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Pre-zygotic factors best explain reproductive isolation between the hybridizing species of brittle-stars Acrocnida brachiata and A. spatulispina (Echinodermata: Ophiuroidea)

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Abstract

The two brittle-stars Acrocnida brachiata (Montagu 1804) and A. spatulispina (Stöhr and Muths in J Mar Biol Assoc, 2009) exhibit strong spatial segregation along the coast of Brittany (France), the first being subtidally distributed relative to the other intertidal species. Despite a very high degree of mitochondrial DNA divergence, previous preliminary results hinted at the potential for hybridization to occur. Therefore, we specifically aim to determine local levels of hybridization between these two species and to investigate the relative roles of pre- and post- zygotic isolation processes acting to decrease local hybridization patterns. Mitochondrial DNA, allozymes and the Internal Transcribed Spacer 2 region of the ribosomal DNA were all used on 529 brittle-stars sampled locally in June and September 2005, among six stations in Douarnenez Bay, a site situated at the tip of Brittany. Only 2.6% of all samples analyzed were identified as potential hybrids. However, these were twice more frequent in June, just after the reproductive period, than in September after selective mortality acted to reduce the proportions of hybrids. In addition to the abrupt bathymetric segregation between the two species, spawning asynchrony also clearly restricts hybridization to low levels, which shows the importance of pre-zygotic mechanisms in maintaining reproductive isolation. Moreover, both limited hybridization events and adult mortalities following reproduction tend to generate local genetic differentiation at the intra-species level. On the contrary, the genetic structure is homogenized by migration of juveniles or adults and hybrids mortalities over the summer period.

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References

  • Arndt A, Smith MJ (1998) Genetic diversity and population structure in two species of sea cucumber: differing patterns according to mode of development. Mol Ecol 7:1053–1064

    Article  Google Scholar 

  • Arndt A, Marquez C, Lambert P, Smith MJ (1996) Molecular phylogeny of eastern Pacific sea cucumbers (Echinodermata: Holothuroidea) based on mitochondrial DNA sequence. Mol Phyl Evol 6:425–437

    Article  CAS  Google Scholar 

  • Asmussen MA, Basten CJ (1994) Sampling theory for cytonuclear disequilibria. Genetics 138:1351–1363

    CAS  PubMed  Google Scholar 

  • Babcock RC, Mundy CN, Whitehead D (1994) Sperm diffusion models and in situ confirmation of long-distance fertilization in the free-spawning asteroid Acanthaster planci. Biol Bull 186:17–28

    Article  Google Scholar 

  • Basten CJ, Asmussen MA (1997) The exact test for cytonuclear disequilibria. Genetics 146:1165–1171

    CAS  PubMed  Google Scholar 

  • Bermingham E, Lessios HA (1993) Rate variation of protein and mitochondrial DNA evolution as revealed by sea urchins separated by the Isthmus of Panama. Proc Nat Acad Sci USA 90:2734–2738

    Article  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. galloprovencialis. Evolution 56:292–298

    PubMed  Google Scholar 

  • Bierne N, Borsa P, Daguin C et al (2003) Introgression patterns in the mosaic hybrid zone between Mytilus edulis and M. galloprovincialis. Mol Ecol 12:447–461

    Article  CAS  PubMed  Google Scholar 

  • Blanchet A, Chevalier C, Gaffet JD, Hamon D (2004) Bionomie benthique subtidale en Baie de Douarnenez, Vol. Ifremer, Brest, p. 51

  • Boissin E, Feral J, Chenuil A (2008) Defining reproductively isolated units in a cryptic and syntopic species complex using mitochondrial and nuclear markers: the brooding brittle star, Amphipholis squamata (Ophiuroidea). Mol Ecol 17:1732–1744

    Article  CAS  PubMed  Google Scholar 

  • Bolnick DI, Near TJ (2005) Tempo of hybrid inviability in Centrarchid fishes (Teleostei: Centrarchidae). Evolution 59:1754–1767

    PubMed  Google Scholar 

  • Bourgoin A (1987) Ecologie et démographie d’Acrocnida brachiata (Montagu) (Echinodermata : Ophiuroidea) en baie de Douarnenez (Bretagne). These 3eme cycle, Océanographie, Université de Bretagne occidentale, p. 146

  • Bourgoin A, Guillou M, Glémarec M (1991) Environmental instability and demographic variability in Acrocnida brachiata (Echinodermata : Ophiuropidea) in Douarnenez Bay (Brittany : France). Mar Ecol 12:89–104

    Article  Google Scholar 

  • Byrne M, Mundy C, Keesing J, Oliver J (1994) Hybridization of sympatric Patiriella species (Echinodermata, Asteroidea) in New South Wales. Evolution 48:564–576

    Article  Google Scholar 

  • Cabioch L (1968) Contribution à la connaissance des peuplements benthiques de la Manche Occidentale. Cah Biol Mar 9:493–720

