Skip to main content

Advertisement

SpringerLink
Log in

Drivers of Population Structure of the Bottlenose Dolphin (Tursiops truncatus) in the Eastern Mediterranean Sea

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

The drivers of population differentiation in oceanic high dispersal organisms, have been crucial for research in evolutionary biology. Adaptation to different environments is commonly invoked as a driver of differentiation in the oceans, in alternative to geographic isolation. In this study, we investigate the population structure and phylogeography of the bottlenose dolphin (Tursiops truncatus) in the Mediterranean Sea, using microsatellite loci and the entire mtDNA control region. By further comparing the Mediterranean populations with the well described Atlantic populations, we addressed the following hypotheses: (1) bottlenose dolphins show population structure within the environmentally complex Eastern Mediterranean Sea; (2) population structure was gained locally or otherwise results from chance distribution of pre-existing genetic structure; (3) strong demographic variations within the Mediterranean basin have affected genetic variation sufficiently to bias detected patterns of population structure. Our results suggest that bottlenose dolphin exhibits population structures that correspond well to the main Mediterranean oceanographic basins. Furthermore, we found evidence for fine scale population division within the Adriatic and the Levantine seas. We further describe for the first time, a distinction between populations inhabiting pelagic and coastal regions within the Mediterranean. Phylogeographic analysis suggests that current genetic structure, results mostly from stochastic distribution of Atlantic genetic variation, during a recent post-glacial expansion. Comparison with Atlantic mtDNA haplotypes, further suggest the existence of a metapopulation across North Atlantic/Mediterranean, with pelagic regions acting as source for coastal environments.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Amaral, A. R., Beheregaray, L. B., Bilgmann, K., Boutov, D., Freitas, L., Robertson, K. M., et al. (2012). Seascape genetics of a globally distributed, highly mobile marine mammal: The short-beaked common dolphin (genus Delphinus). PLoS One, 7, e31482.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

  • Ansmann, I. C., Parra, G. J., Lanyon, J. M., & Seddon, J. M. (2012). Fine-scale genetic population structure in a mobile marine mammal: Inshore bottlenose dolphins in Moreton Bay, Australia. Molecular Ecology, 21, 4472–4485.

    Article  PubMed  Google Scholar 

  • Augusto, J. F., Rachinas-Lopes, P., & dos Santos, M. E. (2011). Social structure of the declining resident community of common bottlenose dolphins in the Sado Estuary, Portugal. Journal of Marine Biology Association of United Kingdom, 92, 1773–1782.

    Article  Google Scholar 

  • Bahri-Sfar, L., Lemaire, C., Hassine, O. K. B., & Bonhomme, F. (2000). Fragmentation of sea bass populations in the western and Eastern Mediterranean as revealed by microsatellite polymorphism. Proceeding of the Royal Society of London B, 267, 929–935.

    Article  CAS  Google Scholar 

  • Bandelt, H.-J., Forster, P., & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48.

    Article  CAS  PubMed  Google Scholar 

  • Banguera-Hinestroza, E., Bjørge, A., Reid, R. J., Jepson, P., & Hoelzel, A. R. (2010). The influence of glacial epochs and habitat dependence on the diversity and phylogeography of a coastal dolphin species: Lagenorhynchus albirostris. Conservation Genetics, 11, 1823–1836.

    Article  Google Scholar 

  • Banguera-Hinestroza, E., Evans, P. G. H., Mirimin, L., Reid, R. J., Mikkelsen, B., Couperus, A. S., et al. (2014). Phylogeography and population dynamics of the white-sided dolphin (Lagenorhynchus acutus) in the North Atlantic. Conservation Genetics,. doi:10.1007/s10592-014-0578-z.

    Google Scholar 

  • Bearzi, G., & Fortuna, C. M. (2006). Common bottlenose dolphin Tursiops truncatus (Mediterranean subpopulation). In R. R. Reeves & G. Notarbartolo di Sciara (Eds.), The status and distribution of cetaceans in the Black Sea and Mediterranean Sea (pp. 64–73). Malaga: IUCN Centre for Mediterranean Cooperation.

