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Environmental Control of Sex Differentiation in Daphnia

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Reproductive and Developmental Strategies

Part of the book series: Diversity and Commonality in Animals ((DCA))

Abstract

The cladoceran crustacean genus Daphnia (daphnids) exhibits a unique reproductive strategy in response to changes in environmental conditions of their habitat. This is known as environmental sex determination (ESD). Under favorable environmental conditions, daphnids produce clonal female offspring by parthenogenesis. Under unfavorable environmental conditions (e.g., short day length, low temperature, food shortage, overpopulation, and/or a combination thereof), daphnids produce male offspring by parthenogenesis and then switch reproductive methods to undergo sexual reproduction. Based on pharmacological and molecular experiments, the juvenile hormone pathway and doublesex1 gene have been identified as responsible factors in the process of ESD and subsequent sexual differentiation in daphnids. Furthermore, morphological observations of the detailed developmental processes that occur during female and male embryogenesis have been made. Despite substantial efforts in studies of the regulatory mechanisms governing sexual differentiation, there remains a large knowledge gap. In this chapter, we provide background information and recent progress in these research fields and present an overview of current knowledge regarding ESD and sexual differentiation in daphnids, mainly focusing on Daphnia pulex and D. magna.

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References

  • Adamowicz SJ, Petrusek A, Colbourne JK, Hebert PDN, Witt JDS (2009) The scale of divergence: a phylogenetic appraisal of intercontinental allopatric speciation in a passively dispersed freshwater zooplankton genus. Mol Phylogenet Evol 50:423–436

    Article  PubMed  Google Scholar 

  • Alekseev VR, Lajus DL (2009) Maternal and direct effects of natural-like changes of photoperiod and food condition manipulation on life history parameters in Daphnia. Aquat Ecol 43:415–421

    Article  Google Scholar 

  • Alekseev V, Lampert W (2001) Maternal control of resting-egg production in Daphnia. Nature 414:899–901

    Article  PubMed  CAS  Google Scholar 

  • Asada M, Kato Y, Matsuura T, Watanabe H (2014) Early embryonic expression of a putative ecdysteroid-phosphate phosphatase in the water flea, Daphnia magna (Cladocera: Daphniidae). J Insect Sci 14(181):181

    PubMed  PubMed Central  Google Scholar 

  • Banta AM, Brown LA (1929) Control of sex in Cladocera. II. The unstable nature of the excretory products involved in male production. Physiol Zool 2(1):93–98

    Article  CAS  Google Scholar 

  • Barton NH, Charlesworth B (1998) Why sex and recombination? Science 281(5385):1986–1990

    Article  PubMed  CAS  Google Scholar 

  • Bayrer JR, Zhang W, Weiss MA (2005) Dimerization of doublesex is mediated by a cryptic ubiquitin-associated domain fold: implications for sex-specific gene regulation. J Biol Chem 280(38):32989–32996

    Article  PubMed  CAS  Google Scholar 

  • Begum M, Breuer M, Kodrik D, Rahman MM, Loof AD (2004) The NMDA receptor antagonist MK-801 inhibits vitellogenesis in the flesh fly Neobellieria bullata and in the desert locust Schistocerca gregaria. J Insect Physiol 50(10):927–934

    Article  PubMed  CAS  Google Scholar 

  • Burtis KC, Baker BS (1989) Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56:997–1010

    Article  PubMed  CAS  Google Scholar 

  • Caceres CE (1998) Interspecific variation in the abundance, production, and emerence of Daphnia diapuasing eggs. Ecology 79(5):1699–1710

    Article  Google Scholar 

  • Cassier P (1979) The corpora allata of insects. Int Rev Cytol 57:1–73

    Article  Google Scholar 

  • Charles J-P, Iwema T, Epa VC, Takaki K, Rynes J, Jindra M (2011) Ligand-binding properties of a juvenile hormone receptor, methoprene-tolerant. Proc Natl Acad Sci U S A 108(52):21128–21133

