Marine Biology

, Volume 156, Issue 3, pp 239–252 | Cite as

Life style and genetic variation in teleosts: the case of pelagic (Aphia minuta) and benthic (Gobius niger) gobies (Perciformes: Gobiidae)

  • Massimo Giovannotti
  • Mario La Mesa
  • Vincenzo CaputoEmail author
Original Paper


The pattern of genetic variability of two species of Mediterranean gobiids was compared, with reference to their different life history traits (Aphia minuta paedomorphic and pelagic; Gobiusniger metamorphosed and benthic). The aim was to evaluate how different life histories can affect the genetic structure in these marine teleosts. The study was carried out on populations of both species sampled in the western Mediterranean and in the Adriatic Sea. Seven restriction endonucleases were used for the RFLP analysis of a mitochondrial DNA segment comprising the NADH dehydrogenase subunits 3, 4L and 4. The results highlighted two different patterns of genetic variation, a weak genetic structure in A. minuta and population subdivision in G. niger. These observations may be explained not only in terms of the different dispersal capabilities of these species, but also considering that A. minuta is an abbreviate iteroparous spawner while G. niger is a protracted iteroparous spawner. Because abbreviate iteroparity is a reproductive strategy selected in stable environments with high resource availability, Pliocene and Pleistocene climate oscillations may have represented factors that negatively influenced the reproductive success of A. minuta, producing demographic fluctuations and bottlenecks, as suggested by the mismatch distribution analysis. The weak genetic structure of A. minuta populations seems to be therefore due to a more recent re-colonization of the Mediterranean basin after a severe population decline, rather than to the high vagility of this pelagic goby.


Minimum Span Tree Restriction Fragment Length Polymorphism Analysis NADH Dehydrogenase Subunit Dispersal Capability Ancestral Haplotype 



This work was supported by grants from Università Politecnica delle Marche (Ancona, Italy). We wish to thank Enrico Arneri (ISMAR-CNR, Ancona, Italy) and Fabrizio Serena (ARPA Toscana, Livorno, Italy) for providing some of the samples of Aphia minuta and Gobius niger. We also wish to thank Betulla Morello for the English revision of the manuscript. The authors declare that the experiments performed in the course of this study comply with the current laws of the country in which the experiments were performed.


  1. Antonioli F, Lambeck K, Amorosi A, Belluomini G, Correggiari A, Devoti S, Depuro S, Monaco C, Marocco R, Pagliarulo R, Orrù P, Silenzi S (2004) Sea level at 8 and 22 ka cal BP on Italian coastline. In: Antonioli F, Vai GB (eds) Climex maps Italy—explanatory notes. Società Geologica Italiana, Bologna, pp 97–123Google Scholar
  2. Artegiani A, Bregant D, Paschini E, Pinardi N, Racich F, Russo A (1997) The Adriatic Sea general circulation. Part II: baroclinic circulation structure. J Phys Oceanogr 27:1515–1532. doi:10.1175/1520-0485(1997)027<1515:TASGCP>2.0.CO;2CrossRefGoogle Scholar
  3. Atarhouch T, Rüber L, Gonzalez EG, Albert EM, Rami M, Dakkak A, Zardoya R (2006) Signature of an early genetic bottleneck of moroccan sardines (Sardina pilchardus). Mol Phylogenet Evol 39:373–383. doi: CrossRefGoogle Scholar
  4. 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. Proc R Soc Lond B Biol Sci 267:929–935. doi: CrossRefGoogle Scholar
