The hidden side of a major marine biogeographic boundary: a wide mosaic hybrid zone at the Atlantic–Mediterranean divide reveals the complex interaction between natural and genetic barriers in mussels

Article metrics

Abstract

The Almeria–Oran Front (AOF) is a recognised hotspot of genetic differentiation in the sea, with genetic discontinuities reported in more than 50 species. The AOF is a barrier to dispersal and an ecological boundary; both can determine the position of these genetic breaks. However, the maintenance of genetic differentiation is likely reinforced by genetic barriers. A general drawback of previous studies is an insufficient density of sampling sites at the transition zone, with a conspicuous lack of samples from the southern coastline. We analysed the fine-scale genetic structure in the mussel Mytilus galloprovincialis using a few ancestry-informative loci previously identified from genome scans. We discovered a 600-km-wide mosaic hybrid zone eastward of the AOF along the Algerian coasts. This mosaic zone provides a new twist to our understanding of the Atlantic–Mediterranean transition because it demonstrates that the two lineages can live in sympatry with ample opportunities to interbreed in a large area, but they hardly do so. This implies that some form of reproductive isolation must exist to maintain the two genetic backgrounds locally cohesive. The mosaic zone ends with an abrupt genetic shift at a barrier to dispersal in the Gulf of Bejaia, Eastern Algeria. Simulations of endogenous or exogenous selection in models that account for the geography and hydrodynamic features of the region support the hypothesis that sister hybrid zones could have been differentially trapped at two alternative barriers to dispersal and/or environmental boundaries, at Almeria in the north and Bejaia in the south. A preponderantly unidirectional north–south gene flow next to the AOF can also maintain a patch of intrinsically maintained genetic background in the south and the mosaic structure, even in the absence of local adaptation. Our results concur with the coupling hypothesis that suggests that natural barriers can explain the position of genetic breaks, while their maintenance depends on genetic barriers.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

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

References

  1. Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N et al. (2013) Hybridization and speciation. J Evol Biol 26:229–246

  2. Anderson E, Thompson E (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229

  3. Andrello M, Jacobi MN, Manel S, Thuiller W, Mouillot D (2015) Extending networks of protected areas to optimize connectivity and population growth rate. Ecography 38:273–282

  4. Arnold (2006) Evolution through genetic exchange. Oxford University Press, Oxford

  5. Aurelle D, Guillemaud T, Afonso P, Morato T, Wirtz P, Santos RS et al. (2003) Genetic study of Coris julis (Osteichtyes, Perciformes, Labridae) evolutionary history and dispersal abilities. C R Biol 326:771–785

  6. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

  7. Avise JC (1992) Molecular population structure and the biogeographic history of a regional fauna: a case history with lessons for conservation biology. Oikos, 62–76

  8. Bahri-Sfar L, Lemaire C, Hassine OKB, Bonhomme F (2000) Fragmentation of sea bass populations in the western and eastern Mediterranean as revealed by microsatellite polymorphism. Proceedings of the Royal Society of London B: Biological Sciences 267(1446):929–935

  9. Barton NH (1979) The dynamics of hybrid zone. Heredity 43:341–359

  10. Barton NH (1986) The effects of linkage and density-dependant regulation on gene flow. Heredity 57:415–426

  11. Barton NH, Bengtsson BO (1986) The barrier to genetic exchange between hybridising populations. Heredity 56:357–376

  12. Barton NH, Gale KS (1993) Genetic analysis of hybrid zones. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, New York, pp 13–45

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

  14. Barton N, Turelli M (2011) Spatial waves of advance with bistable dynamics: cytoplasmic and genetic analogues of Allee effects. Am Nat 178:E48–E75

  15. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2002) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Université de Montpellier 2, Montpellier, France

  16. Berline L, Rammou A-M, Doglioli A, Molcard A, Petrenko A (2014) A connectivity-based eco-regionalization method of the Mediterranean Sea. PLoS ONE 9:e111978