    Article  PubMed  PubMed Central  Google Scholar 

  • Chiang A-S, Lin W-Y, Liu H-P, Pszczolkowski MA, T-F F, Chiu S-L, Holbrook GL (2002) Insect NMDA receptors mediate juvenile hormone biosynthesis. Proc Natl Acad Sci U S A 99(1):37–42

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Colbourne JK, Pfrender ME, Gilbert D, Thomas WK, Tucker A, Oakley TH, Tokishita S, Aerts A, Arnold GJ, Basu MK, Bauer DJ, Cáceres CE, Carmel L, Casola C, Choi J-H, Detter JC, Dong Q, Dusheyko S, Eads BD, Fröhlich T, Geiler-Samerotte KA, Gerlach D, Hatcher P, Jogdeo S, Krijgsveld J, Kriventseva EV, Kültz D, Laforsch C, Lindquist E, Lopez J, Manak JR, Muller J, Pangilinan J, Patwardhan RP, Pitluck S, Pritham EJ, Rechtsteiner A, Rho M, Rogozin IB, Sakarya O, Salamov A, Schaack S, Shapiro H, Shiga Y, Skalitzky C, Smith Z, Souvorov A, Sung W, Tang Z, Tsuchiya D, Tu H, Vos H, Wang M, Wolf YI, Yamagata H, Yamada T, Ye Y, Shaw JR, Andrews J, Crease TJ, Tang H, Lucas SM, Robertson HM, Bork P, Koonin EV, Zdobnov EM, Grigoriev IV, Lynch M, Boore JL (2011) The ecoresponsive genome of Daphnia pulex. Science 331(6017):555–561

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Corbitt TS, Hardie J (1985) Juvenile hormone effects on polymorphism in the pea aphid, Acyrthosiphon pisum. Entomol Exp Appl 38:131–135

    Article  Google Scholar 

  • Cristescu MEA, Colbourne JK, Radivojac J, Lynch M (2006) A microsatellite-based genetic linkage map of the waterflea, Daphnia pulex: on the prospect of crustacean genomics. Genomics 88:415–430

    Article  PubMed  CAS  Google Scholar 

  • Cui Y, Sui Y, Xu J, Zhu F, Palli SR (2014) Juvenile hormone regulates Aedes aegypti Krüppel homolog 1 through a conserved E box motif. Insect Biochem Mol Biol 52:23–32

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Daimon T, Shinoda T (2013) Function, diversity, and application of insect juvenile hormone epoxidases (CYP15). Biotechnol Appl Biochem 60(1):82–91

    Article  PubMed  CAS  Google Scholar 

  • de Kort CAD, Granger NA (1981) Regulation of the juvenile hormone titer. Annu Rev Entomol 26:1–28

    Article  Google Scholar 

  • Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93–122

    Article  PubMed  CAS  Google Scholar 

  • Eads BD, Colbourne JK, Bohuski E, Andrews J (2007) Profiling sex-biased gene expression during parthenogenetic reproduction in Daphnia pulex. BMC Genomics 8:464

    Article  PubMed  PubMed Central  Google Scholar 

  • Eads BD, Andrews J, Colbourne JK (2008) Ecological genomics in Daphnia: stress responses and environmental sex determination. Heredity 100:184–190

    Article  PubMed  CAS  Google Scholar 

  • Emlen DJ, Nijhout HF (1999) Hormonal control of male horn length dimorphism in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae). J Insect Physiol 45:45–53

    Article  PubMed  CAS  Google Scholar 

  • Fröhlich T, Arnold GJ, Fritsch R, Mayr T, Laforsch C (2009) LC-MS/MS-based proteome profiling in Daphnia pulex and Daphnia longicephala: the Daphnia pulex genome database as a key for high throughput proteomics in Daphnia. BMC Genomics 10:171

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gao N, Schantz MV, Foster RG, Hardie J (1999) The putative brain photoperiodic photoreceptors in the vetch aphid, Megoura viciae. J Insect Physiol 45:1011–1019

