Advertisement

Hydrobiologia

, Volume 758, Issue 1, pp 19–30 | Cite as

Disparate past demographic histories of three small Scombridae (Actinopterygii) species in Tunisian waters

  • Hassen AllayaEmail author
  • Abderraouf Ben Faleh
  • Abdallah Hattour
  • Monia Trabelsi
  • Jordi ViñasEmail author
Primary Research Paper

Abstract

The bullet tuna Auxis rochei, the little tunny Euthynnus alletteratus, and the Atlantic Chub mackerel Scomber colias are three small Scombridae with similar life-history traits such as overlapping epipelagic distribution and a shared spawning area in Tunisian waters. In this study, we compared the phylogeography and demographic histories of these species by analyzing the sequence variability of the mitochondrial DNA control region. None of the species showed genetic differentiation in their Tunisian distribution; however, we inferred three completely different population histories. E. alletteratus showed a demographic history of a very recent bottleneck followed by sudden population expansion probably consequence of a population decline in the Last Glacial Maximum. S. colias also presented a population expansion after collapse but in this case about ten-fold older than that observed in E. alletteratus. Finally, A. rochei presented a history of demographic stability. These contrasting population histories were discussed based on their possible differences in life-history traits, but the hypothesis of stochastic factors affecting the demography of these species was also invoked.

Keywords

Small scombridae Bayesian skyline plots Contrasting demographic histories Mismatch distributions 

Notes

Acknowledgments

We thank Hajjej Ghailen for providing some Euthynnus alletteratus samples. We also are indebted to fishermen from localities where we took samples. We also thank Dr. Carles Pla and Dr. Oriol Vidal who help us in the laboratory process and data analysis.

Conflict of interest

All the authors declare that they have no conflict of interest.

Compliance with ethics requirements

All work met the requirements stated by the Spanish (RD53/2013) and Catalonian (D214/1997) laws of animal care and experimentation.

Supplementary material

10750_2015_2261_MOESM1_ESM.docx (61 kb)
Supplementary material 1 (DOCX 61 kb)

