Skip to main content

Sex-Determining Mechanisms in Bivalves

  • Chapter
  • First Online:

Abstract

In this review, we provide an overview of the current knowledge on the different sexual systems and sex-determining mechanisms in bivalves, with a focus on the various epigenetic and genetic factors that may be involved. The final section of the review provides recent discoveries on sex-specific mitochondrial genes in bivalves possessing the unconventional system of doubly uniparental inheritance of mitochondria (which is found in several members of the orders Mytiloida, Unionoida, Veneroida, and Nuculanoida). The genes involved in this developmental pathway could represent the first sex-determination system in animals in which mitochondrially encoded genes are directly involved.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Allen SK Jr, Hidu H, Stanley JG (1986) Abnormal gametogenesis and sex ratio in triploid soft-shell clams (Mya arenaria). Biol Bull 170:198–210

    Article  Google Scholar 

  • Amemiya I (1935) Effect of gill excision upon the sexual differentiation of the oyster (Ostrea gigas). Rept fop Ass Adv Sd 10:1025

    Google Scholar 

  • Ahmed M (1973) Cytogenetics of oysters. Cytologia 38:337–346

    Article  CAS  PubMed  Google Scholar 

  • Avise JC (2011) Hermaphroditism: a primer on the biology, ecology, and evolution of dual sexuality. Columbia University Press, New York

    Book  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bahr LM, Hillman RE (1967) Effects of repeated shell damage on gametogenesis in the American oyster, Crassostrea virginica (Gmelin). Proc Natl Shellfish Assoc 57:59–62

    Google Scholar 

  • Bello G, Paparella P, Corriero A, Santamaria N (2013) Protandric hermaphroditism in the bivalve Arca noae (Mollusca: Arcidae). Mediterr Mar Sci 14:86–91

    Article  Google Scholar 

  • Beukeboom L, Perrin N (2014) The evolution of sex determination. Oxford University Press, Oxford

    Book  Google Scholar 

  • Boyle EE, Etter RJ (2013) Heteroplasmy in a deep-sea protobranch bivalve suggests an ancient origin of doubly uniparental inheritance of mitochondria in Bivalvia. Mar Biol 160:413–422

    Article  CAS  Google Scholar 

  • Breton S, Doucet Beaupré H, Stewart DT, Hoeh WR, Blier PU (2007) The unusual system of doubly uniparental inheritance of mtDNA: isn’t one enough? Trends Genet 23:465–474

    Article  CAS  PubMed  Google Scholar 

  • Breton S, Beaupre HD, Stewart DT, Piontkivska H, Karmakar M, Bogan AE, Blier PU, Hoeh WR (2009) Comparative mitochondrial genomics of freshwater mussels (Bivalvia: Unionoida) with doubly uniparental inheritance of mtDNA: gender-specific open reading frames and putative origins of replication. Genetics 183:1575–1589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breton S, Stewart DT, Shepardson S, Trdan RJ, Bogan AE, Chapman EG, Ruminas AJ, Piontkivska H, Hoeh WR (2011) Novel protein genes in animal mtDNA: a new sex determination system in freshwater mussels (Bivalvia: Unionoida)? Mol Biol Evol 28:1645–1659

    Article  CAS  PubMed  Google Scholar 

  • Breton S, Milani L, Ghiselli F, Guerra D, Stewart DT, Passamonti M (2014) A resourceful genome: updating the functional repertoire and evolutionary role of animal mitochondrial DNAs. Trends Genet 30:555–564

    Article  CAS  PubMed  Google Scholar 

  • Burnell GM (1995) Age-related protandry in the scallop Chlamys varia (L.) on the west coast of Ireland. ICES Mar. Sci Symp 199:26–30

    Google Scholar 

  • Burt A, Trivers R (2006) Genes in conflict: the biology of selfish genetic elements. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Burzynski A, Zbawicka M, Skibinski DOF, Wenne R (2006) Doubly uniparental inheritance is associated with high polymorphism for rearranged and recombinant control region haplotypes in Baltic Mytilus trossulus. Genetics 174:1081–1094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campos A, Tedesco S, Vasconcelos V, Cristobal S (2012) Proteomic research in bivalves: towards the identification of molecular markers of aquatic pollution. J Proteomics 75:4346–4359