    Article  PubMed  CAS  Google Scholar 

  • Geister TL, Lorenz MW, Hoffmann KH, Fischer K (2008) Effects of the NMDA receptor antagonist MK-801 on female reproduction and juvenile hormone biosynthesis in the cricket Gryllus bimaculatus and the butterfly Bicyclus anynana. J Exp Biol 211:1587–1593

    Article  PubMed  CAS  Google Scholar 

  • Gilbert SF, Epel D (2009) Ecological developmental biology: integrating epigenetics, medicine, and evolution. Sinauer Associates, Sunderland

    Google Scholar 

  • Gliwicz M, Slusarczyk A, Slusarczyk M (2001) Life history synchronization in a long-lifespan single-cohort Daphnia population in a fishless alpine lake. Oecologia 128:368–378

    Article  PubMed  Google Scholar 

  • Gorbi G, Moroni F, Sei S, Rossi V (2011) Anticipatory maternal effects in two different clones of Daphnia magna in response to food shortage. J Limnol 70(2):222–230

    Article  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  CAS  Google Scholar 

  • Grosvenor GH, Smith G (1913) The life-cycle of Moina rectirostris. Q J Microsc Sci 2(58):511–522

    Google Scholar 

  • Hardie J (1981) Juvenile hormone and photoperiodically controlled polymorphism in Aphis fabae: prenatal effects on presumptive oviparae. J Insect Physiol 27(4):257–265

    Article  CAS  Google Scholar 

  • Hebert PDN (1977) Niche overlap among species in the Daphnia carinata complex. J Anim Ecol 46(2):399–409

    Article  Google Scholar 

  • Hiruta C, Tochinai S (2012) How does the alteration of meiosis evolve to parthenogenesis? – case study in a water flea, Daphnia pulex. Meiosis, InTech 109:122

    Google Scholar 

  • Hiruta C, Nishida C, Tochinai S (2010) Abortive meiosis in the oogenesis of parthenogenetic Daphnia pulex. Chromosom Res 18:833–840

    Article  CAS  Google Scholar 

  • Hiruta C, Toyota K, Miyakawa H, Ogino Y, Miyagawa S, Tatarazako N, Shaw JR, Iguchi T (2013) Development of a microinjection system for RNA interference in the water flea Daphnia pulex. BMC Biotechnol 13:96

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hiruta C, Ogino Y, Sakuma T, Toyota K, Miyagawa S, Yamamoto T, Iguchi T (2014a) Targeted gene disruption by use of transcription activator-like effector nuclease (TALEN) in the water flea Daphnia pulex. BMC Biotechnol 14:95

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hiruta C, Toyota K, Miyakawa H, Sumiya E, Iguchi T (2014b) Sexual reproduction is a key element in the life history strategy of water fleas, Daphnia magna and Daphnia pulex: casting a spotlight on male induction and its morphology. Daphnia: biology and mathematics perspectives, Nova, pp 261–278

    Google Scholar 

  • Hiruta C, Kakui K, Tollefsen KE, Iguchi T (2018) Targeted gene disruption by use of CRISPR/Cas9 ribonucleoprotein complexes in the water flea Daphnia pulex. Gene Cells in press

    Google Scholar 

  • Hobæk A, Larsson P (1990) Sex determination in Daphnia magna. Ecology 71(6):2255–2268

    Article  Google Scholar 

  • Ignace DD, Dodson SI, Kashian DR (2011) Identification of the critical timing of sex determination in Daphnia magna (Crustacea, Branchiopoda) for use in toxicological studies. Hydrobiologia 668:117–123

    Article  CAS  Google Scholar 

  • Innes DJ, Dunbrack RL (1993) Sex allocation variation in Daphnia pulex. J Evol Biol 6:559–575

    Article  Google Scholar 

  • Ishikawa A, Ogawa K, Gotoh H, Walsh TK, Tagu D, Brisson JA, Rispe C, Jaubert-Possamai S, Kanbe T, Tsubota T, Shiotsuki T, Miura T (2012) Juvenile hormone titre and related gene expression during the change of reproductive modes in the pea aphid. Insect Mol Biol 21(1):49–60