  5. Bembo DG, Carvalho GR, Snow M, Cingolani N, Pitcher TJ (1995) Stock discrimination among European anchovies, Engraulis encrasicolus, by means of PCR-amplified mitochondrial DNA analysis. Fish Bull (Wash D C) 94:31–40Google Scholar
  6. Bonfiglio L, Mangano G, Marra AC, Masini F, Pavia M, Petruso D (2002) Pleistocene Calabrian and Sicilian bioprovinces. Geobios Mem Spec 24:29–39. doi: CrossRefGoogle Scholar
  7. Bowen BW, Grant WS (1997) Phylogeography of the sardines (Sardinops spp.): assessing biogeographic models and population histories in temperate upwelling zones. Evol Int J Org Evol 51(5):1601–1610. doi: CrossRefGoogle Scholar
  8. Bremer JRA, Baker AJ, Mejuto J (1995) Mitochondrial DNA control region sequences indicate extensive mixing of swordfish (Xiphias gladius) populations in the Atlantic Ocean. Can J Fish Aquat Sci 52:1720–1732. doi: CrossRefGoogle Scholar
  9. Bremer JRA, Mejuto J, Greig TW, Ely B (1996) Global population structure of the swordfish (Xiphias gladius L.) as revealed by analysis of the mitochondrial DNA control region. J Exp Mar Biol Ecol 197:295–310. doi: CrossRefGoogle Scholar
  10. Brunelli C (1919) Ricerche sull’anatomia e fisiologia comparata dei pesci. Riv Biol 1:400–404Google Scholar
  11. Brunelli C, Atella F (1914) Ricerche sugli adattamenti alla vita planctonica (i Gobidi planctonici). Biol Zent 34:458–466Google Scholar
  12. Caputo V, Candi G, La Mesa M, Arneri E (2001) Pattern of gonad maturation and the question of semelparity in the paedomorphic goby Aphia minuta. J Fish Biol 58:656–669. doi: CrossRefGoogle Scholar
  13. Caputo V, Candi G, Arneri E, La Mesa M, Cinti C, Provinciali M, Nisi Cerioni P, Gregorini A (2002) Short life span and apoptosis in Aphia minuta. J Fish Biol 60:775–779. doi: CrossRefGoogle Scholar
  14. Caputo V, La Mesa M, Candi G, Nisi Cerioni P (2003) The reproductive biology of the crystal goby with a comparison to that of the transparent goby. J Fish Biol 62:375–385. doi: CrossRefGoogle Scholar
  15. Casabianca ML, Kiener A (1969) Gobiidés des étangs corses: systématique, écologie, régime alimentaire et position dans les chaînes trophiques. Vie Milieu Ser A Biol Mar 20(3):611–634Google Scholar
  16. Crandall KA, Templeton AR (1993) Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134:959–969PubMedPubMedCentralGoogle Scholar
  17. Cronin MA, Spearman WJ, Wilmot RL, Patto JC, Bickham JW (1993) Mitochondrial DNA variation in chinhook (Oncorhynchus tsawytscha) and chum salmon (O. keta) detected by restriction enzyme analysis of polymerase chain reaction (PCR) products. Can J Fish Aquat Sci 50:708–715CrossRefGoogle Scholar
  18. 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 131:479–491PubMedPubMedCentralGoogle Scholar
  19. Giovannotti M, Nisi Cerioni P, La Mesa M, Caputo V (2007) Molecular phylogeny of the three paedomorphic Mediterranean gobies (Perciformes: Gobiidae). J Exp Zool 308B(6):722–729. doi: Mol Dev EvolCrossRefGoogle Scholar
  20. Gosling EM (1994) Speciation and wide-scale genetic differentiation. In: Beaumont AR (ed) Genetic and evolution of aquatic organisms, London, pp 1–15Google Scholar
  21. Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426. doi: CrossRefGoogle Scholar
  22. Grant WS, Waples RS (2000) Spatial and temporal scales of genetic variability in marine and anadromous species: implications for fisheries oceanography. In: Harrison PJ, Parsons T (eds) Fisheries oceanography: an integrative approach to fisheries ecology and management. Blackwell Science, Oxford, pp 61–93Google Scholar