    Article  CAS  PubMed  Google Scholar 

  • Cao L, Kenchington E, Zouros E (2004a) Differential segregation patterns of sperm mitochondria in embryos of the blue mussel (Mytilus edulis). Genetics 166:883–894

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao L, Kenchington EL, Zouros E, Rodakis GC (2004b) Evidence that the large noncoding sequence is the main control region of maternally and paternally transmitted mitochondrial genomes of the marine mussel (Mytilus spp.). Genetics 167:835–850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charnov EL, Maynard Smith J, Bull JJ (1976) Why be a hermaphrodite? Nature 263:125–126

    Article  Google Scholar 

  • Charnov EL (1982) The theory of sex allocation. Princeton University Press, Princeton

    Google Scholar 

  • Chase CD (2007) Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet 23:81–90

    Article  CAS  PubMed  Google Scholar 

  • Chávez-Villalba J, Hernández-Ibarra A, López-Tapia MR, Mazón-Suástegui JM (2008) Prospective culture of the Cortez oyster Crassostrea corteziensis from northwestern Mexico: growth, gametogenic activity, and condition index. J Shellfish Res 27:711–720

    Article  Google Scholar 

  • Chávez-Villalba J, Soyez C, Huvet A, Gueguen Y, Lo C, Le Moullac G (2011) Determination of gender in the pearl oyster Pinctada margaritifera. J Shellfish Res 30:231–240

    Article  Google Scholar 

  • Ciocan CM, Cubero-Leon E, Peck MR, Langston WJ, Pope N, Minier C, Rotchell JM (2012) Intersex in Scrobicularia plana: transcriptomic analysis reveals novel genes involved in endocrine disruption. Environ Sci Technol 46:12936–12942

    Article  CAS  PubMed  Google Scholar 

  • Coe WR (1936) Environment and sex in the oviparous oyster Ostrea virginica. Biol Bull 71:353–359

    Article  Google Scholar 

  • Coe WR (1943) Sexual differentiation in molluscs. 1. Pelecypoda Q Rev Biol 18:154–164

    Article  Google Scholar 

  • Collin R (2013) Phylogenetic patterns and phenotypic plasticity of molluscan sexual systems. Integr Comp Biol 53:723–735

    Article  PubMed  Google Scholar 

  • Cornet M, Soulard C (1989) Number and morphology of the metaphase mitotic chromosomes in Scrobicularia Plana (Da Costa, 1778) (Mollusca, Bivalvia, Tellinacea). Caryologia 42:11–18

    Article  Google Scholar 

  • Cornet M, Soulard C (1990) Chromosome number and karyotype of Donax trunculus L. (Mollusca, Bivalvia, Tellinacea). Genetica 82:93–97

    Article  Google Scholar 

  • Cox C, Mann R (1992) Temporal and spatial changes in fecundity of eastern oysters, Crassostrea virginica (Gmelin, 1791) in the James River, Virginia. J Shellfish Res 11:49–57

    Google Scholar 

  • Croll RP, Wang C (2007) Possible roles of sex steroids in the control of reproduction in bivalve molluscs. Aquaculture 272:76–86

    Article  CAS  Google Scholar 

  • Davis NW, Hillman RE (1971) Effect of artificial shell damage on sex determination in oysters. Proc Natl Shellfish Assoc 61:2

    Google Scholar 

  • Dheilly NM, Lelong C, Huvet A, Kellner K, Dubos M-P, Riviere G, Boudry P, Favrel P (2012) Gametogenesis in the Pacific oyster Crassostrea gigas: a microarrays-based analysis identifies sex and stage specific genes. PLoS One 7:e36353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Downing JA, Amyot J-P, Pérusse M, Rochon Y (1989) Visceral sex, hermaphroditism, and protandry in a population of the freshwater bivalve Elliptio complanata. J N Am Benthol Soc 8:92–99

