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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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
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
Asmussen MA, Basten CJ (1994) Sampling theory for cytonuclear disequilibria. Genetics 138:1351–1363
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
Basten CJ, Asmussen MA (1997) The exact test for cytonuclear disequilibria. Genetics 146:1165–1171
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
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
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
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
Bolnick DI, Near TJ (2005) Tempo of hybrid inviability in Centrarchid fishes (Teleostei: Centrarchidae). Evolution 59:1754–1767
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
Byrne M, Mundy C, Keesing J, Oliver J (1994) Hybridization of sympatric Patiriella species (Echinodermata, Asteroidea) in New South Wales. Evolution 48:564–576
Cabioch L (1968) Contribution à la connaissance des peuplements benthiques de la Manche Occidentale. Cah Biol Mar 9:493–720
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
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
Denny MW, Shibata M (1989) Consequences of surf-zone turbulence for settlement and external fertilization. Am Nat 134:859–889
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
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
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
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
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
Goodacre SL (2006) Marathon mollusc migrations. Heredity 97:1
Gosselin L, Qian P (1997) Juvenile mortality in benthic marine invertebrates. Mar Ecol Prog Ser 146:265–282
Goudet J (1995) FSTAT (vers. 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
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
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
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
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
Hendry AP, Day T (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Mol Ecol 14:901–916
Jiggins CD, Mallet J (2000) Bimodal hybrid zones and speciation. Trends Ecol Evol 15:250–255
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
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
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
Keegan BF, Mercer JP (1986) An oceanographical survey of Killary Harbour on the West coast of Ireland. Proc R Ir Academy 86:91–99
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
Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Systemat 24:189–216
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
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
Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:231–237
McCarthy C (1997) Chromas, Version 1.41. Griffith University, Brisbane
Montagu G (1804) Description of several marine animals found on the south coast of Devonshire. Trans Linn Soc 7:61–85. pl VI–VII
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
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
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
Palumbi SR (1994) Genetic divergence, reproductive isolation and marine speciation. Annu Rev Ecol Sys 25:547–572
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
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
Raymond M, Rousset F (1995) GENEPOP (version 1.2): a population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497
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
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
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
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
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
Waples RS (1989) Temporal variation in allele frequencies: testing the right hypothesis. Evolution 43:1236–1251
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Wiens JJ, Donoghue MJ (2004) Historical biogeography, ecology and species richness. Trends Ecol Evol 19:639–644
Wilke T, Pfenninger M (2002) Separating historic events from recurrent processes in cryptic species: phylogeography of mud snails. Mol Ecol 11:1439–1451
Zühlke R, Reise K (1994) Response of macrofauna to drifting tidal sediments. Helgöl Mar Res 48:277–328
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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DOI: https://doi.org/10.1007/s10709-010-9441-4