scholar 

  • Krzywinska E, Ferretti L, Li J, Li JC, Chen CH, Krzywinski J (2021) femaleless controls sex determination and dosage compensation pathways in females of Anopheles mosquitoes. Curr Biol 31(5):1084–1091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kunte K, Zhang W, Tenger-Trolander A, Palmer DH, Martin A, Reed RD, Mullen SP, Kronforst MR (2014) doublesex is a mimicry supergene. Nature 507(7491):229–232

    Article  CAS  PubMed  Google Scholar 

  • Kuznetsova VG, Golub NV (2020) A checklist of chromosome numbers and a review of karyotype variation in Odonata of the world. Comp Cytogenet 14(4):501–540

    Article  PubMed  PubMed Central  Google Scholar 

  • Laslo M, Just J, Angelini DR (2022) Theme and variation in the evolution of insect sex determination. J Exp Zool B Mol Dev Evol. https://doi.org/10.1002/jez.b.23125

  • Lee J, Kiuchi T, Kawamoto M, Shimada T, Katsuma S (2015) Identification and functional analysis of a Masculinizer orthologue in Trilocha varians (Lepidoptera: Bombycidae). Insect Mol Biol 24(5):561–569

    Article  CAS  PubMed  Google Scholar 

  • Martens A, Wildermuth H (2021) Gynandromorphism and intersexuality in Odonata: a review. Odonatologica 50(1/2):65–80

    Google Scholar 

  • Meccariello A, Salvemini M, Primo P, Hall B, Koskinioti P, Dalíková M, Gravina A, Gucciardino MA, Forlenza F, Gregoriou ME, Ippolito D, Monti SM, Petrella V, Perrotta MM, Schmeing S, Ruggiero A, Scolari F, Giordano E, Tsoumani KT, Marec F, Windbichler N, Arunkumar KP, Bourtzis K, Mathiopoulos KD, Ragoussis J, Vitagliano L, Tu Z, Papathanos PA, Robinson MD, Saccone G (2019) Maleness-on-the-Y (MoY) orchestrates male sex determination in major agricultural fruit fly pests. Science 365(6460):1457–1460

    Article  CAS  PubMed  Google Scholar 

  • Mechoulam R, Brueggemeier RW, Denlinger DL (1984) Estrogens in insects. Experientia 40:942–944

    Article  CAS  Google Scholar 

  • Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, Frandsen PB, Ware J, Flouri T, Beutel RG, Niehuis O, Petersen M, Izquierdo-Carrasco F, Wappler T, Rust J, Aberer AJ, Aspöck U, Aspöck H, Bartel D, Blanke A, Berger S, Böhm A, Buckley TR, Calcott B, Chen J, Friedrich F, Fukui M, Fujita M, Greve C, Grobe P, Gu S, Huang Y, Jermiin LS, Kawahara AY, Krogmann L, Kubiak M, Lanfear R, Letsch H, Li Y, Li Z, Li J, Lu H, Machida R, Mashimo Y, Kapli P, McKenna DD, Meng G, Nakagaki Y, Navarrete-Heredia JL, Ott M, Ou Y, Pass G, Podsiadlowski L, Pohl H, von Reumont BM, Schütte K, Sekiya K, Shimizu S, Slipinski A, Stamatakis A, Song W, Su X, Szucsich NU, Tan M, Tan X, Tang M, Tang J, Timelthaler G, Tomizuka S, Trautwein M, Tong X, Uchifune T, Walzl MG, Wiegmann BM, Wilbrandt J, Wipfler B, Wong TK, Wu Q, Wu G, Xie Y, Yang S, Yang Q, Yeates DK, Yoshizawa K, Zhang Q, Zhang R, Zhang W, Zhang Y, Zhao J, Zhou C, Zhou L, Ziesmann T, Zou S, Li Y, Xu X, Zhang Y, Yang H, Wang J, Wang J, Kjer KM, Zhou X (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science 346(6210):763–767

    Article  CAS  PubMed  Google Scholar 

  • Miyazaki S, Fujiwara K, Kai K, Masuoka Y, Gotoh H, Niimi T, Hayashi Y, Shigenobu S, Maekawa K (2021) Evolutionary transition of doublesex regulation from sex-specific splicing to male-specific transcription in termites. Sci Rep 11(1):15992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mola LM (2007) Cytogenetics of American Odonata. In: Tyagi BK (ed) Odonata: biology of dragonflies. Scientific Publishers, India, pp 153–173

