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Reproductive Strategies in Planarians: Insights Gained from the Bioassay System for Sexual Induction in Asexual Dugesia ryukyuensis Worms

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Reproductive and Developmental Strategies

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

Abstract

Some freshwater planarians (Platyhelminthes, Turbellaria, Seriata, and Tricladida) reproduce asexually by transverse fission and subsequent regeneration. Depending on environmental conditions, some asexual worms also develop complex hermaphroditic reproductive organs from planarian pluripotent stem cells, or neoblasts. Acquired sexual worms then mate, and eventually lay a cocoon filled with several fertilized eggs and a large number of yolk gland cells. The mechanisms underlying the switch from an asexual to a sexual state and the differentiation of germ cells from adult stem cells are of interest because they represent fundamental aspects of both reproductive biology and developmental biology. To study this mechanism, an experimental system was established in a triploid asexual strain, the OH strain of Dugesia ryukyuensis (Kobayashi et al. 1999). In this assay system, asexual worms acquire sexuality and cease asexual reproduction by transverse fission when experimentally dosed with sex-inducing substances produced by sexually mature planarians. Acquired sexual worms are then able to produce sex-inducing substances by themselves to maintain a sexual state, without the intake of sex-inducing substances. Interestingly, triploid acquired sexual worms sexually produce four types of offspring, namely, diploid asexual worms, diploid innate sexual worms, triploid asexual worms, and triploid innate sexual worms. Although the relationship between sexuality and ploidy has not yet been clarified, innate sexuality noticeably differs to acquired sexuality because worms never convert to an asexual state. This review discusses insights obtained from the study of these intricate biological phenomena to help elucidate the mechanisms used for reproductive strategies in planarians, including that of switching from an asexual to a sexual state.

The original version of this chapter was revised. An erratum to this chapter can be found at https://doi.org/10.1007/978-4-431-56609-0_35

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References

  • Baguñà J, Saló E, Auladell C (1989) Regeneration and pattern formation in planarians III. Evidence that neoblasts are totipotent stem cells and the source of blastema cells. Development 107:77–86

    Google Scholar 

  • Benazzi LG (1966a) Amphimixis and pseudogamy in freshwater triclads: experimental reconstitution of polyploid pseudogamic biotypes. Chromosoma 20:1–14

    Article  Google Scholar 

  • Benazzi M (1966b) Considerations on the neoblasts of planarians on the basis of certain karyological evidence. Chromosoma 19:14–27

    Article  CAS  PubMed  Google Scholar 

  • Benazzi LG (1970) Gametogesis and egg fertilization in planarians. Int Rev Cytol 27:101–179

    Article  Google Scholar 

  • Benazzi M (1974) Fissioning in planarians from a genetic standpoint. In: Riser NW, Morse MP (eds) Biology of the Turbellaria. McGraw-Hill, New York, pp 476–492

    Google Scholar 

  • Benazzi M (1982) Speciation events evidenced in Turbellaria. In: Barigozzi C (ed) Mechanisms of speciation. Alan R Liss, New York, pp 307–344

    Google Scholar 

  • Benazzi M, Grasso M (1977) Comparative research on the sexualisation of fissiparous planarians treated with substances contained in sexual planarians. Monitore Zool Ital 11:9–19

    Google Scholar 

  • Best JB, Goodman AB, Pigeon A (1969) Fissioning in planarians: control by the brain. Science 164:565–566

    Article  CAS  PubMed  Google Scholar 

  • Best JB, Abelein M, Kreutzer E, Pigon P (1975) Cephalic mechanism for social control of fissioning in planarians III: central nervous system centers of facilitation and inhibition. J Comp Physiol Psychol 89:923–932

    Article  CAS  PubMed  Google Scholar 

  • Beukeboom LW, Vrijenhoek RC (1998) Evolutionary genetics and ecology of sperm-dependent parthenogenesis. J Evol Biol 11:755–782

    Article  Google Scholar 

  • Beukeboom LW, Weinzierl RP, Reed KM, Michiels NK (1996) Distribution and origin of chromosomal races in the freshwater planarian Dugesia polychroa (Turbellaria: Tricladida). Hereditas 124:7–15

    Article  Google Scholar 

  • Cardona A, Hartenstein V, Romero R (2005) The embryonic development of the triclad Schmidtea polychroa. Dev Genes Evol 215:109–131