  23. Grosberg RK, Cunningham CW (2001) Genetic structure in the sea. From populations to communities. In: Bertness MD, Gaines S, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, pp 61–84Google Scholar
  24. Gysels ES, Hellemans B, Pampoulie C, Volckaert FAM (2004a) Phylogeography of the common goby, Pomatoschistus microps, with particular emphasis on the colonization of the Mediterranean and the North Sea. Mol Ecol 13:403–417. doi: CrossRefGoogle Scholar
  25. Gysels ES, Hellemans B, Patarnello T, Volckaert FAM (2004b) Current and historic gene flow of the sand goby Pomatoschistus minutus on the European continental Shelf and in the Mediterranean Sea. Biol J Linn Soc Lond 83:561–576. doi: CrossRefGoogle Scholar
  26. Hall HJ, Nawrocki LW (1995) A rapid method for detecting mitochondrial DNA variation in the brown trout, Salmo trutta. J Fish Biol 46:360–364. doi: CrossRefGoogle Scholar
  27. Hauser L, Carvalho GR, Pitcher TJ (1995) Morphological and genetic differentiation of the Africa clupeid Limnothrissa miodon 34 years after its introduction to the Lake Kivu. J Fish Biol 47(Suppl A):127–144. doi: CrossRefGoogle Scholar
  28. Hauser L, Turan C, Carvalho GR (2001) Haplotype frequency distribution and discriminatory power of two mtDNA fragments in a marine pelagic teleost (Atlantic herring, Clupea harengus). Heredity 87:621–630. doi: CrossRefGoogle Scholar
  29. Hewitt GM (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913. doi: CrossRefGoogle Scholar
  30. Iglesias M, Morales-Nin B (2001) Life cycle of the pelagic goby Aphia minuta (Pisces: Gobiidae). Sci Mar 65(3):183–192CrossRefGoogle Scholar
  31. Incze LS, Ortner PB, Schumacher JD (1990) Microzooplankton, vertical mixing and advection in a larval fish patch. J Plankton Res 12:365–379. doi: CrossRefGoogle Scholar
  32. Jaarola M, Tegelstrom H (1996) Mitochondrial DNA variation in the field vole (Microtus agrestis): regional population structure and colonization history. Evol Int J Org Evol 50:2073–2085. doi: Google Scholar
  33. Jones GP, Milicich MJ, Emsli MJ, Lunow C (1999) Self-recruitment in a coral reef fish population. Nature 402:802–804. doi: CrossRefGoogle Scholar
  34. Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200. doi: CrossRefGoogle Scholar
  35. La Mesa M (1999) Age and growth of Aphia minuta (Pisces, Gobiidae) from the central Adriatic Sea. Sci Mar 63(2):147–155CrossRefGoogle Scholar
  36. La Mesa M, Arneri E, Caputo V, Iglesias M (2005) The transparent goby, Aphia minuta: review of biology and fisheries of a paedomorphic European fish. Rev Fish Biol Fish 15:89–109. doi: CrossRefGoogle Scholar
  37. Lecomte F, Grant WS, Dodson JJ, Rodríguez-Sánchez R, Bowen BW (2004) Living with uncertainty: genetic imprints of climate shifts in East Pacific anchovy (Engraulis mordax) and sardine (Sardinops sagax). Mol Ecol 13:2169–2182. doi: CrossRefGoogle Scholar
  38. Magoulas A (2004) Mitochondrial DNA. In: Stocks identification methods. Academic Press, Dublin, pp 311–330CrossRefGoogle Scholar
  39. Magoulas A, Tsimenides N, Zouros E (1996) Mitochondrial DNA phylogeny and the reconstruction of the population history of a species: the case of the European anchovy (Engraulis encrasicolus). Mol Biol Evol 13(1):178–190CrossRefGoogle Scholar
  40. Magoulas A, Castilho R, Caetano S, Marcato S, Patarnello T (2006) Mitochondrial DNA reveals a mosaic pattern of phylogeographical structure in Atlantic and Mediterranean populations of anchovy (Engraulis encrasicolus). Mol Phylogenet Evol 39:734–746. doi: CrossRefGoogle Scholar