    Google Scholar 

  • Mola LM, Papeschi AG, Carrillo ET (1999) Cytogenetics of seven species of dragonflies. A novel sex chromosome determining system in Micrathyria ungulate. Hereditas 131:147–153

    Article  Google Scholar 

  • Morita S, Ando T, Maeno A, Mizutani T, Mase M, Shigenobu S, Niimi T (2019) Precise staging of beetle horn formation in Trypoxylus dichotomus reveals the pleiotropic roles of doublesex depending on the spatiotemporal developmental contexts. PLoS Genet 15(4):e1008063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narita S, Pereira RAS, Kjellberg F, Kageyama D (2010) Gynandromorphs and intersexes: potential to understand the mechanism of sex determination in arthropods. Terr Arthropod Rev 3:63–96

    Article  Google Scholar 

  • Nishikawa H, Iijima T, Kajitani R, Yamaguchi J, Ando T, Suzuki Y, Sugano S, Fujiyama A, Kosugi S, Hirakawa H, Tabata S, Ozaki K, Morimoto H, Ihara K, Obara M, Hori H, Itoh T, Fujiwara H (2015) A genetic mechanism for female-limited Batesian mimicry in Papilio butterfly. Nat Genet 47(4):405–409

    Article  CAS  PubMed  Google Scholar 

  • Nissen I, Müller M, Beye M (2012) The Am-tra2 gene is an essential regulator of female splice regulation at two levels of the sex determination hierarchy of the honeybee. Genetics 192(3):1015–1026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nokkala S, Laukkanen A, Nokkala C (2002) Mitotic and meiotic chromosomes in Somatochlora metallica (Corduliidae, Odonata). The absence of localized centromeres and inverted meiosis. Hereditas 136:7–12

    Article  PubMed  Google Scholar 

  • Normark BB (2003) The evolution of alternative genetic systems in insects. Annu Rev Entomol 48:397–423

    Article  CAS  PubMed  Google Scholar 

  • Normark BB (2014) Modes of reproduction. In: Shuker D, Simmons L (eds) The evolution of insect mating systems. University Press Oxford, Oxford (UK), pp 1–19

    Google Scholar 

  • Ohbayashi F, Suzuki MG, Mita K, Okano K, Shimada T (2001) A homologue of the Drosophila doublesex gene is transcribed into sex-specific mRNA isoforms in the silkworm, Bombyx mori. Comp Biochem Physiol B Biochem Mol Biol 128(1):145–158

    Article  CAS  PubMed  Google Scholar 

  • Okude G, Fukatsu T, Futahashi R (2020) Interspecific crossing between blue-tailed damselflies Ischnura elegans and I. senegalensis in the laboratory. Entomol Sci 23:165–172

    Article  Google Scholar 

  • Okude G, Fukatsu T, Futahashi R (2021) Electroporation-mediated RNA interference method in Odonata. J Vis Exp 168:e61952

    Google Scholar 

  • Okude G, Futahashi R (2021) Pigmentation and color pattern diversity in Odonata. Curr Opin Genet Dev 69:14–20

    Article  CAS  PubMed  Google Scholar 

  • Okude G, Moriyama M, Kawahara-Miki R, Yajima S, Fukatsu T, Futahashi R (2022) Molecular mechanisms underlying metamorphosis in the most-ancestral winged insect. Proc Natl Acad Sci U S A 119(9):e2114773119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ozono A, Kawashima I, Futahashi R (2021) Dragonflies of Japan, Revised edition. Bunichi-Sogo Syuppan., Co. Ltd, Tokyo

    Google Scholar 

  • Pane A, Salvemini M, Delli Bovi P, Polito C, Saccone G (2002) The transformer gene in Ceratitis capitata provides a genetic basis for selecting and remembering the sexual fate. Development 129(15):3715–3725

    Article  CAS  PubMed  Google Scholar 

  • Papeschi AG, Bressa MJ (2006) Evolutionary cytogenetics in Heteroptera. J Biol Res 5:3–21

