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Early Pleistocene divergence of Pelagia noctiluca populations (Cnidaria, Medusozoa) between the Atlantic Ocean and the Mediterranean Sea

Published online by Cambridge University Press:  07 November 2019

Ezequiel Ale ,
Andreja Ramšak ,
David Stanković ,
André Carrara Morandini ,
Diogo Meyer  and
Antonio C. Marques
Ezequiel Ale
Affiliation:
Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil
Andreja Ramšak*
Affiliation:
National Institute of Biology, Marine Biology Station, Piran, Slovenia
David Stanković
Affiliation:
National Institute of Biology, Marine Biology Station, Piran, Slovenia
André Carrara Morandini
Affiliation:
Departamento de Zoologia, Instituto de Biociências, and Centro de Biologia Marinha, Universidade de São Paulo, São Paulo, Brazil
Diogo Meyer
Affiliation:
Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil
Antonio C. Marques
Affiliation:
Departamento de Zoologia, Instituto de Biociências, and Centro de Biologia Marinha, Universidade de São Paulo, São Paulo, Brazil
*
Author for correspondence: Andreja Ramšak, E-mail: [email protected]
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Abstract

A previous study detected mixing of two deeply split mtDNA clades (Clade I and Clade II) for Atlantic and Mediterranean populations of the medusozoan Pelagia noctiluca. The north hemisphere glaciations and the Messinian salinity crisis have been proposed as the two main biogeographic events related to the isolation between the Atlantic Ocean and the Mediterranean Sea. We tested if the splitting time between Clade I and Clade II of P. noctiluca was associated with one of these geological events. Our study was based on DNA sequence data of mitochondrial (COI and 16S ribosomal RNA) and nuclear (18S ribosomal RNA, internal transcribed spacer 1 and 5.8S ribosomal RNA) genes from populations of the Atlantic and Pacific Ocean and the Mediterranean Sea. The rise of the Isthmus of Panama was used to calibrate substitution rates for COI. This calibration was based on the detection of a shallow but significant genetic structure between P. noctiluca populations from the Pacific and the Atlantic Oceans. Considering our calibration for COI, we refute a possible origin of Clades I and II during the Messinian salinity crisis. Our estimates suggest the origin for a putative common ancestor of Clades I and II around 2.57 Ma (with 95% 2.91–2.22 HPD), roughly corresponding to the Gelasian stage of the early Pleistocene. These alterations include changes in the sea level and oceanic currents at the Strait of Gibraltar and other regions of the Mediterranean basin, and could explain the origin of the two P. noctiluca clades.

Keywords

Molecular clockPelagia noctilucaPleistocenesubstitution rates
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 8 , December 2019 , pp. 1753 - 1764
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