  41. Maynard NG (1976) The relationships between diatoms in the surface sediments of the Atlantic Ocean and the biological and physical oceanography of overlying waters. Palaeobiology 2:91–121CrossRefGoogle Scholar
  42. McElroy D, Moran PE, Bermingham E, Kornfield I (1991) REAP. The restriction enzyme analysis package, version 4.0. Orono, Department of Zoology, Migratory Fish Research Institute and Centre for Marine Studies, University of MaineGoogle Scholar
  43. McGowan JA, Walker PW (1985) Dominance and diversity maintenance in an oceanic ecosystem. Ecol Monogr 55:113–118. doi: CrossRefGoogle Scholar
  44. Miller PJ (1973) The species of Pseudaphya (Teleostei: Gobiidae) and the evolution of aphyiine gobies. J Fish Biol 5:353–365. doi: CrossRefGoogle Scholar
  45. Miller PJ (1979) Adaptiveness and implications of small size in Teleosts. In: Symposium of the zoological society, London, vol 44, pp 263–306Google Scholar
  46. Miller PJ (1986) Gobiidae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the North-Eastern Atlantic and Mediterranean, vol 3. UNESCO, Bungay, pp 1019–1085Google Scholar
  47. Miller PJ (1989) The tokology of gobioid fishes. In: Potts GW, Wootton RJ (eds) Fish reproduction: strategies and tactics. Academic Press, New York, pp 118–153Google Scholar
  48. Miller PJ (1997) Persistent postlarvae. The case of progenetic gobies. J Fish Biol 51(Suppl. A):412Google Scholar
  49. Muss A, Ross RD, Stepien CA, Wirtz P, Bowen BW (2001) Phylogeography of Ophioblennius: the role of ocean currents and geography in reef fish evolution. Evol Int J Org Evol 55:561–572. doi:[0561:POOTRO]2.0.CO;2 CrossRefGoogle Scholar
  50. Nielsen EE, Hansen MM, Mensberg K-LD (1998) Improved primer sequences for the mitochondrial ND1, ND3/4 and ND5/6 segments in salmonid fishes: application to RFLP analysis of Atlantic salmon. J Fish Biol 53:216–220. doi: CrossRefGoogle Scholar
  51. Palumbi SR (1992) Marine speciation on a small planet. Trends Ecol Evol 7:114–118. doi: CrossRefGoogle Scholar
  52. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572. doi: CrossRefGoogle Scholar
  53. Pampoulie C, Gysels ES, Maes GE, Hellemans B, Leentjes V, Jones AG, Volckaert FAM (2004) Evidence for fine-scale genetic structure and estuarine colonisation in a potential high gene flow marine goby (Pomatoschistus minutus). Heredity 92:434–445. doi: CrossRefGoogle Scholar
  54. Park LK, Brainard MA, Dightman DA (1993) Low levels of intraspecific variation in the mitochondrial DNA of chum salmon (Oncorhynchus keta). Mol Mar Biol Biotechnol 2:362–370PubMedGoogle Scholar
  55. Pinardi N, Korres G, Lascarotos A, Roussenov V, Stanev E (1997) Numerical simulation of the interannual variability of the Mediterranean sea upper ocean circulation. Geophys Res Lett 24:425–428. doi: CrossRefGoogle Scholar
  56. Planes S (1998) Genetic diversity and dispersal capabilities in marine fish. In: Hecht MK et al (eds) Evolutionary biology. Plenum Press, New York, pp 253–298Google Scholar
  57. Rand DM (1996) Neutraity test of molecular markers and the connection between DNA polymorphism, demography, and conservation biology. Conserv Biol 10:665–671. doi: CrossRefGoogle Scholar
  58. Raymond M, Rousset F (1995) An exact test for population differentiation. Evol Int J Org Evol 49:1280–1283. doi: CrossRefGoogle Scholar
  59. Riginos C, Nachman MW (2001) Population subdivision in marine environments : the contributions of biogeography, geographical distance and discontinuous habitat to genetic differentiation in a blennioid fish, Axoclinus nigricaudus. Mol Ecol 10:1439–1453. doi: CrossRefGoogle Scholar