    Article  Google Scholar 

  • Doucet-Beaupré H, Breton S, Chapman EG, Blier PU, Bogan AE, Stewart DT, Hoeh WR (2010) Mitochondrial phylogenomics of the Bivalvia (Mollusca): searching for the origin and mitogenomic correlates of doubly uniparental inheritance of mtDNA. BMC Evol Biol 10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Egami N (1953) Studies on sexuality in the Japanese oyster, Ostrea gigas VII. Effects of gill removal on growth and sexuality. Annotat Zool Jap 26:145–150

    Google Scholar 

  • Evans JP, Sherman CDH (2013) Sexual selection and the evolution of egg-sperm interactions in broadcast-spawning invertebrates. Biol Bull 224:166–183

    Article  CAS  PubMed  Google Scholar 

  • Fabioux C, Pouvreau S, Le Roux F, Huvet A (2004) The oyster vasa-like gene: a specific marker of the germline in Crassostrea gigas. Biochem Biophys Res Commun 315:897–904

    Article  CAS  PubMed  Google Scholar 

  • Fabioux C, Huvet A, Le Souchu P, Le Pennec M, Pouvreau S (2005) Temperature and photoperiod drive Crassostrea gigas reproductive internal clock. Aquaculture 250:458–470

    Article  Google Scholar 

  • Fabioux C, Corporeau C, Quillien V, Favrel P, Huvet A (2009) In vivo RNA interference in oyster—vasa silencing inhibits germ cell development. FEBS J 276:2566–2573

    Article  CAS  PubMed  Google Scholar 

  • Gagné F, Blaise C, Pellerin J, Pelletier E, Douville M, Gauthier-Clerc S, Viglino L (2003) Sex alteration in soft-shell clams (Mya arenaria) in an intertidal zone of the Saint Lawrence River (Quebec, Canada). Comp Biochem Physiol C 134:189–198

    Article  Google Scholar 

  • Galbraith HS, Vaughn CC (2011) Effects of reservoir management on abundance, condition, parasitism and reproductive traits of downstream mussels. River Res Appl 27:193–201

    Article  Google Scholar 

  • Gamble T, Zarkower D (2012) Sex determination. Curr Biol 22:R257–R262

    Article  CAS  PubMed  Google Scholar 

  • Gauthier-Clerc S, Pellerin J, Blaise C, Gagné F (2002) Delayed gametogenesis of Mya arenaria in the Saguenay fjord (Canada): a consequence of endocrine disruptors? Comp Biochem Physiol C 131:457–467

    Article  CAS  Google Scholar 

  • Ghiselin MT (1969) The evolution of hermaphroditism among animals. Q Rev Biol 44:189–208

    Article  CAS  PubMed  Google Scholar 

  • Ghiselli F, Milani L, Passamonti M (2011) Strict sex-specific mtDNA segregation in the germ line of the DUI species Venerupis philippinarum (Bivalvia: Veneridae). Mol Biol Evol 28:949–961

    Article  CAS  PubMed  Google Scholar 

  • Ghiselli F, Milani L, Chang PL, Hedgecock D, Davis JP, Nuzhdin SV, Passamonti M (2012) De novo assembly of the manila clam Ruditapes philippinarum transcriptome provides new insights into expression bias, mitochondrial doubly uniparental inheritance and sex determination. Mol Biol Evol 29:771–786

    Article  CAS  PubMed  Google Scholar 

  • Gosling EM (2015) Marine bivalve molluscs, 2nd edn. Wiley-Blackwell, Hoboken

    Book  Google Scholar 

  • Guerra D, Ghiselli F, Milani L, Breton S, Passamonti M (2016) Early replication dynamics of sex linked mitochondrial DNAs in the doubly uniparental inheritance species Ruditapes philippinarum (Bivalvia Veneridae). Heredity 116:324–332

    Article  CAS  PubMed  Google Scholar 

  • Guo X, Allen SK (1994) Sex determination and polyploid gigantism in the dwarf surfclam (Mulinia lateralis Say). Genetics 138:1199–1206

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo X, Hedgecock D, Hershberger WK, Cooper K, Allen SK (1998) Genetic determinants of protandric sex in the Pacific oyster, Crassostrea gigas Thunberg. Evolution 52:394–402