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References

Akaike, H (1973) Information theory as an extension of the maximum-likelihood principle. In Petrov, BN and Csaki, F (eds), Second International Symposium on Information Theory. Budapest: Akademiai Kiado, pp. 267–281.Google Scholar
Arribas, A, Garrido, G, Viseras, C, Soria, JM, Pla, S, Solano, JG, Garcés, M, Beamud, J and Carrio, JS (2009) A mammalian lost world in Southwest Europe during the Late Pliocene. PLoS ONE 4, e7127.Google Scholar
Avian, M, Ramšak, A, Tirelli, V, D'Ambra, I and Malej, A (2016) Redescription of Pelagia benovici into a new jellyfish genus, Mawia, gen. nov., and its phylogenetic position within Pelagiidae (Cnidaria: Scyphozoa: Semaeostomeae). Invertebrate Systematics 30, 523–546.Google Scholar
Avise, JC (2009) Phylogeography: retrospect and prospect. Journal of Biogeography 36, 3–15.Google Scholar
Ayres, DL, Darling, A, Zwickl, DJ, Beerli, P, Holder, MT, Lewis, PO, Huelsenbeck, JP, Ronquist, F, Swofford, DL, Cummings, MP, Rambaut, A and Suchard, MA (2012) BEAGLE: an application programming interface and high-performance computing library for statistical phylogenetics. Systematic Biology 61, 170–173.Google Scholar
Bartoli, G, Sarnthein, M, Weinelt, M, Erlenkeuser, H, Garbe-Schönberg, D and Lea, DW (2005) Final closure of Panama and the onset of northern hemisphere glaciation. Earth and Planetary Science Letters 237, 33–44.Google Scholar
Baxter, EJ, Walne, AW, Purcell, JE, McAllen, R and Doyle, TK (2010) Identification of jellyfish from Continuous Plankton Recorder samples. Hydrobiologia 645, 193–201.Google Scholar
Belinky, F, Szitenberg, A, Goldfarb, I, Feldstein, T, Wörheide, G, Ilan, M and Huchon, D (2012) ALG11 – a new variable DNA marker for sponge phylogeny: comparison of phylogenetic performances with the 18S rDNA and the COI gene. Molecular Phylogenetics and Evolution 63, 702–713.Google Scholar
Bermingham, E and Lessios, HA (1993) Rate variation of proteins and mitochondrial DNA evolution as revealed by sea urchins separated by the Isthmus of Panama. PNAS 90, 2734–2738.Google Scholar
Blondel, J, Aronson, J, Bodiou, J-Y and Boeuf, G (2010) The Mediterranean Region: Biological Diversity in Space and Time, 2nd Edn. New York, NY: Oxford University Press.Google Scholar
Bouckaert, R, Heled, J, Kühnert, D, Vaughan, T, Wu, C-H, Xie, D, Suchard, MA, Rambaut, A and Drummond, AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10, e1003537.Google Scholar
Burridge, CP, Craw, D, Fletcher, D and Waters, JM (2008) Geological dates and molecular rates: fish DNA sheds light on time dependency. Molecular Biology and Evolution 25, 624–633.Google Scholar
Cartwright, P, Halgedahl, SL, Hendricks, JR, Jarrard, RD, Marques, AC, Collins, AG and Lieberman, BS (2007) Exceptionally preserved jellyfishes from the Middle Cambrian. PLoS ONE 2, e1121.Google Scholar
Catarino, D, Knutsen, H, Veríssimo, A, Olsen, EM, Jorde, PE, Menezes, G, Sannæs, H, Stanković, D, Company, JB, Neat, F, Danovaro, R, Dell'Anno, A, Rochowski, B and Stefanni, S (2015) The Pillars of Hercules as a bathymetric barrier to gene flow promoting isolation in a global deep-sea shark (Centroscymnus coelolepis). Molecular Ecology 24, 6061–6079.Google Scholar
Catarino, D, Stanković, D, Menzes, G and Stefanni, S (2017) Insights into the genetic structure of the rabbitfish Chimaera monstrosa (Holocephali) across the Atlantic-Mediterranean transition zone. Journal of Fish Biology 91, 1109–1122.Google Scholar
Clement, M, Snell, Q, Walke, P, Posada, D and Crandall, K (2002) TCS: estimating gene genealogies. Proc. 16th Int. Parallel. Distrib. Process. Symp 2, pp. 184.Google Scholar
Coates, AG and Obando, JA (1996) The geologic evolution of the Central American isthmus. In Jackson, JBC, Budd, AF and Coates, AG (eds), Evolution and Environment in Tropical America. Chicago, IL: University of Chicago Press, pp. 21–56.Google Scholar
Cunningham, C and Buss, LW (1993) Molecular evidence for multiple episodes of paedomorphosis in the family Hydractiniidae. Biochemical Systematics and Ecology 21, 57–69.Google Scholar
da Silveira, FL and Morandini, AC (1997) Nausithoe aurea n. sp. (Scyphozoa, Coronatae, Nausithoidae), a species with two pathways of reproduction after strobilation: sexual and asexual. Contributions to Zoology 66, 235–246.Google Scholar
Dawson, MN and Jacobs, DK (2001) Molecular evidence for cryptic species of Aurelia aurita (Cnidaria, Scyphozoa). Biological Bulletin 200, 92–96.Google Scholar
Dawson, MN, Gupta, AS and England, MH (2005) Coupled biophysical global ocean model and molecular genetic analyses identify multiple introductions of cryptogenic species. PNAS 34, 11968–11973.Google Scholar
Drummond, AJ, Nicholls, GK, Rodrigo, AG and Solomon, W (2002) Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161, 1307–1320.Google Scholar
Drummond, AJ, Rambaut, A, Shapiro, B and Pybus, OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution 22, 1185–1192.Google Scholar