    Google Scholar 

  • Bearzi, G., Fortuna, C. M., & Reeves, R. R. (2009). Ecology and conservation of common bottlenose dolphins (Tursiops truncatus) in the Mediterranean Sea. Mammal Review, 39, 92–123.

    Article  Google Scholar 

  • Bearzi, G., Notarbartolo di Sciara, G., & Politi, E. (1997). Social ecology of bottlenose dolphins in the Kvarneric (northern Adriatic Sea). Marine Mammal Science, 13, 650–668.

    Article  Google Scholar 

  • Bearzi, G., Politi, E., Agazzi, S., Bruno, S., Costa, M., & Bonizzoni, S. (2005). Occurrence and present status of coastal dolphins (Delphinus delphis and Tursiops truncatus) in the eastern Ionian sea. Aquatic Conservation: Marine Freshwater Ecosystem, 15, 243–357.

    Article  Google Scholar 

  • Becker, J. J., Sandwell, D. T., Smith, W. H. F., Braud, J., Binder, B., Depner, J., et al. (2009). Global bathymetry and elevation data at 30 arc seconds resolution: STRM30_PLUS. Marine Geodesy, 32, 355–371.

    Article  Google Scholar 

  • Bérubé, M., & Palsbøll, P. (1996). Identification of sex in cetaceans by multiplexing with three ZFX and ZFY specific primers. Molecular Ecology, 5, 283–287.

    Article  PubMed  Google Scholar 

  • Bierne, N., Bonhomme, F., & David, P. (2003). Habitat preference and the marine-speciation paradox. Proceeding of the Royal Society of London B, 270, 1399–1406.

    Article  Google Scholar 

  • Bilgmann, K., Möller, L. M., Harcourt, R. G., Kemper, C. M., & Beheregaray, L. B. (2011). The use of carcasses for the analysis of cetacean population genetic structure: A Comparative study in two dolphin species. PLoS One, 6(5), e20103.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Borsa, P., Blanquer, A., & Berrebi, P. (1997). Genetic structure of the flounders Platichthys flesus and P. stellatus at different geographic scales. Marine Biology, 129, 233–246.

    Article  CAS  Google Scholar 

  • Bowen, B., Avise, J. C., Richardson, J. I., Meylan, A. B., Margaritoulis, D., & Hopkins-Murphy, S. R. (1993). Population structure of loggerhead turtles (Caretta caretta) in the northwestern Atlantic Ocean and Mediterranean Sea. Conservation Biology, 7, 834–844.

    Article  Google Scholar 

  • Caballero, S., Islas-Villanueva, V., Tezanos-Pinto, G., Duchene, S., Delgado-Estrella, A., Sanchez-Okrucky, R., et al. (2012). Phylogeography, genetic diversity and population structure of common bottlenose dolphins in the wider Caribbean inferred from analyses of mitochondrial DNA control region sequences and microsatellite loci: Conservation and management implications. Animal Conservation, 15, 95–112.

    Article  Google Scholar 

  • Caldwell, M., Gaines, M. S., & Hughes, C. R. (2002). Eight polymorphic microsatellite loci for bottlenose dolphin and other cetacean species. Molecular Ecolology Notes, 2, 393–395.

    Article  CAS  Google Scholar 

  • Calvo, M., Templado, J., Oliverio, M., & Machordom, A. (2009). Hidden Mediterranean biodiversity: Molecular evidence for a cryptic species complex within the reef building vermetid gastropod Dendropoma petraeum (Mollusca: Caenogastropoda). Biological Journal of Linnean Society, 96, 898–912.

    Article  Google Scholar 

  • Carreras, C., Pascual, M., Cardona, L., Aguilar, A., Margaritoulis, D., Rees, A., et al. (2006). The genetic structure of the loggerhead sea turtle (Caretta caretta) in the Mediterranean as revealed by nuclear and mitochondrial DNA and its conservation implications. Conservation Genetics, 8, 761–775.

