Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Mitochondrial and nuclear intraspecific variation in the rusty blenny (Parablennius sanguinolentus, Blenniidae)

Abstract

The genetic structure of Parablennius sanguinolentus from the northeastern Atlantic and Mediterranean was assessed using sequences from the mitochondrial control region (CR) and the first intron of the nuclear S7 ribosomal protein gene (S7). Our data show high genetic diversity for the central Mediterranean populations, contrasting with very low diversity in the Atlantic populations and in the westernmost Mediterranean population of Cabo de Gata. Both CR mismatch analysis and neutrality tests provide evidence of demographic and spatial expansion for the Atlantic and central Mediterranean populations. The significant correlation between genetic and geographic distances supported isolation-by-distance for the S7, but not for the CR, suggesting a complex scenario for the history of the rusty blenny in the Mediterranean Sea. The pattern of genetic structure displayed by P. sanguinolentus could be explained as the result of a post-glacial colonization of the Atlantic coast of Europe from the Mediterranean Sea.

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

Fig. 1
Fig. 2
Fig. 3

References

  1. Almada, V. C. & R. S. Santos, 1995. Parental care in the rocky intertidal: a case study of adaptation and adaptation in Mediterranean and Atlantic blennies. Reviews of Fish Biology and Fisheries 5: 23–37.

  2. Almada, V. C., R. F. Oliveira, E. J. Gonçalves, A. J. Almeida, R. S. Santos & P. Wirtz, 2001. Patterns of diversity of the north-eastern Atlantic blenniid fish fauna (Pisces: Blenniidae). Global Ecology & Biogeography 10: 411–422.

  3. Almada, F., V. C. Almada, T. Guillemaud & P. Wirtz, 2005a. Phylogenetic relationships of the north-eastern Atlantic and Mediterranean blenniids. Biological Journal of the Linnean Society 86: 283–295.

  4. Almada, F., V. C. Almada, V. Domingues, A. Brito & R. S. Santos, 2005b. Molecular validation of the specific status of Parablennius sanguinolentus and Parablennius parvicornis (Pisces: Blenniidae). Scientia Marina 64: 519–523.

  5. Bandelt, H., P. Forster & A. Rohl, 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48.

  6. Bargelloni, L., J. A. Alarcon, M. C. Alvarez, E. Penzo, A. Magoulas, C. Reis & T. Patarnello, 2003. Discord in the family Sparidae (Teleostei): divergent phylogeographical patterns across the Atlantic-Mediterranean divide. Journal of Evolutionary Biology 16: 1149–1158.

  7. Bath, H. 1990. Blenniidae. In: Quero J.C., J.C Hureau, C. Karrer, A. Post & L. Saldanha (eds), Check-list of the fishes of the eastern tropical Atlantic (CLOFETA). JNICT, SEI, UNESCO, Lisbon & Paris: 905–915.

  8. Bernardi, G. & J. Lape, 2005. Tempo and mode of speciation in the Baja California disjunct fish species Anisotremus davidsonii. Molecular Ecology 14: 4085–4096.

  9. Bernardi, G., L. Findley & A. Rocha-Olivares, 2003. Vicariance and dispersal across Baja California in disjunct marine fish populations. Evolution 57(7): 1599–1609.

  10. Bianco, P. G., 1990. Potential role of the palaeohistory of the Mediterranean and Paratethys basins on the early dispersal of Euro-Mediterranean freshwater fishes. Ichthyological Exploration of Freshwaters 1: 167–184.

  11. Bowen, B. W., A. Muss, L. A. Rocha & W. S. Grant, 2006. Shallow mtDNA coalescence in Atlantic pygmy angelfishes (Genus Centropyge) indicates a recent invasion from the Indian Ocean. Journal of Heredity 97: 1–12.

  12. Bouckaert, R., J. Heled, D. Kühnert, T. Vaughan, C.-H. Wu, D. Xie, M. A. Suchard, A. Rambaut & A. J. Drummond, 2014. BEAST 2: a Software Platform for Bayesian Evolutionary Analysis. PloS Computational Biology 10(4): e1003537.

  13. Breder, C. M. & D. E. Rosen, 1966. Modes of reproduction in fishes. Publications, Neptune City, New Jersey, T.F.H: 941.

  14. Charrier, G., T. Chenel, J. D. Durand, M. Girard, L. Quiniou & J. Laroche, 2006. Discrepancies in phylogeographical patterns of two European anglerfishes (Lophius budegassa and Lophius piscatorius). Molecular Phylogenetics and Evolution 38: 742–754.