    Article  PubMed  Google Scholar 

  • Haley LE (1977) Sex determination in the American oyster. J Hered 68:114–116

    Article  Google Scholar 

  • Haley LE (1979) Genetics of sex determination in the American oyser. Proc Nat Shellfish Assoc 69:54–57

    Google Scholar 

  • Hedrick PW, Hedgecock D (2010) Sex determination: genetic models for oysters. J Hered 101:602–611

    Article  PubMed  Google Scholar 

  • Heller J (1993) Hermaphroditism in molluscs. Biol J Linn Soc 48:19–42

    Article  Google Scholar 

  • Hinzmann M, Lopes-Lima M, Teixeira A, Varandas S, Sousa R, Lopes A, Froufe E, Machado J (2013) Reproductive cycle and strategy of Anodonta anatina (L., 1758): Notes on hermaphroditism. J Exp Zool 319A:378–390

    Article  Google Scholar 

  • Hoeh WR, Stewart DT, Sutherland BW, Zouros E (1996) Multiple origins of gender-associated mitochondrial DNA lineages in bivalves (Mollusca: Bivalvia). Evolution 50:2276–2286

    Article  CAS  PubMed  Google Scholar 

  • Jenkinson JJ (2014) Chromosomal characteristics of North American and other naiades (Bivalvia: Unionida). Malacologia 57:377–397

    Article  Google Scholar 

  • Jiao W, Fu X, Dou J, Li H, Su H, Mao J, Yu Q, Zhang L, Hu X, Huang X et al (2014) High-resolution linkage and quantitative trait locus mapping aided by genome survey sequencing: building up an integrative genomic framework for a bivalve mollusc. DNA Res 21:85–101

    Article  CAS  PubMed  Google Scholar 

  • Johnston MO, Das B, Hoeh WR (1998) Negative correlation between male allocation and rate of self-fertilization in a hermaphroditic animal. Proc Natl Acad Sci USA 95:617–620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamiya T, Kai W, Tasumi S, Oka A, Matsunaga T, Mizuno N, Fujita M, Suetake H, Suzuki S, Hosoya S et al (2012) A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (Fugu). PLoS Genet 8:e1002798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kenchington E, MacDonald B, Cao L, Tsagarakis D, Zouros E (2002) Genetics of mother-dependent sex ratio in blue mussels (Mytilus spp.) and implications for doubly uniparental inheritance of mitochondrial DNA. Genetics 161:1579–1588

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kenchington EL, Hamilton L, Cogswell A, Zouros E (2009) Paternal mtDNA and maleness are co-inherited but not causally linked in mytilid mussels. PLoS One 4:e6976

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kennedy VS (1983) Sex ratios in oysters, emphasizing Crassostrea virginica from Chesapeake Bay, Maryland. Veliger 25:329–338

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Korpelainen H (1990) Sex ratios and conditions required for environmental sex determination in animals. Biol Rev 65:147–184

    Article  CAS  PubMed  Google Scholar 

  • Kyriakou E, Kravariti L, Vasilopoulos T, Zouros E, Rodakis GC (2015) A protein binding site in the M mitochondrial genome of Mytilus galloprovincialis may be responsible for its paternal transmission. Gene 562:83–94

    Article  CAS  PubMed  Google Scholar 

  • Lango-Reynoso F (1999) Détermination de la sexualité chez l’huître Crassostrea gigas (Thunberg, 1793). Doctoral Thesis, Université de Bretagne Occidentale, Brest, 176 pp

    Google Scholar 

  • Lango-Reynoso F, Chávez-Villaba J, Le Pennec M (2006) Reproductive patterns of the Pacific oyster Crassostrea gigas in France. Invertebr Reprod Dev 49:41–50

    Article  Google Scholar 

  • Legube G, McWeeney SK, Lercher MJ, Akhtar A (2006) X-chromosome-wide profiling of MSL-1 distribution and dosage compensation in Drosophila. Genes Dev 20:871–883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leitão A, Chaves R (2008) Banding for chromosomal identification in bivalves: a 20-year history. Dyn Biochem Process Biotechnol Mol Biol 2:44–49