  17. Bialozyt R, Ziegenhagen B, Petit RJ (2006) Contrasting effects of long distance seed dispersal on genetic diversity during range expansion. J Evol Biol 19:12–20

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

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

  20. 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

  21. Bierne N, Gagnaire P-A, David P (2013) The geography of introgression in a patchy environment and the thorn in the side of ecological speciation. Curr Zool 59:72–86

  22. Bierne N, Welch J, Loire E, Bonhomme F, David P (2011) The coupling hypothesis: why genome scans may fail to map local adaptation genes. Mol Ecol 20:2044–2072

  23. Borrero-Pérez GH, González-Wangüemert M, Marcos C, Pérez-Ruzafa A (2011) Phylogeography of the Atlanto-Mediterranean sea cucumber Holothuria (Holothuria) mammata: the combined effects of historical processes and current oceanographical pattern. Mol Ecol 20:1964–1975

  24. Borsa P, Naciri M, Bahri L, Chikhi L, Garcia de Leon FJ, Kotoulas G et al. (1997) Zoogéographie infra-spécifique de la mer Méditerranée. Vie Milieu 47:295–305

  25. Burton RS (1998) Intraspecific phylogeography across the Point Conception biogeographic boundary. Evolution 52(3):734–745

  26. Charlesworth B, Charlesworth D, Barton NH (2003) The effects of genetic and geographic structure on neutral variation. Annu Rev Ecol Syst 34:99–125

  27. Chevolot M, Hoarau G, Rijnsdorp AD, Stam WT, Olsen JL (2006) Phylogeography and population structure of thornback rays (Raja clavata L., Rajidae). Mol Ecol 15:3693–3705

  28. Cordero D, Peña JB, Saavedra C (2014) Phylogeographic analysis of introns and mitochondrial DNA in the clam Ruditapes decussatus uncovers the effects of Pleistocene glaciations and endogenous barriers to gene flow. Mol Phylogenet Evol 71:274–287

  29. Cruickshank TE, Hahn MW (2014) Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol Ecol 23:3133–3157

  30. Diz AP, Presa P (2008) Regional patterns of microsatellite variation in Mytilus galloprovincialis from the Iberian Peninsula. Mar Biol 154:277–286

  31. Duranton M, Allal F, Fraïsse C, Bierne N, Bonhomme F, Gagnaire PA (2018) The origin and remolding of genomic islands of differentiation in the European sea bass. Nature communications 9(1):2518

  32. Ewers-Saucedo C, Pringle JM, Sep£lveda HH, Byers JE, Navarrete SA, Wares JP (2016) The oceanic concordance of phylogeography and biogeography: a case study in N otochthamalus. Ecology and evolution 6(13):4403–4420

  33. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

  34. Feder JL, Nosil P (2010) The efficacy of divergence hitchhiking in generating genomic islands during ecological speciation. Evolution 64:1729–1747

  35. Flaxman SM, Feder JL, Nosil P (2012) Spatially explicit models of divergence and genome hitchhiking. J Evol Biol 25:2633–2650

  36. Fourcade Y, Chaput‐Bardy A, Secondi J, Fleurant C, Lemaire C (2013) Is local selection so widespread in river organisms? Fractal geometry of river networks leads to high bias in outlier detection. Mol Ecol 22:2065–2073

  37. Font J, Millot C, Salas J, Julià A, Chic O (1998) The drift of Modified Atlantic Water from the Alboran Sea to the eastern Mediterranean. Sci Mar 62:211–216

  38. Fraïsse C, Belkhir K, Welch JJ, Bierne N (2016) Local interspecies introgression is the main cause of extreme levels of intraspecific differentiation in mussels. Mol Ecol 25:269–286

  39. Gagnaire PA, Broquet T, Aurelle D, Viard F, Souissi A, Bonhomme F et al. (2015) Using neutral, selected and hitchhiker loci to assess connectivity of marine populations in the genomic era. Evol Appl 8:769–786