    Article  PubMed  CAS  Google Scholar 

  • Kato Y, Kobayashi K, Oda S, Colbourn JK, Tatarazako N, Watanabe H, Iguchi T (2008) Molecular cloning and sexually dimorphic expression of DM-domain genes in Daphnia magna. Genomics 91:94–101

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kato Y, Kobayashi K, Watanabe H, Iguchi T (2010b) Introduction of foreign DNA into the water flea, Daphnia magna, by electroporation. Ecotoxicology 19:589–592

    Article  PubMed  CAS  Google Scholar 

  • Kato Y, Kobayashi K, Watanabe H, Iguchi T (2011a) 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  PubMed  PubMed Central  CAS  Google Scholar 

  • Kato Y, Shiga Y, Kobayashi K, Tokishita S, Yamagata H, Iguchi T, Watanabe H (2011b) Development of an RNA interference method in the cladoceran crustacean Daphnia magna. Dev Genes Evol 220:337–345

    Article  PubMed  CAS  Google Scholar 

  • Kato Y, Matsuura T, Watanabe H (2012) Genomic integration and germline transmission of plasmid injected into crustacean Daphnia magna eggs. PLoS One 7(9):e45318

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kayukawa T, Minakuchi C, Namiki T, Togawa T, Yoshiyama M, Kamimura M, Mita K, Imanishi S, Kiuchi M, Ishikawa Y, Shinoda T (2012) Transcriptional regulation of juvenile hormone-mediated induction of Krüppel homolog 1, a repressor of insect metamorphosis. Proc Natl Acad Sci U S A 109(29):11729–11734

    Article  PubMed  PubMed Central  Google Scholar 

  • Kayukawa T, Tateishi K, Shinoda T (2013) Establishement of a versatile cell line for juvenile hormone signaling analysis in Tribolium casteanum. Sci Rep 3:1570

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim K, Kotov AA, Taylor DJ (2006) Hormonal induction of undescribed males resolves cryptic species of cladocerans. Proc R Soc Lond Ser B Biol Sci 273:141–147

    Article  Google Scholar 

  • Kleiven OT, Larsson P, Hobæk A (1992) Sexual reproduction in Daphnia magna requires three stimuli. Oikos 65(2):197–206

    Article  Google Scholar 

  • Kopp A (2012) Dmrt genes in the development and evolution of sexual dimorphism. Trends Genet 28(4):175–184

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kotov A, Forró L, Korovchinsky NM, Petrusek A (2013) Crustacea-Cladocera checkList. World checklist of freshwater Cladocera species World Wide Web electronic publication. http://fada.biodiversity.be/group/show/17

  • LaMontagne JM, McCauley E (2001) Maternal effects in Daphnia: what mothers are telling their offspring and do they listen? Ecol Lett 4:64–71

    Article  Google Scholar 

  • Laufer H, Biggers WJ (2001) Unifying concepts learned from methyl farnesoate for invertebrate reproduction and post-embryonic development. Am Zool 41:442–457

    CAS  Google Scholar 

  • Laufer H, Borst D, Baker FC, Carrasco C, Sinkus M, Reuter CC, Tsai LW, Schooley DA (1987) Identification of a juvenile hormone-like compound in a crustacean. Science 235(4785):202–205

    Article  PubMed  CAS  Google Scholar 

  • Lees AD (1964) The location of the photoperiodic receptors in the aphid Megoura viciae buckton. J Exp Biol 41:119–133

    PubMed  CAS  Google Scholar 

  • Lees AD (1973) Photoperiodic time measurement in the aphid Megoura viciae. J Insect Physiol 19(12):2279–2316

    Article  Google Scholar 

  • Lees AD (1981) Action spectra for the photoperiodic control of polymorphism in the aphid Megoura viciae. J Insect Physiol 27(11):761–771