    Article  Google Scholar 

  • Carreras-Carbonell, J., Macpherson, E., & Pascual, M. (2006). Population structure within and between subspecies of the Mediterranean triplefin fish Tripterygion delaisi revealed by highly polymorphic microsatellite loci. Molecular Ecology, 15, 3527–3539.

    Article  CAS  PubMed  Google Scholar 

  • Casado-Amezúa, P., Goffredo, S., Templado, J., & Machordom, A. (2012). Genetic assessment of population structure and connectivity in the threatened Mediterranean coral Astroides calycularis (Scleractinia, Dendrophylliidae) at different spatial scales. Molecular Ecology, 21, 3671–3685.

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cheney, B., Thompson, P. M., Ingram, S. N., Hammond, P. S., Stevick, P. T., Durban, J. W., et al. (2013). Integrating multiple data sources to assess the distribution and abundance of bottlenose dolphins Tursiops truncatus in Scottish waters. Mammal Review, 43, 71–88.

    Article  Google Scholar 

  • Coll, M., Piroddi, C., Steenbeek, J., Kaschner, K., Lasram, F. B. R., Aguzzi J., et al. (2010). The biodiversity of the Mediterranean Sea: Estimates, patterns, and threats. PLoS One, 5, e11842.

    Article  PubMed Central  PubMed  Google Scholar 

  • Cornuet, J. M., & Luikart, G. (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144, 2001–2014.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Domingues, V. S., Bucciarelli, G., Almada, V. C., & Bernardi, G. (2005). Historical colonization and demography of the Mediterranean damselfish, Chromis chromis. Molecular Ecology, 14, 4051–4063.

    Article  PubMed  Google Scholar 

  • Domingues, V. S., Santos, R. S., Brito, A., Alexandrou, M., & Almada, V. C. (2007). 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.

    Article  CAS  Google Scholar 

  • Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Earl, D. A., & vonHoldt, B. M. (2012). Structure harvester: A website and program for visualizing structure output and implementing the Evanno method. Conservation Genetics Resources, 4, 359–361.

    Article  Google Scholar 

  • Excoffier, L., Laval, G., & Schneider, S. (2005). Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47–50.

    PubMed Central  CAS  Google Scholar 

  • Fernández, R., Santos, M. B., Pierce, G. J., Llavona, Á., López, A., Silva, M. A., et al. (2011). Fine-scale genetic structure of bottlenose dolphins, Tursiops truncatus, in Atlantic coastal waters of the Iberian Peninsula. Hydrobiologia, 670, 111–125.

    Article  Google Scholar 

  • Fontaine, M. C., Roland, K., Calves, I., Austerlitz, F., Palstra, F. P., Tolley, K. A., et al. (2014). Postglacial climate changes and rise of three ecotypes of harbor porpoises, Phocoena phocoena, in western palearctic waters. Molecular Ecology,. doi:10.1111/mec.12817.

    PubMed  Google Scholar 

  • Foote, A. D., Kaschner, K., Schultze, S. E., Garilao, C., Ho, S. Y. W., Post, K., et al. (2013). Ancient DNA reveals that bowhead whale lineages survived late pleistocene climate change and habitat shifts. Nature Communications, 4, 1677.

    Article  PubMed  Google Scholar 

  • Galarza, J. A., Carreras-Carbonell, J., Macpherson, E., Pascual, M., Roques, S., Turner, G. F., et al. (2009). The influence of oceanographic fronts and early-life-history traits on connectivity among littoral fish species. Proceeding of the National Academy of Sciences USA, 106, 1473–1478.

    Article  CAS  Google Scholar 

  • Gaspari, S., Airoldi, S., & Hoelzel, A. R. (2007a). Risso’s dolphins (Grampus griseus) in UK waters are differentiated from a population in the Mediterranean Sea and genetically less diverse. Conservation Genetics, 8, 727–732.

