Marine Biology

, Volume 161, Issue 11, pp 2509–2520 | Cite as

Phylogeographic pattern and glacial refugia of a rocky shore species with limited dispersal capability: the case of Montagu’s blenny (Coryphoblennius galerita, Blenniidae)

  • S. M. FranciscoEmail author
  • V. C. Almada
  • C. Faria
  • E. M. Velasco
  • J. I. Robalo
Original Paper


Phylogeographic patterns among coastal fishes are expected to be influenced by distinct ecological, biological and life history traits, along with historical events and oceanography (past and present). This study focuses on the broad range phylogeography of the Montagu’s blenny Coryphoblennius galerita, a species with well-known ecological features, strictly tied to rocky environments and with limited dispersal capability. Eleven locations from the western Mediterranean to the Bay of Biscay (including the Macaronesian archipelagos) were sampled. Mitochondrial DNA control region (CR) and the first intron of the S7 ribosomal protein gene were used to address the population structure, the signatures of expansion/contraction events retained in the genealogies and potential glacial refugia. The genetic diversity of the Montagu’s blenny was high throughout the sampled area, reaching maximum values in the Mediterranean and western Iberian Peninsula. The results confirmed a marked structure of C. galerita along the sampled area, with a major separation found between the Mediterranean and the Atlantic populations, and suggesting also a separation between the Azores and the remaining Atlantic locations. This study revealed complex and deep genealogies for this species, with Montagu’s blenny populations presenting signatures of events clearly older than the Last Glacial Maximum, with lineages coalescing in early Pleistocene and Pliocene. Three potential glacial refugia where this species might have survived Pleistocene glaciations and from where the recolonization process might have taken place are suggested: South of Iberian Peninsula/North Africa, Mediterranean and Azores.


Control Region Iberian Peninsula Glacial Refugium Phylogeographic Pattern Bayesian Skyline Plot 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We are grateful to Sonia Chenu for her help with the lab work and Carla Sousa Santos for her help with the labwork and her skilful help with editing the nuclear sequences and with network drawing. This study was funded by the Eco-Ethology Research Unit’ Strategic Plan (PEst-OE/MAR/UI0331/2011) – Fundação para a Ciência e a Tecnologia - FCT (partially FEDER funded). SMF was supported by an FCT Grant (SFRH/BPD/84923/2012). We dedicate this paper to the loving memory of Professor Vítor Almada whose tragic loss we suffered during the course of this work. He was our inspiration and the one responsible for the idea behind this study.

Supplementary material

227_2014_2523_MOESM1_ESM.docx (77 kb)
Supplementary material 1 (DOCX 76 kb)
227_2014_2523_MOESM2_ESM.docx (39 kb)
Supplementary material 2 (DOCX 38 kb)
227_2014_2523_MOESM3_ESM.docx (26 kb)
Supplementary material 3 (DOCX 26 kb)