    Article  Google Scholar 

  • Li M, Mead EA, Zhu J (2011) Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression. Proc Natl Acad Sci U S A 108(2):638–643

    Article  PubMed  CAS  Google Scholar 

  • Little TJ, O’Connor B, Colegrave N, Watt K, Read AF (2003) Maternal transfer of strain-specific immunity in an invertebrate. Curr Biol 13:489–492

    Article  PubMed  CAS  Google Scholar 

  • Matson CK, Zarkower D (2012) Sex and the singular DM domain: insights into sexual regulation, evolution and plasticity. Nat Rev Genet 13:163–174

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mittmann B, Ungerer P, Klann M, Stollewerk A, Wolff C (2014) Development and staging of the water flea Daphnia magna (Straus, 1820; Cladocera, Daphniidae) based on morphological landmarks. EvoDevo 5:12

    Article  PubMed  PubMed Central  Google Scholar 

  • Miura T (2005) Developmental regulation of caste-specific characters in social-insect polyphenism. Evol Dev 7(2):122–129

    Article  PubMed  Google Scholar 

  • Miyakawa H, Gotoh H, Sugimoto N, Miura T (2013a) Effect of juvenoids on predator-induced polyphenism in the water flea, Daphnia pulex. J Exp Zool A Comp Exp Biol 319(8):440–450

    Article  CAS  Google Scholar 

  • Miyakawa H, Toyota K, Hirakawa I, Ogino Y, Miyagawa S, Oda S, Tatarazako N, Miura T, Colbourne JK, Iguchi T (2013b) A mutation in the receptor methoprene-tolerant alters juvenile hormone response in insects and crustaceans. Nat Commun 4:1856

    Article  PubMed  CAS  Google Scholar 

  • Miyakawa H, Toyota K, Sumiya E, Iguchi T (2014) Comparison of JH signaling in insects and crustaceans. Curr Opin Insect Sci 1:81–87

    Article  PubMed  Google Scholar 

  • Naitou A, Kato Y, Nakanishi T, Matsuura T, Watanabe H (2015) Heterodimeric TALENs induce targeted heritable mutations in the crustacean Daphnia magna. Biol Open 4:364–369

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nakanishi T, Kato Y, Matsuura T, Watanabe H (2014) CRISPR/Cas-mediated targeted mutagenesis in Daphnia magna. PLoS One 9(5):e98363

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nakanishi T, Kato Y, Matsuura T, Watanabe H (2015) TALEN-mediated homologous recombination in Daphnia magna. Sci Rep 5:18312

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nijhout HF (1994) Insect hormones. Princeton University Press, Princeton

    Google Scholar 

  • Oda S, Tatarazako N, Watanabe H, Morita M, Iguchi T (2005) Production of male neonates in four cladoceran species exposed to a juvenile hormone analog, fenoxycarb. Chemosphere 60:74–78

    Article  PubMed  CAS  Google Scholar 

  • Oda S, Tatarazako N, Watanabe H, Morita M, Iguchi T (2006) Genetic differences in the production of male neonates in Daphnia magna exposed to juvenile hormone analogs. Chemosphere 63:1477–1484

    Article  PubMed  CAS  Google Scholar 

  • Oda S, Kato Y, Watanabe H, Tatarazako N, Iguchi T (2011) Morphological changes in Daphnia galeata induced by a crustacean terpenoid hormone and its analog. Environ Toxicol Chem 30(1):232–238

    Article  PubMed  CAS  Google Scholar 

  • Olesen J (1998) A phylogenetic analysis of the Conchostraca and Cladocera (Crustacea, Branchiopoda, Diplostraca). Zool J Linnean Soc 122:491–536

    Article  Google Scholar 

  • Olmstead AW, LeBlanc GA (2002) Juvenoid hormone methyl farnesoate is a sex determinant in the crustacean Daphnia magna. J Exp Zool 293:736–739

