Genetic diversity and population structure of the rockpool shrimp Palaemon elegans based on microsatellites: evidence for a cryptic species and differentiation across the Atlantic–Mediterranean transition

González-Ortegón, E. & Cuesta, J. A. An illustrated key to species of Palaemon and Palaemonetes (Crustacea: Decapoda: Caridea) from European waters, including the alien species Palaemon macrodactylus. J. Mar. Biol. Assoc. UK 86, 93–102. https://doi.org/10.1017/S0025315406012896 (2006).

Article  Google Scholar 

Taylor, A. C. & Spicer, J. I. Metabolic responses of the prawns Palaemon elegans and P. serratus (Crustacea: Decapoda) to acute hypoxia and anoxia. Mar. Biol. 95, 521–530. https://doi.org/10.1007/BF00393095 (1987).

CAS  Article  Google Scholar 

Janas, U., Pilka, M. & Lipinska, D. Temperature and salinity requirements of Palaemon adspersus Rathke 1837 and Palaemon elegans Rathke, 1837. Do they explain the occurrence and expansion of prawns in the Baltic Sea?. Mar. Biol. Res. 9, 293–300. https://doi.org/10.1080/17451000.2012.739699 (2013).

Article  Google Scholar 

d’Acoz, U. Inventaire et distribution des crustacés décapodes de l’Atlantique nord-orienal, de la Méditerranée et des eaux continentals adjacentes au nord de 25°N. Collection Patrimoines Naturels (Muséum National d’Histoire Naturelle (S.P.N.)) https://doi.org/10.1016/s0990-7440(02)01163-4 (1999).

Article  Google Scholar 

Grabowski, M. Rapid colonization of the Polish Baltic coast by an Atlantic palaemonid shrimp Palaemon elegans Rathke, 1837. Aquat. Invasions 1, 116–123. https://doi.org/10.3391/ai.2006.1.3.3 (2006).

Article  Google Scholar 

Katajisto, T., Kotta, J., Lehtiniemi, M., Malavin, S. A. & Panov, V. E. Palaemon elegans Rathke, 1837 (Caridea: Palaemonoidea: Palaemonidae) established in the Gulf of Finland. Bioinvasions Rec. 2, 125–132. https://doi.org/10.3391/bir.2013.2.2.05 (2013).

Article  Google Scholar 

González-Ortegón, E., Sargent, P., Pohle, G. & Martínez-Lage, A. The Baltic prawn Palaemon adspersus Rathke, 1837 (Decapoda, Caridea, Palaemonidae): First record, possible establishment, and illustrated key of the subfamily Palaemoninae in northwest Atlantic waters. Aquat. Invasions 10, 299–312. https://doi.org/10.3391/ai.2015.10.3.05 (2015).

Article  Google Scholar 

Reuschel, S., Cuesta, J. A. & Schubart, C. D. Marine biogeographic boundaries and human introduction along the European coast revealed by phylogeography of the prawn Palaemon elegans. Mol. Phylogenet. Evol. 55, 765–775. https://doi.org/10.1016/j.ympev.2010.03.021 (2010).

Article  PubMed  Google Scholar 

Ward, R. D. The importance of identifying spatial population structure in restocking and stock enhancement programmes. Fish. Res. 80, 9–18. https://doi.org/10.1016/j.fishres.2006.03.009 (2006).

Article  Google Scholar 

Pascual, M., Rives, B., Schunter, C. & Macpherson, E. Impact of life history traits on gene flow: a multispecies systematic review across oceanographic barriers in the Mediterranean Sea. PLoS ONE 12, e0176419. https://doi.org/10.1371/journal.pone.0176419 (2017).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Patarnello, T., Volckaert, F. A. M. J. & Castilho, R. Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographical break?. Mol. Ecol. 16, 4426–4444. https://doi.org/10.1111/j.1365-294X.2007.03477.x (2007).

Article  PubMed  Google Scholar 

Bilgin, R., Utkan, M. A., Kalkan, E., Karhan, S. & Bekbolet, M. DNA barcoding of twelve shrimp species (Crustacea: Decapoda) from Turkish seas reveals cryptic diversity. Mediterr. Mar. Sci. 16, 36–45. https://doi.org/10.12681/mms.548 (2014).

Article  Google Scholar 

Deli, T., Pfaller, M. & Schubart, C. D. Phylogeography of the littoral prawn species Palaemon elegans (Crustacea: Caridea: Palaemonidae) across the Mediterranean Sea unveils disparate patterns of population genetic structure and demographic history in the two sympatric genetic types II and III. Mar. Biodiv. https://doi.org/10.1007/s12526-017-0711-6 (2018).

Article  Google Scholar 

Bickford, D. et al. Cryptic species as a window on diversity and conservation. Trends Ecol. Evol. 22, 148–155. https://doi.org/10.1016/j.tree.2006.11.004 (2007).

Article  PubMed  Google Scholar 

Lejeusne, C., Chevaldonné, P., Pergent-Martini, C., Boudouresque, C. F. & Pérez, T. Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends Ecol. Evol. 25, 250–260. https://doi.org/10.1016/j.tree.2009.10.009 (2010).

Article  PubMed  Google Scholar 

Fernández, M. V., Heras, S., Maltagliati, F. & Roldán, M. I. Deep genetic divergence in giant red shrimp Aristaeomorpha foliacea (Risso, 1827) across a wide distributional range. J. Sea Res. 76, 146–153. https://doi.org/10.1016/j.seares.2012.08.004 (2013).

ADS  Article  Google Scholar 

Fernández, M. V., Heras, S., Vinas, J., Maltagliati, F. & Roldán, M. I. 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. https://doi.org/10.1371/journal.pone.0059033 (2013).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

Barba, De. et al. High-throughput microsatellite genotyping in ecology: improved accuracy, efficiency, standardization and success with low-quantity and degraded DNA. Mol. Ecol. Resour. 17, 492–507. https://doi.org/10.1111/1755-0998.12594 (2017).

CAS  Article  PubMed  Google Scholar 

Goldstein, D. B. & Schlotterer, C. Microsatellites—Evolution and Applications. Oxford University Press, Oxford. https://doi.org/10.1017/S0016672300239141 (1999).

Article  Google Scholar 

Wright, J. M. & Bentzen, P. Microsatellites: genetic markers for the future. Mol. Genet. Fish. 1, 117–121. https://doi.org/10.1007/978-94-011-1218-5_7 (1995).

Article  Google Scholar 

Valles-Jiménez, R., Cruz, P. & Pérez-Enríquez, R. Population genetic structure of pacific white shrimp (Litopenaus vannamei) from Mexico to Panama: microsatellite DNA variation. Mar. Biotechnol. 6, 475–484. https://doi.org/10.1007/s10126-004-3138-6 (2004).

CAS  Article  PubMed  Google Scholar 

Waqairatu, S. S. et al. Genetic analysis of black tiger shrimp (Penaeus monodon) across its natural distribution range reveals more recent colonization of Fiji and other South Pacific islands. Ecol. Evol. 2, 2057–2071. https://doi.org/10.1002/ece3.316 (2012).

Article  PubMed  PubMed Central  Google Scholar 

Jorde, P. E. et al. Genetically distinct populations of northern shrimp, Pandalus borealis, in the North Atlantic: adaptation to different temperatures as an isolation factor. Mol. Ecol. 24, 1742–1757. https://doi.org/10.1111/mec.13158 (2015).

Article  PubMed  Google Scholar 

Heras, S., Planella, L., García-Marín, J. L., Vera, M. & Roldán, M. I. Genetic structure and population connectivity of the blue and red shrimp Aristeus antennatus. Sci. Rep. 9, 1–11. https://doi.org/10.1038/s41598-019-49958-5 (2019).

CAS  Article  Google Scholar 

Perina, A. et al. Assessment of genetic diversity and population structure of the common littoral shrimp Palaemon serratus (Pennant, 1777) by microsatellites: towards a sustainable management. Aquatic Conserv. Mar. Freshw. Ecosyst. https://doi.org/10.1002/aqc.3011 (2019).

Article  Google Scholar 

Davey, J. W. et al. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat. Rev. Genet. 12, 499–510. https://doi.org/10.1038/nrg3012 (2011).

ADS  CAS  Article  PubMed  Google Scholar 

González-Castellano, I., Perina, A., González-Tizón, A. M., Torrecilla, Z. & Martínez-Lage, A. Isolation and characterization of 21 polymorphic microsatellite loci for the rockpool shrimp Palaemon elegans using Illumina MiSeq sequencing. Sci. Rep. 8, 17197. https://doi.org/10.1038/s41598-018-35408-1 (2018).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

Chapuis, M. P. & Estoup, A. Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24, 621–631. https://doi.org/10.1093/molbev/msl191 (2007).

CAS  Article  PubMed  Google Scholar 

Perina, A., González-Tizón, A. M., Vizcaíno, A., González-Ortegón, E. & Martínez-Lage, A. Isolation and characterization of 20 polymorphic microsatellite loci in Palaemon serratus and cross-amplification in Palaemon species by 454 pyrosequencing. Conserv. Genet. Resour. 8, 169–196. https://doi.org/10.1007/s12686-016-0549-4 (2016).

Article  Google Scholar 

Dailianis, T., Tsigenopoulos, C. S., Dounas, C. & Voultsiadou, E. Genetic diversity of the imperilled bath sponge Spongia officinalis Linnaeus, 1759 across the Mediterranean Sea: patterns of population differentiation and implications for taxonomy and conservation. Mol. Ecol. 20, 3757–3772. https://doi.org/10.1111/j.1365-294X.2011.05222.x (2011).

CAS  Article  PubMed  Google Scholar 

Plough, L. V. & Marko, P. B. Characterization of microsatellite loci and repeat density in the gooseneck barnacle, Pollicipes elegans, using next generation sequencing. J. Hered. 105, 136–142. https://doi.org/10.1093/jhered/est064 (2014).

CAS  Article  PubMed  Google Scholar 

Boissin, E., Féral, J. P. & Chenuil, A. Defining reproductively isolated units in a cryptic and syntopic species complex using mitochondrial and nuclear markers: the brooding brittle star, Amphipholis squamata (Ophiuroidea). Mol. Ecol. 17, 1732–1744. https://doi.org/10.1111/j.1365-294X.2007.03652.x (2008).

CAS  Article  PubMed  Google Scholar 

Griffiths, A. M. et al. Molecular markers reveal spatially segregated cryptic species in a critically endangered fish, the common skate (Dipturus batis). Proc. R. Soc. B. Biol. Sci. 277, 1497–1503. https://doi.org/10.1098/rspb.2009.2111 (2010).

Article  Google Scholar 

Andrews, K. R., Norton, E. L., Fernandez-Silva, I., Portner, E. & Goetze, E. Multilocus evidence for globally distributed cryptic species and distinct populations across ocean gyres in a mesopelagic copepod. Mol. Ecol. 23, 5462–5479. https://doi.org/10.1111/mec.12950 (2014).

CAS  Article  PubMed  Google Scholar 

Naughton, K. M., O’Hara, T. D., Appleton, B. & Gardner, M. G. Sympatric cryptic species in the crinoid genus Cenolia (Echinodermata: Crinoidea: Comasteridae) delineated by sequence and microsatellite markers. Mol. Phylogenet. Evol. 78, 160–171. https://doi.org/10.1016/j.ympev.2014.05.006 (2014).

CAS  Article  PubMed  Google Scholar 

García-Castellanos, D. et al. Catastrophic flood of the Mediterranean after the Messinian salinity crisis. Nature 462, 778. https://doi.org/10.1038/nature08555 (2009).

ADS  CAS  Article  PubMed  Google Scholar 

Marino, I. A., Pujolar, J. M. & Zane, L. 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. https://doi.org/10.1371/journal.pone.0028567 (2011).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

Pérez-Portela, R., Almada, V. & Turon, X. Cryptic speciation and genetic structure of widely distributed brittle stars (Ophiuroidea) in Europe. Zool. Scr. 42, 151–169. https://doi.org/10.1111/j.1463-6409.2012.00573.x (2013).

Article  Google Scholar 

Tintoré, J., La Violette, P. E., Blade, I. & Cruzado, A. A study of an intense density front in the eastern Alboran Sea: the Almeria-Oran front. J. Phys. Oceanogr. 18, 1384–1397. https://doi.org/10.1175/1520-0485(1988)018<1384:ASOAID>2.0.CO;2 (1988).

ADS  Article  Google Scholar 

Pérez-Losada, M., Guerra, A., Carvalho, G. R., Sanjuan, A. & Shaw, P. W. Extensive population subdivision of the cuttlefish Sepia officinalis (Mollusca: Cephalopoda) around the Iberian Peninsula indicated by microsatellite DNA variation. Heredity 89, 417–424. https://doi.org/10.1038/sj.hdy.6800160 (2002).

CAS  Article  PubMed  Google Scholar 

Galarza, J. A. et al. The influence of oceanographic fronts and early-life-history traits on connectivity among littoral fish species. Proc. Natl. Acad. Sci. USA 106, 1473–1478. https://doi.org/10.1073/pnas.0806804106 (2009).

ADS  Article  PubMed  Google Scholar 

Pannacciulli, F. G., Maltagliati, F., De Guttry, C. & Achituv, Y. Phylogeography on the rocks: the contribution of current and historical factors in shaping the genetic structure of Chthamalus montagui (Crustacea, Cirripedia). PLoS ONE 12, e0178287. https://doi.org/10.1371/journal.pone.0178287 (2017).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Nantón, A. et al. Microsatellite variation in Donax trunculus from the Iberian Peninsula, with particular attention to Galician estuaries (NW Spain). Estuar. Coast. Shelf Sci. 197, 27–34. https://doi.org/10.1016/j.ecss.2017.08.011 (2017).

ADS  Article  Google Scholar 

Fratini, S. et al. Unravelling population genetic structure with mitochondrial DNA in a notional panmictic coastal crab species: sample size makes the difference. BMC Evol. Biol. 16, 150. https://doi.org/10.1186/s12862-016-0720-2 (2016).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Schunter, C. et al. Matching genetics with oceanography: directional gene flow in a Mediterranean fish species. Mol. Ecol. 20, 5167–5181. https://doi.org/10.1111/j.1365-294X.2011.05355.x (2011).

CAS  Article  PubMed  Google Scholar 

García-Merchán, V. H. et al. Phylogeographic patterns of decapod crustaceans at the Atlantic–Mediterranean transition. Mol. Phylogenet. Evol. 62, 664–672. https://doi.org/10.1016/j.ympev.2011.11.009 (2012).

Article  PubMed  Google Scholar 

Weiss, R. et al. Genetic differentiation between Mediterranean and Atlantic populations of the common prawn Palaemon serratus (Crustacea: Palaemonidae) reveals uncommon phylogeographic break. J. Mar. Biol. Assoc. UK 98, 1425–1434. https://doi.org/10.1017/S0025315417000492 (2018).

Article  Google Scholar 

Sá-Pinto, A., Branco, M., Sayanda, D. & Alexandrino, P. Patterns of colonization, evolution and gene flow in species of the genus Patella in the Macaronesian Islands. Mol. Ecol. 17, 519–532. https://doi.org/10.1111/j.1365-294X.2007.03563.x (2008).

CAS  Article  PubMed  Google Scholar 

Pérez-Portela, R., Villamor, A. & Almada, V. Phylogeography of the sea star Marthasterias glacialis (Asteroidea, Echinodermata): deep genetic divergence between mitochondrial lineages in the north-western mediterranean. Mar. Biol. 157, 2015–2028. https://doi.org/10.1007/s00227-010-1470-0 (2010).

Article  Google Scholar 

Pérez-Portela, R., Rius, M. & Villamor, A. Lineage splitting, secondary contacts and genetic admixture of a widely distributed marine invertebrate. J. Biogeogr. 44, 446–460. https://doi.org/10.1111/jbi.12917 (2017).

Article  Google Scholar 

Borrero-Pérez, G. H., González-Wangüemert, M., Marcos, C. & Pérez-Ruzafa, A. Phylogeography of the Atlanto-Mediterranean Sea cucumber Holothuria (Holothuria) mammata: the combined effects of historical processes and current oceanographical pattern. Mol. Ecol. 20, 1964–1975. https://doi.org/10.1111/j.1365-294X.2011.05068.x (2011).

Article  PubMed  Google Scholar 

Domingues, V. S., Almada, V. C., Santos, R. S., Brito, A. & Bernardi, G. Phylogeography and evolution of the triplefin Tripterygion delaisi (Pisces, Blennioidei). Mar. Biol. 150, 509–519. https://doi.org/10.1007/s00227-006-0367-4 (2007).

Article  Google Scholar 

González-Wangüemert, M., Froufe, E., Pérez-Ruzafa, A. & Alexandrino, P. Phylogeographical history of the white seabream Diplodus sargus (Sparidae): implications for insularity. Mar. Biol. Res. 7, 250–260. https://doi.org/10.1080/17451000.2010.499438 (2011).

Article  Google Scholar 

Mason, E., Coombs, S. & Oliveira, P.B. An overview of the literature concerning the oceanography of the eastern North Atlantic region. Relatórios Científicos e Técnicos IPIMAR Série digital no. 33.

Primmer, R. C., Painter, N. J., Koskinen, T. M., Palo, U. J. & Merilä, J. Factors affecting avian cross-species microsatellite amplification. J. Avian Biol. 36, 348–360. https://doi.org/10.1111/j.0908-8857.2005.03465.x (2005).

Article  Google Scholar 

Barbará, T. et al. Cross-species transfer of nuclear microsatellite markers: potential and limitations. Mol. Ecol. 16, 3759–3767. https://doi.org/10.1111/j.1365-294X.2007.03439.x (2007).

Article  PubMed  Google Scholar 

Rutkowski, R., Sielezniew, M. & Szostak, A. Contrasting levels of polymorphism in cross-amplified microsatellites in two endangered xerothermophilous, obligatorily myrmecophilous, butterflies of the genus Phengaris (Maculinea) (Lepidoptera: Lycaenidae). Eur. J. Entomol. 106, 457–469. https://doi.org/10.14411/eje.2009.058 (2009).

CAS  Article  Google Scholar 

Yue, G. H., Balazs, K. & Laszlo, O. A new problem with cross-species amplification of microsatellites: generation of non-homologous products. Zool. Res. 31, 131–140. https://doi.org/10.3724/SP.J.1141.2010.02131 (2010).

CAS  Article  PubMed  Google Scholar 

Kearse, M. et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649. https://doi.org/10.1093/bioinformatics/bts199 (2012).

Article  PubMed  PubMed Central  Google Scholar 

Peakall, R. & Smouse, P. E. GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Resour. 6, 288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x (2006).

Article  Google Scholar 

Goudet, J. FSTAT version 2. 9. 4: a program to estimate and test population genetics parameters. Updated from Goudet [1995]. Available from https://www.unil.ch/izea/softwares/fstat.html (2003).

Rousset, F. Genepop’007: a complete re-implementation of the Genepop software for Windows and Linux. Mol. Ecol. Resour. 8, 103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x (2008).

Article  PubMed  Google Scholar 

Manly, B. F. J. The statistics of natural selection (Chapman and Hall, London, 1985).

Google Scholar 

Yeh, F. C. et al. Popgene, the User Friendly Shareware for Population Genetic Analysis (Molecular Biology and Biotechnology Centre, University of Alberta, Alberta, Canada, 1997).

Google Scholar 

Dempster, A. P., Laird, N. M. & Rubin, D. B. Maximum likelihood from incomplete data via the EM algorithm. J. R. Stat. Soc. Ser. B (methodological) https://doi.org/10.1111/j.2517-6161.1977.tb01600.x (1977).

Article  MATH  Google Scholar 

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

CAS  PubMed  PubMed Central  Google Scholar 

Hubisz, M. J., Falush, D., Stephens, M. & Pritchard, J. K. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Resour. 9, 1322–1332. https://doi.org/10.1111/j.1755-0998.2009.02591.x (2009).

Article  PubMed  PubMed Central  Google Scholar 

Earl, D. A. & von Holdt, B. M. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet. Resour. 4, 359–361. https://doi.org/10.1007/s12686-011-9548-7 (2012).

Article  Google Scholar 

Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x (2005).

CAS  Article  PubMed  Google Scholar 

Jakobsson, M. & Rosenberg, N. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806. https://doi.org/10.1093/bioinformatics/btm233 (2007).

CAS  Article  PubMed  Google Scholar 

Ramasamy, R. K., Ramasamy, S., Bindroo, B. B. & Naik, V. G. STRUCTURE PLOT: a program for drawing elegant STRUCTURE bar plots in user friendly interface. SpringerPlus 3, 431. https://doi.org/10.1186/2193-1801-3-431 (2014).

Article  PubMed  PubMed Central  Google Scholar 

Belkhir, K., Borsa, P., Chikhi, L., Raufaste N. & Bonhomme F. GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France). (1996–2004).

Excoffier, L. & Lischer, H. E. L. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 546–67. https://doi.org/10.1111/j.1755-0998.2010.02847.x (2010).

Article  Google Scholar 

Narum, S. R. Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv. Genet. 7, 783–787. https://doi.org/10.1007/s10592-005-9056-y (2006).

CAS  Article  Google Scholar 

Mantel, N. The detection of disease clustering and a generalized regression approach. Cancer Res. 27, 209–220 (1967).

CAS  PubMed  Google Scholar