References

  1. Allaya, H., A. Hattour, G. Hajjej & M. Trabelsi, 2013a. Biologic characteristics of Scomber japonicus (Houttuyn, 1782) in Tunisian waters (Central Mediterranean Sea). African Journal of Biotechnology 12: 3040–3048.Google Scholar
  2. Allaya, H., A. Hattour, G. Hajjej & M. Trabelsi, 2013b. Some biological parameters of the bullet tuna Auxis rochei (Risso, 1810) in Tunisian waters. Cahiers de Biologie Marine 54: 287–292.Google Scholar
  3. Alvarado Bremer, J. R., 1994. Assessment of morphological and genetic variation of the swordfish (Xiphias gladius Linnaeus): evolutionary patterns of nucleotide substitution in the mitochondrial genome. University of Toronto, Canada.Google Scholar
  4. Alvarado Bremer, J. R., J. Mejuto, T. W. Greig & B. Ely, 1996. Global population structure of the swordfish (Xiphias gladius L.) as revealed by analysis of the mitochondrial DNA control region. Journal of Experimental Marine Biology and Ecology 197: 295–310.CrossRefGoogle Scholar
  5. Alvarado Bremer, J., B. Stequert, N. W. Robertson & B. Ely, 1998. Genetic evidence for inter-oceanic subdivision of bigeye tuna (Thunnus obesus) populations. Marine Biology 132: 547–557.CrossRefGoogle Scholar
  6. Alvarado Bremer, J. R., J. Viñas, J. Mejuto, B. Ely & C. Pla, 2005. Comparative phylogeography of Atlantic bluefin tuna and swordfish: the combined effects of vicariance, secondary contact, introgression, and population expansion on the regional phylogenies of two highly migratory pelagic fishes. Molecular Phylogenetics and Evolution 36: 169–187.PubMedCrossRefGoogle Scholar
  7. Avise, J. C., 2000. Phylogeography: the history and formation of species. Harvard University Press, Cambridge.Google Scholar
  8. Bandelt, H. J., P. Forster, B. C. Sykes & M. B. Richards, 1995. Mitochondrial portraits of human populations using median networks. Genetics 141: 743–753.PubMedCentralPubMedGoogle Scholar
  9. Bandelt, H. J., P. Forster & A. Rohl, 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48.PubMedCrossRefGoogle Scholar
  10. 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.PubMedCrossRefGoogle Scholar
  11. Bargelloni, L., J. A. Alarcón, M. C. Alvarez, E. Penzo, A. Magoulas, J. Palma & T. Patarnello, 2005. The Atlantic–Mediterranean transition: discordant genetic patterns in two seabream species, Diplodus puntazzo (Cetti) and Diplodus sargus (L.). Molecular Phylogenetics and Evolution 36: 523–535.PubMedCrossRefGoogle Scholar
  12. Catanese, G., M. Manchado & C. Infante, 2010. Evolutionary relatedness of mackerels of the genus Scomber based on complete mitochondrial genomes: strong support to the recognition of Atlantic Scomber colias and Pacific Scomber japonicus as distinct species. Gene 452: 35–43.PubMedCrossRefGoogle Scholar
  13. Collette, B. B., 1999. Mackerels, molecules, and morphology. Proceedings of the 5th Indo-Pacific Fishereis Conference: 149–164.Google Scholar
  14. Collette, B. B. & D. A. Nauen, 1983. FAO species catalogue, Vol. 2. Scombrids of the world: an annotated and illustrated catalogue of tunas, mackerels, bonitos, and related species known to date. FAO fisheries Synopsis 125: 1–137.Google Scholar
  15. Collette, B. B., C. A. Reeb & B. A. Block, 2001. Systematics of the Tunas and Mackerels (Scombridae). In Block, B. A. & E. D. Stevens (eds), Tuna: Physiology, Ecology and Evolution. Academic, San Diego, California, USA.Google Scholar
  16. Crandall, E. D., M. A. Frey, R. K. Grosberg & P. H. Barber, 2008. Contrasting demographic history and phylogeographical patterns in two Indo-Pacific gastropods. Molecular Ecology 17: 611–626.PubMedCrossRefGoogle Scholar
  17. Drummond, A. J., M. A. Suchard, D. Xie & A. Rambaut, 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29: 1969–1973.PubMedCentralPubMedCrossRefGoogle Scholar
  18. Ely, B., J. Viñas, J. R. Alvarado Bremer, D. Black, L. Lucas, K. Covello, A. V. Labrie & E. Thelen, 2005. Consequences of the historical demography on the global population structure of two highly migratory cosmopolitan marine fishes: the yellowfin tuna (Thunnus albacares) and the skipjack tuna (Katsuwonus pelamis). BMC Evolutionary Biology 5: 19.PubMedCentralPubMedCrossRefGoogle Scholar
