Skip to main content
Log in

Genetic diversity and biogeographical patterns of Caulerpa prolifera across the Mediterranean and Mediterranean/Atlantic transition zone

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Knowledge of spatial patterns of genetic differentiation between populations is key to understanding processes in evolutionary history of biological species. Caulerpa is a genus of marine green algae, which has attracted much public attention, mainly because of the impacts of invasive species in the Mediterranean. However, very little is known about the ecological and evolutionary history of the Mediterranean native Caulerpa prolifera, a species which is currently found at sites distributed worldwide. C. prolifera provides a good model to explore the patterns of genetic diversity at different scales across the Mediterranean and Atlantic area. This study aims to investigate the biogeographical patterns of diversity and differentiation of C. prolifera in the Mediterranean, with special focus on the Mediterranean/Atlantic transition zone. We used two nuclear (ITS rDNA and the hypervariable microsatellite locus CaPr_J2) and one chloroplast (tufA) DNA markers on samples of C. prolifera from its entire range. Analyses of 51 sequences of the cpDNA tufA of C. prolifera, 87 ITS2 sequences and genotypes of 788 ramets of C. prolifera for the locus CaPr_J2 revealed three different biogeographical areas: West Atlantic, East Atlantic and a larger area representing the Mediterranean, the Mediterranean/Atlantic transition zone and a Pacific site (Bali). It was found out that the Mediterranean/Atlantic transition zone is a biogeographical boundary for C. prolifera. A lack of connectivity was revealed between Atlantic and Mediterranean types, and identical sequences found in the Mediterranean and Indo-Pacific suggest either recent gene flow along the Red Sea connection or a possible ancient Indo-Pacific origin.

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

Access this article

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

  • Aguirre J, Perez-Munoz AB, Sanchez-Almazo I (2006) Benthic foraminifera assemblages on the lower. Pliocene deposits of the Almeria-Nijar Basin (SE Spain). Rev Esp Micropaleontol 38(2–3):411–428

    Google Scholar 

  • Alberto F, Massa S, Manent P, Diaz-Almela E, Arnaud-Haond S, Duarte CM, Serrão EA (2008) Genetic differentiation and secondary contact zone in the seagrass Cymodocea nodosa across the Mediterranean–Atlantic transition region. J Biogeogr 35:1270–1294

    Article  Google Scholar 

  • Almada VC, Oliveira RF, Gonçalves EJ, Almeida AJ, Santos RS, Wirtz P (2001) Patterns of diversity of the north-eastern Atlantic blenniid fish fauna (Pisces: Blenniidae). Glob Ecol Biogeogr 10:411–422

    Article  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Baus E, Darrock DJ, Bruford MW (2005) Gene-flow patterns in Atlantic and Mediterranean populations of the Lusitanian Sea star Asterina gibbosa. Mol Ecol 14:3373–3382

    Article  CAS  Google Scholar 

  • Belton GS, Prud’homme van Reine W, Huisman JM, Draisma GA, Gurgel FD (2013) Resolving phenotypic plasticity and species designation in the morphologically challenging Caulerpa racemosapeltata complex (Chlorophyta, Caulerpaceae). J Phycol 50:32–54. doi:10.1111/jpy.12132

    Article  Google Scholar 

  • Benzie JAH, Price IR, Ballment E (1997) Population genetics and taxonomy of Caulerpa (Chlorophyta) from the Great Barrier Reef, Australia. J Phycol 33:491–504

    Article  Google Scholar 

  • Bryden HL, Candela J, Kinder TH (1994) Exchange through the Strait of Gibraltar. Prog Oceanogr 33:201–248

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  Google Scholar 

  • Cunha AH, Varela-Álvarez E, Paulo DS, Sousa I, Serrão EA (2013) The rediscovery of Caulerpa prolifera in Ria Formosa, Portugal, 60 years after being undetected. Cah Biol Mar 54:359–364

    Google Scholar 

  • Domingues VS, Bucciarelli G, Almada VC, Bernardi G (2005) Historical colonization and demography of the Mediterranean damselfish, Chromis chromis. Mol Ecol 14:4051–4063

    Article  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Duran S, Pascual M, Estoup A, Turon X (2004) Strong population structure in the marine sponge Crambe crambe (Poecilosclerida) as revealed by microsatellite markers. Mol Ecol 13:511–522

    Article  CAS  Google Scholar 

  • Durand C, Manuel M, Boudouresque CF, Meinesz A, Verlaque M, Le Parco Y (2002) Molecular data suggest a hybrid origin for the invasive Caulerpa racemosa (Caulerpales, Chlorophyta) in the Mediterranean Sea. J Evol Biol 15:122–133

    Article  CAS  Google Scholar 

  • Famà P, Olsen JL, Stam WT, Procaccini G (2000) High levels of intra- and inter-individual polymorphism in the rDNA ITS1 of Caulerpa racemosa (Chlorophyta). Eur J Phycol 35:349–356