    Article  PubMed  Google Scholar 

  • Chinone A, Nodono H, Matsumoto M (2014) Triploid planarian reproduces truly bisexually with euploid gametes produced through a different meiotic system between sex. Chromosoma 123:265–272

    Article  PubMed  Google Scholar 

  • Collins JJ III, Hou X, Romanova EV, Lambrus BG, Miller CM, Saberi A, Sweedler JV, Newmark PA (2010) Genome-wide analysis reveal a role for peptide hormones in planarian germline development. PLoS Biol 8:1–21

    Google Scholar 

  • Curtis W (1902) The life history, the normal fission and the reproductive organs of Planaria maculata. Proc Boston Soc Nat Hist 30:515–559

    Google Scholar 

  • Curtis WC, Schulze LM (1924) Formative cells of planarians. Anat Rec 29:105

    Google Scholar 

  • D’Souza TG, Michiels NK (2008) Correlations between sex rate estimates and fitness across predominantly parthenogenetic flatworm populations. J Evol Biol 21:276–286

    Article  PubMed  Google Scholar 

  • D’Souza TG, Michiels NK (2010) The costs and benefits of occasional sex: theoretical predictions and a case study. J Hered 101:S34–S41

    Article  PubMed  Google Scholar 

  • D’Souza TG, Storhas M, Schulenburg H, Beukeboom LW, Michiels NK (2004) Occasional sex in an ‘asexual’ polyploidy hermaphrodite. Proc R Soc Lond B 271:1001–1007

    Article  Google Scholar 

  • D’Souza TG, Storhas M, Michiels NK (2005) The effect of ploidy level on fitness in parthenogenetic flatworms. Biol J Linn Soc 85:191–198

    Article  Google Scholar 

  • D’Souza TG, Schulte RD, Schulenburg H, Michiels NK (2006) Paternal inheritance in parthenogenetic forms of the planarian Schmidtea polychroa. Heredity 97:97–101

    Article  CAS  PubMed  Google Scholar 

  • Fukushima M, Funabiki I, Hashizume T, Osada K, Yoshida W, Ishida S (2008) Detection and changes in levels of testosterone during spermatogenesis in the freshwater planarian Bdellocephala brunnea. Zool Sci 25:760–765

    Article  Google Scholar 

  • Grasso M, Benazzi M (1973) Genetic and physiologic control of fissioning and sexuality in planarians. J Embryol Exp Morpholog 30:317–328

    CAS  Google Scholar 

  • Gremigni V, Banchetti R (1972a) Submicroscopic morphology of hyperplasic ovaries of ex-fissiparous individuals in Dugesia gonocephala s.l. Acc Naz Lincei 52:539–543

    Google Scholar 

  • Gremigni V, Banchetti R (1972b) The origin of hyperplasia in the ovaries of ex-fissiparous specimens of Dugesia gonocephala s.l. Acc Naz Lincei 53:477–448

    Google Scholar 

  • Gremigni V, Miceli C, Picano E (1980a) On the role of germ cells in planarian regeneration. I. A karyological investigation. J Embryol Exp Morpholog 55:53–63

    CAS  Google Scholar 

  • Gremigni V, Miceli C, Picano E (1980b) On the role of germ cells in planarian regeneration. II. Cytophotometric analysis of the nuclear Feulgen-DNA content in cells of regenerated somatic tissues. J Embryol Exp Morpholog 55:65–76

    CAS  Google Scholar 

  • Gremigni V, Miceli C, Picano E (1982) Evidence of male germ cell redifferentiation into female germ cells in planarian regeneration. J Embryol Exp Morpholog 70:29–36

    CAS  Google Scholar 

  • Hamase K (2015) Recent advances on d-amino acid research. J Pharm Biomed Anal 116:1

    Article  CAS  PubMed  Google Scholar 

  • Harrath H, Sluys R, Zghal F, Tekaya S (2009) First report of adelphophagy in flatworms during the embryonic development of the planarian Schmidtea mediterranea (Benazzi, Baguñà, Ballester, Puccinelli & Del Papa, 1975) (Platyhelminthes, Tricladida). Invert Reprod Develop 53:117–124

