Abstract
The honmoroko has been inferred to have an XX/XY sex determination system, but the parental genome can also affect the sex ratio of the offspring. The extent of parental effects on sex determination was examined by checking the sex ratios of F1 and F2 gynogenetic diploids and control diploids. Eleven gynogenetic broods from different females consisted of all or nearly all females, but eight broods showed a variable proportion of males (<50 %). One second-generation brood of gynogenetic diploids consisted wholly of females, but others produced some males. In crosses with a control diploid female, four males from a high-percentage male brood of gynogenetic diploids produced offspring with a balanced sex ratio. Sib-mating between a gynogenetic female and three gynogenetic males from the brood produced predominantly male progeny. These results suggest that there are at least four possible genotypes: genotypic female (XX), phenotypic female carrying a silent Y chromosome, genotypic male (XY), and genotypic supermale (YY). These inferences suggest that this fish has an XY system but a relatively high proportion of females possess a mutated, silent Y chromosome which does not lead to testis formation.
Similar content being viewed by others
References
Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364
Mank JE, Avise JC (2009) Evolutionary diversity and turn-over of sex determination in teleost fishes. Sex Dev 3:60–67
Conover DO (2004) Temperature-dependent sex determination in fishes. In: Valenzuela N, Lance VA (eds) Temperature-dependent sex determination in vertebrates. Smithsonian Books, Washington DC, pp 11–20
Baroiller JF, D’Cotta HD, Saillant E (2009) Environmental effects on fish sex determination and differentiation. Sex Dev 3:118–135
Yamazaki F (1983) Sex control and manipulation in fish. Aquaculture 33:329–354
Purdom CE (1993) Sex determination. In: Purdom CE (ed) Genetics and fish breeding. Chapman and Hall, London, pp 134–157
Arai K (2001) Genetic improvement of aquaculture finfish species by chromosome manipulation techniques in Japan. Aquaculture 197:205–228
Stanley JG (1976) Female homogamety in grass carp (Ctenopharyngodon idella) determined by gynogenesis. J Fish Res Boar Can 33:1372–1374
Nagy A, Rajki K, Horváth L, Csányi V (1978) Investigation on carp, Cyprinus carpio L. gynogenesis. J Fish Biol 13:215–224
Nagy A, Bercsényi M, Csányi V (1981) Sex reversal in carp (Cyprinus carpio) by oral administration of methyltestosterone. Can J Fish Aquat Sci 38:725–728
Komen J, Wiegertjes GF, van Ginneken VJT, Eding EH, Richter CJJ (1992) Gynogenesis in common carp (Cyprinus carpio L.). III The effects of inbreeding on gonadal development of heterozygous and homozygous gynogenetic offspring. Aquaculture 104:51–66
Chourrout D, Quillet E (1982) Induced gynogenesis in the rainbow trout: sex and survival of progenies production of all-triploid populations. Theo Appl Gen 63:201–205
Suzuki R, Oshiro T, Nakanishi T (1985) Survival, growth and fertility of gynogenetic diploids induced in the cyprinid loach, Misgurnus anguillicaudatus. Aquaculture 48:45–55
Naruse K, Ijiri K, Shima A, Egami N (1985) The production of cloned fish in the medaka (Oryzias latipes). J Exp Zool 236:335–341
Kawamura K (1998) Sex determination system of the rosy bitterling, Rhodeus ocellatus ocellatus. Environ Biol Fish 52:251–260
Flynn SR, Matsuoka M, Reith M, Martin-Robichaud DJ, Benfey TJ (2006) Gynogenesis and sex determination in shortnose sturgeon, Acipenser brevirostrum Lesuere. Aquaculture 253:721–727