    Article  Google Scholar 

  • Famà P, Wysor B, Kooistra WHCF, Zuccarello GC (2002) Molecular phylogeny of the genus Caulerpa (Caulerpales, Chlorophyta) inferred from chloroplast tufA gene. J Phycol 38:1040–1050

    Article  Google Scholar 

  • Fuertes Aguilar J, Rossello JA, Nieto Feliner G (1999) Molecular evidence for the compilospecies model of reticulate evolution in Armeria (Plumbaginaceae). Syst Biol 48:735–775

    Article  CAS  Google Scholar 

  • Galil BS (2009) Taking stock: inventory of alien species in the Mediterranean Sea. Biol Invasions 11:359–372

    Article  Google Scholar 

  • Galtier N, Gouy M, Gautier C (1996) SeaView and Phylo_win, two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548

    CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  Google Scholar 

  • Guiry MD, Guiry GM (2014) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org. Accessed 05 Nov 2014

  • Hrbek T, Meyer A (2003) Closing of the Tethys Sea and the phylogeny of Eurasian killifishes (Cyprinodontiformes: Cyprinodontidae). J Evol Biol 16(1):17–36

    Article  CAS  Google Scholar 

  • Jongma D, Campo D, Dattolo E, D’Esposito D, Duchi D, Grewe P, Huisman J, Verlaque M, Yokes M, Procaccini G (2013) Identity and origin of a slender Caulerpa taxifolia strain introduced into the Mediterranean Sea. Bot Mar 56(1):27–39

    Article  Google Scholar 

  • Jousson O, Pawlowski J, Zaninetti L, Meinesz A, Boudouresque CF (1998) Molecular evidence for the aquariologic origin of the green alga Caulerpa taxifolia invading the Mediterranean Sea. Mar Ecol Prog Ser 172:275–280

    Article  Google Scholar 

  • Jousson O, Pawlowski J, Zaninetti L, Zechman FW, Dini F, Di Guiseppe G, Woodfield R, Millar A, Meinesz A (2000) Invasive alga reaches California. Nature 408:9

    Article  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  Google Scholar 

  • Lehman R, Manhart JR (1997) A preliminary comparison of restriction fragment patterns in the genus Caulerpa (Chlorophyta) and the unique structure of the chloroplast genome of Caulerpa sertularioides. J Phycol 33:1055–1062

    Article  CAS  Google Scholar 

  • Lowe CD, Martin LE, Montagnesa DJS, Watts PC (2012) A legacy of contrasting spatial genetic structure on either side of the Atlantic–Mediterranean transition zone in a marine protest. Proc Natl Acad Sci USA 109(51):20998–21003

    Article  CAS  Google Scholar 

  • Masucci AP, Arnaud-Haond S, Eguiluz VM, Hernandez-Garcia E, Serrao EA (2012) Genetic flow directionality and geographical segregation in a Cymodocea nodosa genetic diversity network. EPJ Data Sci 1:11

    Article  Google Scholar 

  • Matschiner M, Salzburger W (2009) TANDEM: integrating automated allele binning into genetics and genomics workflows. Bioinformatics 25:1982–1983

    Article  CAS  Google Scholar 

  • Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794

    Article  Google Scholar 

  • Meusnier I, Olsen JL, Stam WT, Destombe C, Valero M (2001) Phylogenetic analyses of Caulerpa taxifolia (Chlorophyta) and of its associated bacterial microflora provide clues to the origin of the Mediterranean introduction. Mol Ecol 10(4):931–946

    Article  CAS  Google Scholar 

  • Meusnier I, Valero M, Destombe C, Godé C, Desmarais E, Stam WT, Olsen JL (2002) Polymerase chain reaction-single strand conformation polymorphism analyses of nuclear and chloroplast DNA provide evidence for recombination, multiple introductions and nascent speciation in the Caulerpa taxifolia complex. Mol Ecol 11:2317–2325

    Article  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Parilla G, Kinder TH (1992) The physical oceanography of the Alborán Sea. Rep Meteorol Oceanogr 40:143–184

    Google Scholar 

  • Patarnello T, Filipa AM, Volckaert MJ, Castilho R (2007) Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographical break? Mol Ecol 16:4426–4444

    Article  Google Scholar 

  • Pérès JM (1967) The Mediterranean benthos. Oceanogr Mar Biol Annu Rev 5:449–553

    Google Scholar 

  • Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14:689–701

    Article  CAS  Google Scholar 

  • Por FD (2009) Tethys returns to the Mediterranean: success and limits of tropical re-colonization. In: Krupp F, Musselman JL, Kotb MMA, Weidig I (eds) Environment, biodiversity and conservation in the Middle East. Proceedings of the first middle eastern biodiversity congress, Aqaba, Jordan, 20–23 October 2008. BioRisk 3:5–19. doi:10.3897/biorisk.3.30

  • Posada D, Crandall KA (1998) Model test testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  Google Scholar 

  • Quijada A, Liston A, Robinson W, Alvarez-Buylla E (1997) The ribosomal ITS region as a marker to detect hybridization in pines. Mol Ecol 6:995–996