  1. Almada VC, Carreiro H, Faria C, Gonçalves EJ (1996) The breeding season of Coryphoblennius galerita in Portuguese waters. J Fish Biol 48:295–297Google Scholar
  2. Almada F, Almada VC, Guillemaud T, Wirtz P (2005) Phylogenetic relationships of the north-eastern Atlantic and Mediterranean blenniids. Biol J Linn Soc 86:283–295CrossRefGoogle Scholar
  3. Almada VC, Pereira AM, Robalo JI, Fonseca JP, Levy A, Maia C, Valente A (2008) Mitochondrial DNA fails to reveal genetic structure in sea-lampreys along European shores. Mol Phylogenet Evol 46:391–396CrossRefGoogle Scholar
  4. Almada VC, Robalo JI, Levy A, Freyhof J, Bernardi G, Doadrio I (2009) Phylogenetic analysis of Peri-Mediterranean blennies of the genus Salaria: molecular insights on the colonization of freshwaters. Mol Phylogenet Evol 52:424–431CrossRefGoogle Scholar
  5. Almada V, Almada F, Francisco S, Castilho R, Robalo JI (2012) Unexpected high genetic diversity at the extreme northern geographic limit of Taurulus bubalis (Euphrasen, 1786). PLoS One 7:e44404CrossRefGoogle Scholar
  6. Alveirinho-Dias J, Rodrigues A, Magalhães F (1997) Evolução da linha de costa em Portugal, desde o último máximo glaciário até à actualidade: síntese dos conhecimentos. Estudos Do Quaternário 1:53–66Google Scholar
  7. Bahri-Sfar L, Lemaire C, Hassine OKB, Bonhnomme F (2000) Fragmentation of sea bass populations in the western and eastern Mediterranean as revealed by microsatellite polymorphism. Proc R Soc Lond B 267:929–935CrossRefGoogle Scholar
  8. Bandelt H, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefGoogle Scholar
  9. Bath H (1978) Geographische variation der körperfärbung und flossenformel von Coryphoblennius galerita (Linnaeus 1758) (Pisces: blenniidae). Senckenb Biol 59:317–324Google Scholar
  10. Beebee T, Rowe G (2004) Phylogeography. An introduction to molecular ecology. Oxford University Press, Oxford, pp 165–197Google Scholar
  11. Bernardi G, Lape J (2005) Tempo and mode of speciation in the Baja California disjunct fish species Anisotremus davidsonii. Mol Ecol 14:4085–4096CrossRefGoogle Scholar
  12. Bowen BW, Bass AL, Rocha LA, Grant WS, Robertson DR (2001) Phylogeography of the trumpetfishes (Aulostomus): ring species complex on a global scale. Evolution 55:1029–1039CrossRefGoogle Scholar
  13. Briggs JC (1974) Marine zoogeography. McGraw-Hill Book Co., New YorkGoogle Scholar
  14. Chevolot M, Hoarau G, Rinjsdorp AD, Stam WT, Olsen JL (2006) Phylogeography and population structure of thornback rays (Raja clavata L., Rajidae). Mol Ecol 15:3693–3705CrossRefGoogle Scholar
  15. Chow S, Hazama K (1998) Universal PCR primers for S7 ribosomal protein gene introns in fish. Mol Ecol 7:1247–1263CrossRefGoogle Scholar
  16. Climap Project Members (1984) The last interglacial ocean. Quat Res 21:123–224CrossRefGoogle Scholar
  17. Crowley TJ (1981) Temperature and circulation changes in the eastern north Atlantic during the last 150,000 years: evidence from the planktonic foraminiferal record. Mar Micropaleontol 6:97–129CrossRefGoogle Scholar
  18. Debes PV, Zachos FE, Hanel R (2008) Mitochondrial phylogeography of the European sprat (Sprattus sprattus L., Clupeidae) reveals isolated climatically vulnerable populations in the Mediterranean Sea and range expansion in the northeast Atlantic. Mol Ecol 17:3873–3888CrossRefGoogle Scholar
  19. Domingues VS, Bucciarelli G, Almada VC, Bernardi G (2005) Historical colonization and demography of the Mediterranean damselfish, Chromis chromis. Mol Ecol 14:4051–4063CrossRefGoogle Scholar
  20. Domingues VS, Faria C, Stefanni S, Santos RS, Brito A, Almada VC (2007) Genetic divergence in the Atlantic-Mediterranean Montagu’s blenny, Coryphoblennius galerita (Linnaeus 1758) revealed by molecular and morphological characters. Mol Ecol 16:3592–3605CrossRefGoogle Scholar
  21. Domingues VS, Alexandrou M, Almada VC, Robertson DR, Brito A, Santos RS, Bernardi G (2008) Tropical fishes in a temperate sea: evolution of the wrasse Thalassoma pavo and the parrotfish Sparisoma cretense in the Mediterranean and the adjacent Macaronesian and Cape Verde Archipelagos. Mar Biol 154:465–474CrossRefGoogle Scholar
  22. Drummond AJ, Rambaut A (2007) BEAST: bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214CrossRefGoogle Scholar
  23. Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192CrossRefGoogle Scholar
  24. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581CrossRefGoogle Scholar
  25. Excoffier L, Lischer H (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefGoogle Scholar
  26. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491Google Scholar