  40. Galarza JA, Carreras-Carbonell J, Macpherson E, Pascual M, Roques S, Turner GF et al. (2009) The influence of oceanographic fronts and early-life-history traits on connectivity among littoral fish species. Proc Natl Acad Sci 106:1473–1478

  41. Gilg MR, Hilbish TJ (2003) The geography of marine larval dispersal: coupling genetics with fine‐scale physical oceanography. Ecology 84:2989–2998

  42. Goldberg EE, Lande R (2007) Species’ borders and dispersal barriers. Am Nat 170:297–304

  43. Gosset C, Bierne N (2013) Differential introgression from a sister species explains high Fst outlier loci within a mussel species. J Evol Biol 26:14–26

  44. Haney RA, Silliman BR, Fry AJ, Layman CA, Rand DM (2007) The Pleistocene history of the sheepshead minnow (Cyprinodon variegatus): non-equilibrium evolutionary dynamics within a diversifying species complex. Molecular phylogenetics and evolution 43(3):743–754

  45. Harrison RG (1993) Hybrid zones and the evolutionary process. Oxford University Press, Oxford

  46. Harrison RG, Larson EL (2016) Heterogeneous genome divergence, differential introgression, and the origin and structure of hybrid zones. Mol Ecol 25:2454–2466

  47. Hellberg ME (2009) Gene flow and isolation among populations of marine animals. Annu Rev Ecol, Evol, Syst 40:291–310

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

  49. Hewitt GM (1975) A sex-chromosome hybrid zone in the grasshopper Podisma pedestris (Orthoptera: Acrididae). Heredity 35:375–387

  50. Hewitt, G. M. (1989). The subdivision of species by hybrid zones. Speciation and its Consequences, 85-110

  51. Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276

  52. Hewitt GM (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913

  53. Hoban S, Kelley JL, Lotterhos KE, Antolin MF, Bradburd G, Lowry DB, Poss ML, Reed LK et al. (2016) Finding the Genomic Basis of Local Adaptation: Pitfalls, Practical Solutions, and Future Directions. The American Naturalist 188:379–397

  54. Ibrahim KM, Nichols RA, Hewitt GM (1996) Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77:282–291

  55. Johannesson K, Andre C (2006) Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea. Mol Ecol 15:2013–2029

  56. Johannesson K, Panova M, Kemppainen P, Andre C, Rolan-Alvarez E, Butlin RK (2010) Repeated evolution of reproductive isolation in a marine snail: unveiling mechanisms of speciation. Philos Trans R Soc Lond B Biol Sci 365:1735–1747

  57. Jombart T, Ahmed I (2011) adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071

  58. Kruuk LEB, Baird SJE, Gale KS, Barton NH (1999) A comparison of multilocus clines maintained by environmental adaptation or by selection against hybrids. Genetics 153(4):1959–1971

  59. Launey S, Ledu C, Boudry P, Bonhomme F, Naciri-Graven Y (2002) Geographic structure in the European flat oyster, Ostrea edulis L, as revealed by microsatellite polymorphism. J Hered 93:331–351

  60. Le Corre V, Machon N, Petit RJ, Kremer A (1997) Colonization with long-distance seed dispersal and genetic structure of maternally inherited genes in forest trees: a simulation study. Genet Res 69:117–125

  61. Lemaire C, Versini JJ, Bonhomme F (2005) Maintenance of genetic differentiation across a transition zone in the sea: discordance between nuclear and cytoplasmic markers. J Evol Biol 18:70–80

  62. Librado P, Rozas J (2009) DnaSPv5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

  63. Lourenço CR, Nicastro KR, Serrão EA, Castilho R, Zardi GI (2015) Behind the mask: cryptic genetic diversity of Mytilus galloprovincialis along southern European and northern African shores. J Mollusca Stud 81:380–387

  64. M’Gonigle LK, FitzJohn RG (2010) Assortative mating and spatial structure in hybrid zones. Evolution 64:444–455

  65. Manel S, Holderegger R (2013) Ten years of landscape genetics. Trends Ecol Evol 28:614–621

  66. Marshall DJ, Monro K, Bode M, Keough MJ, Swearer S (2010) Phenotype–environment mismatches reduce connectivity in the sea. Ecol Lett 13:128–140