Van Enennaam AL, Van Enennaam JP, Medrano JF, Doroshov SI (1999) Evidence of female heterogametic genetic sex determination in white sturgeon. J Hered 90:231–233
Felip A, Zanuy S, Carrillo M, Piferrer F (2001) Induction of triploidy and gynogenesis in teleost fish with emphasis on marine species. Genetica 111:175–195
Nomura T, Arai K, Hayashi T, Suzuki R (1998) Effect of temperature on sex ratios of normal and gynogenetic diploid loach. Fish Sci 64:753–758
Oshiro T (1987) Sex ratios of diploid gynogenetic progeny derived from five different females of goldfish. Nippon Suisan Gakkaishi 53:1899
Goto-Kazeto R, Abe Y, Masai K, Yamaha E, Adachi S, Yamauchi K (2006) Temperature-dependent sex differentiation in goldfish: establishing the temperature-sensitive period and effect of constant and fluctuating water temperatures. Aquaculture 254:617–624
Yamamoto E (1999) Studies on sex-manipulation and production of cloned population in hirame, Paralichthys olivaceus (Temminck et Schlegel). Aquaculture 173:235–246
Quillet E, Aubard G, Quéau I (2002) Mutation in a sex-determining gene in rainbow trout: detection and genetic analysis. J Hered 93:91–99
Howell BR, Baynes SM (1995) Progress towards the identification of the sex-determining mechanism of the sole, Solea solea (L.), by the induction of diploid gynogenesis. Aqua Res 26:135–140
Müller-Belecke A, Hörstgen-Schwark G (1995) Sex determination in tilapia (Oreochromis niloticus): sex ratios in homozygous gynogenetic progeny and their offspring. Aquaculture 137:57–65
Mori T, Saito S, Matsuda T, Kayaba T, Kishioka C, Lahrech Z, Arai K (2011) Sex ratio and growth performance of gynogenetic diploid barfin flounder Verasper moseri. Aqua Sci 59:375–382
Tabata K (1991) Induction of gynogenetic diploid males and presumption of sex determination mechanisms in the hirame Paralichthys olivaceus. Nippon Suisan Gakkaishi 57:845–850
Nakamura M (1949) The life history of a cyprinid fish, Gnathopogon elongatus caerulescens (Sawage) in Lake Biwa. Nippon Suisan Gakkaishi 15:88–96 (in Japanese)
Fujioka Y, Taguchi T, Kikko T (2013) Spawning time, spawning frequency, and spawned egg number in a multiple-spawning fish, the honmoroko Gnathopogon caerulescens. Nippon Suisan Gakkaishi 79:31–37 (in Japanese)
Ueno K, Ye Y, Umeoka T (1992) A comparative study of chromosomes in the cyprinid fish genera Gnathopogon and Squalidus of Japan. Nippon Suisan Gakkaishi 58:1273–1277 (in Japanese)
Fujioka Y (1998) Survival, growth and sex ratios of gynogenetic diploid honmoroko. J Fish Biol 52:430–442
Fujioka Y (1993) Sex reversal in honmoroko Gnathopogon caerulescens by immersion in 17-methyltestosterone and an attempt to produce all-female progeny. Suisanzoushoku 41:409–416 (in Japanese)
Fujioka Y (2001) Thermolabile sex determination in honmoroko. J Fish Biol 59:851–861
Fujioka Y (2006) Patterns of sex ratio response to water temperature during sex determination in honmoroko Gnathopogon caerulescens. Fish Sci 72:1034–1041
Fujioka Y (1993) Induction of gynogenetic diploid and cytological studies in honmoroko Gnathopogon caerulescens. Nippon Suisan Gakkaishi 59:493–500
Fujioka Y (2011) Sex differentiation in honmoroko Gnathopogon caerulescens. Bull Shiga Pref Fish Exp Sta 54:167–172 (in Japanese)
Liew WC, Bartfai R, Lim Z, Sreenivasan R, Siegfried KR, Orban L (2012) Polygenic sex determination system in zebrafish. PLoS ONE 7:e34397
