Skip to main content
Log in

Geographic variation in allele frequency of the gamete recognition protein M7 lysin throughout a mosaic blue mussel hybrid zone

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Divergence at gamete recognition loci is hypothesized to result in speciation in broadcast spawning invertebrates. Many gamete recognition loci evolve quickly and show patterns of positive selection, yet the advantage of divergence is rarely known. M7 lysin is a sperm protein in the Mytilus edulis species complex that shows evidence of adaptive evolution. This locus is polymorphic with two distinct clades within Mytilus galloprovincialis, one of which, the D clade, shows the strongest signal of positive selection. We tested whether the geographic patterns in allele frequency were consistent with the hypothesis that positive selection on D clade alleles (G D ) was due to reinforcement. Populations of M. edulis showed little evidence of introgression of G D alleles, but there was no consistent evidence of reproductive character displacement. The lack of consistent patterns expected of reinforcement suggests that another mechanism is likely responsible for the adaptive divergence of M7 lysin.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Ann Rev Ecol Syst 16:113–148

    Article  Google Scholar 

  • Bierne N, David P, Langlade A, Bonhomme F (2002) Can habitat specialization maintain a mosaic hybrid zone in marine bivalves? Mar Ecol Prog Ser 245:157–170

    Article  Google Scholar 

  • Bierne N, Bonhomme F, Boudry P, Szulkin M, David P (2006) Fitness landscapes support the dominance theory of post-zygotic isolation in the mussels M. edulis and M. galloprovicialis. Proc R Soc B 273:1253–1260

    Article  CAS  Google Scholar 

  • Brannock PM, Wethey DS, Hilbish TJ (2009) Extensive hybridization with minimal introgression in Mytilus galloprovincialis and M. trossulus in Hokkaido, Japan. Mar Ecol Prog Ser 383:161–171

    Article  CAS  Google Scholar 

  • Carney SE, Hodges SA, Arnold ML (1996) Effect of differential pollen-tube growth on hybridization in the Louisiana irises. Evolution 50:1871–1878

    Article  Google Scholar 

  • Chapman MA, Forbes DG, Abbot RJ (2005) Pollen competition among two species of Senecio (Asteraceae) that form a hybrid zone on Mt. Etna, Sicily. Am J Bot 92:730–735

    Article  Google Scholar 

  • Coustau C, Renaud F, Delay B (1991) Genetic characterization of the hybridization between M. edulis and M. galloprovincialis on the Atlantic coast of France. Mar Biol 11:87–93

    Article  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Inc., Sunderland

    Google Scholar 

  • Daguin C, Borsa P (1999) Genetic characterization of Mytilus galloprovincialis Lmk. In North West Africa using nuclear DNA markers. J Exp Mar Biol Ecol 235:55–65

    Article  CAS  Google Scholar 

  • Diaz A, Macnair MR (1999) Pollen tube competition as a mechanism of prezygotic reproductive isolation between Mimulus nasutus and its presumed progenitor M. guttatus. New Phytol 144:471–478

    Article  Google Scholar 

  • Emms SK, Hodges SA, Arnold ML (1996) Pollen-tube competition, siring success, and consistent asymmetric hybridization in Louisiana irises. Evolution 50:2201–2206

    Article  Google Scholar 

  • Faure MF, David P, Bonhomme F, Bierne N (2008) Genetic hitchhiking in a subdivided population of Mytilus edulis. BMC Evol Biol 8:164

    Article  Google Scholar 

  • Gardner JPA, Skibinski DOF, Bajdik CD (1993) Shell growth and viability differences between the marine mussels Mytilus edulis (L.), Mytilus galloprovincialis (Lmk.), and their hybrids from two sympatric populations in S.W England. Biol Bull 185:405–416

    Article  Google Scholar 

  • Geyer LB, Palumbi SR (2003) Reproductive character displacement and the genetics of gamete recognition in tropical sea urchins. Evolution 57:1049–1060

    Google Scholar 

  • Geyer LB, Palumbi SR (2004) Conspecific sperm precedence in two species of tropical sea urchins. Evolution 59:97–105

    Google Scholar 

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

    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

    Article  CAS  Google Scholar 

  • Heß A-K, Bartel M, Roth K, Messerschmidt K, Heilmann K, Kenchington E, Micheel B, Stuckas H (2012) Expression of M6 and M7 lysin in Mytilus edulis is not restricted to sperm, but occurs also in oocytes and somatic tissue of males and females. Mol Reprod Dev 79:517–524

    Article  Google Scholar 

  • Hilbish TJ, Carson EW, Plante JR, Weaver LA, Gilg MR (2002) Distribution of Mytilus edulis, M. galloprovincialis, and their hybrids in open-coast populations of mussels in southwestern England. Mar Biol 140:137–142

    Article  Google Scholar 

  • Howard DJ (1993) Reinforcement: origin, dynamics, and fate of an evolutionary hypothesis. In: Hybrid Zones and the evolutionary process. Oxford university press, New York

    Google Scholar 

  • Howard DJ (1999) Conspecific sperm and pollen precedence and speciation. Ann Rev Ecol Syst 30:109–132

    Article  Google Scholar 

  • Howard DJ, Gregory PG, Chu J, Cain ML (1998) Conspecific sperm precedence is an effective barrier to hybridization between closely related species. Evolution 52:511–516

    Article  Google Scholar 

  • Inoue K, Waite JH, Matsuoka M, Odo S, Harayama S (1995) Interspecific variations in adhesive protein sequences of Mytilus edulis, M. galloprovincialis, and M. trossulus. Biol Bull 189:370–375