    Article  Google Scholar 

  • Harrath AH, Semlali A, Mansour L, Ahmed M, Sirotkin AV, Al Omar SY, Arfah M, Al Anazi MS, Alhazza IM, Nyengaard JR, Alwasel S (2014) Infertility in the hyperplasic ovary of freshwater planarians: the role of programmed cell death. Cell Tissue Res 358:607–620

    Article  CAS  PubMed  Google Scholar 

  • Hase S, Kobayashi K, Koyanagi R, Hoshi M, Matsumoto M (2003) Transcriptional pattern of a novel gene, expressed specifically after the point-of-no-return during sexualization, in planaria. Dev Genes Evol 212:585–592

    PubMed  CAS  Google Scholar 

  • Hauser J (1987) Sexualization of Dugesia anderlani by feeding. Acta Biol Leopoldensia 9:111–128

    Google Scholar 

  • Hoshi M, Kobayashi K, Arioka S, Hase S, Matsumoto M (2003) Switching from asexual to sexual reproduction in the planarian Dugesia ryukyuensis. Integr Comp Biol 43:242–246

    Article  PubMed  Google Scholar 

  • Inoue T, Kumamoto H, Okamoto K, Umesono Y, Sakai M, Sanchez Alvarado A, Agata K (2004) Morphological and functional recovery of the planarian photosensing system during head regeneration. Zool Sci 21:275–283

    Article  CAS  Google Scholar 

  • Inoue T, Yamashita T, Agata K (2014) Thermosensory signaling by TRPM is processed by brain serotonergic neurons to produce planarian thermotaxis. J Neurosci 34:15701–15714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inoue T, Hoshino H, Yamashita T, Shimoyama S, Agata K (2015) Planarian shows decision-making behavior in response to multiple stimuli by integrative brain function. Zool Lett 1:7

    Article  Google Scholar 

  • Ishizuka H, Maezawa T, Kawauchi J, Nodono H, Hirao Y, Nishimura O, Nakagawa H, Sekii K, Tasaka K, Tarui H, Agata K, Hoshi M, Kobayashi K, Sakakibara Y, Matsumoto M (2007) The Dugesia ryukyuensis database as a molecular resource for studying switching of the reproductive system. Zool Sci 24:31–37

    Article  CAS  Google Scholar 

  • Jenkins MM (1967) Aspects of planarian biology and behavior. In: Corning WC, Ratner SC (eds) Chemistry of learning. Plenum Press, New York, pp 117–143

    Google Scholar 

  • Kawakatsu M, Oki I, Tamura S, Sugino H (1976) Studies on the morphology, karyology and taxonomy of the Japanese freshwater planarian Dugesia japonica Ichikawa et Kawakatsu, with a description of a new subspecies, Dugesia japonica ryukyuensis subspec. Bull Fuji Womens Coll 23:127–132

    Google Scholar 

  • Kawakatsu M, Oki I, Tamura S (1995) Taxonomy and geographical distribution of Dugesia japonica and D. ryukyuensis in the Far East. Hydrobiologia 305:55–61

    Article  Google Scholar 

  • Kenk R (1937) Sexual and asexual reproduction in Euplanaria tigrina (Girard). Biol Bull 73:280–294

    Article  Google Scholar 

  • Kenk R (1941) Induction of sexuality in the asexual form of Dugesia tigrina. J Exp Zool 87:55–69

    Google Scholar 

  • Khoronenkova SV, Tishkov VI (2008) d-amino acid oxidase: physiological role and applications. Biochemistry (Mosc) 73:1511–1518

    Article  CAS  Google Scholar 

  • Kobayashi K, Hoshi M (2002) Switching from asexual to sexual reproduction in the planarian Dugesia ryukyuensis: change of the fissiparous capacity along with the sexualizing process. Zool Sci 19:661–666

    Article  Google Scholar 

  • Kobayashi K, Hoshi M (2011) Sex-inducing effect of a hydrophilic fraction on reproductive switching in the planarian Dugesia ryukyuensis (Seriata, Tricladida). Front Zool 8:24

    Article  Google Scholar 

  • Kobayashi S, Yamada M, Asaoka M, Kitamura T (1996) Essential role of the posterior morphogen nanos for germline development in Drosophila. Nature 380:708–711