    CAS  Google Scholar 

  • Poggio MG, Bressa MJ, Papeschi AG (2007) Karyotype evolution in Reduviidae (Insecta: Heteroptera) with special reference to Stenopodainae and Harpactorinae. Comp Cytogenet 1(2):159–168

    Google Scholar 

  • Qi Y, Wu Y, Saunders R, Chen XG, Mao C, Biedler JK, Tu ZJ (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 

  • Riddiford LM (2012) How does juvenile hormone control insect metamorphosis and reproduction? Gen Comp Endocrinol 179(3):477–484

    Article  CAS  PubMed  Google Scholar 

  • Ross L, Pen I, Shuker DM (2010) Genomic conflict in scale insects: the causes and consequences of bizarre genetic systems. Biol Rev 85:807–828

    PubMed  Google Scholar 

  • Ruiz MF, Esteban MR, Doñoro C, Goday C, Sánchez L (2000) Evolution of dosage compensation in Diptera: the gene maleless implements dosage compensation in Drosophila (Brachycera suborder) but its homolog in sciara (Nematocera suborder) appears to play no role in dosage compensation. Genetics 156(4):1853–1865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakai H, Oshima H, Yuri K, Gotoh H, Daimon T, Yaginuma T, Sahara K, Niimi T (2019) Dimorphic sperm formation by sex-lethal. Proc Natl Acad Sci U S A 116(21):10412–10417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakai H, Sakaguchi H, Aoki F, Suzuki MG (2015) Functional analysis of sex-determination genes by gene silencing with LNADNA gapmers in the silkworm, Bombyx mori. Mech Dev 137:45–52

    Article  CAS  PubMed  Google Scholar 

  • Salvemini M, Polito C, Saccone G (2010) fruitless alternative splicing and sex behaviour in insects: an ancient and unforgettable love story? J Genet 89(3):287–289

    Article  PubMed  Google Scholar 

  • Sánchez L (2008) Sex-determining mechanisms in insects. Int J Dev Biol 52(7):837–856

    Article  PubMed  Google Scholar 

  • Sánchez-Guillén RA, Fadia-Ceccarelli S, Villalobos F, Neupane S, Rivas-Torres A, Sanmartín-Villar I, Wellenreuther M, Bybee SM, Velásquez-Vélez M, Realpe E, Chávez-Ríos JR, Dumont HJ, Cordero-Rivera A (2020) The evolutionary history of colour polymorphism in Ischnura damselflies (Odonata: Coenagrionidae). Odonatologica 49:333–370

    Google Scholar 

  • Sharma A, Heinze SD, Wu Y, Kohlbrenner T, Morilla I, Brunner C, Wimmer EA, van de Zande L, Robinson MD, Beukeboom LW, Bopp D (2017) Male sex in houseflies is determined by Mdmd, a paralog of the generic splice factor gene CWC22. Science 356(6338):642–645

    Article  CAS  PubMed  Google Scholar 

  • Shukla JN, Palli SR (2012a) Sex determination in beetles: production of all male progeny by parental RNAi knockdown of transformer. Sci Rep 2:602

    Article  PubMed  PubMed Central  Google Scholar 

  • Shukla JN, Palli SR (2012b) Doublesex target genes in the red flour beetle, Tribolium castaneum. Sci Rep 2:948

    Article  PubMed  PubMed Central  Google Scholar 

  • Shukla JN, Palli SR (2013) Tribolium castaneum Transformer-2 regulates sex determination and development in both males and females. Insect Biochem Mol Biol 43(12):1125–1132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shukla JN, Palli SR (2014) Production of all female progeny: evidence for the presence of the male sex determination factor on the Y chromosome. J Exp Biol 217(Pt 10):1653–1655

    PubMed  PubMed Central  Google Scholar 

  • Siegal ML, Baker BS (2005) Functional conservation and divergence of intersex, a gene required for female differentiation in Drosophila melanogaster. Dev Genes Evol 215(1):1–12

    Article  PubMed  Google Scholar 

  • Suzuki KJ, Saitoh K (1990) A revised chromosome study of Japanese Odonates (II). Chromosomes of 13 species belonging to two families. Sci Rep Hirosaki Univ 37(2):111–123