    Article  CAS  Google Scholar 

  • Kijewski T, Smietanka B, Zbawicka M, Gosling E, Hummel H, Wenne R (2011) Distribution of Mytilus taxa in European coastal areas as inferred from molecular markers. J Sea Res 65:224–234

    Article  Google Scholar 

  • Kresge N, Vacquier VD, Stout CD (2000) Abalone lysin: the dissolving and evolving sperm protein. BioEssays 23:95–103

    Article  Google Scholar 

  • Levitan DR, Ferrel DL (2006) Selection on gamete recognition proteins depends on sex, density, and genotype frequency. Science 312:267–269

    Article  CAS  Google Scholar 

  • Levitan DR, Strapper AP (2010) Simultaneous positive and negative frequency dependent selection on sperm bind in, a gamete recognition protein in the sea urchin Strongylocentrotus purpuratus. Evolution 64:785–797

    Article  CAS  Google Scholar 

  • McCartney MA, Lima TG (2011) Evolutionary consequences of introgression at M7 lysin, a gamete recognition locus, following secondary contact between a blue mussel species. Integr Comp Biol 51:474–484

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Palumbi SR (2009) Speciation and the evolution of gamete recognition genes: pattern and process. Heredity 102:66–76

    Article  CAS  Google Scholar 

  • Price CSC (1997) Conspecific sperm precedence in Drosophila. Nature 388:663–666

    Article  CAS  Google Scholar 

  • Quesada H, Beynom CM, Skibinski DO (1995) A mitochondrial DNA discontinuity in the mussel Mytilus galloprovincialis Lmk: pleistocene vicariance biogeography and secondary intergradation. Mol Biol Evol 12:521–524

    CAS  Google Scholar 

  • Ramsey J, Bradshaw HD Jr, Schemske DW (2003) Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution 57:1520–1534

    Google Scholar 

  • Rawson PD, Joyner KL, Meetze 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

    Article  CAS  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 

  • Rawson PD, Slaughter C, Yund PO (2003) Patterns of gamete incompatibility between the blue mussels Mytilus edulis and M. trossulus. Mar Biol 143:317–325

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) Genepop (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249

    Google Scholar 

  • Rieseberg LH, Desrochers AM, Youn SJ (1995) Interspecific pollen competition as a reproductive barrier between sympatric species of Helianthus (Asteraceae). Am J Bot 82:515–519

    Article  Google Scholar 

  • Riginos C, Cunningham CW (2005) Local adaptation and species segregation in two mussel (Mytilus edulis x Mytilus trossulus) hybrid zones. Mol Ecol 14:381–400

    Article  CAS  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  Google Scholar 

  • Riginos C, Sukhdeo K, Cunningham CW (2002) Evidence for selection at multiple allozyme loci across a mussel hybrid zone. Mol Biol Evol 19:347–351

    Article  CAS  Google Scholar 

  • Riginos C, Wang D, Abrams AJ (2006) Geographic variation and positive selection on M7 lysin, an acrosomal sperm protein in mussels (Mytilus spp.). Mol Biol Evol 23:1952–1965

    Article  CAS  Google Scholar 

  • Rousset F (2008) Genepop ‘007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Sanjuan A, Zapata C, Alvarez C (1997) Genetic differentiation in Mytilus galloprovincialis Lmk. Throughout the world. Ophelia 47:13–31

    Article  Google Scholar 

  • Slaughter C, McCartney MA, Yund PO (2008) Comparison of gamete compatibility between two blue mussel species in sympatry and allopatry. Biol Bull 214:57–66

    Article  Google Scholar 

  • Smietanka B, Burzynski A, Wenne R (2009) Molecular population genetics of male and female mitochondrial genomes in European mussels Mytilus. Mar Biol 156:913–925

    Article  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry. W. H Freeman, New York

    Google Scholar 

  • Springer SA, Crespi BJ (2007) Adaptive gamete-recognition divergence in a hybridizing Mytilus population. Evolution 61(4):772–783

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Takagi T, Nakamura A, Deguchi R, Kyozuka K (1994) Isolation, characterization, and primary structure of three major proteins obtained from Mytilus edulis sperm. J Biochem 116(3):598–605

    CAS  Google Scholar 

  • Tomaiuolo M, Levitan DR (2010) Modeling how reproductive ecology can drive protein diversification and result in linkage disequilibrium between sperm and egg proteins. Am Nat 176:14–25

    Article  Google Scholar 

  • Toro J, Innes DJ, Thompson RJ (2004) Genetic variation among life-history stages of mussels in a M. edulisM. trossulus hybrid zone. Mar Biol 145:713–725

    Google Scholar 

  • Vacquier VD, Carner KR, Stout CD (1990) Species specific sequences of abalone lysine, the sperm protein that creates a whole in the egg envelope. Proc Natl Acad Sci USA 87:5792–5796

    Article  CAS  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 

  • Williams JH Jr, Friedman WE, Arnold ML (1999) Developmental selection within the angiosperm style: using gamete DNA to visualize interspecific pollen competition. Proc Natl Acad Sci USA 96:9201–9206

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank R.R. Kirby for valuable discussions of the results and for providing laboratory space at the Marine Biological Association in Plymouth, UK, and also Rhiannon Rognstad for mapping input. Funding for this project was provided by the National Science Foundation grant number DEB-0818661 and a UNF Undergraduate Summer Research Award.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Matthew R. Gilg.

Additional information

Communicated by T. Reusch.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gilg, M.R., Camila Restrepo, M., Walton, R. et al. Geographic variation in allele frequency of the gamete recognition protein M7 lysin throughout a mosaic blue mussel hybrid zone. Mar Biol 160, 1737–1750 (2013). https://doi.org/10.1007/s00227-013-2226-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-013-2226-4

Keywords

Navigation