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi K, Koyanagi R, Matsumoto M, Cabrera JP, Hoshi M (1999) Switching from asexual to sexual reproduction in the planarian Dugesia ryukyuensis: bioassay system and basic description of sexualizing process. Zool Sci 16:291–298

    Article  Google Scholar 

  • Kobayashi K, Arioka S, Hoshi M (2002a) Seasonal changes in the sexualization of the planarian Dugesia ryukyuensis. Zool Sci 19:1267–1278

    Article  Google Scholar 

  • Kobayashi K, Arioka S, Hase S, Hoshi M (2002b) Signification of the sexualizing substance produced by the sexualized planarians. Zool Sci 19:667–672

    Article  Google Scholar 

  • Kobayashi K, Ishizu H, Arioka S, Cabrera JP, Hoshi M, Matsumoto M (2008a) Production of diploid and triploid offspring by inbreeding of the triploid planarian Dugesia ryukyuensis. Chromosoma 117:289–296

    Article  PubMed  Google Scholar 

  • Kobayashi K, Hashiguchi T, Ichikawa T, Ishino Y, Hoshi M, Matsumoto M (2008b) Neoblast-enriched fraction rescues eye formation in eye-defective planarian ‘menashi’ Dugesia ryukyuensis. Develop Growth Differ 50:689–696

    Article  Google Scholar 

  • Kobayashi K, Arioka S, Hoshi M, Matsumoto M (2009) Production of asexual and sexual offspring in the triploid planarian Dugesia ryukyuensis. Integr Zool 4:265–271

    Article  PubMed  Google Scholar 

  • Kobayashi K, Maezawa T, Nakagawa H, Hoshi M (2012) Existence of two sexual races in the planarian species switching between asexual and sexual reproduction. Zool Sci 29:265–272

    Article  Google Scholar 

  • Kobayashi K, Maezawa T, Tanaka H, Onuki H, Horiguchi Y, Hirota H, Ishida T, Horiike K, Agata Y, Aoki M, Hoshi M, Matsumoto M (2017) The identification of d-tryptophan as a bioactive substance for postembryonic ovarian development in the planarian Dugesia ryukyuensis. Sci Rep 7: 45175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lange CS, Gilbert CW (1968) Studies on the cellular basis of radiation lethality: III. The measurement of stem-cell repopulation probability. Int J Radiat Biol 14:373–388

    CAS  Google Scholar 

  • Maezawa T, Aria K, Shigenobu S, Kobayashi S (2009) Expression of the apoptosis inducer gene head involution defective in primordial germ cells of the Drosophila embryo requires eiger, p53, and loki function. Develop Growth Differ 51:453–461

    Article  CAS  Google Scholar 

  • Maezawa T, Tanaka H, Nakagawa H, Ono M, Aoki M, Matsumoto M, Ishida T, Horiike K, Kobayashi K (2014) Planarian d-amino acid oxidase is involved in ovarian development during sexual induction. Mech Dev 132:69–78

    Article  CAS  PubMed  Google Scholar 

  • Miyashita H, Nakagawa H, Kobayashi K, Hoshi M, Matsumoto M (2011) Effects of 17ß-estradiol and bisphenol A on the formation of reproductive organs in planarian. Biol Bull 220:47–56

    Article  CAS  PubMed  Google Scholar 

  • Morita M (1990) Photoperiod and melatonin control of planarian asexual reproduction. In: Hoshi M, Yamashita O (eds) Advances in invertebrate reproduction 5. Elsevier Science Publishers, Amsterdam, pp 33–36

    Google Scholar 

  • Nagata Y (1992) Involvement of d-amino acid oxidase in elimination of d-serine in mouse brain. Experientia 48:753–755

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa H, Ishizu H, Chinone A, Kobayashi K, Matsumoto M (2012a) The Dr-nanos gene is essential for germ cell specification in the planarian Dugesia ryukyuensis. Int J Dev Biol 56:165–171

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa H, Ishizu H, Hasegawa R, Kobayashi K, Matsumoto M (2012b) Drpiwi-1 is essential for germline cell formation during sexualization of the planarian Dugesia ryukyuensis. Dev Biol 361:167–176

    Article  CAS  PubMed  Google Scholar 

  • Newmark PA, Sánchez Alvarado A (2000) Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev Biol 220:142–153