    Google Scholar 

  • Suzuki MG, Ohbayashi F, Mita K, Shimada T (2001) The mechanism of sex-specific splicing at the doublesex gene is different between Drosophila melanogaster and Bombyx mori. Insect Biochem Mol Biol 31(12):1201–1211

    Article  CAS  PubMed  Google Scholar 

  • Suzuki MG, Funaguma S, Kanda T, Tamura T, Shimada T (2003) Analysis of the biological functions of a doublesex homologue in Bombyx mori. Dev Genes Evol 213(7):345–354

    Article  CAS  PubMed  Google Scholar 

  • Suzuki MG, Funaguma S, Kanda T, Tamura T, Shimada T (2005) Role of the male BmDSX protein in the sexual differentiation of Bombyx mori. Evol Dev 7(1):58–68

    Article  CAS  PubMed  Google Scholar 

  • Suzuki MG, Imanishi S, Dohmae N, Nishimura T, Shimada T, Matsumoto S (2008) Establishment of a novel in vivo sex-specific splicing assay system to identify a trans-acting factor that negatively regulates splicing of Bombyx mori dsx female exons. Mol Cell Biol 28(1):333–343

    Article  CAS  PubMed  Google Scholar 

  • Suzuki MG, Imanishi S, Dohmae N, Asanuma M, Matsumoto S (2010) Identification of a male-specific RNA binding protein that regulates sex-specific splicing of Bmdsx by increasing RNA binding activity of BmPSI. Mol Cell Biol 30(24):5776–5786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki MG, Kobayashi S, Aoki F (2014) Male-specific splicing of the silkworm Imp gene is maintained by an autoregulatory mechanism. Mech Dev 131:47–56

    Article  CAS  PubMed  Google Scholar 

  • Suzuki MG, Suzuki K, Aoki F, Ajimura M (2012) Effect of RNAi-mediated knockdown of the Bombyx mori transformer-2 gene on the sex-specific splicing of Bmdsx pre-mRNA. Int J Dev Biol 56(9):693–699

    Article  CAS  PubMed  Google Scholar 

  • Svensson EI (2017) Back to basics: using colour polymorphisms to study evolutionary processes. Mol Ecol 26:2204–2211

    Article  PubMed  Google Scholar 

  • Svensson EI, Abbott JK, Gosden TP, Coreau A (2009) Female polymorphisms, sexual conflict and limits to speciation processes in animals. Evol Ecol 23:93–108

    Article  Google Scholar 

  • Takahashi M, Okude G, Futahashi R, Takahashi Y, Kawata M (2021) The effect of the doublesex gene in body colour masculinization of the damselfly Ischnura senegalensis. Biol Lett 17(6):20200761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi M, Takahashi Y, Kawata M (2019) Candidate genes associated with color morphs of female-limited polymorphisms of the damselfly Ischnura senegalensis. Heredity 122(1):81–92

    Article  CAS  PubMed  Google Scholar 

  • Tillyard RJ (1917) The biology of dragonflies. Cambridge University Press, Cambridge

    Google Scholar 

  • Traut W, Marec F (1996) Sex chromatin in Lepidoptera. Q Rev Biol 71(2):239–256

    Article  CAS  PubMed  Google Scholar 

  • Traut W, Sahara K, Marec F (2007) Sex chromosomes and sex determination in Lepidoptera. Sex Dev 1(6):332–346

    Article  CAS  PubMed  Google Scholar 

  • Tree of Sex Consortium (2014) Tree of sex: a database of sexual systems. Sci Data 1:140015

    Article  Google Scholar 

  • Verhulst EC, van de Zande L, Beukeboom LW (2010a) Insect sex determination: it all evolves around transformer. Curr Opin Genet Dev 20(4):376–383

    Article  CAS  PubMed  Google Scholar 

  • Verhulst EC, Beukeboom LW, van de Zande L (2010b) Maternal control of haplodiploid sex determination in the wasp Nasonia. Science 328(5978):620–623

    Article  CAS  PubMed  Google Scholar 

  • Vershinina AO, Kuznetsova VG (2016) Parthenogenesis in Hexapoda: Entognatha and non-holometabolous insects. J Zool Syst Evol Res 54:257–268