  15. Chow, S. & K. Hazama, 1998. Universal PCR primers for S7 ribosomal protein gene introns in fish. Molecular Ecology 7: 1247–1263.

  16. Cimmaruta, R., F. Scialanca, F. Luccioli & G. Nascetti, 2003. Genetic diversity and environmental stress in Italian populations of the Cyprinodont fish Aphanius fasciatus. Oceanologica Acta 26: 101–110.

  17. Cimmaruta, R., P. Bondanelli & G. Nascetti, 2005. Genetic structure and environmental heterogeneity in the European hake (Merluccius merluccius). Molecular Ecology 14: 2577–2591.

  18. Colantoni, P., A. Fabbri, E. Rossi & R. Sartori, 1984. Panoramica sulla geologia dei mari italiani. Acqua & Aria 8: 803–820.

  19. Costa, S. S., R. Andrade, L. A. Carneiro, E. J. Goncalves, K. Kotrschalf & R. F. Oliveira, 2011. Sex differences in the dorsolateral telencephalon correlate with home range size in Blenniid fish. Brain, Behavior and Evolution 77: 55–64.

  20. Costagliola, D., D. R. Robertson, P. Guidetti, S. Stefanni, P. Wirtz, J. B. Heiser & G. Bernardi, 2004. Evolution of coral reef fish Thalassoma spp. (Labridae).2. Evolution of the eastern Atlantic species. Marine Biology 144: 377–383.

  21. CLIMAP, 1976. The surface of the ice-age earth. Science 191: 1131–1137.

  22. De Jong, K., N. Bouton & H. Slabbekoorn, 2007. Azorean rock-pool blennies produce size-dependent calls in a courtship context. Animal Behaviour 74: 1285–1292.

  23. Debes, P. V., F. E. Zachos & R. Hanel, 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. Molecular Ecology 17: 3873–3888.

  24. Di Natale, A., M. Bilecenoglu, M. Bariche, C. Bizsel, E. Massuti, J. Williams & M. Craig, 2014. Parablennius sanguinolentus. The IUCN Red List of Threatened Species 2014: e.T185193A1779730. (available on internet at http://dx.doi.org/10.2305/IUCN.UK.2014-3.RLTS.T185193A1779730.en).

  25. Domingues, V. S., R. S. Santos, A. Brito & V. C. Almada, 2006. Historical population dynamics and demography of the eastern Atlantic pomacentrid Chromis limbata (Valenciennes, 1833). Molecular Phylogenetics and Evolution 40: 139–147.

  26. Domingues, V. S., C. Faria, S. Stefanni, R. S. Santos, A. Brito & V. C. Almada, 2007a. Genetic divergence in the Atlantic-Mediterranean Montagu’s blenny, Coryphoblennius galerita (Linnaeus 1758) revealed by molecular and morphological characters. Molecular Ecology 16: 3592–3605.

  27. Domingues, V. S., R. S. Santos, A. Brito, M. Alexandrou & V. C. Almada, 2007b. Mitochondrial and nuclear markers reveal isolation by distance and effects of Pleistocene glaciations in the northeastern Atlantic and Mediterranean populations of the white seabream (Diplodus sargus, L.). Journal of Experimental Marine Biology and Ecology 346: 102–113.

  28. Domingues, V. S., V. C. Almada, R. S. Santos, A. Brito & G. Bernardi, 2007c. Phylogeography and evolution of the triplefin Tripterygion delaisi (Pisces, Blennioidei). Marine Biology 150: 509–519.

  29. Domingues, V. S., S. Stefanni, A. Brito, R. S. Santos & V. C. Almada, 2008a. Phylogeography and demography of the Blenniid Parablennius parvicornis and its sister species P. sanguinolentus from the northeastern Atlantic Ocean and the western Mediterranean Sea. Molecular Phylogenetics and Evolution 46: 397–402.

  30. Domingues, V. S., M. Alexandrou, V. C. Almada, D. R. Robertson, A. Brito, R. S. Santos & G. Bernardi, 2008b. 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. Marine Biology 154: 465–474.

  31. Drummond, A. J., A. Rambaut, B. Shapiro & O. G. Pybus, 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution 22: 1185–1192.

  32. Excoffier, L. & H. Lischer, 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Research 10: 564–567.

  33. Excoffier, L., P. E. Smouse & J. M. Quattro, 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491.

  34. Excoffier, L., I. Dupanloup, E. Huerta-Sanchez, V. C. Susa & M. Foll, 2013. Robust demographic inference from genomic and SNP data. PLoS Genetics 9(10): e1003905. doi:10.1371/journal.pgen.1003905.