    Google Scholar 

  • Llera-Herrera R, García-Gasca A, Abreu-Goodger C, Huvet A, Ibarra AM (2013) Identification of male gametogenesis expressed genes from the scallop Nodipecten subnodosus by suppressive subtraction hybridization and pyrosequencing. PLoS One 8:e73176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lubet P (1959) Recherches sur le cycle sexuel et l’émission des gametes chez les mytilides et les pectinides (Mollusques bivalves). Rev Trav Inst Pêches Marit 23:387–548

    Google Scholar 

  • Lucas A (1965) Recherche sur la sexualité des mollusques bivalves. Bull Biol Fr Berg 99:115–247

    Google Scholar 

  • Machordom A, Araujo R, Toledo C, Zouros E, Ladoukakis ED (2015) Female-dependent transmission of paternal mtDNA is a shared feature of bivalve species with doubly uniparental inheritance (DUI) of mitochondrial DNA. J Zool Syst Evol Res 53:200–204

    Article  Google Scholar 

  • Mackie GL (1984) Bivalves. In: Tompa A, Verdonk NH, Biggelaar JA (eds) The Mollusca, Reproduction, vol 7. Academic, New York, pp 351–418

    Google Scholar 

  • Manolakou P, Lavranos G, Angelopoulou R (2006) Molecular patterns of sex determination in the animal kingdom: a comparative study of the biology of reproduction. Reprod Biol Endocrinol 4:59

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Matsumoto T, Masaoka T, Fujiwara A, Nakamura Y, Satoh N, Awaji M (2013) Reproduction-related genes in the pearl oyster genome. Zoolog Sci 30:826–850

    Article  CAS  PubMed  Google Scholar 

  • McMahon RF (1999) Invasive characteristics of the freshwater bivalve Corbicula fluminea. In: Claudi R, Leach JH (eds) Nonindigenous freshwater organisms: vectors, biology and impact. Lewis Press, Washington, DC, pp 315–343

    Google Scholar 

  • McKoy JL (1980) Biology, exploitation and management of giant clams (Tridacnidae) in the Kingdom of Tonga. Fish Bull Tongu 1:1–6

    Google Scholar 

  • Menzel RW (1968) Chromosome number in nine families of marine pelecypod mollusks. Nautilus 82:49–50

    Google Scholar 

  • Merrill AS, Burch JB (1960) Hermaphroditism in the sea scallop Placopecten magellanicus. Biol Bull 119:197–201

    Article  Google Scholar 

  • Milani L, Ghiselli F, Guerra D, Breton S, Passamonti M (2013) A comparative analysis of mitochondrial ORFans: new clues on their origin and role in species with doubly uniparental inheritance of mitochondria. Genome Biol Evol 5:1408–1434

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Milani L, Ghiselli F, Maurizii MG, Nuzhdin SV, Passamonti M (2014) Paternally transmitted mitochondria express a new gene of potential viral origin. Genome Biol Evol 6:391–405

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mori K, Muramatsu T, Nakamura Y (1969) Effect of steroid on oyster III: sex reversal from male to female in Crassostrea gigas by estradiol-17β. Bull Jap Soc Sci Fish 35:1072–1076

    Article  CAS  Google Scholar 

  • Morton B (1981) The Anomalodesmata. Malacologia 21:35–60

    Google Scholar 

  • Morton B (1991) Do the Bivalvia demonstrate environment-specific sexual strategies? A Hong Kong model. J Zool Lond 223:131–142

    Article  Google Scholar 

  • Moss SM (1989) Effects of exogenous androgens on growth, biochemical composition, and reproduction of the coot clam, Mulinia lateralis. Pac Sci 43:200

    Google Scholar 

  • Naimi A, Martinez A-S, Specq M-L, Mrac A, Diss B, Mathieu M, Sourdaine P (2009a) Identification and expression of a factor of the DM family in the oyster Crassostrea gigas. Comp Biochem Physiol A Mol Integr Physiol 152:189–196

    Article  CAS  PubMed  Google Scholar 

  • Naimi A, Martinez A-S, Specq M-L, Diss B, Mathieu M, Sourdaine P (2009b) Molecular cloning and gene expression of Cg-Foxl2 during the development and the adult gametogenetic cycle in the oyster Crassostrea gigas. Comp Biochem Physiol B Biochem Mol Biol 154:134–142