    Article  PubMed  CAS  Google Scholar 

  • Pijanowska J, Stolpe G (1996) Summer diapause in Daphnia as a reaction to the presence of fish. J Plankton Res 18(8):1407–1412

    Article  Google Scholar 

  • Poynton HC, Taylor NS, Hicks J, Scanlan L, Loguinov AV, Vulpe C, Viant MR (2011) Metabolomics of microliter hemolymph samples enables an improved understanding of the combined metabolic and transcriptional responses of Daphnia magna to cadmium. Environ Sci Technol 45:3710–3717

    Article  PubMed  CAS  Google Scholar 

  • Raymond CS, Shamu CE, Shen MM, Seifert KJ, Hirsch B, Hodgkin J, Zarkower D (1998) Evidence for evolutionary conservation of sex-determining genes. Nature 391:691–695

    Article  PubMed  CAS  Google Scholar 

  • Raymond CS, Murphy MW, O’Sullivan MG, Bardwell VJ, Zarkower D (2000) Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 14(20):2587–2595

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Robinett CC, Vaughan AG, Knapp J-M, Baker BS (2010) Sex and the single cell. II. There is a time and place for sex. PLoS Biol 8(5):e1000365

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Robinson CD, Lourido S, Whelan SP, Dudycha JL, Lynch M, Isern S (2006) Viral transgenesis of embryonic cell cultures from the freshwater microcrustacean Daphnia. J Exp Zool 305:62–67

    Article  Google Scholar 

  • Rossi F (1980) Comparative observations on the female reproductive system and parthenogenetic oogenesis in Cladocera. Boll Zool 47:21–38

    Article  Google Scholar 

  • Routtu J, Jansen B, Colson I, Meester LD, Ebert D (2010) The first-generation Daphnia magna linkage map. BMC Genomics 11:508

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sagawa K, Yamagata H, Shiga Y (2005) Exploring embryonic germ line development in the water flea, Daphnia magna, by zinc-finger-containing VASA as a marker. Gene Expr Patterns 5:669–678

    Article  PubMed  CAS  Google Scholar 

  • Shaw JR, Colbourne JK, Davey JC, Glaholt SP, Hampton TH, Chen CY, Folt CL, Hamilton JW (2007) Gene response profiles for Daphnia pulex exposed to the environmental stressor cadmium reveals novel crustacean metallothioneins. BMC Genomics 8:477

    Article  PubMed  PubMed Central  Google Scholar 

  • Shen MM, Hodgkin J (1988) Mab-3, a gene required for sex-specific yolk protein expression and a male-specific lineage in C. elegans. Cell 54:1019–1031

    Article  PubMed  CAS  Google Scholar 

  • Simon J-C, Pfrender ME, Tollrian R, Tagu D, Colbourne JK (2011) Genomics of environmentally induced phenotypes in 2 extremely plastic arthropods. J Hered 102(5):512–525

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sin YW, Kenny NJ, Qu Z, Chan KW, Chan KWS, Cheong SPS, Leung RWT, Chan TF, Bendena WG, Chu KH, Tobe SS, Hui JHL (2015) Identification of putative ecdysteroid and juvenile hormone pathway genes in the shrimp Neocaridina denticulata. Gen Comp Endocrinol 214:167–176. https://doi.org/10.1016/j.ygcen.2014.07.018

    Article  PubMed  CAS  Google Scholar 

  • Sinev AY, Sanoamuang L-O (2011) Hormonal induction of males as a method for studying tropical cladocerans: description of males of four chydorid species (Cladocera: Anomopoda: Chydoridae). Zootaxa 2826:45–56

    Google Scholar 

  • Smith G (1915) The life-cycle of Cladocera, with remarks on the physiology of growth and reproduction in crustacea. Proc R Soc Lond B Biol Sci 88(605):418–435

    Article  CAS  Google Scholar 

  • Smith KC, Macagno ER (1990) UV photoreceptors in the compound eye of Daphnia magna (Crustacea, Branchiopoda). A fourth spectral class in single ommatidia. J Comp Physiol A Sens Neural Behav Physiol 166:597–606