    Article  Google Scholar 

  • Visser S, Voleníková A, Nguyen P, Verhulst EC, Marec F (2021) A conserved role of the duplicated Masculinizer gene in sex determination of the Mediterranean flour moth, Ephestia kuehniella. PLoS Genet 17(8):e1009420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang YH, Chen XE, Yang Y, Xu J, Fang GQ, Niu CY, Huang YP, Zhan S (2019) The Masc gene product controls masculinization in the black cutworm. Agrotis ipsilon Insect Sci 26(6):1037–1044

    Article  CAS  PubMed  Google Scholar 

  • Wang YH, Engel MS, Rafael JA, Wu HY, Rédei D, Xie Q, Wang G, Liu XG, Bu WJ (2016) Fossil record of stem groups employed in evaluating the chronogram of insects (Arthropoda: Hexapoda). Sci Rep 6:38939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watanabe T (2019) Evolution of the neural sex-determination system in insects: does fruitless homologue regulate neural sexual dimorphism in basal insects? Insect Mol Biol 28(6):807–827

    Article  CAS  PubMed  Google Scholar 

  • Went DF, Camenzind R (1984) Sex determination in the dipteran insect Heteropeza pygmaea. Genetica 52(1):373–377

    Article  Google Scholar 

  • Wexler J, Delaney EK, Belles X, Schal C, Wada-Katsumata A, Amicucci MJ, Kopp A (2019) Hemimetabolous insects elucidate the origin of sexual development via alternative splicing. Elife 8:e47490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willhoeft U, Franz G (1996) Identification of the sex-determining region of the Ceratitis capitata Y chromosome by deletion mapping. Genetics 144:737–745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willink B, Duryea MC, Svensson EI (2019) Macroevolutionary origin and adaptive function of a polymorphic female signal involved in sexual conflict. Am Nat 194:707–724

    Article  PubMed  Google Scholar 

  • Willink B, Duryea MC, Wheat C, Svensson EI (2020) Changes in gene expression during female reproductive development in a color polymorphic insect. Evolution 74(6):1063–1081

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Liu W, Yang D, Chen S, Chen K, Liu Z, Yang X, Meng J, Zhu G, Dong S, Zhang Y, Zhan S, Wang G, Huang Y (2020) Regulation of olfactory-based sex behaviors in the silkworm by genes in the sex-determination cascade. PLoS Genet 16(6):e1008622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Yu Y, Chen K, Huang Y (2019) Intersex regulates female external genital and imaginal disc development in the silkworm. Insect Biochem Mol Biol 108:1–8

    Article  CAS  PubMed  Google Scholar 

  • Zheng ZZ, Sun X, Zhang B, Pu J, Jiang ZY, Li M, Fan YJ, Xu YZ (2019) Alternative splicing regulation of doublesex gene by RNA-binding proteins in the silkworm Bombyx mori. RNA Biol 16(6):809–820

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhuo JC, Hu QL, Zhang HH, Zhang MQ, Jo SB, Zhang CX (2018) Identification and functional analysis of the doublesex gene in the sexual development of a hemimetabolous insect, the brown planthopper. Insect Biochem Mol Biol 102:31–42

    Article  CAS  PubMed  Google Scholar 

  • Zhuo JC, Zhang HH, Hu QL, Zhang JL, Lu JB, Li HJ, Xie YC, Wang WW, Zhang Y, Wang HQ, Huang HJ, Lu G, Chen JP, Li JM, Tu ZJ, Zhang CX (2021) A feminizing switch in a hemimetabolous insect. Sci Adv 7(48):eabf9237

    Article  PubMed  PubMed Central  Google Scholar 

  • Zou Y, Geuverink E, Beukeboom LW, Verhulst EC, van de Zande L (2020) A chimeric gene paternally instructs female sex determination in the haplodiploid wasp Nasonia. Science 370(6520):1115–1118

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The author would like to thank Mitsutoshi Sugimura for photograph of gynandromorphic dragonfly and damselfly, Genta Okude and Mizuko Osanai-Futahashi for helpful comments of the manuscript. The writing was partly supported by JSPS KAKENHI (JP18H02491 and JP20H04936).

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Futahashi, R. (2022). Sexual Differentiation in Dragonflies and Damselflies. In: Tanaka, M., Tachibana, M. (eds) Spectrum of Sex. Springer, Singapore. https://doi.org/10.1007/978-981-19-5359-0_2

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