    Article  CAS  PubMed  Google Scholar 

  • Newmark PA, Sánchez Alvarado A (2002) Not your father’s planarian: a classic model enters the era of functional genomics. Nat Rev Genet 3:210–219

    Article  CAS  PubMed  Google Scholar 

  • Nishikawa T (2005) Metabolism and functional roles of endogenous d-serine in mammalian brains. Biol Pharm Bull 28:1561–1565

    Article  CAS  Google Scholar 

  • Nodono H, Ishino Y, Hoshi M, Matsumoto M (2012) Stem cells from innate sexual but acquired sexual planarians have the capability to form a sexual individual. Mol Reprod Dev 79:757–766

    Article  CAS  PubMed  Google Scholar 

  • Oki I, Tamura S, Yamayoshi T, Kawakatsu M (1981) Karyological and taxonomic studies of Dugesia japonica Ichikawa et Kawakatsu in the Far East. Hydrobiologia 84:53–68

    Article  Google Scholar 

  • Okugawa KI, Kawakatsu M (1954) Studies on the fission of Japanese fresh-water planaria, Dugesia gonocephala (Dugès) III. Comparative studies on breeding and fission frequencies of sexual and assumed asexual races which had been collected in ten localities in Japan; with an additional study on the fission plane. Bull Kyoto Gakugei Univ Ser B 5:42–52. (In Japanese)

    Google Scholar 

  • Orii H, Sakurai T, Watanabe K (2005) Distribution of the stem cells (neoblasts) in the planarian Dugesia japonica. Dev Genes Evol 215:143–157

    Article  CAS  PubMed  Google Scholar 

  • Panatier A, Theodosis DT, Mothet JP, Touquet B, Pollegioni L, Poulain DA, Oliet SH (2006) Glia-derived d-serine controls NMDA receptor activity and synaptic memory. Cell 125:775–784

    Article  CAS  PubMed  Google Scholar 

  • Pearse V, Pearse J, Buchsbaum M, Buchsbaum R (1987) Flatworm body plan: bilateral symmetry, three layers of cells, organ-system level of construction, regeneration. In: Living invertebrates. The Boxwood Press, Pacific Grove, pp 204–221

    Google Scholar 

  • Pollegioni L, Piubelli L, Sacchi S, Pilone MS, Molla G (2007) Physiological functions of d-amino acid oxidases: from yeast to humans. Cell Mol Life Sci 64:1373–1394

    Article  CAS  PubMed  Google Scholar 

  • Sakurai T (1981) Sexual induction by feeding in an asexual strain of the fresh-water planarian, Dugesia japonica japonica. Annot Zool Jpn 54:103–112

    Google Scholar 

  • Sakurai T (1991) An electron-microscopic study of syncytium formation during early embryonic development of the freshwater planarian Bdellocephala brunnea. Hydrobiologia 227:113–118

    Article  Google Scholar 

  • Saló E, Baguñà J (1985) Cell movement in intact and regenerating planarians. Quantitation using chromosomal, nuclear and cytoplasmic markers. J Embryol Exp Morpholog 89:57–70

    Google Scholar 

  • Saló E, Baguñà J (2002) Regeneration in planarians and other worms: new findings, new tools, and new perspectives. J Exp Zool 292:528–539

    Article  PubMed  Google Scholar 

  • Sánchez Alvarado A, Tsonis PA (2006) Bridging the regeneration gap: genetic insights from diverse animal models. Nat Rev Genet 7:873–884

    Article  CAS  PubMed  Google Scholar 

  • Sato Y, Kobayashi K, Matsumoto M, Hoshi M, Negishi S (2005) Comparative study of eye defective worm ‘menashi’ and regenerating wild-type in planarian, Dugesia ryukyuensis. Pigment Cell Res 18:86–91

    Article  PubMed  Google Scholar 

  • Shibata N, Hayashi T, Fukumura R, Fujii J, Kudome-Takamatsu T, Nishimura O, Sano S, Son F, Suzuki N, Araki R, Abe M, Agata K (2012) Comprehensive gene expression analyses in pluripotent stem cells of a planarian, Dugesia japonica. Int J Dev Biol 56:93–102