  27. Francisco SM, Castilho R, Soares M, Congiu L, Brito A, Vieira MN, Almada VC (2009) Phylogeography and demographic history of Atherina presbyter (Pisces: Atherinidae) in the North-eastern Atlantic based on mitochondrial DNA. Mar Biol 156:1421–1432CrossRefGoogle Scholar
  28. Francisco SM, Faria C, Lengkeek W, Vieira MN, Velasco EM, Almada VC (2011) Phylogeography of the shanny Lipophrys pholis (Pisces: Blenniidae) in the NE Atlantic records signs of major expansion event older than the last glaciation. J Exp Mar Bio Ecol 403:14–20CrossRefGoogle Scholar
  29. Francisco SM, Robalo JI, Levy A, Almada VC (2014) In search of phylogeographic patterns in the northeastern Atlantic and adjacent seas. In: Pontarotti P (ed) Evolutionary biology, Genome, Speciation, Coevolution and Origin of life. Springer, pp 323–338. doi: 10.1007/978-3-319-07623-2_15
  30. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:437–460Google Scholar
  31. Galarza JA, Carreras-Carbonell J, Macpherson E, Pascual M, Roques S, Turner GF, Rico C (2009) The influence of oceanographic fronts and early-life-history traits on connectivity among littoral fish species. PNAS 106:1473–1478CrossRefGoogle Scholar
  32. Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704CrossRefGoogle Scholar
  33. Gysels ES, Hellemans B, Pampoulie C, Volckaert FAM (2004) Phylogeography of the common goby, Pomatoschistus microps, with particular emphasis on the colonization of the Mediterranean and the North Sea. Mol Ecol 13:403–417CrossRefGoogle Scholar
  34. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–9013CrossRefGoogle Scholar
  35. Hickerson MJ, Cunningham CW (2006) Nearshore fish (Pholis gunnellus) persists across the North Atlantic through multiple glacial episodes. Mol Ecol 15:4095–4107CrossRefGoogle Scholar
  36. Kuhner MK (2006) LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22:768–770CrossRefGoogle Scholar
  37. Lambeck K, Esat TM, Potter E-K (2002) Links between climate and sea levels for the past three million years. Nature 419:199–206CrossRefGoogle Scholar
  38. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948CrossRefGoogle Scholar
  39. Larmuseau MHD, Van Houdt JKJ, Guelinckx J et al (2009) Distributional and demographic consequences of Pleistocene climate fluctuations for a marine demersal fish in the north-eastern Atlantic. J Biogeogr 36:1138–1151CrossRefGoogle Scholar
  40. Maggs CA, Castilho R, Foltz D et al (2008) Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology 89:S108–S122CrossRefGoogle Scholar
  41. Mäkinen HS, Merilä J (2008) Mitochondrial DNA phylogeography of the three-spined stickleback (Gasterosteus aculeatus) in Europe-evidence for multiple glacial refugia. Mol Phylogenet Evol 46:167–182CrossRefGoogle Scholar
  42. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220Google Scholar
  43. Martins CS, Hamann M, Fuiza AFG (2002) Surface circulation in the eastern North Atlantic from drifters and altimetry. J Geophys Res 107:3217–3240CrossRefGoogle Scholar
  44. Millot C (1999) Circulation in the Western Mediterranean Sea. J Mar Sys 20:423–442CrossRefGoogle Scholar
  45. Morton B, Britton JC (2000) The origins of the coastal and marine flora and fauna of the Azores. Oceanogr Mar Biol 38:13–84Google Scholar
  46. Muss A, Robertson DR, Stepien CA, Wirtz P, Bowen BW (2001) Phylogeography of Ophioblennius: the role of ocean currents and geography in reef fish evolution. Evolution 55:561–572CrossRefGoogle Scholar
  47. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, OxfordGoogle Scholar
  48. Nikula R, Väinölä R (2003) Phylogeography of Cerastoderma glaucum (Bivalvia: Cardiidae) across Europe: a major break in the Eastern Mediterranean. Mar Biol 143:339–350CrossRefGoogle Scholar
  49. Olsen JL, Stam WT, Coyer JA, Reusch TBH, Billingham M, Boström C, Calvert E, Christie H, Granger S, La Lumière R, Milchakova N, Oudot-Le Secq MP, Procaccini G, Sanjabi B, Serrão E, Veldsink J, Widdicombe S, Wyllie-Echeverria S (2004) North Atlantic phylogeography and large-scale population differentiation of the seagrass Zostera marina L. Mol Ecol 13:1923–1941CrossRefGoogle Scholar
  50. Ostellari L, Bargelloni L, Penzo E, Patarnello P, Patarnello T (1996) Optimization of single-strand conformation polymorphism and sequence analysis of the mitochondrial control region in Pagellus bogaraveo (Sparidae, Teleostei): rationalized tools in fish population biology. Anim Genet 27:423–427CrossRefGoogle Scholar
  51. Patarnello T, Volckaert FMJ, Castilho R (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Mol Ecol 16:4426–4444. doi: 10.1111/j.1365-294X.2007.03477.x CrossRefGoogle Scholar
