Skip to main content
SpringerLink
Log in

Patterns of gamete incompatibility between the blue mussels Mytilus edulis and M. trossulus

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Previous research on gametic incompatibility in marine invertebrates suggests that for highly dispersive marine invertebrate species, barriers to fertilization among closely related taxa are often incomplete and sometimes asymmetric. The nature of these barriers can dramatically affect the patterns of gene flow and genetic differentiation between species, and thus speciation. Blue mussels, in the genus Mytilus, are genetically distinct in allopatry yet hybrids are present wherever any two species within the group co-occur. The present study sampled M. edulis (L.) and M. trossulus (Gould) in May and June 2001 from the East Bay section of Cobscook Bay, Maine, USA (latitude 44°56′30″N; longitude 67°07′50″W), where the two species are sympatric. Gamete incompatibility was investigated in a series of laboratory fertilizations carried out in July 2001. The proportion of fertilized eggs typically exceeded 80% at sperm concentrations of 103–104 ml−1 among intraspecific matings (n=18), but was <30% even at sperm concentrations in excess of 105–106 ml−1 for interspecific matings (n=13). Further analysis indicated that approximately 100- to 700-fold higher sperm concentrations were required to achieve 20% fertilization in interspecific matings relative to intraspecific matings, indicating strong barriers to interspecific fertilization. The proportion of fertilized eggs did not follow this general pattern in all matings, however. The eggs from two (out of five) M. edulis females were almost as receptive to M. trossulus sperm as they were to M. edulis sperm. In contrast, the eggs from all M. trossulus females (n=3) were unreceptive to M. edulis sperm, suggesting that fertilization barriers between these species may be asymmetric. Given the experimental design employed in this study, the results are also consistent with a strong maternal or egg effect on the level of interspecific gamete compatibility in M. edulis.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

References

  • Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New York

  • Banks MA, McGoldrick DJ, Borgeson W, Hedgecock D (1994) Gametic incompatibility and genetic divergence of Pacific and Kumamoto oysters, Crassostrea gigas and C. sikamea. Mar Biol 121:127–135

    Google Scholar 

  • Bates JA, Innes DJ (1995) Genetic variation among populations of Mytilus spp. in eastern Newfoundland. Mar Biol 124:417–424

    Google Scholar 

  • Biermann CH (1998) The molecular evolution of sperm bindin in six species of sea urchins (Echinodia: Strongylocentrotidae). Mol Biol Evol 15:1761–1767

    CAS  PubMed  Google Scholar 

  • Bierne N, David P, Boudry P, Bonhomme F (2002) Assortative fertilization and selection at larval stage in the mussels Mytilus edulis and M. galloprovincialis. Evolution 56:292–298

    PubMed  Google Scholar 

  • Boecklen WJ, Howard DJ (1997) Genetic analysis of hybrid zones: numbers of markers and power of resolution. Ecology 78:2611–2616

    Google Scholar 

  • Buss LW, Yund PO (1989) A sibling species group of Hydractinia in the northeastern United States. J Mar Biol Assoc UK 69:857–874

    Google Scholar 

  • Butlin R (1989) Reinforcement of pre-mating isolation. In: Otte D, Endler JA (eds) Speciation and it's consequences. Sinauer, Sunderland, pp 158–179

  • Comesaña AS, Sanjuan A (1997) Microgeographic allozyme differentiation in the hybrid zone of Mytilus galloprovincialis Lmk. and M. edulis L. on the continental European coast. Helgol Meeresunters 51:107–124

    Google Scholar 

  • Comesaña AS, Toro JE, Innes DJ, Thompson RJ (1999) A molecular approach to the ecology of a mussel (Mytilus edulis–M. trossulus) hybrid zone on the east coast of Newfoundland, Canada. Mar Biol 133:213–221

    Article  Google Scholar 

  • Dobzhansky T (1940) Speciation as a stage in evolutionary divergence. Am Nat 74:312–321

    Article  Google Scholar 

  • Garbers DL (1989) Molecular basis of fertilization. Annu Rev Biochem 58:719–742

    Article  CAS  PubMed  Google Scholar 

  • Gardner JPA (1994) The structure and dynamics of naturally occurring hybrid Mytilus edulis and M. galloprovincialis (Bivalvia, Mollusca) populations: review and interpretation. Arch Hydrobiol Suppl 99:37–71

    Google Scholar 

  • Gardner JPA, Thompson R J (2001) The effects of coastal and estuarine conditions on the physiology and survivorship of the mussels Mytilus edulis, M. trossulus and their hybrids. J Exp Mar Biol Ecol 265:119–140