  19. Emig, C. C. & P. Geistdoerfer, 2004. The Mediterranean deep-sea fauna: historical evolution, bathymetric variations and geographical changes. Carnets de Géologie / Notebooks on Geology, Maintenon, Article 2004/01 (CG2004_A01_CCE-PG).Google Scholar
  20. Excoffier, L. & H. E. L. Lischer, 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.PubMedCrossRefGoogle Scholar
  21. 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.PubMedCentralPubMedGoogle Scholar
  22. Fernández, M. V., S. Heras, J. Vinas, F. Maltagliati & M. I. Roldan, 2013. Multilocus comparative phylogeography of two aristeid shrimps of high commercial interest (Aristeus antennatus and Aristaeomorpha foliacea) reveals different responses to past environmental changes. PLoS ONE 8: e59033.PubMedCentralPubMedCrossRefGoogle Scholar
  23. González, E. G. & R. Zardoya, 2007. Relative role of life-history traits and historical factors in shaping genetic population structure of sardines (Sardina pilchardus). BMC Evolutionary Biology 7: 197.PubMedCentralPubMedCrossRefGoogle Scholar
  24. González, E. G., P. Beerli & R. Zardoya, 2008. Genetic structuring and migration patterns of Atlantic bigeye tuna, Thunnus obesus (Lowe, 1839). BMC Evolutionary Biology 8: 252.PubMedCentralPubMedCrossRefGoogle Scholar
  25. Grant, W. S., 2005. A second look at mitochondrial DNA variability in European anchovy (Engraulis encrasicolus): assessing models of population structure and the Black Sea isolation hypothesis. Genetica 125: 293–309.PubMedCrossRefGoogle Scholar
  26. Grant, W. S., M. Liu, T. X. Gao & T. Yanagimoto, 2012. Limits of Bayesian skyline plot analysis of mtDNA sequences to infer historical demographies in Pacific herring (and other species). Molecular Phylogenetics and Evolution 65: 203–212.PubMedCrossRefGoogle Scholar
  27. Hajjej, G., A. Hattour, H. Allaya, O. Jarboui & A. Bouain, 2011. Some biological parameters of little tuna Euthynnus alletteratus (Rafinesque, 1810) in Tunisian waters. Cahiers de Biologie Marine 53: 33–40.Google Scholar
  28. Hall, T. A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.Google Scholar
  29. Harpending, H. C., M. A. Batzer, M. Gurven, L. B. Jorde, A. R. Rogers & S. T. Sherry, 1998. Genetic traces of ancient demography. Proceedings of the National Academy of Sciences of the United States of America 95: 1961–1967.PubMedCentralPubMedCrossRefGoogle Scholar
  30. Hasegawa, M., H. Kishino & T. A. Yano, 1985. Dating of the human ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22: 160–174.PubMedCrossRefGoogle Scholar
  31. ICCAT, 2008. Report of the joint GFCM/ICCAT meeting on small tunas fisheries in the mediterranean. ICCAT, 18.Google Scholar
  32. Infante, C., E. Blanco, E. Zuasti, A. Crespo & M. Manchado, 2007. Phylogenetic differentiation between Atlantic Scomber colias and Pacific Scomber japonicus based on nuclear DNA sequences. Genetica 130: 1–8.PubMedCrossRefGoogle Scholar
  33. Juan-Jordá, M. J., I. Mosqueira, J. Freire & N. K. Dulvy, 2013. The conservation and management of tunas and their relatives: setting life history research priorities. PLoS ONE 8: e70405.PubMedCentralPubMedCrossRefGoogle Scholar
  34. Karl, S. A., R. J. Toonen, W. S. Grant & B. W. Bowen, 2012. Common misconceptions in molecular ecology: echoes of the modern synthesis. Molecular Ecology 21: 4171–4189.PubMedCrossRefGoogle Scholar
  35. Koched, W., A. Hattour, F. Alemany, A. Garcia & K. Said, 2013. Spatial distribution of tuna larvae in the Gulf of Gabes (Eastern Mediterranean) in relation with environmental parameters. Mediterranean Marine Science 14: 5–14.CrossRefGoogle Scholar
  36. Kumar, G. & S. P. Kunal, 2013. Historic demography and phylogenetic relationship of Euthynnus species based on COI sequence analyses. International Journal of Bioinformatics Research and Applications 9: 547–555.PubMedCrossRefGoogle Scholar