  60. Riginos C, Victor BC (2001) Larval spatial distributions and other early life-history characteristics predict genetic differentiation in eastern Pacific blennioid fishes. Proc R Soc Lond Biol Sci 268:1931–1936. doi: CrossRefGoogle Scholar
  61. Rocha LA, Bass AL, Robertson DR, Bowen BW (2002) Adult habitat preferences, larval dispersal, and the comparative phylogeography of three Atlantic surgeonfishes (Teleostei: Acanthuridae). Mol Ecol 11:243–252. doi: CrossRefGoogle Scholar
  62. Roff DA, Bentzen P (1989) The statistical analysis of mitochondrial DNA polymorphisms: χ2 and the problem of small samples. Mol Biol Evol 6(5):539–545PubMedGoogle Scholar
  63. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9(3):552–569PubMedGoogle Scholar
  64. Roughgarden J, Gaines S, Possingham H (1998) Recruitment dynamics in complex life cycles. Science 241:1460–1466. doi: CrossRefGoogle Scholar
  65. Rüber L, Van Tassel JL, Zardoya R (2003) Rapid speciation and ecological divergence in the American seven-spine gobies (Gobiidae, Gobiosomatini) inferred from a molecular phylogeny. Evol Int J Org Evol 57(7):1584–1598CrossRefGoogle Scholar
  66. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring HarborGoogle Scholar
  67. Schneider S, Excoffier L (1999) Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089PubMedPubMedCentralGoogle Scholar
  68. Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN, Version 2.000: a software for population genetics data analysis, Genetics and Biometry Laboratory, Department of Anthropology, University of Geneva, GenevaGoogle Scholar
  69. Shulman M, Bermingham E (1995) Early life histories, ocean currents, and the population genetics of Caribbean reef fishes. Evol Int J Org Evol 49(5):897–910. doi: CrossRefGoogle Scholar
  70. Sinclair M, Iles TD (1989) Population regulation and speciation in the oceans. J Cons Int Explorat Mer 45:165–175CrossRefGoogle Scholar
  71. Stepien CA (1999) Phylogeographical structure of the Dover sole Microstomus pacificus: the larval retention hypothesis and genetic divergence along the deep continental slope of the northeastern Pacific Ocean. Mol Ecol 8:923–939. doi: CrossRefGoogle Scholar
  72. Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402:799–802. doi: CrossRefGoogle Scholar
  73. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  74. Takahata N, Palumbi SR (1985) Extranuclear differentiation and gene flow in the finite island model. Genetics 109:441–457PubMedPubMedCentralGoogle Scholar
  75. Taylor MS, Hellberg ME (2005) Marine radiations at small geographic scales: speciation in neotropical reef gobies (Elacatinus). Evol Int J Org Evol 59(2):374–385Google Scholar
  76. Thiede J (1978) A glacial Mediterranean. Nature 276:680–683. doi: CrossRefGoogle Scholar
  77. Viñas J, Alvarado Bremer J, Pla C (2004) Phylogeography of the Atlantic bonito (Sarda sarda) in the northern Mediterranean: the combined effects of historical vicariance, population expansion, secondary invasion, and isolation by distance. Mol Phylogenet Evol 33:32–42. doi: CrossRefGoogle Scholar
  78. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Massimo Giovannotti
    • 1
  • Mario La Mesa
    • 2
  • Vincenzo Caputo
    • 1
    Email author
  1. 1.Istituto di Biologia e GeneticaUniversità Politecnica delle MarcheAnconaItaly
  2. 2.ISMAR-CNR, Istituto di Scienze MarineSezione di AnconaAnconaItaly

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