  52. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256CrossRefGoogle Scholar
  53. Quéro JC, Hureau JC, Karrer C, Post A, Saldanha L (1990) Check-list of the fishes of the eastern Tropical Atlantic. JNICT, LisbonGoogle Scholar
  54. Rambaut A, Drummond AJ (2007) Tracer v1.4, Available from
  55. Raventós N, Macpherson E (2001) Planktonic larval duration and settlement marks on the otoliths of Mediterranean littoral fishes. Mar Biol 138:1115–1120CrossRefGoogle Scholar
  56. Richtarski U, Patzner RA (2000) Comparative morphology of male reproductive systems in Mediterranean blennies (Blenniidae). J Fish Biol 56:22–36CrossRefGoogle Scholar
  57. Robalo JI, Castilho R, Francisco SM et al (2012) Northern refugia and recent expansion in the North Sea: the case of the wrasse Symphodus melops (Linnaeus, 1758). Ecol Evol 2:153–164CrossRefGoogle Scholar
  58. Rogers AR (1995) Genetic evidence for a Pleistocene population explosion. Evolution 49:608–615CrossRefGoogle Scholar
  59. Rogers AR, Harpending HC (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569Google Scholar
  60. Santos RS, Hawkins S, Monteiro LR, Alves M, Isidro EJ (1995) Marine research, resources and conservation in the Azores. Aquat Conserv 5:311–354CrossRefGoogle Scholar
  61. Shakun JD, Carlson AE (2010) A global perspective on Last Glacial Maximum to Holocene climate change. Quat Sci Rev 29:1801–1816CrossRefGoogle Scholar
  62. Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool 35:627–632CrossRefGoogle Scholar
  63. Sotka EE, Wares JP, Barth JA, Grosberg RK, Palumbi SR (2004) Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula. Mol Ecol 13:2143–2156CrossRefGoogle Scholar
  64. Sousa-Santos C, Robalo IJ, Collares-Pereira MJ, Almada VC (2005) Heterozygous indels as useful tools in the reconstruction of DNA sequences and in the assessment of ploidy level and genomic constitution of hybrid organisms. DNA Seq 16:462–467Google Scholar
  65. Stefanni S, Knutsen H (2007) Phylogeography and demographic history of the deep-sea fish Aphanopus carbo (Lowe, 1839) in the NE Atlantic: vicariance followed by secondary contact or speciation? Mol Phylogenet Evol 42:38–46CrossRefGoogle Scholar
  66. Stefanni S, Domingues V, Bouton N, Santos RS, Almada F, Almada V (2006) Phylogeny of the shanny, Lipophrys pholis, from the NE Atlantic using mitochondrial DNA markers. Mol Phylogenet Evol 39:282–287CrossRefGoogle Scholar
  67. Stramma L (1984) Geostrophic transport in the warm water sphere of the eastern subtropical North Atlantic. J Mar Res 42:537–558CrossRefGoogle Scholar
  68. Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–446Google Scholar
  69. Thiede J (1978) A glacial Mediterranean. Nature 276:680–683CrossRefGoogle Scholar
  70. Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55:2455–2469CrossRefGoogle Scholar
  71. Weersing K, Toonen RJ (2009) Population genetics, larval dispersal, and connectivity in marine systems. Mar Ecol Prog Ser 393:1–12CrossRefGoogle Scholar
  72. Willebrand J, Barnier B, Böning C, Dieterich PD, Le Provost C, Jia Y, Molines JM, New AL (2001) Circulation characteristics in three eddy-permitting models of the North Atlantic. Prog Oceanogr 48:123–161CrossRefGoogle Scholar
  73. Zander CD (1986) Blenniidae. In: Whitehead PJP, Bauchot M-L, Hureau J-C, Nielsen J, Tortonese E (eds) Fishes of the North-Eastern Atlantic and the Mediterranean. UNESCO, Paris, pp 1096–1112Google Scholar
  74. Zaragosi S, Eynaud F, Pujol C, Auffret GA, Turon JL, Garlan T (2001) Initiation of the European deglaciation as recorded in the northwestern Bay of Biscay slope environments (Meriadzek Terrace and Travelyan Escarpment): a multi-proxy approach. Earth Planet Sci Lett 188:493–507CrossRefGoogle Scholar
  75. Zardoya R, Castilho R, Grande C, Favre-Krey L, Caetano S, Marcato S, Krey G, Patarnello T (2004) Differential population structuring of two closely related fish species, the mackerel (Scomber scombrus) and the chub mackerel (Scomber japonicus), in the Mediterranean Sea. Mol Ecol 13:1785–1798CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • S. M. Francisco
    • 1
    Email author
  • V. C. Almada
    • 1
  • C. Faria
    • 2
  • E. M. Velasco
    • 3
  • J. I. Robalo
    • 1
  1. 1.MARE - Marine and Environmental Sciences Centre and Eco-Ethology Research UnitISPA University InstituteLisbonPortugal
  2. 2.Centro de Investigação em Educação. Faculdade de Ciências daUniversidade de LisboaLisbonPortugal
  3. 3.Instituto Español de Oceanografía. Centro Oceanográfico de Gijón.GíjonSpain

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