    Article  Google Scholar 

  • Gosling EM (1992) Systematics and geographic distribution of Mytilus. In: Gosling EM (ed) The mussel Mytilus: ecology, physiology, genetics, and culture. Elsevier, New York, pp 1–20

  • Heath DD, Rawson PD, Hilbish TJ (1995) PCR-based nuclear markers identify alien blue mussel (Mytilus spp.) genotypes on the west coast of Canada. Can J Fish Aquat Sci 52:2621–2627

    CAS  Google Scholar 

  • Hellberg ME, Vacquier VD (1999) Rapid evolution of fertilization selectivity and lysin cDNA sequences in teguline gastropods. Mol Biol Evol 16:839–848

    CAS  PubMed  Google Scholar 

  • Hilbish TJ, Bayne BL, Day A (1994) Genetics of physiological differentiation within the marine mussel genus Mytilus. Evolution 48:267–286

    Google Scholar 

  • Johannesson K, Kautsky N, Tedengren M (1990) Genotypic and phenotypic differences between Baltic and North Sea populations of Mytilus edulis evaluated through reciprocal transplantations. II. Genetic variation. Mar Ecol Prog Ser 59:203–210

    Google Scholar 

  • Koehn RK, Hall JG, Innes DJ, Zera AZ (1984) Genetic differentiation of Mytilus edulis in eastern North America. Mar Biol 70:117–126

    Google Scholar 

  • Knowlton N, Maté J, Guzman H, Rowan R (1997) Direct evidence for reproductive isolation among the three species of the Montastraea annularis complex in Central America (Panama and Honduras). Mar Biol 127:705–711

    Article  Google Scholar 

  • Leighton DL, Lewis CA (1982) Experimental hybridization in abalone. Int J Invertebr Reprod Dev 5:273–282

    Google Scholar 

  • Lessios HA, Cunningham CW (1990) Gametic incompatibility between species of the sea urchin Echinometra on the two sides of the Isthmus of Panama. Evolution 44:933–941

    Google Scholar 

  • Mallet AL, Carver CE (1995) Comparative growth and survival patterns of Mytilus trossulus and Mytilus edulis in Atlantic Canada. Can J Fish Aquat Sci 52:1873–1880

    Google Scholar 

  • Maloy A, Barber BJ, Rawson PD (2003) Gametogenesis in a sympatric population of blue mussels, Mytilus edulis and Mytilus trossulus, from Cobscook Bay, Maine (USA). J. Shellfish Res (in press)

  • McCartney MA, Lessios HA (2002) Quantitative analysis of gametic incompatibility between closely related species of neotropical sea urchins. Biol Bull (Woods Hole) 202:166–181

    Google Scholar 

  • McDonald JH, Seed R, Koehn RK (1991) Allozymes and morphometric characters of three species of Mytilus in the Northern and Southern Hemispheres. Mar Biol 111:323–333

    Google Scholar 

  • Metz EC, Palumbi SR (1996) Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol Biol Evol 13:397–406

    CAS  PubMed  Google Scholar 

  • Metz EC, Kane RE, Yanagimachi H, Palumbi SR (1994) Fertilization between closely related sea urchins is blocked by incompatibilities during sperm–egg attachment and early stages of fusion. Biol Bull (Woods Hole) 187:23–34

    Google Scholar 

  • Neter J, Wasserman W, Kutner MH (1985) Applied linear statistical models. Irwin, Homewood, Ill.

  • Palumbi SR (1992) Marine speciation on a small planet. Trends Ecol Evol 7:114–118

    Google Scholar 

  • Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572

    Article  Google Scholar 

  • Palumbi SR (1999) All males are not created equal: fertility differences depend on gamete recognition polymorphisms in sea urchins. Proc Natl Acad Sci USA 96:12632–12637

    Article  CAS  Google Scholar 

  • Pawlik J (1988) Larval settlement and metamorphosis of sabellariid polychaetes, with special reference to Phragmatopoma lapidosa, a reef-building species, and Sabellaria floridens, a non-gregarious species. Bull Mar Sci 43:41–60

    Google Scholar 

  • Pernet B (1999) Gamete interactions and genetic differentiation among three sympatric polychaetes. Evolution 53:435–446

    CAS  Google Scholar 

  • Rawson PD, Hilbish TJ (1995) Evolutionary relationships among the male and female mitochondrial DNA lineages in the Mytilus edulis species complex. Mol Biol Evol 12:893–901

    CAS  PubMed  Google Scholar 

  • Rawson PD, Joyner K, Hilbish TJ (1996) Evidence for intragenic recombination within a novel genetic marker that distinguishes mussels in the Mytilus edulis species complex. Heredity 77:599–607