    Google Scholar 

  • Chenuil A, Féral JP (2003) Sequences of mitochondrial DNA suggest that Echinocardium cordatum is a complex of several sympatric or hybridizing species : a pilot study. In: David F (ed) Echinoderm research 2001. Swets & Zeitlinger, Lisse, pp 15–21

    Google Scholar 

  • Cruz R, Carballo M, Conde-Padin P, Rolan-Alvarez E (2004) Testing alternative models for sexual isolation in natural populations of Littorina saxatilis: indirect support for by-product ecological speciation? J Evol Biol 17:288–293

    Article  CAS  PubMed  Google Scholar 

  • Denny MW, Shibata M (1989) Consequences of surf-zone turbulence for settlement and external fertilization. Am Nat 134:859–889

    Article  Google Scholar 

  • Edmands S, Deimler JK (2004) Local adaptation, intrinsic coadaptation and the effects of environmental stress on interpopulation hybrids in the copepod Tigriopus californicus. J Exp Mar Biol Ecol 303:183–196

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure : a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Farke H, Berghuis EM (1979) Spawning, larval development and migration behaviour of Arenicola marina under field conditions in the western Wadden Sea. Neth J Sea Res 13:529–535

    Article  Google Scholar 

  • Gardner JPA, Thompson RJ (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 

  • Gentil F, Zakardjian B (1989) Premières données sur la dynamique de population d’Acrocnida brachiata (Montagu) en Baie de Seine orientale. Vie marine HS 10:148

    Google Scholar 

  • Goodacre SL (2006) Marathon mollusc migrations. Heredity 97:1

    Article  CAS  PubMed  Google Scholar 

  • Gosselin L, Qian P (1997) Juvenile mortality in benthic marine invertebrates. Mar Ecol Prog Ser 146:265–282

    Article  Google Scholar 

  • Goudet J (1995) FSTAT (vers. 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Grant J, Turner S, Legendre P, Hume T, Bell R (1997) Patterns of sediment reworking and transport over small spatial scales on an intertidal sandflat, Manujau Harbour, New Zealand. J Exp Mar Biol Ecol 216:33–50

    Article  Google Scholar 

  • Guillou J (1980) Les peuplements de sables fins du littoral Nord-Gascogne. Université de Bretagne Occidentale, p 209

  • Hall TA (1999) BioEdit : a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harrison R (1993) Hybrids and hybrid zones: historical perspective. In: Hybrids zones and the evolutionary process. Oxford University Press, Oxford, pp 3–12

  • Hellberg ME, Burton RS, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Bull Mar Sci 70:273–290

    Google Scholar 

  • Hendler G, Miller JE (1991) Swimming ophiuroids—Real and imagined. In: Yanagisawa Y, Oguro, Suzuki & Motokawa (ed) Proceedings of the Seventh International Echinoderm Conference, Biology of Echinodermata. Balkema, Rotterdam, Atami, 9–14 September, 1990

  • Hendler G, Baldwin CC, Smith DG, Thacker CE (1999) Planktonic dispersal of juvenile brittle stars (Echinodermata: Ophiuroidea) on a caribbean reef. Bull Mar Sci 65:283–288

    Google Scholar 

  • Hendry AP, Day T (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Mol Ecol 14:901–916

    Article  CAS  PubMed  Google Scholar 

  • Jiggins CD, Mallet J (2000) Bimodal hybrid zones and speciation. Trends Ecol Evol 15:250–255

    Article  PubMed  Google Scholar 

  • Jollivet D, Comtet T, Chevaldonné P, Hourdez S, Jouin-Toulmond C, Desbruyères D, Dixon DR (1998) Unexpected relationship between dispersal strategies and speciation within the association Bathymodiolus (Bivalvia) - Branchipolinoe (Polychate) using the rDNA neutral ITS2 marker. Cah Biol Mar 39:359–362

    Google Scholar 

  • Jolly MT, Jollivet D, Gentil F, Thiébaut E, Viard F (2005) Sharp genetic break between Atlantic and English Channel populations of the polychaete Pectinaria koreni, along the north coast of Brittany, France. Heredity 94:23–32

    Article  CAS  PubMed  Google Scholar 

  • Jolly MT, Viard F, Gentil F, Thiebaut E, Jollivet D (2006) Comparative phylogeography of two coastal polychaete tubeworms in the North East Atlantic supports shared history and vicariant events. Mol Ecol 15:1841–1855

    Article  CAS  PubMed  Google Scholar 

  • Keegan BF, Mercer JP (1986) An oceanographical survey of Killary Harbour on the West coast of Ireland. Proc R Ir Academy 86:91–99