    Article  CAS  PubMed  Google Scholar 

  • Naylor RL, Goldburg RJ, Primavera JH, Kautsky N, Beveridge MC, Clay J, Folke C, Lubchenco J, Mooney H, Troell M (2000) Nature 405:1017–1024

    Article  CAS  PubMed  Google Scholar 

  • Oldfield E (1961) The functional morphology of Kellia suborbicularis (Montagu), Montacuta ferruginosa (Montagu) and M. substriata (Montagu), (Mollusca, Lamellibranchiata). J Moll Stud 34:255–295

    Article  Google Scholar 

  • Park JJ, Shin YK, Hung SSO, Romano N, Cheon Y-P, Kim JW (2015) Reproductive impairment and intersexuality in Gomphina veneriformis (Bivalvia: Veneridae) by the tributyltin compound. Anim Cells Syst 19:61–68

    Article  CAS  Google Scholar 

  • Passamonti M, Ghiselli F (2009) Doubly uniparental inheritance: two mitochondrial genomes, one precious model for organelle DNA inheritance and evolution. DNA Cell Biol 28:79–89

    Article  CAS  PubMed  Google Scholar 

  • Pigneur L-M, Marescaux J, Roland K, Etoundi E, Descy J-P, Van Doninck K (2011) Phylogeny and androgenesis in the invasive Corbicula clams (Bivalvia, Corbiculidae) in Western Europe. BMC Evol Biol 11:147

    Article  PubMed  PubMed Central  Google Scholar 

  • Pigneur L-M, Hedtke SM, Etoundi E, Van Doninck K (2012) Androgenesis: a review through the study of selfish shellfish Corbicula spp. Heredity 108:581–591

    Article  PubMed  PubMed Central  Google Scholar 

  • Policansky D (1982) Sex change in plants and animals. Annu Rev Ecol Syst 13:471–495

    Article  Google Scholar 

  • Purchon RD (1968) The biology of the Mollusca. Pergamon Press, Oxford, 560 pp

    Google Scholar 

  • Rhen T, Metzger K, Schroeder A, Woodward R (2007) Expression of putative sex determining genes during the thermosensitive period of gonad development in the snapping turtle, Chelydra serpentina. Sex Dev 1:255–270

    Article  CAS  PubMed  Google Scholar 

  • Robicheau BM (2016) Doubly uniparental inheritance of mitochondrial DNA in the marine horse mussel (Modiolus modiolus): a comparison of female- and male-associated mitochondrial genomes. Msc. Thesis, Acadia University, Wolfville, N.S. 170 pp

    Google Scholar 

  • Rodríguez-Jaramillo C, Hurtado MA, Romero-Vivas E, Ramírez JL, Manzano M, Palacios E (2008) Gonadal development and histochemistry of the tropical oyster, Crassostrea corteziensis (Hertlein, 1951) during an annual reproductive cycle. J Shellfish Res 27:1129–1141

    Article  Google Scholar 

  • Romo Piñera AK, Ceballos-Vázquez BP, García-Domínguez F, Arellano-Martínez M (2009) Unusual high frequency of hermaphroditism in the gonochoric bivalve Megapitaria Squalida (Sowerby, 1835) (Veneridae). J Shellfish Res 28:785–789

    Article  Google Scholar 

  • Russell-Hunter WD (1979) The evolution of filter-feeding bivalves. In: A life of invertebrates. Macmillan, New York

    Google Scholar 

  • Saavedra C, Reyero MI, Zouros E (1997) Male-dependent doubly uniparental inheritance of mitochondrial DNA and female-dependent sex ratio in the mussel Mytilus galloprovincialis. Genetics 145:1073–1082

    CAS  PubMed  PubMed Central  Google Scholar 

  • Santerre C, Sourdaine P, Martinez A-S (2012) Expression of a natural antisense transcript of Cg-Foxl2 during the gonadic differentiation of the oyster Crassostrea gigas: first demonstration in the gonads of a lophotrochozoa species. Sex Dev 6:210–221