  35. Felsenstein, J., 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution 17: 368–376.

  36. Ferrito, V., F. Maltagliati, A. Mauceri, A. Adorno & C. Tigano, 2003. Morphological and genetic variation in four Italian populations of Lebias fasciata (Teleostei, Cyprinodontidae). Italian Journal of Zoology 70: 115–121.

  37. Ferrito, V., A. M. Pappalardo, A. Canapa, M. Barucca, I. Doadrio, E. Olmo & C. Tigano, 2013. Mitochondrial phylogeography of the killifish Aphanius fasciatus (Teleostei, Cyprinodontidae) reveals highly divergent Mediterranean populations. Marine Biology 160(12): 3193–3208.

  38. Francisco, S. M., J. I. Robalo, A. Levy & V. C. Almada, 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, Berlin: 323–338.

  39. Fruciano, C., R. Hanel, P. V. Debes, C. Tigano & V. Ferrito, 2011. Atlantic-Mediterranean and within-Mediterranean molecular variation in Coris julis (L. 1758) (Teleostei, Labridae). Marine Biology 158: 1271–1286.

  40. Fruciano, C., A. M. Pappalardo, C. Tigano & V. Ferrito, 2014. Phylogeographical relationships of Sicilian brown trout and the effect of genetic introgression on morphospace occupation. Biological Journal of the Linnean Society 112: 387–398.

  41. Fruciano, C., P. Franchini, F. Raffini, S. Fan & A. Meyer, 2016. Are sympatrically speciating Midas cichlid fish special? Patterns of morphological and genetic variation in the closely related species Archocentrus centrarchus. Ecology and Evolution 6(12): 4102–4114.

  42. Fu, Y. X., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 437–460.

  43. Gaffney, P. M., J. Rupnow & M. L. Domeier, 2007. Genetic similarity of disjunct populations of the giant sea bass Stereolepis gigas. Journal of Fish Biology 70: 111–124.

  44. Galarza, J. A., J. Carreras-Carbonell, E. Macpherson, M. Pascual, S. Roques, G. F. Turner & C. Rico, 2009. The influence of oceanographic fronts and early-life-history traits on connectivity among littoral fish species. Proceedings of the National Academy of Sciences of the United States of America 106: 1473–1478.

  45. Gibson, R. N., 1999. Movement and homing in intertidal fishes. In Horn, M. H., K. L. M. Martin & M. A. Chotkowski (eds), Intertidal Fishes: Life in Two Worlds. Academic Press, London: 1–399.

  46. Gubili, C., D. W. Sims, A. Veríssimo, P. Domenici, J. Ellis, P. Grigoriou, A. F. Johnson, M. McHugh, F. Neat, A. Satta, G. Scarcella, B. Serra-Pereira, A. Soldo, M. J. Genner & A. M. Griffiths, 2014. A tale of two seas: contrasting patterns of population structure in the small-spotted catshark across Europe. Royal Society Open Science 1: 140–175.

  47. Harzhauser, M., A. Kroh, O. Mandic, W. E. Piller, U. Göhlich, M. Markus Reuter & B. Berning, 2007. Biogeographic responses to geodynamics: a key study all around the Oligo-Miocene Tethyan Seaway. Zoologischer Anzeiger 246: 241–256.

  48. Hayes, A., M. Kucera, N. Kallel, L. Sbaffi & E. J. Rohling, 2005. Glacial Mediterranean sea surface temperatures based on planktonic foraminiferal assemblages. Quaternary Science Reviews 24(7–9): 999–1016.

  49. Incarbona, A., M. Sprovieri, A. Di Stefano, E. Di Stefano, D. Salvagio Manta, N. Pelosi, M. R. d’Alcalà, R. Sprovieri & P. Ziveri, 2013. Productivity modes in the Mediterranean Sea during Dansgaard-Oeschger (20,000–70,000 yr ago) oscillations. Palaeogeography Palaeoclimatology and Palaeoecology 392: 128–137.

  50. Jesus, F. F., J. F. Wilkins, V. N. Solferini & J. Wakeley, 2006. Expected coalescence times and segregating sites in a model of glacial cycles. Genetics and Molecular Research 5: 466–474.

  51. Karaiskou, N., A. Triantafyllidis & C. Triantaphyllidis, 2004. Shallow genetic structure of three species of the genus Trachurus in European waters. Marine Ecology Progress Series 281: 193–205.