  67. McQuaid CD, Phillips TE (2000) Limited wind-driven dispersal of intertidal mussel larvae: in situ evidence from the plankton and the spread of the invasive species Mytilus galloprovincialis in South Africa. Mar Ecol Prog Ser 201:211–220

  68. Meirmans PG (2015) Seven common mistakes in population genetics and how to avoid them. Mol Ecol 24:3223–3231

  69. Nichols RA, Hewitt GM (1994) The genetic consequences of long distance dispersal during colonization. Heredity 72:312–317

  70. Nosil P, Vines TH, Funk DJ (2005) Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59:705–719

  71. Ouagajjou Y, Presa P (2015) The connectivity of Mytilus galloprovincialis in northern Morocco: a gene flow crossroads between continents. Estuar, Coast Shelf Sci 152:1–10

  72. Palero F, Abelló P, Macpherson E, Gristina M, Pascual M (2008) Phylogeography of the European spiny lobster (Palinurus elephas): influence of current oceanographical features and historical processes. Mol Phylogenet Evol 48:708–717

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

  74. Patarnello T, Volckaert FA, Castilho R (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Mol Ecol 16:4426–4444

  75. Pelc RA, Warner RR, Gaines SD (2009) Geographical patterns of genetic structure in marine species with contrasting life histories. J Biogeogr 36:1881–1890

  76. Piálek J, Barton NH (1997) The spread of an advantageous allele across a barrier: the effects of random drift and selection against heterozygotes. Genetics 145:493–504

  77. Polechová J, Barton N (2011) Genetic drift widens the expected cline but narrows the expected cline width. Genetics 189:227–235

  78. Qin XX, Coyne KJ, Waite JH (1997) Tough tendons mussel byssus has collagen with silk-like domains. J Biol Chem 51:32623–32627

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

  80. Quesada H, Warren M, Skibinski DOF (1998) Nonneutral evolution and differential mutation rate of gender-associated mitochondrial DNA lineages in the marine mussel Mytilus. Genetics 149:1511–1526

  81. Quesada H, Zapata C, Alvarez G (1995b) A multilocus allozyme discontinuity in the mussel Mytilus galloprovincialis: the interaction of ecological and life-history factors. Mar Ecol Prog Ser 116:99–115

  82. Rand DM, Harrison RG (1989) Ecological genetics of a mosaic hybrid zone: mitochondrial, nuclear, and reproductive differentiation of crickets by soil type. Evolution 43:432–449

  83. Ravinet M, Faria R, Butlin RK, Galindo J, Bierne N, Rafajlović M et al. (2017) Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow. J Evol Biol 30:1450–1477

  84. Remington CL (1968). Suture-zones of hybrid interaction between recently joined biotas. In: Dobzhansky T, Hecht MK, Steere WC (eds) Evolutionary biology, Vol. 2. Plenum Press, New York, pp 321–428

  85. Riginos C, Douglas KE, Jin Y, Shanahan DF, Treml EA (2011) Effects of geography and life history traits on genetic differentiation in benthic marine fishes. Ecography 34:566–575

  86. Riginos C, Liggins L (2013) Seascape genetics: populations, individuals, and genes marooned and adrift. Geogr Compass 7:197–216

  87. Riginos C, Crandall ED, Liggins L, Bongaerts P, Treml EA (2016) Navigating the currents of seascape genomics: how spatial analyses can augment population genomic studies. Current zoology 62(6):581–601

  88. Rocha L, Bowen B (2008) Speciation in coral‐reef fishes. J Fish Biol 72:1101–1121

  89. Rossi V, Ser‐Giacomi E, López C, Hernández‐García E (2014) Hydrodynamic provinces and oceanic connectivity from a transport network help designing marine reserves. Geophys Res Lett 41:2883–2891