    Article  Google Scholar 

  • Gaspari, S., Azzelino, A., Airoldi, S., & Hoelzel, A. R. (2007b). Social kin associations and genetic structuring of striped dolphin populations (Stenella coeruleoalba) in the Mediterranean Sea. Molecular Ecology, 16, 2922–2933.

    Article  PubMed  Google Scholar 

  • Gaspari, S., Holcer, D., Mackelworth, P., Fortuna, C., Frantzis, A., Genov, T., et al. (2013). Population genetic structure of common bottlenose dolphins (Tursiops truncatus) in the Adriatic Sea and contiguous regions: Implications for international conservation. Aquatic Conservation: Marine Freshwater Ecosystem. doi:10.1002/aqc.2415.

    Google Scholar 

  • Gayevskiy, V., Klaere, S., Knight, S., & Goddard, M. R. (2014). ObStruct: A method to objectively analyse factors driving population structure using Bayesian ancestry profiles. PLoS One, 9, e85196.

    Article  PubMed Central  PubMed  Google Scholar 

  • Genov, T., Kotnjek, P., Lesjak, J., Hace, A., & Fortuna, C. M. (2008). Bottlenose dolphins (Tursiops truncatus) in Slovenian and adjacent waters (northern Adriatic Sea). Annales Series Historia Naturalis, 18(2), 227–244.

    Google Scholar 

  • Gonzalez, R. J. (2011). The physiology of hyper-salinity tolerance in teleost fish: A review. Journal of Compatrative Physiology B, 182, 321–329.

    Article  Google Scholar 

  • Goudet, J. (2001). FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html

  • Hayes, A., Kucera, M., Kallel, N., Sbaffi, L., & Rohling, E. J. (2005). Glacial Mediterranean Sea surface temperatures based on planktonic foraminiferal assemblages. Quaternary Science Review, 24, 999–1016.

    Article  Google Scholar 

  • Hey, J., & Nielsen, R. (2007). Integration within the Felsenstein equation for improved Markov Chain Monte Carlo methods in population genetics. Proceeding of the national academy of sciences USA, 104, 2785–2790.

    Article  CAS  Google Scholar 

  • Ho, S. Y., & Lanfear, R. (2010). Improved characterisation of among-lineage rate variation in cetacean mitogenomes using codon-partitioned relaxed clocks. Mitochondrial DNA, 21, 138–146.

    Article  CAS  PubMed  Google Scholar 

  • Ho, S. Y., Phillips, M. J., Cooper, A., & Drummond, A. J. (2005). Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Molecular Biology and Evolution, 22, 1561–1568.

    Article  CAS  PubMed  Google Scholar 

  • Ho, S. Y., Saarma, U., Barnett, R., Haile, J., & Shapiro, B. (2008). The effect of inappropriate calibration: Three case studies in molecular ecology. PLoS One, 3, e1615.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hoelzel, A. R., Natoli, A., Dahlheim, M. E., Olavarria, C., Baird, R. W., & Black, N. A. (2002). Low worldwide genetic diversity in the killer whale (Orcinus orca): Implications for demographic history. Proceedingof the Royal Society of London B, 269, 1467–1473.

    Article  Google Scholar 

  • Hoelzel, A. R., Potter, C. W., & Best, P. B. (1998). Genetic differentiation between parapatric `nearshore’ and `offshore’ populations of the bottlenose dolphin. Proceedingof the Royal Society of London B, 265, 1177–1183.

    Article  CAS  Google Scholar 

  • Ingram, S. N., & Rogan, E. (2002). Identifying critical areas and habitat preferences of bottlenose dolphins Tursiops truncatus. Marine Ecology Progress Series, 244, 247–255.

    Article  Google Scholar 

  • Kiszka, J., Simon-Bouhet, B., Gastebois, C., Pusineri, C., & Ridoux, V. (2012). Habitat partitioning and fine scale population structure among insular bottlenose dolphins (Tursiops aduncus) in a tropical lagoon. Journal of Experimental Marine Biology and Ecology, 416–417, 176–184.

    Article  Google Scholar 

  • Louis, M., Fontaine, M. C., Spitz, J., Schlund, E., Dabin, W., Deaville, R., et al. (2014a). Ecological opportunities and specializations shaped genetic divergence in a highly mobile marine top predator. Proceedingof the Royal Society of London B, 281, 20141558.

    Article  Google Scholar 

  • Louis, M., Viricel, A., Lucas, T., Peltier, H., Alfonsi, E., Berrow, S., et al. (2014b). Habitat-driven population structure of bottlenose dolphins, Tursiops truncatus, in the North-East Atlantic. Molecular Ecology, 23, 857–874.

    Article  PubMed  Google Scholar 

  • Marino, I. A. M., Pujolar, J. M., & Zane, L. (2011). Reconciling deep calibration and demographic history: Bayesian inference of post glacial colonization patterns in Carcinus aestuarii (nardo, 1847) and C. Maenas (Linnaeus, 1758). PLoS One, 6, e28567.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martinho, F., Pereira, A., Brito, C., Gaspar, R., & Carvalho, I. (2014). Structure and abundance of bottlenose dolphins (Tursiops truncatus) in coastal Setúbal Bay, Portugal. Marine Biology Research. doi:10.1080/17451000.2014.894244.

    Google Scholar 

  • Mendez, M., Subramaniam, A., Collins, T., Minton, G., Baldwin, R., Berggren, P., et al. (2011). Molecular ecology meets remote sensing: Environmental drivers to population structure of humpback dolphins in the Western Indian Ocean. Heredity, 107, 349–361.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mikolajewicz, U. (2011). Modeling Mediterranean ocean climate of the Last Glacial Maximum. Climate of the Past, 7, 161–180.

    Article  Google Scholar 

  • Mirimin, L., Miller, R., Dillane, E., Berrow, S. D., Ingram, S., Cross, T. F., et al. (2011). Fine-scale population genetic structuring of bottlenose dolphins in Irish coastal waters. Animal Conservation, 14, 342–353.

    Article  Google Scholar 

  • Morris, R. W. (1960). Temperature, salinity, and southern limits of three species of Pacific cottid fishes. Limnology Oceanography, 5, 175–179.

    Article  Google Scholar 

  • Mossman, C. A., & Waser, P. M. (1999). Genetic detection of sex-biased dispersal. Molecular Ecology, 8, 1063–1067.

    Article  CAS  PubMed  Google Scholar 

  • Moura, A. E., Janse van Rensburg, C., Pilot, M., Tehrani, A., Best, P. B., Thornton, M., et al. (2014). Killer whale nuclear genome and mtDNA reveal widespread population bottleneck during the last glacial maximum. Molecular Biology and Evolution, 31, 1121–1131.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Moura, A. E., Kenny, J. G., Chaudhuri, R. R., Hughes, M. A., Reisinger, R. R., de Bruyn, P. J. N., et al. (2015). Phylogenomics of the killer whale indicates ecotype divergence in sympatry. Heredity, 114, 48–55.

    Article  CAS  PubMed  Google Scholar 

  • Moura, A. E., Natoli, A., Rogan, E., & Hoelzel, A. R. (2013a). Atypical panmixia in a European dolphin species (Delphinus delphis): Implications for the evolution of diversity across oceanic boundaries. Journal of Evolutionary Biology, 26, 63–75.

    Article  CAS  PubMed  Google Scholar 

  • Moura, A. E., Nielsen, S. C. A., Vilstrup, J. T., Moreno-Mayar, J. V., Gilbert, M. T. P., Gray, H., et al. (2013b). Recent diversification of a marine genus (Tursiops spp.) tracks habitat preference and environmental change. Systematic Biology, 62, 865–877.

    Article  PubMed  Google Scholar 

  • Naciri, M., Lemaire, C., Borsa, P., & Bonhomme, F. (1999). Genetic study of the Atlantic/Mediterranean transition in sea bass (Dicentrarchus labrax). Journal of Heredity, 90, 591–596.

    Article  Google Scholar 

  • Natoli, A., Birkun, A., Aguilar, A., Lopez, A., & Hoelzel, A. R. (2005). Habitat structure and the dispersal of male and female bottlenose dolphins (Tursiops truncatus). Proceeding of the Royal Society of London B, 272, 1217–1226.

    Article  CAS  Google Scholar 

  • Natoli, A., Cañadas, A., Vaquero, C., Politi, E., Fernandez-Navarro, P., & Hoelzel, A. R. (2008). Conservation genetics of the short-beaked common dolphin (Delphinus delphis) in the Mediterranean Sea and in the Eastern North Atlantic Ocean. Conservation Genetics, 9, 1479–1487.

    Article  Google Scholar 

  • Natoli, A., Peddemors, V. M., & Hoelzel, A. R. (2004). Population structure and speciation in the genus Tursiops based on microsatellite and mitochondrial DNA analyses. Journal of Evolutionary Biology, 17, 363–375.

    Article  CAS  PubMed  Google Scholar 

  • Nichols, C., Herman, J., Gaggiotti, O. E., Dobney, K. M., Parsons, K., & Hoelzel, A. R. (2007). Genetic isolation of a now extinct population of bottlenose dolphins (Tursiops truncatus). Proceedingof the Royal Society of London B, 274, 1611–1616.

    Article  CAS  Google Scholar 

  • Norris, R. D. (2000). Pelagic species diversity, biogeography, and evolution. Paleobiology, 26, 236–258.

    Article  Google Scholar 

  • Oremus, M., Poole, M. M., Steel, D., & Baker, C. S. (2007). Isolation and interchange among insular spinner dolphin communities in the South Pacific revealed by individual identification and genetic diversity. Marine Ecology Progress Seriess, 336, 275–289.

    Article  CAS  Google Scholar 

  • Park, S. D. E. (2008). Excel microsatellite toolkit. Computer program and documentation distributed by the author. http://animalgenomics.ucd.ie/sdepark/ms-toolkit/. Accessed June 2013.

  • Parsons, K. M., Noble, L. R., Reid, R. J., & Thompson, P. M. (2002). Mitochondrial genetic diversity and population structuring of UK bottlenose dolphins (Tursiops truncatus): Is the NE Scotland population demographically and geographically isolated? Biology Conservation, 108, 175–182.

    Article  Google Scholar 

  • Patarnello, T., Volckaert, F. A., & Castilho, R. (2007). Pillars of Hercules: Is the Atlantic-Mediterranean transition a phylogeographical break? Molecular Ecology, 16, 4426–4444.

    Article  PubMed  Google Scholar 

  • Peakall, R. O. D., & Smouse, P. E. (2006). Genalex 6: Genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288–295.

    Article  Google Scholar 

  • Peery, M. Z., Kirby, R., Reid, B. N., Stoelting, R., Doucet-Bëer, E., Robinson, S., et al. (2012). Reliability of genetic bottleneck tests for detecting recent population declines. Molecular Ecology, 21, 3403–3418.

    Article  PubMed  Google Scholar 

  • Perez-Losada, M., Nolte, M. J., Crandall, K. A., & Shaw, P. W. (2007). Testing hypotheses of population structuring in the Northeast Atlantic Ocean and Mediterranean Sea using the common cuttlefish Sepia officinalis. Molecular Ecology, 16, 2667–2679.

    Article  PubMed  Google Scholar 

  • Perez-Portela, R., & Turon, X. (2008). Cryptic divergence and strong population structure in the colonial invertebrate Pycnoclavella communis (Ascidiacea) inferred from molecular data. Zoology, 111, 163–178.

    Article  PubMed  Google Scholar 

  • Pleslić, G., Rako, N., Mackelworth, P., Wiemann, A., Holcer, D., & Fortuna, C. (2013). The abundance of common bottlenose dolphins (Tursiops truncatus) in the former marine protected area of the Cres-Lošinj archipelago, Croatia. Aquatic Conservation: Marine Freshwater Ecosystem. doi:10.1002/aqc.2416.

    Google Scholar 

  • Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pujolar, J. M., Marčeta, T., Saavedra, C., Bressan, M., & Zane, L. (2010). Inferring the demographic history of the Adriatic Flexopecten complex. Molecular Phylogenetics and Evolution, 57, 942–947.

    Article  CAS  PubMed  Google Scholar 

  • Pujolar, J. M., Zane, L., & Congiu, L. (2012). Phylogenetic relationships and demographic histories of the Atherinidae in the Eastern Atlantic and Mediterranean Sea re-examined by Bayesian inference. Molecular Phylogenetics and Evolution, 63, 857–865.

    Article  CAS  PubMed  Google Scholar 

  • Quérouil, S., Silva, M. A., Freitas, L., Prieto, R., Magalhães, S., Dinis, A., et al. (2007). High gene flow in oceanic bottlenose dolphins (Tursiops truncatus) of the North Atlantic. Conservation Genetics, 8, 1405–1419.

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Rolland, J. L., Bonhomme, F., Lagardère, F., Hassan, M., & Guinand, B. (2006). Population structure of the common sole (Solea solea) in the Northeastern Atlantic and the Mediterranean Sea: Revisiting the divide with epic markers. Marine Biology, 151, 327–341.

    Article  Google Scholar 

  • Rosel, P. E., Forgetta, V., & Dewar, K. (2005). Isolation and characterization of twelve polymorphic microsatellite markers in bottlenose dolphins (Tursiops truncatus). Molecular Ecology Notes, 5, 830–833.

    Article  CAS  Google Scholar 

  • Rosel, P. E., Hansen, L., & Hohn, A. A. (2009). Restricted dispersal in a continuously distributed marine species: Common bottlenose dolphins Tursiops truncatus in coastal waters of the western North Atlantic. Molecular Ecology, 18, 5030–5045.

    Article  CAS  PubMed  Google Scholar 

  • Segura, I., Rocha-Olivares, A., Flores-Ramírez, S., & Rojas-Bracho, L. (2006). Conservation implications of the genetic and ecological distinction of Tursiops truncatus ecotypes in the Gulf of California. Biological Conservation, 133, 336–346.

    Article  Google Scholar 

  • Sharir, Y., Kerem, D., Goldin, P., & Spanier, E. (2011). Small size in the common bottlenose dolphin Tursiops truncatus in the Eastern Mediterranean: A possible case of Levantine nanism. Marine Ecology Progress Seriess, 438, 241–251.

    Article  Google Scholar 

  • Shinohara, M., Domingo-Roura, X., & Takenaka, O. (1997). Microsatellites in the bottlenose dolphin Tusiops truncatus. Molecular Ecology, 6, 695–696.

    Article  CAS  PubMed  Google Scholar 

  • Spitz, J., Trites, A. W., Becquet, V., Brind’Amour, A., Cherel, Y., Galois, R., et al. (2012). Cost of living dictates what whales, dolphins and porpoises eat: The importance of prey quality on predator foraging strategies. PLoS One, 7, e50096.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stoneking, M. (2000). Hypervariable sites in the mtDNA control region are mutational hotspots. The American Journal of Human Genetics, 67, 1029–1032.

    Article  CAS  Google Scholar 

  • Sušnik, S., Snoj, A., Wilson, I. F., Mrdak, D., & Weiss, S. (2007). Historical demography of brown trout (Salmo trutta) in the Adriatic drainage including the putative S. letnica endemic to lake Ohrid. Molecular Phylogenetics and Evolution, 44, 63–76.

    Article  PubMed  Google Scholar 

  • Tezanos-Pinto, G., Baker, C. S., Russell, K., Martien, K., Baird, R. W., Hutt, A., et al. (2008). A worldwide perspective on the population structure and genetic diversity of bottlenose dolphins (Tursiops truncatus) in New Zealand. Journal of Heredity, 100, 11–24.

    Article  PubMed  Google Scholar 

  • Thiede, J. (1978). A glacial Mediterranean. Nature, 276, 680–683.