  37. Kumar, G., S. P. Kunal & S. K. Shyama, 2013. Evolutionary history and phylogenetic relationship between Auxis thazard and Auxis rochei inferred from COI sequences of mtDNA. International Journal of Bioinformatics Research and Applications 9: 604–613.PubMedCrossRefGoogle Scholar
  38. Li, W. H., 1977. Distribution of nucleotide differences between 2 randomly chosen cistrons in a finite population. Genetics 85: 331–337.PubMedCentralPubMedGoogle Scholar
  39. Librado, P. & J. Rozas, 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.PubMedCrossRefGoogle Scholar
  40. Macías, D., M. J. Gómez-Vives & J. M. De La Serna, 2005. Some reproductive aspects of bullet tuna (Auxis rochei) from the south western spanish mediterranean. ICCAT Collective Volume of Scientific Papers 48: 484–495.Google Scholar
  41. Magoulas, A., N. Tsimenides & E. Zouros, 1996. Mitochondrial DNA phylogeny and the reconstruction of the population history of a species: the case of the European anchovy (Engraulis encrasicolus). Molecular Biology and Evolution 13: 178–190.PubMedCrossRefGoogle Scholar
  42. 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.PubMedCrossRefGoogle Scholar
  43. Mejri, R., S. Lo Brutto, O. K. Ben Hassine & M. Arculeo, 2009. A study on Pomatoschistus tortonesei Miller 1968 (Perciformes, Gobiidae) reveals the Siculo-Tunisian Strait (STS) as a breakpoint to gene flow in the Mediterranean basin. Molecular Phylogenetics and Evolution 53: 596–601.PubMedCrossRefGoogle Scholar
  44. Montes, I., D. Conklin, A. Albaina, S. Creer, G. R. Carvalho, M. Santos & A. Estonba, 2013. SNP discovery in European anchovy (Engraulis encrasicolus, L) by high-throughput transcriptome and genome sequencing. PLoS ONE 8: 12.Google Scholar
  45. Nei, M., 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.Google Scholar
  46. Nei, M. & F. Tajima, 1981. DNA polymorphism detectable by restriction endonucleases. Genetics 97: 145–163.PubMedCentralPubMedGoogle Scholar
  47. Nesbø, C. L., E. K. Rueness, S. A. Iversen, D. W. Skagen & K. S. Jakobsen, 2000. Phylogeography and population history of Atlantic mackerel (Scomber scombrus L.): a genealogical approach reveals genetic structuring among the eastern Atlantic stocks. Proceedings of the Royal Society of London Series B: Biological Sciences 267: 281–292.PubMedCentralPubMedCrossRefGoogle Scholar
  48. Palumbi, S. R., 1994. Genetic-divergence, reproductive isolation, and marine speciation. Annual Review of Ecology and Systematics 25: 547–572.CrossRefGoogle Scholar
  49. Papetti, C., A. Di Franco, L. Zane, P. Guidetti, V. De Simone, M. Spizzotin, B. Zorica, V. C. Kec & C. Mazzoldi, 2013. Single population and common natal origin for Adriatic Scomber scombrus stocks: evidence from an integrated approach. ICES Journal of Marine Science 70: 387–398.CrossRefGoogle Scholar
  50. Patarnello, T., F. A. M. J. Volckaert & R. Castilho, 2007. Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographical break? Molecular Ecology 16: 4426–4444.PubMedCrossRefGoogle Scholar
  51. Quere, N., E. Desmarais, C. S. Tsigenopoulos, K. Belkhir, F. Bonhomme & B. Guinand, 2012. Gene flow at major transitional areas in sea bass (Dicentrarchus labrax) and the possible emergence of a hybrid swarm. Ecology and Evolution 2: 3061–3078.PubMedCentralPubMedCrossRefGoogle Scholar
  52. Rambaut, A. & A. J. Drummond, 2007. Tracer v.1.6 [available on internet at http://beast.bio.ed.ac.uk/Tracer].
  53. Ramos-Onsins, S. E. & J. Rozas, 2002. Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution 19: 2092–2100.PubMedCrossRefGoogle Scholar
  54. Rogers, A. R., 1995. Genetic evidence for a Pleistocene explosion. Evolution 49: 608–615.CrossRefGoogle Scholar
  55. Rogers, A. R. & H. Harpending, 1992. Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9: 552–569.PubMedGoogle Scholar
  56. Sabatés, A. & L. Recasens, 2001. Seasonal distribution and spawning of small tunas (Auxis rochei and Sarda sarda) in the northwestern Mediterranean. Scientia Marina 65: 95–100.CrossRefGoogle Scholar