  52. Kimura, M., 1981. Estimation of evolutionary distances between homologous nucleotide sequences. Proceedings of the National Academy of Sciences of the United States of America 78: 454–458.

  53. Koblmüller, S., B. Steinwender, S. Weiß & K. M. Sefc, 2015. Gene flow, population growth and a novel substitution rate estimate in a subtidal rock specialist, the black-faced blenny Tripterygion delaisi (Perciformes, Blennioidei, Tripterygiidae) from the Adriatic Sea. Journal of Zoological Systematics and Evolutionary Research 53: 291–299.

  54. Krijgsman, W., F. J. Hilgen, I. Raf, F. J. Sierro & D. S. Wilson, 1999. Chronology, causes and progression of the Messinian salinity crisis. Nature 400: 652–655.

  55. Kuhner, M. K., 2006. LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22: 768–770.

  56. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson & D. G. Higgins, 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948.

  57. Lemaire, C., J. J. Versini & F. Bonhomme, 2005. Maintenance of genetic differentiation across a transition zone in the sea: discordance between nuclear and cytoplasmic markers. Journal of Evolutionary Biology 18: 70–80.

  58. Maggio, T., S. Lo Brutto, F. Garoia, F. Tinti & M. Arculeo, 2009. Microsatellite analysis of red mullet Mullus barbatus (Perciformes, Mullidae) reveals the isolation of the Adriatic Basin in the Mediterranean Sea. ICES Journal of Marine Science 66: 1883–1891.

  59. Maggs, C. A., R. Castilho, D. Foltz, C. Henzler, M. T. Jolly, J. Kelly, J. Olsen, K. E. Perez, W. Stam, R. Vainola, F. Viard & J. Wares, 2008. Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology 89(11): S108–S122.

  60. Magoulas, A., R. Castilho, S. Caetano, S. Marcato & T. Patarnello, 2006. Mitochondrial DNA reveals a mosaic pattern of phylogeographical structure in Atlantic and Mediterranean populations of anchovy (Engraulis encrasicolus). Molecular Phylogenetics and Evolution 39: 734–746.

  61. Mantel, N., 1967. The detection of disease clustering and a generalized regression approach. Cancer Research 27: 209–220.

  62. Mejri, R., M. Arculeo, O. K. Ben Hassine & S. Lo Brutto, 2011. Genetic architecture of the marbled goby Pomatoschistus marmoratus (Perciformes, Gobiidae) in the Mediterranean Sea. Molecular Phylogenetics and Evolution 58: 395–403.

  63. Nei, M. & S. Kumar, 2000. Molecular Evolution and Phylogenetics. Oxford University Press, Oxford: 1–333.

  64. Ostellari, L., L. Bargelloni, E. Penzo, P. Patarnello & T. Patarnello, 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. Animal Genetics 27: 423–427.

  65. Palumbi, S. R., F. Cipriano & M. P. Hare, 2001. Predicting nuclear gene coalescence from mitochondrial data: the three-times rule. Evolution 55: 859–868.

  66. Pappalardo, A. M., V. Ferrito, A. Messina, F. Guarino, T. Patarnello, V. De Pinto & C. Tigano, 2008. Genetic structure of the killifish Aphanius fasciatus, Nardo 1827 (Teleostei, Cyprinodontidae) results of mitochondrial DNA analysis. Journal of Fish Biology 72 (Supplement X): 1–20.

  67. Pappalardo, A. M., F. Guarino, S. Reina, A. Messina & V. De Pinto, 2011. Geographically widespread swordfish barcode stock identification: a case study of its application. PloS One 6: e25516.

  68. Pappalardo, A. M., E. G. Gonzalez, C. Tigano, I. Doadrio & V. Ferrito, 2015a. Comparative pattern of genetic structure in two Mediterranean killifishes (Aphanius fasciatus and A. iberus) inferred from both mitochondrial and nuclear data. Journal of Fish Biology 87: 69–87.

  69. Pappalardo, A. M., C. Federico, G. Sabella, S. Saccone & V. Ferrito, 2015b. A COI non-synonymous mutation as diagnostic tool for intraspecific discrimination in European anchovy Engraulis encrasicolus (Linnaeus). PloS One 10: e0143297.

  70. Paradis, E., J. Claude & K. Strimmer, 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290.

  71. Patarnello, T., F. M. J. Volckaert & R. Castilho, 2007. Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Molecular Ecology 16: 4426–4444.

  72. Pielou, E. C., 1979. Biogeography. Wiley, New York: 1–351.

  73. Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.