    Article  CAS  Google Scholar 

  • Song J, Zhongxia W, Wang Z, Deng S, Zhou S (2014) Krüppel-homolog 1 mediates juvenile hormone action to promote vitellogenesis and oocyte maturation in the migratory locust. Insect Biochem Mol Biol 52:94–101

    Article  PubMed  CAS  Google Scholar 

  • Stenderup JT, Olesen J, Glenner H (2006) Molecular phylogeny of the Branchiopoda (Crustacea) – multiple approaches suggest a ‘diplostracan’ ancestry of the Notostraca. Mol Phylogenet Evol 41:182–194

    Article  PubMed  CAS  Google Scholar 

  • Suzuki Y, Truman JW, Riddiford LM (2008) The role of broad in the development of Tribolium castaneum: implications for the evolution of the holometabolous insect pupa. Development 135:569–577

    Article  PubMed  CAS  Google Scholar 

  • Tanaka S (2001) Endocrine mechanisms controlling body-color polymorphism in locusts. Arch Insect Biochem Physiol 47:139–149

    Article  PubMed  CAS  Google Scholar 

  • Tatarazako N, Oda S, Watanabe H, Morita M, Iguchi T (2003) Juvenile hormone agonists affect the occurrence of male Daphnia. Chemosphere 53:827–833

    Article  PubMed  CAS  Google Scholar 

  • Taylor DJ, Crease TJ, Brown WM (1999) Phylogenetic evidence for a single long-lived clade of crustacean cyclic parthenogens and its implications for the evolution of sex. Proc R Soc Lond B Biol Sci 266:791–797

    Article  Google Scholar 

  • Threlkeld ST (1979) Estimating cladoceran birth rates: the importance egg mortality and the egg age distribution. Limnol Oceanogr 24(4):601–611

    Article  Google Scholar 

  • Tollrian R (1995) Predator-induced morphological defenses: costs, life history shifts, and maternal effects in Daphnia pulex. Ecology 76(6):1691–1705

    Article  Google Scholar 

  • Toyota K, Kato Y, Sato M, Sugiura N, Miyagawa S, Miyakawa H, Watanabe H, Oda S, Ogino Y, Hiruta C, Mizutani T, Tatarazako N, Paland S, Jackson C, Colbourne JK, Iguchi T (2013) Molecular cloning of doublesex genes of four cladocera (water flea) species. BMC Genomics 14:239

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Toyota K, Kato Y, Miyakawa H, Yatsu R, Mizutani T, Ogino Y, Miyagawa S, Watanabe H, Nishide H, Uchiyama I, Tatarazako N, Iguchi T (2014) Molecular impact of juvenile hormone agonists on neonatal Daphnia magna. J Appl Toxicol 34:537–544

    Article  PubMed  CAS  Google Scholar 

  • Toyota K, Miyakawa H, Hiruta C, Furuta K, Ogino Y, Shinoda T, Tatarazako N, Miyagawa S, Shaw JR, Iguchi T (2015a) Methyl farnesoate synthesis is necessary for the environmental sex determination in the water flea Daphnia pulex. J Insect Physiol 80:22–30

    Article  PubMed  CAS  Google Scholar 

  • Toyota K, Miyakawa H, Yamaguchi K, Shigenobu S, Ogino Y, Tatarazako N, Miyagawa S, Iguchi T (2015b) NMDA receptor activation upstream of methyl farnesoate signaling for short day-induced male offspring production in the water flea, Daphnia pulex. BMC Genomics 16:186

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Toyota K, Hiruta C, Ogino Y, Miyagawa S, Okamura T, Onishi Y, Tatarazako N, Iguchi T (2016) Comparative developmental staging of the female and male water fleas Daphnia pulex and Daphnia magna during embryogenesis. Zool Sci (in press)

    Google Scholar 

  • Tsuchiya D, Eads BD, Zolan ME (2009) Methods for meiotic chromosome preparation, immunofluorescence, and fluorescence in situ hybridization in Daphnia pulex. Methods Mol Biol 558:235–249