    Article  CAS  PubMed  Google Scholar 

  • Santerre C, Sourdaine P, Marc N, Mingant C, Robert R, Martinez A-S (2013) Oyster sex determination is influenced by temperature—first clues in spat during first gonadic differentiation and gametogenesis. Comp Biochem Physiol Part A Mol Integr Physiol 165:61–69

    Article  CAS  Google Scholar 

  • Santerre C, Sourdaine P, Adeline B, Martinez A-S (2014) Cg-SoxE and Cg-β-catenin, two new potential actors of the sex-determining pathway in a hermaphrodite lophotrochozoan, the Pacific oyster Crassostrea gigas. Comp Biochem Physiol Part A Mol Integr Physiol 167:68–76

    Article  CAS  Google Scholar 

  • Sastry AN (1968) Relationship among food, temperature and gonad development of the bay scallop Argopecten irradians Lamarck. Physiol Zool 6:374–375

    Google Scholar 

  • Sastry AN (1979) Pelecypoda (excluding ostreidae). In: Giese AC, Pearse JC (eds) Reproduction of marine invertebrates. Academic, New York, pp 113–192

    Chapter  Google Scholar 

  • Shi J, Hong Y, Sheng J, Peng K, Wang J (2015) De novo transcriptome sequencing to identify the sex-determination genes in Hyriopsis schlegelii. Biosci Biotechnol Biochem 79:1257–1265

    Article  CAS  PubMed  Google Scholar 

  • Shoemaker-Daly CM, Jackson K, Yatsu R, Matsumoto Y, Crews D (2010) Genetic network underlying temperature-dependent sex determination is endogenously regulated by temperature in isolated cultured Trachemys scripta gonads. Dev Dyn 239:1061–1075

    Article  CAS  PubMed  Google Scholar 

  • Shumway SE (ed) (2011) Shellfish aquaculture and the environment. Wiley-Blackwell, Singapore

    Google Scholar 

  • Shumway SE, Parsons GJ (eds) (2011) Scallops: biology, ecology and aquaculture, vol 40. Elsevier, Oxford

    Google Scholar 

  • Soria RG, Pascual MS, Cartes VHF (2002) Reproductive cycle of the cholga paleta Atrina seminuda Lamarck 1819 (Bivalvia Pinnidae) from northern Patagonia, Argentina. J Shellfish Res 21:479–488

    Google Scholar 

  • Stenyakina A, Walters LJ, Hoffman EA, Calestani C (2010) Food availability and sex reversal in Mytella charruana, an introduced bivalve in the southeastern United States. Mol Reprod Dev 77:222–230

    CAS  PubMed  Google Scholar 

  • Stewart DT, Breton S, Blier PU, Hoeh WR (2009) Masculinization events and doubly uniparental inheritance of mtDNA: a model for understanding the evolutionary dynamics of gender-associated mtDNA in mussels. In: Pontarotti P (ed) Evolutionary biology from concept to application II. Springer, Berlin, pp 163–173

    Google Scholar 

  • Sutherland B, Stewart D, Kenchington ER, Zouros E (1998) The fate of paternal mitochondrial DNA in developing female mussels, Mytilus edulis: implications for the mechanism of doubly uniparental inheritance of mitochondrial DNA. Genetics 148:341–347

    CAS  PubMed  PubMed Central  Google Scholar 

  • Teaniniuraitemoana V, Huvet A, Levy P, Klopp C, Lhuillier E, Gaertner-Mazouni N, Gueguen Y, Le Moullac G (2014) Gonad transcriptome analysis of pearl oyster Pinctada margaritifera: identification of potential sex differentiation and sex determining genes. BMC Genomics 15:491

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Teaniniuraitemoana V, Huvet A, Levy P, Gaertner-Mazouni N, Gueguen Y, Le Moullac G (2015) Molecular signatures discriminating the male and the female sexual pathways in the pearl oyster Pinctada margaritifera. PLoS One 10:e0122819