  90. Sanjuan A, Zapata C, Alvarez G (1994) Mytilus galloprovincialis and M. edulis on the coasts of the Iberian Peninsula. Mar Ecol Prog 113:131–46

  91. Schunter C, Carreras-Carbonell J, Macpherson E, Tintoré J, Vidal‐Vijande E et al. (2011) Matching genetics with oceanography: directional gene flow in a Mediterranean fish species. Mol Ecol 20:5167–5181

  92. Sivasundar A, Palumbi SR (2010) Life history, ecology and the biogeography of strong genetic breaks among 15 species of Pacific rockfish, Sebastes. Marine biology 157(7):1433–1452

  93. Stanley RR, DiBacco C, Lowen B, Beiko RG, Jeffery NW et al. (2018) A climate-associated multispecies cryptic cline in the northwest Atlantic. Sci Adv 4:eaaq0929

  94. Slatkin (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792

  95. Slatkin M (1973) Gene flow and selection in a cline. Genetics 75:733–756

  96. Stuckas H, Knöbel L, Schade H, Breusing C, Hinrichsen HH, Bartel M et al. (2017) Combining hydrodynamic modelling with genetics: can passive larval drift shape the genetic structure of Baltic Mytilus populations? Mol Ecol 26:2765–2782

  97. Swenson NG, Howard DJ (2005) Clustering of contact zones, hybrid zones, and phylogeographic breaks in North America. Am Nat 166:581–591

  98. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

  99. Teske PR, Papadopoulos I, Barker NP, McQuaid CD, Beheregaray LB (2014) Mitonuclear discordance in genetic structure across the Atlantic/Indian Ocean biogeographical transition zone. J Biogeogr 41:293–401

  100. Thibert-Plante X, Hendry A (2010) When can ecological speciation be detected with neutral loci? Mol Ecol 19:2301–2314

  101. Tine M, Kuhl H, Gagnaire P-A, Louro B, Desmarais E, Martins RST et al. (2014) The European seabass genome and its variation provide insights into adaptation to euryhalinity and speciation. Nat Commun 5:5770

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

  103. Vines TH, Dalziel AC, Albert AY, Veen T, Schulte PM, Schluter D (2016) Cline coupling and uncoupling in a stickleback hybrid zone. Evolution 70:1023–1038

  104. Viúdez Á, Tintoré J (1995) Time and space variability in the eastern Alboran Sea from March to May 1990. J Geophys Res: Oceans 100:8571–8586

  105. Zouros E, Oberhauser Ball A, Saavedra C, Freeman KR (1994) A unusual type of mtDNA inheritance in the blue mussel Mytilus. Proc Natl Acad Sci USA 91:7463–7467

Download references

Acknowledgements

It is a pleasure to thank Marie-Thérèse Augé and Cathy Haag-Liautard for their technical help in the lab, and Marina Albentosa as well as Carlos Saavedra for Spanish samples. We also thank Pierre-Alexandre Gagnaire, Christelle Fraïsse, François Bonhomme, Nathalie Charbonnel, Sophie Arnaud-Haond and Lilia Bahri-Sfar for discussion, as well as Cynthia Riginos, Heiko Stuckas and six anonymous referees for their insightful comments on earlier drafts. Molecular data were produced through the ISEM platform Génomique des Populations Marines (PGPM7) at the Station Marine de Sète (OSU OREME, Observatoire de Recherche Méditerranéen de l’Environnement) and the platform Génomique Environnementale of the LabEx CeMEB (Laboratoire d’Excellence Centre Méditerranéen de l’Environnement et de la Biodiversité). This work was funded by a Languedoc-Roussillon “Chercheur(se)s d’Avenir” grant (Connect7 project). This is article 2018-286 of Institut des Sciences de l’Evolution de Montpellier.

Data archiving

Sequence data have been deposited in GenBank: accession numbers MK259098–MK259664. Genotype data have been deposited in Dryad: https://doi.org/10.5061/dryad.m3t6p5g.

Author information

Correspondence to Nicolas Bierne.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary File

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark