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Genetic differentiation between Mediterranean and Atlantic populations of the common prawn Palaemon serratus (Crustacea: Palaemonidae) reveals uncommon phylogeographic break

Published online by Cambridge University Press:  08 June 2017

Ronja Weiss ,
Zeltia Torrecilla ,
Enrique González-Ortegón ,
Ana M. González-Tizón ,
Andrés Martínez-Lage  and
Christoph D. Schubart
Ronja Weiss
Affiliation:
Zoologie & Evolutionsbiologie, Universität Regensburg, D-93040 Regensburg, Germany
Zeltia Torrecilla
Affiliation:
El Departamento de Biología Celular y Molecular, CICA, Universidade da Coruña, E-15008 A Coruña, Spain
Enrique González-Ortegón
Affiliation:
Instituto Español de Oceanografía, Centro Oceanográfico de Cádiz, Puerto Pesquero, Muelle de Levante s/n, E-11006 Cádiz, Spain Instituto de Ciencias Marinas de Andalucía (CSIC), Campus Universitario Río San Pedro, 11519 Puerto Real, Cádiz, Spain
Ana M. González-Tizón
Affiliation:
El Departamento de Biología Celular y Molecular, CICA, Universidade da Coruña, E-15008 A Coruña, Spain
Andrés Martínez-Lage
Affiliation:
El Departamento de Biología Celular y Molecular, CICA, Universidade da Coruña, E-15008 A Coruña, Spain
Christoph D. Schubart*
Affiliation:
Zoologie & Evolutionsbiologie, Universität Regensburg, D-93040 Regensburg, Germany
*
Correspondence should be addressed to: C. D. Schubart, Zoologie & Evolutionsbiologie, Universität Regensburg, D-93040 Regensburg, Germany. email: [email protected]
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Abstract

The Atlantic–Mediterranean transition zone between the Alborán Sea and the Gulf of Cádiz constitutes the most prominent marine geographic barrier in European waters and includes known phylogeographic breaks such as the Strait of Gibraltar and the Almería-Oran Front. A genetic shift in this area has been previously documented for the European littoral shrimp Palaemon elegans. Here we carried out a phylogeographic analysis with the congeneric and sympatric species Palaemon serratus to test for similar intraspecific genetic differentiation and geographic structure. This littoral prawn is distributed in the Northeastern Atlantic Ocean, the Mediterranean Sea and the Black Sea. We compared DNA sequences from the mitochondrial genes Cox1 and to a lesser extent from 16S rRNA of several Atlantic and Mediterranean populations. Furthermore, sequences from the nuclear gene Enolase were included for corroborating differences between Mediterranean and Atlantic individuals. A pronounced genetic differentiation was detected between the Mediterranean and Atlantic populations, amounting to 10.14% in Cox1 and 2.0% in 16S, indicating the occurrence of two independent evolutionary lineages. Interestingly, specimens from the Atlantic Gulf of Cadiz cluster together with the Mediterranean individuals, indicating that a biogeographic barrier appears to be located west of the Strait of Gibraltar.

Keywords

Decapoda CarideaMediterranean SeaAtlantic OceanGulf of CadizphylogeographymtDNA Cox1
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 6 , September 2018 , pp. 1425 - 1434
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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References

REFERENCES

Ashelby, A.C.W., De Grave, S. and Johnson, M.L. (2013) The global invader Palaemon macrodactylus (Decapoda, Palaemonidae): an interrogation of records and a synthesis of data. Crustaceana 86, 594–624.Google Scholar
Belfiore, N.M., Hoffmann, F.G., Baker, R.J. and Dewoody, J.A. (2003) The use of nuclear and mitochondrial single nucleotide polymorphisms to identify cryptic species. Molecular Ecology 12, 2011–2017.Google Scholar
Bilgin, R., Utkan, M.A., Kalkan, E., Karhan, S.Ü. and Bekbolet, M. (2014) DNA barcoding of twelve shrimp species (Crustacea: Decapoda) from Turkish seas reveals cryptic diversity. Mediterranean Marine Science 16, 36–45.Google Scholar
Carlisle, D.B. (1955) Local variations in the colour pattern of the prawn Leander serratus (Pennant). Journal of the Marine Biological Association of the United Kingdom 34, 559–563.Google Scholar
Cartaxana, A. (2015) Morphometric and molecular analyses for populations of Palaemon longirostris and Palaemon garciacidi (Crustacea, Palaemonidae): evidence for a single species. Estuarine Coastal Shelf Science 154, 194–204.Google Scholar
Carvalho, F., De Grave, S. and Mantelatto, F.L. (2016) An integrative approach to the evolution of shrimps of the genus Palaemon (Decapoda, Palaemonidae). Zoologica Scripta. doi: 10.1111/zsc.12228.Google Scholar
Clement, M., Posada, D. and Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1660.Google Scholar
Costa, F.O., de Waard, J.R., Boutillier, J., Ratnasingham, S., Dooh, R.T., Hajibabaei, M. and Hebert, P.D.N. (2007) Biological identifications through DNA barcodes: the case of the Crustacea. Canadian Journal of Fisheries and Aquatic Science 64, 272–295.Google Scholar
Crandall, K.A. and Fitzpatrick, J.E. (1996) Crayfish molecular systematic: using a combination of procedures to estimate phylogeny. Systematic Biology 45, 1–26.Google Scholar
Cuesta, J.A., Drake, P., Martínez-Rodríguez, G., Rodríguez, A. and Schubart, C.D. (2012) Molecular phylogeny of the genera Palaemon and Palaemonetes (Decapoda, Caridea, Palaemonidae) from a European perspective. Crustaceana 85, 877–888.Google Scholar
De Grave, S. and Ashelby, A.C.W. (2013) A re-appraisal of the systematic status of selected genera in Palaemoninae (Crustacea: Decapoda: Palaemonidae). Zootaxa 3734, 331–344.Google Scholar
Deli, T., Fratini, S., Ragionieri, L., Said, K., Chatti, N. and Schubart, C.D. (2016) Phylogeography of the marbled crab Pachygrapsus marmoratus (Decapoda, Grapsidae) along part of the African Mediterranean coast reveals genetic homogeneity across the Siculo-Tunisian Strait versus heterogeneity across the Gibraltar Strait. Marine Biology Research 12, 5, 471–487. doi: 10.1080/17451000.2016.Google Scholar
De Man, J.G. (1915) On some European species of the genus Leander Desm., also a contribution to the fauna of Dutch waters. Tijdschrift van de Nederlandse Dierkunde Vereniging 2, 115–179.Google Scholar
d'Udekem d'Acoz, C. (1999) Inventaire et distribution des crustacés décapodes de l'Atlantique nord-oriental, de la Méditerranée et des eaux continentales adjacentes au nord de 25 N. Collection patrimoines naturels 40, 1–383.Google Scholar
Fahy, E., Forrest, N., O'Toole, M., Mortimer, R. and Carroll, J. (2006) Indicators of performance in the fishery for shrimp Palaemon serratus (Pennant) in Irish coastal waters. Journal of Shellfish Research 25, 1021–1026.Google Scholar
Fratini, S., Ragionieri, L., Deli, T., Harrer, A., Marino, I.A.M., Cannicci, S., Zane, L. and Schubart, C.D. (2016) Unravelling population genetic structure with mitochondrial DNA in a notional panmictic coastal crab species: sample size makes the difference. BMC Evolutionary Biology 16, 150. doi: 10.1186/s12862-016-0720-2.Google Scholar
Galarza, J.A., Carreras-Carbonell, J., Macpherson, E., Pascual, M., Roques, S., Turner, G.F. and Rico, C. (2009) The influence of oceanographic fronts and early-life-history traits on connectivity among littoral fish species. Proceedings of the National Academy of Sciences USA 106, 1473–1478.Google Scholar
García-Castellanos, D., Estrada, F., Jiménez-Munt, I., Gorini, C., Fernàndez, M., Vergés, J. and De Vicente, R. (2009) Catastrophic flood of the Mediterranean after the Messinian salinity crisis. Nature 462, 778–781.Google Scholar
García-Merchán, V.H., Robainas-Barcia, A., Abelló, P., Macpherson, E., Palero, F., García-Rodríguez, M., Gil de Sola, L. and Pascual, M. (2012) Phylogeographic patterns of decapod crustaceans at the Atlantic–Mediterranean transition. Molecular Phylogenetics and Evolution 62, 664–672.Google Scholar
Geller, J.B., Walton, E.D., Grosholz, E.D. and Ruiz, G.M. (1997) Cryptic invasions of the crab Carcinus detected by molecular phylogeography. Molecular Ecology 6, 901–906.Google Scholar
González-Ortegón, E. and Cuesta, J.A. (2006) An illustrated key to species of Palaemon and Palaemonetes (Crustacea: Decapoda: Caridea) from European waters, including the alien species Palaemon macrodactylus. Journal of the Marine Biological Association of the United Kingdom 86, 93–102.Google Scholar
González-Ortegón, E., Cuesta, J.A. and Schubart, C.D. (2007) First report of the oriental shrimp Palaemon macrodactylus Rathbun, 1902 (Decapoda, Caridea, Palaemonidae) from German waters. Helgoland Marine Research 61, 67–69.Google Scholar
González-Ortegón, E., Baldó, F., Arias, A., Cuesta, J.A., Fernández-Delgado, C., Vilas, C. and Drake, P. (2015) Freshwater scarcity effects on the aquatic macrofauna of a European Mediterranean-climate estuary. Science of the Total Environment 503–504, 213–221.Google Scholar
González-Ortegón, E. and Giménez, L. (2014) Environmentally mediated phenotypic links and performance in larvae of a marine invertebrate. Marine Ecology Progress Series 502, 185–195.Google Scholar
González-Ortegón, E., Palero, F., Lejeusne, C., Drake, P. and Cuesta, J.A. (2016) A salt bath will keep you going? Euryhalinity tests and genetic structure of caridean shrimps from Iberian rivers. Science of the Total Environment 540, 11–19.Google Scholar
Haig, J., Ryan, N.M., Williams, K.F. and Kaiser, M.J. (2014) A review of the Palaemon serratus fishery: biology, ecology and management. Fisheries and Conservation Report. Bangor: Bangor University, 38 pp.Google Scholar
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
Hofrichter, A.A. (2002) Das Mittelmeer – Fauna, Flora, Ökologie Band I. Heidelberg: Spektrum Akademischer Verlag.Google Scholar
Hsü, K.J., Montadert, L., Bernoulli, D., Cita, M.B., Erickson, A., Garrison, R.E., Kidd, R.B., Mèlierés, F., Müller, C. and Wright, R. (1977) History of the Mediterranean salinity crisis. Nature 267, 399–403.Google Scholar
Ip, B.H.Y., Schubart, C.D., Tsang, L.M. and Chu, K.H. (2015) Phylogeny of the shore crab family Grapsidae (Decapoda: Brachyura: Thoracotremata) based on a multilocus approach. Zoological Journal of the Linnean Society 174, 217–227.Google Scholar
Kingman, J.F.C. (1982) On the genealogy of large populations. Journal of Applied Probability 19A, 27–43.Google Scholar
Krijgsman, W., Hilgen, F.J., Raffi, I., Sierro, F.J. and Wilson, D.S. (1999) Chronology, causes and progression of the Messinian salinity crisis. Nature 400, 652–655.Google Scholar
Lagardère, J.P. (1971) Les crevettes des côtes du Maroc. Travaux de l'Institut Scientifique Chérifien 36, 1–140.Google Scholar
Lefébure, T., Douady, C.J., Gouy, M. and Gibert, J. (2006) Relationship between morphological taxonomy and molecular divergence within Crustacea: proposal of a molecular threshold to help species delimitation. Molecular Phylogenetics and Evolution 40, 435–447.Google Scholar
Librado, P. and Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.Google Scholar
Luttikhuizen, P.C., van Bleijswijk, J.C.J., Peijnenburg, K.T.C.A. and van der Veer, H.W. (2008) Phylogeography of the common shrimp, Crangon crangon (L.) across its distribution range. Molecular Phylogenetics and Evolution 46, 1015–1030.Google Scholar
Mathews, L.M. (2006) Cryptic biodiversity and phylogeographic patterns in a snapping shrimp complex. Molecular Ecology 15, 4049–4063.Google Scholar
Patarnello, T., Volckaert, F. and Castilho, R. (2007) Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographical break? Molecular Ecology 16, 4426–4444.Google Scholar
Pennant, T. (1777) Crustacea Mollusca Testacea. British Zoology 4, London, 1–157; plates 1–93.Google Scholar
Ragionieri, L., Fratini, S., Vannini, M. and Schubart, C.D. (2009) Phylogenetic and morphometric differentiation reveal geographic radiation and pseudo-cryptic speciation in a mangrove crab from the Indo-West Pacific. Molecular Phylogenetics and Evolution 52, 825–834.Google Scholar
Ragionieri, L. and Schubart, C.D. (2013) Population genetics, gene flow, and biogeographical boundaries of Carcinus aestuarii (Crustacea: Brachyura: Carcinidae) along the European Mediterranean coast. Biological Journal of the Linnean Society 109, 771–790.Google Scholar
Reeve, M.R. (1968) The suitability of the English prawn Palaemon serratus (Pennant) for cultivation – a preliminary assessment. In Proceedings of the world scientific conference on the biology and culture of shrimps and prawns. Vol. 3. Conway, North Wales: Fisheries and Aquaculture Department.Google Scholar
Reeve, M.R. (1969) Growth, metamorphosis and energy conversion in the larvae of the prawn, Palaemon serratus. Journal of the Marine Biological Association of the United Kingdom 49, 77–96.Google Scholar
Remerie, T., Vierstraete, A., Weekers, P.H.H., Vanfleteren, J.R. and Vanreusel, A. (2009) Phylogeography of an estuarine mysid, Neomysis integer (Crustacea, Mysida), along the north-east Atlantic coasts. Journal of Biogeography 36, 39–54.Google Scholar
Reuschel, S., Cuesta, J.A. and Schubart, C.D. (2010) Marine biogeographic boundaries and human introduction along the European coast revealed by phylogeography of the prawn Palaemon elegans. Molecular Phylogenetics and Evolution 55, 765–775.Google Scholar
Ríos, C., Sanz, S., Saavedra, C. and Peña, J.B. (2002) Allozyme variation in populations of scallops, Pecten jacobaeus (L.) and P. maximus (L.) (Bivalvia: Pectinidae), across the Almeria–Oran front. Journal of Experimental Marine Biology and Ecology 267, 223–244.Google Scholar
Rodríguez, A. (1981) Growth and sexual maturation of Penaeus kerathurus (Forskäl, 1775) and Palaemon serratus (Pennant) in salt ponds. Aquaculture 24, 257–266.Google Scholar
Roman, J. and Palumbi, S.R. (2004) A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Molecular Ecology 13, 2891–2898.Google Scholar
Schubart, C.D. (2009) Mitochondrial DNA and decapod phylogenies: the importance of pseudogenes and primer optimization. In Martin, J.W., Crandall, K.A. and Felder, D.L. (eds) Decapod Crustacean phylogenetics. Crustacean Issues. Boca Raton, Florida: Taylor & Francis/CRC Press. 18, 47–65.Google Scholar
Schubart, C.D., Cuesta, J.A. and Rodríguez, A. (2001) Molecular phylogeny of the crab genus Brachynotus (Brachyura: Varunidae) based on the 16S rRNA gene. Hydrobiologia 449, 41–46.Google Scholar
Schubart, C.D., Neigel, J.E. and Felder, D.L. (2000) The use of the mitochondrial 16S rRNA gene for phylogenetic and biogeographic studies of Crustacea. In The biodiversity crisis and Crustacea. Proceedings of the Fourth International Crustacean Congress. Amsterdam, 20–24 July 1998, Vol. 2. Crustacean Issues 12, 817–830.Google Scholar
Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.Google Scholar
Tintoré, J., La Violette, P., Blade, I. and Cruzado, A. (1988) A study of an intense density front in the eastern Alboran Sea: the Almeria-Oran Front. Journal of Physical Oceanography 18, 1284–1397.Google Scholar
Tsang, L.M., Schubart, C.D., Ahyong, S.T., Lai, J.C.Y., Au, E.Y.C., Chan, T., Ng, P.K.L. and Chu, K.H. (2014) Evolutionary history of true crabs (Crustacea: Decapoda: Brachyura) and the origin of freshwater crabs. Molecular Biology and Evolution 31, 1173–1187.Google Scholar
Zane, L., Ostellari, L., Maccatrozzo, L., Bargelloni, L., Cuzin-Roudy, J., Buchholz, F. and Patarnello, T. (2000) Genetic differentiation in pelagic crustacean (Meganyctiphanes norvegica: Euphausiacea) from the North Atlantic and the Mediterranean Sea. Marine Biology 136, 191–199.Google Scholar
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