  57. Sambrook, J., E. J. Fritsch & T. Maniatis, 1989. Molecular Cloning. A Laboratory Manual. Cold spring Harbor, Laboratory, New York.Google Scholar
  58. Sanz, N., J. L. Garcia-Marin, J. Vinas, M. Roldan & C. Pla, 2008. Spawning groups of European anchovy: population structure and management implications. ICES Journal of Marine Science 65: 1635–1644.CrossRefGoogle Scholar
  59. Schneider, S. & L. Excoffier, 1999. Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152: 1079–1089.PubMedCentralPubMedGoogle Scholar
  60. Scoles, D. R., B. B. Collette & J. E. Graves, 1998. Global phylogeography of mackerels of the genus Scomber. Fishery Bulletin 96: 823–842.Google Scholar
  61. Simon, M., J.-M. Fromentin, S. Bonhommeau, D. Gaertner, J. Brodziak & M.-P. Etienne, 2012. Effects of stochasticity in early life history on steepness and population growth rate estimates: an illustration on Atlantic Bluefin Tuna. PLoS ONE 7: e48583.PubMedCentralPubMedCrossRefGoogle Scholar
  62. Slatkin, M. & R. Hudson, 1991. Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129: 555–562.PubMedCentralPubMedGoogle Scholar
  63. Tajima, F., 1989a. The effect of change in population size on DNA polymorphism. Genetics 123: 597–601.PubMedCentralPubMedGoogle Scholar
  64. Tajima, F., 1989b. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.PubMedCentralPubMedGoogle Scholar
  65. Tamura, K., 1992. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Molecular Biology and Evolution 9: 678–687.PubMedGoogle Scholar
  66. Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.PubMedCentralPubMedCrossRefGoogle Scholar
  67. Thiede, J., 1978. A glacial Mediterranean. Nature 276: 680–683.CrossRefGoogle Scholar
  68. Vasconcelos, J., M. Afonso-Dias & G. Faria, 2012. Atlantic chub mackerel (Scomber colias) spawning season, size and age at first maturity in Madeira waters. Life and Marine Sciences 29: 43–51.Google Scholar
  69. Viñas, J., N. Sanz, L. Penarrubia, R.-M. Araguas, J.-L. Garcia-Marin, M.-I. Roldan & C. Pla, 2014. Genetic population structure of European anchovy in the Mediterranean Sea and the Northeast Atlantic Ocean using sequence analysis of the mitochondrial DNA control region. ICES Journal of Marine Science 71: 391–397.CrossRefGoogle Scholar
  70. Viñas, J., J. R. Alvarado Bremer & C. Pla, 2004a. Inter-oceanic genetic differentiation among albacore (Thunnus alalunga) populations. Marine Biology 145: 225–232.CrossRefGoogle Scholar
  71. Viñas, J., J. R. Alvarado Bremer & C. Pla, 2004b. 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. Molecular Phylogenetics and Evolution 33: 32–42.PubMedCrossRefGoogle Scholar
  72. Viñas, J., J. R. Alvarado Bremer & C. Pla, 2010. Phylogeography and phylogeny of the epineritic cosmopolitan bonitos of the genus Sarda (Cuvier): inferred patterns of intra- and inter-oceanic connectivity derived from nuclear and mitochondrial DNA data. Journal of Biogeography 37: 557–570.CrossRefGoogle Scholar
  73. Ward, R. D., M. Woodwark & D. O. F. Skibinski, 1994. A comparison of genetic diversity levels in marine, fresh-water, and anadromous fishes. Journal of Fish Biology 44: 213–232.CrossRefGoogle Scholar
  74. 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.PubMedCrossRefGoogle Scholar
  75. Zarraonaindia, I., M. A. Pardo, M. Iriondo, C. Manzano & A. Estonba, 2009. Microsatellite variability in European anchovy (Engraulis encrasicolus) calls for further investigation of its genetic structure and biogeography. ICES Journal of Marine Science 66: 2176–2182.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Marine Biology Unit, Faculty of Sciences of TunisUniversity of Tunis-El ManarTunisTunisia
  2. 2.National Institute of Sea Sciences and Technologies (I.N.S.T.M)TunisTunisia
  3. 3.Department of Biology, Faculty of Sciences of GafsaUniversity of GafsaGafsaTunisia
  4. 4.Laboratori Ictiologia Genètica, Departament de BiologiaUniversitat de GironaGironaSpain

Personalised recommendations