Anderson JL, Mari AR, Braasch I, Amores A, Hohenlohe P, Batzel P, Postlethwait JH (2012) Multiple sex-associated regions and a putative sex chromosome in zebrafish revealed by RAD mapping and population genomics. PLoS One 7:e40701
Liew WC, Orban L (2013) Zebrafish sex: a complicated affair. Brief Funct Genomics, doi. 10. 1093/bfgp/elt041
Miura I, Ohtani H, Kashiwagi A, Hanada H, Nakamura M (1996) Structural differences between XX and ZW sex lampbrush chromosomes in Rana rugosa female (Anura: Ranidae). Chromosoma 105:237–241
Miura I, Ohtani H, Nakamura M, Ichikawa Y, Saitoh K (1998) The origin and differentiation of the heteromorphic sex chromosomes Z, W, X, and Y in the frog Rana rugosa, inferred from the sequences of a sex-linked gene, ADP/ATP translocase. Mol Bio Evol 15:1612–1619
Maki I (1966) Population studies of honmoroko, Gnathopogon caerulescens Sauvage, in Lake Biwa, Japan, 1. On the critical life-cycle stages related to the annual fluctuation of the population. Jap J Ecol 16:183–190 (in Japanese)
Yamamoto T (1955) Progeny of artificially induced sex-reversal of male genotype (XY) in the medaka (Oryzias latipes) with special reference to YY-male. Genetics 40:406–419
Yamamoto T (1964) The problem of viability of YY zygotes in the medaka, Oryzias latipes. Genetics 50:45–58
Yamamoto T, Kajishima T (1968) Sex hormone induction of sex reversal in the goldfish and evidence for male heterogamety. J Exp Zool 168:215–221
Yamamoto T (1975) A YY male goldfish from mating estrone-induced XY female and normal male. J Hered 66:2–4
Bongers ABJ, Zandieh-Doulabi B, Richter CJJ, Komen J (1999) Viable androgenetic YY genotypes of common carp (Cyprinus carpio L.). J Hered 90:195–198
Scott AG, Penman DJ, Beardmore JA, Skibinski DOF (1989) The ‘YY’ supermale in Oreochromis niloticus (L.) and its potential in aquaculture. Aquaculture 78:237–251
Abucay JS, Mair GC, Skibinski DOF, Beardmore JA (1999) Environmental sex determination: the effect of temperature and salinity on sex ratio in Oreochromis niloticus L. Aquaculture 173:219–234
Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417:559–563
Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A, Shan Z, Haaf T, Shimizu N, Shima A, Schmid M, Schartl M (2002) A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci USA 99:11778–11783
Otake H, Shinomiya A, Matsuda M, Hamaguchi S, Sakaizumi M (2006) Wild-derived XY sex-reversal mutants in the medaka, Oryzias latipes. Genetics 173:2083–2090
Yamamoto T (1969) Sex differentiation. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 3, Reproduction and growth, bioluminescence, pigments, and poisons. Academic, New York, pp 117–177
Matsuda M (2010) Sex determination in medaka. Fish Gen Breed Sci 40:3–9 (in Japanese)
Kallman KD (1984) A new look at sex determination in poeciliid fishes. In: Turner BJ (ed) Evolutionary genetics of fish. Plenum, New York, pp 95–171
Shinomiya A, Otake H, Togashi K, Hamaguchi S, Sakaizumi M (2004) Field survey of sex-reversals in the medaka, Oryzias latipes: genotypic sexing of wild populations. Zool Sci 21:613–619
Acknowledgments
We thank Mark Joseph Grygier for his critical reading of the manuscript, Taisuke Ohtsuka for his help with statistical analyses, and the staff of the Shiga Prefecture Fisheries Experiment Station for help.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Fujioka, Y., Ueno, S. Genetic contribution of parents in sex determination of honmoroko Gnathopogon caerulescens . Fish Sci 80, 943–950 (2014). https://doi.org/10.1007/s12562-014-0766-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12562-014-0766-2