    Article  CAS  Google Scholar 

  • Sauvage T, Payri CE, Draisma SGA, Prud’homme van Reine WF, Verbruggen H, Belton GS, Gurgel CFD, Gabriel D, Sherwood AR, Fredericq S (2013) Molecular diversity of the Caulerpa racemosaCaulerpa peltata complex (Caulerpaceae, Bryopsidales) in New Caledonia, with new Australasian records for C. racemosa var. cylindracea. Phycologia 52:6–13

    Article  Google Scholar 

  • Schaal BA, Hayworth DA, Olsen KM, Rauscher JT, Smith WA (1998) Phylogeographic studies in plants: problems and prospects. Mol Ecol 7:465–474

    Article  Google Scholar 

  • Schaffelke B, Murphy N, Uthicke S (2002) Using genetic techniques to investigate the sources of the invasive alga Caulerpa taxifolia in three new locations in Australia. Mar Pollut Bull 44:204–221

    Article  CAS  Google Scholar 

  • Stam WF, Olsen JL, Zaleski SF, Murray SN, Brown KR, Walters LW (2006) A forensic and phylogenetic survey of Caulerpa species (Caulerpales, chlorophyta) from the Florida Coast, local aquarium shops, and E-commerce: establishing a proactive baseline for early detection. J Phycol 42:113–1124

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  Google Scholar 

  • Tintore J, Violette PE, Blade I, Cruzado A (1988) A study of an intense density front in the eastern Alboran sea: the Almeria–Oran front. J Phys Oceanogr 18:1384–1397

    Article  Google Scholar 

  • Varela-Álvarez E, Glenn TC, Serrão EA, Duarte CM, Martínez-Daranas B, Valero M, Marba N (2011) Dinucleotide microsatellite markers in the genus Caulerpa. J Appl Phycol 23:715–719

    Article  Google Scholar 

  • Varela-Álvarez E, Gómez Garreta A, Rull Lluch J, Salvador Soler N, Serrao EA, Ribera Siguan MA (2012) Mediterranean species of Caulerpa are polyploid with smaller genomes in the invasive ones. PLoS ONE 7(10):e47728

    Article  Google Scholar 

  • Verlaque M, Durand C, Huisman JM, Boudouresque CF, Le Parco Y (2003) On the identity and origin of the Mediterranean invasive Caulerpa racemosa (Caulerpales, Chlorophyta). Eur J Phycol 38:325–339

    Article  Google Scholar 

  • Voisin M, Engel CR, Viard F (2005) Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture versus maritime traffic effects. Proc Natl Acad Sci USA 102:5432–5437

    Article  CAS  Google Scholar 

  • White T, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T (eds) PCR-protocols a guide to methods and applications. Academic press, Orlando, Florida, pp 315–322

    Chapter  Google Scholar 

  • Zuljevic A, Antolic B, Nikolic V, Despalatovic M, Cvitkovic I (2012) Absence of successful sexual reproduction of Caulerpa racemosa var. cylindracea in the Adriatic Sea. Phycologia 51:283–286

    Article  Google Scholar 

Download references

Acknowledgments

We thank all the people and Institutions that collected plants and/or helped with the sampling collection: Liam Cronin, Ligia Collado-Vides, Gísela Dionisio, Elvira Álvarez, Rocío Santiago, Elena Díaz-Almela, Ricardo Bermejo, Fernando Ojeda Copete, Alexandra Cunha, Pablo Manent, Estibaliz Berecibar, Antonia Ribera-Siguan, Carolina Peña-Martín, Pablo Sanchez Jerez, Felio Lozano, Jacinto Barquín and Francisco Valdés; Natural Park of s’Albufera des Grau (Government of the Balearic Islands: http://www.balearsnatura.com/parc-natural-de-s-albufera-des-grau/equipamiento.html) and the Marine Reserve of Tabarca (Alicante). We also thank for the sequencing work Marta Valente and Cristina Paulino. Financial support for this study was provided by several research projects: CAULERPA_GENETICS (PTDC/MAR/70921/2006) by FCT (Portuguese Science Foundation) co-funded by FEDER and a postdoctoral fellowship (SFRH/BPD/17206/2004) from FCT, Portugal, co-funded by FSE, both to EVA, EXCL/AAG-GLO/0661/2012 to ES, CAULEXPAN (Spanish Ministry of Education, REN2002-00701) to NM, MedVeg (EU contract no. Q5RS-2001-02456), PRADERAS by the Foundation BBVA (Banco Bilbao Vizcaya Argentaria) to CD.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elena Varela-Álvarez.

Additional information

Communicated by T. Reusch.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Varela-Álvarez, E., Balau, A.C., Marbà, N. et al. Genetic diversity and biogeographical patterns of Caulerpa prolifera across the Mediterranean and Mediterranean/Atlantic transition zone. Mar Biol 162, 557–569 (2015). https://doi.org/10.1007/s00227-014-2605-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-014-2605-5

Keywords

Navigation