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Systemat 24:189–216

    Article  Google Scholar 

  • Koehler R (1921) Faune de France—Echinodermes, Vol 1, Paris, p 210

  • Lessios HA (1984) Possible prezygotic reproductive isolation in sea urchins separated by the Isthmus of Panama. Evolution 38:1144–1148

    Article  Google Scholar 

  • Levitan DR, Fukami H, Jara J, Kline D, McGovern TM, McGhee KE, Swanson CA, Knowlton N (2004) Mechanisms of reproductive isolation among sympatric broadcast-spawning corals of the Montastraea annularis species complex. Evolution 58:308–323

    PubMed  Google Scholar 

  • Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:231–237

    Google Scholar 

  • McCarthy C (1997) Chromas, Version 1.41. Griffith University, Brisbane

    Google Scholar 

  • Montagu G (1804) Description of several marine animals found on the south coast of Devonshire. Trans Linn Soc 7:61–85. pl VI–VII

    Article  Google Scholar 

  • Muths D, Davoult D, Gentil F, Jollivet D (2006) Incomplete cryptic speciation between intertidal and subtidal morphs of Acrocnida brachiata (Echinoderm : Ophiuroidea) in the North East Atlantic. Mol Ecol 15:3303–3318

    Article  CAS  PubMed  Google Scholar 

  • Nichols D, Barker MF (1984) A comparative study of reproductive and nutritional periodicities in two populations of Asterias rubens (Echinodermata : Asteroidea) from the English Channel. J Mar Biol Assoc UK 64:471–484

    Article  Google Scholar 

  • O’Loughlin PM, Waters JM, Roy SM (2002) Description of a new species of Patiriella from New Zealand, and review of Patiriella regularis (Echinodermata, Asteroidea) based on morphological and molecular data. J Roy Soc New Zeal 32:697–711

    Google Scholar 

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

    Article  Google Scholar 

  • Palumbi SR, Grabowsky G, Duda T, Greyer L, Tachino N (1997) Speciation and population genetic structure in tropical pacific sea urchins. Evolution 51:1506–1517

    Article  Google Scholar 

  • Pasteur N, Pasteur G, Bonhomme F, Catalan J, Britton-Davidan J (1987) Manuel technique de génétique par électrophorèse des protéines, Vol, Paris, p 459

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Schmidt PS, Rand DM (2001) Adaptive maintenance of genetic polymorphism in an intertidal barnacle: habitat- and life-stage-specific survivorship of Mpi genotypes. Evolution 55:1336–1344

    CAS  PubMed  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2001) Arlequin (v 2.0): software for population Genetics Data Analysis. Genetics and Biometry Laboratory. Department of Anthropology, University of Geneva, Geneva

    Google Scholar 

  • Stöhr S, Muths D (2009) Morphological diagnosis of the two genetic lineages of Acrocnida brachiata (Echinodermata: Ophiuroidea), with description of a new species. J Mar Biol Assoc UK, 1–13. doi:10.1017/S0025315409990749

  • Tamaki A (1987) Comparison of resistivity to transport by wave action in several polychaete species on an intertidal sand flat. Mar Ecol Prog Ser 37:181–189

    Article  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  • Tyler PA, Banner FT (1977) The effect of coastal hydrodynamics on the Echinoderm distribution in the sublittoral of Oxwich Bay, Bristol Channel. Estuar Coast Shelf Sci 5:293–308

    Google Scholar 

  • Waples RS (1989) Temporal variation in allele frequencies: testing the right hypothesis. Evolution 43:1236–1251

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wiens JJ, Donoghue MJ (2004) Historical biogeography, ecology and species richness. Trends Ecol Evol 19:639–644

    Article  PubMed  Google Scholar 

  • Wilke T, Pfenninger M (2002) Separating historic events from recurrent processes in cryptic species: phylogeography of mud snails. Mol Ecol 11:1439–1451

    Article  CAS  PubMed  Google Scholar 

  • Zühlke R, Reise K (1994) Response of macrofauna to drifting tidal sediments. Helgöl Mar Res 48:277–328

    Google Scholar 

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Acknowledgments

We are very grateful to people who helped us in the collection of samples, particularly to the crews of the N/O “Côtes de la Manche” and “Côtes d’Aquitaine”. Many thanks also to the divers of the “Station Biologique de Roscoff”, Caroline Broudin and to Yvan Lebras. This work was funded by the “PNEC-AT” (Programme National sur l’Environnement Côtier), the European network of excellence “Marbef” (Marine Biodiversity and Ecosystem Functioning) and supported by a PhD grant from the French Ministry of Research.

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Muths, D., Davoult, D., Jolly, M.T. et al. Pre-zygotic factors best explain reproductive isolation between the hybridizing species of brittle-stars Acrocnida brachiata and A. spatulispina (Echinodermata: Ophiuroidea). Genetica 138, 667–679 (2010). https://doi.org/10.1007/s10709-010-9441-4

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