    CAS  PubMed  Google Scholar 

  • Rawson PD, Hayhurst S, Vanscoyoc B (2001) Species composition of blue mussel populations in the northeastern Gulf of Maine. J Shellfish Res 20:31–38

    Google Scholar 

  • Riginos C, McDonald JH (2003) Positive selection on an acrosomal sperm protein, M7 lysin, in three species of the mussel genus Mytilus. Mol Biol Evol 20:200–207

    Article  CAS  PubMed  Google Scholar 

  • Strathmann RR (1981) On barriers to hybridization between Strongylocentrotus droebachiensis (O.F. Muller) and S. pallidus (G.O. Sars). J Exp Mar Biol Ecol 55:39–47

    Google Scholar 

  • Swanson WJ, Vacquier VD (1997) The abalone egg receptor for sperm lysin is a giant multivalent molecule. Proc Natl Acad Sci USA 94:6724–6729

    Article  CAS  Google Scholar 

  • Swanson WJ, Vacquier VD (1998) Concerted evolution in an egg receptor for a rapidly evolving abalone sperm protein. Science 281:710–712

    Article  CAS  PubMed  Google Scholar 

  • Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3:137–144

    Article  CAS  PubMed  Google Scholar 

  • Takagi T, Nakamura A, Ryusaku D, Kyozuka K (1994) Isolation, characterization, and primary structure of three major proteins obtained from Mytilus edulis sperm. J Biochem 116:598–605

    CAS  PubMed  Google Scholar 

  • Toro JE, Thompson RJ, Innes DJ (2002) Reproductive isolation and reproductive output in two sympatric mussel species (Mytilus edulis, M. trossulus) and their hybrids from Newfoundland. Mar Biol 141:897–909

    Article  Google Scholar 

  • Väinöla R, Hvilsom MM (1991) Genetic divergence and a hybrid zone between Baltic Sea and North Sea Mytilus populations (Mytilidae: Mollusca). Biol J Linn Soc 43:127–148

    Google Scholar 

  • Varvio S-L, Koehn RK, Väinöla R (1988) Evolutionary genetics of the Mytilus edulis complex in the North Atlantic region. Mar Biol 98:51–60

    Google Scholar 

  • Vermeij GJ (1991) Anatomy of an invasion: the trans-Arctic interchange. Paleobiology 17:281–307

    Google Scholar 

  • Vogel H, Czihak G, Chang P, Wolf W (1982) Fertilization kinetics of sea urchin eggs. Math Biosci 58:189–216

    Article  Google Scholar 

  • Waelbroeck C, Duplessy J-C, Michel E, Labeyrie L, Paillard D, Duprat J (2001) The timing of the last deglaciation in North Atlantic climate records. Nature 412:724–727

    Article  CAS  PubMed  Google Scholar 

  • Wilhelm R, Hilbish TJ (1998) Assessment of natural selection in a hybrid population of mussels: evaluation of exogenous vs endogenous selection models. Mar Biol 131:505–514

    Article  Google Scholar 

Download references

Acknowledgements

C. Slaughter participated in this research as part of the National Science Foundation Research Experience for Undergraduates program at the Darling Marine Center (OCE-99-10188). Additional support was provided by the University of Maine Sea Grant Program under contract 99-343 and Hatch funds provided by the U.S. Department of Agriculture and the Maine Agriculture and Forestry Experiment Station (project no. ME08510) to P. Rawson; P. Yund was supported by funding from the National Science Foundation (OCE-01-22031). A previous draft of this manuscript was strengthened appreciably by comments from E. Fisher. This is Maine Agricultural and Forest Experiment Station external publication no. 2636 and contribution no. 378 from the Darling Marine Center. We certify that the research described within this document complies with the current laws of our country.

Author information

Authors and Affiliations

  1. School of Marine Sciences, University of Maine, Orono, ME 04469, USA

    P. D. Rawson & P. O. Yund

  2. Department of Biological Sciences, University of North Carolina at Wilmington, Wilmington, NC 28403, USA

    C. Slaughter

  3. The Darling Marine Center, University of Maine, Walpole, ME 04573, USA

    P. O. Yund

Authors
  1. P. D. Rawson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. Slaughter
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. O. Yund
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. D. Rawson.

Additional information

Communicated by J.P. Grassle, New Brunswick

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rawson, P.D., Slaughter, C. & Yund, P.O. Patterns of gamete incompatibility between the blue mussels Mytilus edulis and M. trossulus . Marine Biology 143, 317–325 (2003). https://doi.org/10.1007/s00227-003-1084-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-003-1084-x

Keywords

Search

Navigation