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Teaniniuraitemoana V, Leprêtre M, Levy P, Vanaa V, Parrad S, Gaertner-Mazouni N, Gueguen Y, Huvet A, Le Moullac G (2016) Effect of temperature, food availability, and estradiol injection on gametogenesis and gender in the pearl oyster Pinctada margaritifera. J Exp Zool 325A:13–24

    Article  CAS  Google Scholar 

  • Thiriot-Quiévreux C (2002) Review of the literature on bivalve cytogenetics in the last ten years. Cah Biol Mar 43:17–26

    Google Scholar 

  • Thiriot-Quiévreux C, Insua A (1992) Nucleolar organiser region variation in the chromosomes of three oyster species. J Exp Mar Biol Ecol 157:33–40

    Article  Google Scholar 

  • Tong Y, Zhang Y, Huang J, Xiao S, Zhang Y, Li J, Chen J, Yu Z (2015) Transcriptomics analysis of Crassostrea hongkongensis for the discovery of reproduction-related genes. PLoS One 10:e0134280

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tsuda M, Sasaoka Y, Kiso M, Abe K, Haraguchi S, Kobayashi S, Saga Y (2003) Conserved role of nanos proteins in germ cell development. Science 301:1239–1241

    Article  CAS  PubMed  Google Scholar 

  • Van Doninck K, Schön I, De Bruyn L, Martens K (2002) A general purpose genotype in an ancient asexual. Oecologia 132:205–212

    Article  PubMed  Google Scholar 

  • Vaught KC (1989) A classification of the living Mollusca. American Malacologists, Melbourne

    Google Scholar 

  • Veitia RA (2010) FOXL2 vs. SOX9: a lifelong “battle of the sexes”. Bioessays 32:375–380

    Article  CAS  PubMed  Google Scholar 

  • Wada K (1978) Chromosome karyotypes of three bivalves: the oysters, Isognomon alatus and Pinctada imbricata, and the bay scallop, Argopecten irradians. Biol Bull 155:235–245

    Article  Google Scholar 

  • Wallis MC, Waters PD, Graves JA (2008) Sex determination in mammals – before and after the evolution of SRY. Cell Mol Life Sci 65:3182

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Croll RP (2004) Effects of sex steroids on gonadal development and gender determination in the sea scallop, Placopecten magellanicus. Aquaculture 238:483–498

    Article  CAS  Google Scholar 

  • Yamaguchi T, Yamaguchi S, Hirai T, Kitano T (2007) Follicle-stimulating hormone signaling and Foxl2 are involved in transcriptional regulation of aromatase gene during gonadal sex differentiation in Japanese flounder, Paralichthys olivaceus. Biochem Biophys Res Commun 359:935–940

    Article  CAS  PubMed  Google Scholar 

  • Yanovych LM, Pampura MM, Vasilieva LA, Mezhherin SV (2010) Mass hermaphroditism of Unionidae (Mollusca, Bivalvia, Unionidae) in the Central Polissya region. Rep Nat Acad Sci Ukr 6:158–167

    Google Scholar 

  • Yu FF, Wang MF, Zhou L, Gui JF, Yu XY (2011) Molecular cloning and expression characterization of Dmrt2 in Akoya Pearl oysters, Pinctada Martensii. J Shellfish Res 30:247–254

    Article  Google Scholar 

  • Zhang N, Xu F, Guo X (2014) Genomic analysis of the Pacific oyster (Crassostrea gigas) reveals possible conservation of vertebrate sex determination in a Mollusc. G3 (Bethesda) 4:2207–2217

    Article  Google Scholar 

  • Zouros E (2000) The exceptional mitochondrial DNA system of the mussel family Mytilidae. Genes Genet Syst 75:313–318

    Article  CAS  PubMed  Google Scholar 

  • Zouros E (2013) Biparental inheritance through uniparental transmission: the doubly uniparental inheritance (DUI) of mitochondrial DNA. Evol Biol 40:1–31

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sophie Breton .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Breton, S., Capt, C., Guerra, D., Stewart, D. (2018). Sex-Determining Mechanisms in Bivalves. In: Leonard, J. (eds) Transitions Between Sexual Systems. Springer, Cham. https://doi.org/10.1007/978-3-319-94139-4_6

Download citation

Publish with us

Policies and ethics