    Article  CAS  PubMed  Google Scholar 

  • Stöck M, Lamatsc DK, Steinlein C, Epplen JT, Grosse W-R, Hock R, Klapperstück T, Lampert KP, Scheer U, Schmid M, Schartl M (2002) A bisexually reproducing all-triploid vertebrate. Nat Genet 30:325–328

    Article  PubMed  Google Scholar 

  • Tamura S, Oki I, Kawakatsu M (1995) A review of chromosomal variation in Dugesia japonica and D. ryukyuensis in the Far East. Hydrobiologia 305:79–84

    Article  Google Scholar 

  • Tamura S, Yamamoto K, Takai M, Oki I, Kawakatsu (1998) Karyology and biogeography of Dugesia japonica and Dugesia ryukyuensis in Kyushu, southern Japan. Hydrobiologia 383:321–327

    Article  Google Scholar 

  • Tanaka H, Yamamoto A, Ishida T, Horiike K (2007) Simultaneous measurement of d-serine dehydratase and d-amino acid oxidase activities by the detection of 2-oxo-acid formation with reverse-phase high-performance liquid chromatography. Anal Biochem 362:83–88

    Article  CAS  PubMed  Google Scholar 

  • Teshirogi W (1986) On the origin of neoblasts in freshwater planarians (Turbellaria). Hydrobiologia 132:207–216

    Article  Google Scholar 

  • Vowinckel C (1970) The role of illumination and temperature in the control of sexual reproduction in the planarian Dugesia tigrina (Girard). Biol Bull 138:77–87

    Article  Google Scholar 

  • Vowinckel C, Marsden JR (1971a) Reproduction of Dugesia tigrina under short-day and long-day conditions at different temperatures. I. Sexually derived individuals. J Embryol Exp Morpholog 26:587–598

    CAS  Google Scholar 

  • Vowinckel C, Marsden JR (1971b) Reproduction of Dugesia tigrina under short-day and long-day conditions at different temperatures. II. Asexually derived individuals. J Embryol Exp Morpholog 26:599–609

    CAS  Google Scholar 

  • Wagner DE, Wang IE, Reddien PW (2011) Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332:811–816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wenemoser D, Reddien PW (2010) Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev Biol 344:979–991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams G (1966) Adaptation and natural selection. Princeton University Press, Princeton

    Google Scholar 

  • Wolff E, Dubois MF (1948) Sur la migration des cellules de régénération chez les planaires. Rev Suisse Zool 55:218–227

    Article  Google Scholar 

  • Yamamoto A, Tanaka H, Ishida T, Horiike K (2010) d-aspartate oxidase localisation in pituitary and pineal glands of the female pig. J Neuroendocrinol 22:1165–1172

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Dr. Yuni Nakauchi’s group (Yamagata University) for providing invaluable assistance with collecting B. brunnea and S. auriculata. We also thank Dr. Hidefumi Orii (University of Hyogo), Dr. Kimitoshi Sakamoto (Hirosaki University), and Dr. P. A. Newmark (University of Wisconsin-Madison) for their kind gifts of D. japonica worms and sexual specimens of S. mediterranea (Dr. Orii), G. dorotocephala worms (Dr. Sakamoto), and asexual specimens of S. mediterranea (Dr. Newmark). We also thank Miss Sachiko Arioka for producing 3D images. This study was supported in part by a Grant-in-Aid for Scientific Research (Nos. 26114501 [KK], 15K07121 [KK], and 25650103 [TM]) from the Ministry of Science, Culture, Sports and Education, Japan, The NAITO Foundation (KK), The Sumitomo Foundation (TM), and Ryobi Teien Memory Foundation (TM).

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  1. Advanced Science Course, Department of Integrated Science and Technology, National Institute of Technology, Tsuyama College, Okayama, Japan

    Takanobu Maezawa

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

    Kiyono Sekii, Masaki Ishikawa, Hikaru Okamoto & Kazuya Kobayashi

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  1. Takanobu Maezawa
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  2. Kiyono Sekii
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  5. Kazuya Kobayashi
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Correspondence to Kazuya Kobayashi .

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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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Maezawa, T., Sekii, K., Ishikawa, M., Okamoto, H., Kobayashi, K. (2018). Reproductive Strategies in Planarians: Insights Gained from the Bioassay System for Sexual Induction in Asexual Dugesia ryukyuensis Worms. 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_9

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