    Article  Google Scholar 

  • Torres, L. G., Rosel, P. E., D’Agrosa, C., & Read, A. J. (2003). Improving management of overlapping bottlenose dolphin ecotypes through spatial analysis and genetics. Marine Mammal Science, 19, 502–514.

    Article  Google Scholar 

  • Valsecchi, E., & Amos, W. (1996). Microsatellite markers for the study of cetacean populations. Molecular Ecology, 5, 151–156.

    Article  CAS  PubMed  Google Scholar 

  • Williams, T. M., Haun, J., Davis, R. W., Fuiman, L. A., & Kohin, S. (2001). A killer appetite: Metabolic consequences of carnivory in marine mammals. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 129, 785–796.

    Article  CAS  Google Scholar 

  • Wilson, G. A., & Rannala, B. (2003). Bayesian inference of recent migration rates using multilocus genotypes. Genetics, 163, 1177–1191.

    PubMed Central  PubMed  Google Scholar 

  • Zulliger, D. E., Tanner, S., Ruch, M., & Ribi, G. (2009). Genetic structure of the high dispersal Atlanto-Mediterreanean sea star Astropecten aranciacus revealed by mitochondrial DNA sequences and microsatellite loci. Marine Biology, 156, 597–610.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was funded by the Italian DG Fishery within the research framework of the Italian obligations to the Council Regulation (EC) n. 812/2004 (BYCATCH programme). The authors acknowledge the people that have provided samples: Israeli Marine Mammal Research and Assistance Center (IMMRAC, Dan Karem); Blue World Institute, Croatia, Marine Mammals Tissue Bank, University of Padoa, Italy (Bruno Cozzi, Maristella Giurisato); Università degli Studi di Siena, Italy (Letizia Marsili); Morigenos, Slovenia A.R.C.H.E. Porto Garibaldi, Italy (Carola Vallini); Fondazione Cetacea, Italy (Marco Affronte); Tethys Research Institute, Italy (Ada Natoli); Capitaneria di Porto di Brindisi, Italy (Paola Pino d’Astore). We would also like to thank the researchers and volunteers of IMMRAC, Israel.

Author information

Authors and Affiliations

  1. Department of Biology, University of Florence, Florence, Italy

    Stefania Gaspari, Chiara Natali & Guido Chelazzi

  2. The Leon Recanati Institute for Maritime Studies and the Department of Maritime Civilizations, The Leon H. Charney School for Marine Sciences, University of Haifa, Haifa, Israel

    Aviad Scheinin

  3. IMMRAC (Israel Marine Mammal Research and Assistance Center), Michmoret, Israel

    Aviad Scheinin

  4. Department of Zoology, Croatian Natural History Museum, Demetrova 1, Zagreb, Croatia

    Draško Holcer

  5. Blue World Institute of Marine Research and Conservation, Kaštel 24, Veli Lošinj, Croatia

    Draško Holcer

  6. Italian National Institute for Environmental Protection and Research, Rome, Italy

    Caterina Fortuna

  7. Morigenos, Slovenian Marine Mammal Society, Piran, Slovenia

    Tilen Genov

  8. Institute for Biodiversity Studies, Science and Research Centre, University of Primorska, Koper, Slovenia

    Tilen Genov

  9. Pelagos Cetacean Research Institute, Vouliagmeni, Greece

    Alexandros Frantzis

  10. School of Life Sciences, University of Lincoln, Lincoln, UK

    André E. Moura

Authors
  1. Stefania Gaspari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aviad Scheinin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Draško Holcer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Caterina Fortuna
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chiara Natali
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tilen Genov
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alexandros Frantzis
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Guido Chelazzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. André E. Moura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to André E. Moura.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 614 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gaspari, S., Scheinin, A., Holcer, D. et al. Drivers of Population Structure of the Bottlenose Dolphin (Tursiops truncatus) in the Eastern Mediterranean Sea. Evol Biol 42, 177–190 (2015). https://doi.org/10.1007/s11692-015-9309-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-015-9309-8

Keywords

Search

Navigation