    Article  PubMed  CAS  Google Scholar 

  • Ventura T, Rosen O, Sagi A (2015) From the discovery of the crustacean androgenic gland to the insulin-like hormone in six decades. Gen Comp Endocrinol 173:381–388

    Article  CAS  Google Scholar 

  • Watanabe H, Tatarazako N, Oda S, Nishide H, Uchiyama I, Morita M, Iguchi T (2005) Analysis of expressed sequence tags of the water flea Daphnia magna. Genome 48(4):606–609

    Article  PubMed  CAS  Google Scholar 

  • Watanabe H, Takahashi E, Nakamura Y, Oda S, Tatarazako N, Iguchi T (2007) Development of a Daphnia magna DNA microarray for evaluating the toxicity of environmental chemicals. Environ Toxicol Chem 26(4):669–676

    Article  PubMed  CAS  Google Scholar 

  • Weiss LC, Tollrian R, Herbert Z, Laforsch C (2012) Morphology of the Daphnia nervous system: a comparative study on Daphnia pulex, Daphnia lumholtzi, and Daphnia longicephala. J Morphol 273:1392–1405

    Article  PubMed  Google Scholar 

  • Yampolsky LY (1992) Genetic variation in the sexual reproduction rate within a population of a cyclic parthenogen, Daphnia magna. Evolution 46(3):833–837

    Article  PubMed  Google Scholar 

  • Zhang Z, Xu J, Sheng Z, Sui Y, Palli SR (2011) Steroid receptor co-activator is required for juvenile hormone signal transduction through a bHLH-PAS transcription factor, methoprene tolerant. J Biol Chem 286(10):8437–8447

    Article  PubMed  CAS  Google Scholar 

  • Zmora N, Chung JS (2014) A novel hormone is required for the development of reproductive phenotypes in adult female crabs. Endocrinology 155(1):230–239

    Article  PubMed  CAS  Google Scholar 

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Author information

Authors and Affiliations

  1. Okazaki Institute for Integrative Bioscience, National Institute for Basic Biology, National Institutes of Natural Sciences, SOKENDAI (The Graduate University for Advanced Studies), Okazaki, Aichi, Japan

    Kenji Toyota & Taisen Iguchi

  2. Department of Biological Science and Technology, Tokyo University of Science, Katsushika, Tokyo, Japan

    Kenji Toyota

  3. Department of Biological Science, Faculty of Science, Kanagawa University, Hiratsuka, Kanagawa, Japan

    Kenji Toyota

  4. Graduate School of Agriculture, Ehime University, Matsuyama, Japan

    Norihisa Tatarazako

  5. Graduate School of Nanobioscience, Yokohama City University, Yokohama, Japan

    Taisen Iguchi

Authors
  1. Kenji Toyota
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  2. Norihisa Tatarazako
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  3. Taisen Iguchi
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Corresponding author

Correspondence to Taisen Iguchi .

Editor information

Editors and Affiliations

  1. Department of Biology, Faculty of Agriculture and Life Science, Hirosaki University, Hirosaki, Japan

    Kazuya Kobayashi

  2. Department of Biological Sciences, Graduate School of Science and Technology Kumamoto University, Kumamoto, Japan

    Takeshi Kitano

  3. Laboratory of Reproductive Developmental Biology, Division of Earth Sciences, Biology, and Chemistry, Graduate School of Sciences and Technology for Innovation Yamaguchi University, Yamaguchi, Japan

    Yasuhiro Iwao

  4. Misaki Marine Biological Station, Graduate School of Science The University of Tokyo, Miura, Japan

    Mariko Kondo

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Toyota, K., Tatarazako, N., Iguchi, T. (2018). Environmental Control of Sex Differentiation in Daphnia . In: Kobayashi, K., Kitano, T., Iwao, Y., Kondo, M. (eds) Reproductive and Developmental Strategies. Diversity and Commonality in Animals. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56609-0_12

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