  74. Rambaut, A. & A.J. Drummond, 2007. Tracer v1.4. [available on internet at http://beast.bio.ed.ac.uk/Tracer.

  75. Raventós, N. & E. Macpherson, 2001. Planktonic larval duration and settlement marks on the otoliths of Mediterranean littoral fishes. Marine Biology 138: 1115–1120.

  76. Rinaldi, E., B. Buongiorno Nardelli, E. Zambianchi, R. Santoleri & P. M. Poulain, 2010. Lagrangian and Eulerian observations of the surface circulation in the Tyrrehenian Sea. Journal of Geophysical Research 115: C04024.

  77. Robalo, J. I., R. Castilho, S. M. Francisco, F. Almada, H. Knutsen, P. E. Jorde, A. M. Pereira & V. C. Almada, 2011. Northern refugia and recent expansion in the North Sea: the case of the wrasse Symphodus melops (Linnaeus, 1758). Ecology and Evolution 2: 153–164.

  78. Robalo, J. I., A. M. Crespo, R. Castilho, S. M. Francisco, M. C. P. Amorim & V. C. Almada, 2013. Are local extinctions and recolonizations continuing at the colder limits of marine fish distributions? Halobatrachus didactylus (Bloch & Schneider, 1801), a possible candidate. Marine Biology 160: 2461–2467.

  79. Robinson, A. R., W. G. Leslie, A. Theocharis & A. Lascaratos, 2001. Mediterranean Sea Circulation. Ocean Currents. Academic Press, London.

  80. Rogers, A. R., 1995. Genetic evidence for a Pleistocene population explosion. Evolution 49: 608–615.

  81. Rogers, A. R. & H. C. Harpending, 1992. Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9: 552–569.

  82. Rossi, A. R., E. Perrone & L. Sola, 2006. Genetic structure of gilthead seabream, Sparus aurata, in the Central Mediterranean Sea. Central European Journal of Biology 1(4): 636–647.

  83. Smouse, P. E., J. C. Long & R. R. Sokal, 1986. Multiple regression and correlation extensions of the Mantel Test of matrix correspondence. Systematic Zoology 35: 627–632.

  84. Tajima, F., 1983. Evolutionary relationship of DNA sequences in finite populations. Genetics 105: 437–446.

  85. Thiede, J., 1978. A glacial Mediterranean. Nature 276: 680–683.

  86. Thyssen, L., R. Triay-Portella, A. Santana del Pino & J. J. Castro, 2014. Homing behaviour of rock pool blenny Parablennius parvicornis (Pisces: Blenniidae). Journal of Natural History 48: 1169–1179.

  87. Toews, D. P. L. & A. Brelsford, 2012. The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology 21: 3907–3930.

  88. Watson, W., 2009. Larval development in blennies. In Patzner, R. A., E. J. Gonçalves, P. A. Hastings & B. G. Kapoor (eds), The Biology of Blennies. Science Publishers, Enfield, NH, USA: 309–350.

  89. Zardoya, R., R. Castilho, C. Grande, L. Favre-Krey, S. Caetano, S. Marcato, G. Krey & T. Patarnello, 2004. Differential population structuring of two closely related fish species, the mackerel (Scomber scombrus) and the chub mackerel (Scomber japonicus), in the Mediterranean Sea. Molecular Ecology 13: 1785–1798.

Download references

Acknowledgements

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), now included in the MARE (UID/MAR/04292/2013). SMF was supported by an FCT grant (SFRH/BPD/84923/2012). Funding was also provided by the University of Catania (PRA/2011/020204001104/VF), including part of the results of the doctoral thesis by Valentina Pulvirenti entitled “Struttura genetica del Blenniidae Parablennius sanguinolentus (Pallas, 1814), un valido bioindicatore dell’inquinamento delle acque costiere” (http://archivia.unict.it/handle/10761/1295). We dedicate this paper to the loving memory of Professor Vítor Almada, wonderful mentor and dear friend.

Author information

Correspondence to V. Ferrito.

Additional information

Handling editor: Christian Sturmbauer

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pappalardo, A.M., Francisco, S.M., Fruciano, C. et al. Mitochondrial and nuclear intraspecific variation in the rusty blenny (Parablennius sanguinolentus, Blenniidae). Hydrobiologia 802, 141–154 (2017). https://doi.org/10.1007/s10750-017-3248-6

Download citation

Keywords

  • Parablennius sanguinolentus
  • Atlantic
  • Mediterranean
  • Mitochondrial control region
  • S7 gene intron
  • Genetic structure