Drummond, AJ, Ashton, B, Buxton, S, Cheung, M and Cooper, A. (2010) Geneious v5.5.7. Available at http://www.geneious.com (Accessed 15 March 2012).Google Scholar
Duque-Caro, H (1990) Neogene stratigraphy, paleoceanography and paleobiogeography in northwest South America and the evolution of the Panama seaway. Paleogeography, Paleoclimatology, Paleoecology 77, 203–234.Google Scholar
Emig, CC and Geistdoerfer, P (2004) The Mediterranean deep-sea fauna: historical evolution, bathymetric variations and geographical changes. Carnets de Géologie/Notebooks on Geology. Article 2004/01 (CG2004_A01_CCE-PG), 10 pp.Google Scholar
Excoffier, L and Lischer, HE (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.Google Scholar
Folmer, O, Black, M, Hoeh, W, Lutz, R and Vrijenhoek, R (1994) DNA primers for amplification of mitochondrial Cytochrome C Oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
France, SC and Hoover, IL (2002) DNA sequences of the mitochondrial COI gene have low levels of divergence among deep-sea octocorals (Cnidaria: Anthozoa). Hydrobiology 471, 149–155.Google Scholar
Fredj, G, Bellan-Santini, D and Meinardi, M (1992) Etat des connaissances sur la faune marine méditerranéenne. Bulletin de l'Institut Oceanographique 9, 133–145.Google Scholar
Funk, DJ and Omland, KE (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution, and Systematics 34, 397–423.Google Scholar
Gernhard, T (2008) The conditioned reconstructed process. Journal of Theoretical Biology 253, 769–778.Google Scholar
Gibert, J, Gibert, L and Iglesias, A (2003) The Gibraltar Strait: a Pleistocene door of Europe? Human Evolution 18, 147–160.Google Scholar
Govers, R (2009) Choking the Mediterranean to dehydration: the Messinian salinity crisis. Geology 37, 167–170.Google Scholar
Govindarajan, AF, Halanych, KM and Cunningham, CW (2005) Mitochondrial evolution and phylogeography in the hydrozoan Obelia geniculata (Cnidaria). Marine Biology 146, 213–222.Google Scholar
Goy, J, Dalot, S and Morand, P (1989) Long term fluctuations of Pelagia noctiluca (Cnidaria, Scyphomedusae) in the western Mediterranean Sea. Deep-Sea Research 36, 269–279.Google Scholar
Guindon, S, Dufayard, JF, Lefort, V, Anisimova, M, Hordijk, W and Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.Google Scholar
Hebert, PDN, Ratnasingham, S and de Waard, JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London, Series B: Biological Sciences 270(suppl. 1), S96–S99.Google Scholar
Ho, SY, Phillips, MJ, Cooper, A and Drummond, AJ (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Molecular Biology and Evolution 22, 1561–1568.Google Scholar
Holland, BS, Dawson, MN, Crow, GL and Hofmann, DK (2004) Global phylogeography of Cassiopea (Scyphozoa: Rhizostomeae): molecular evidence for cryptic species and multiple invasions of the Hawaiian Islands. Marine Biology 145, 1119–1128.Google Scholar
Huang, D, Meier, R, Todd, PA and Chou, LM (2008) Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. Journal of Molecular Evolution 66, 167–174.Google Scholar
Hurt, C, Anker, A and Knowlton, N (2009) A multilocus test of simultaneous divergence across the Isthmus of Panama using snapping shrimp in the genus Alpheus. Evolution 63, 514–530.Google Scholar
Katoh, K, Kuma, K, Toh, H and Miyata, T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33, 511–518.Google Scholar
Keigwin, LD (1982) Isotopic paleoceanography of the Caribbean and east Pacific: role of Panama uplift in late Neogene time. Science 217, 350–352.Google Scholar
Knowlton, N and Weigt, LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proceedings of the Royal Society of London, Series B: Biological Sciences 265, 2257–2263.Google Scholar
Krijgsman, W, Hilgen, FJ, Raffi, I, Sierro, FJ and Wilson, DS (1999) Chronology, causes and progression of the Messinian salinity crisis. Nature 400, 652–655.Google Scholar
Lanfear, R, Frandsen, PB, Wright, AM, Senfeld, T and Calcott, B (2017) Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.Google Scholar
Larsson, A (2014) Aliview: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics (Oxford, England) 30, 3276–3278.Google Scholar
Leigh, JW and Bryant, D (2015) PopART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.Google Scholar
Lessios, HA (1979) Use of Panamanian sea urchins to test the molecular clock. Nature 280, 599–601.Google Scholar
Librado, P and Rozas, J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics (Oxford, England) 25, 1451–1452.Google Scholar
Marko, PB (2002) Fossil calibration of molecular clocks and the divergence times of geminate species pairs separated by the Isthmus of Panama. Molecular Biology and Evolution 19, 2005–2021.Google Scholar
McCartney, MA, Keller, G and Lessios, HA (2000) Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Molecular Ecology 9, 1391–1400.Google Scholar
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, pp. 1–8.Google Scholar
Miller, BJ, von der Hayden, S and Gibbons, MJ (2012) Significant population genetic structuring of the holoplanktic scyphozoan Pelagia noctiluca in the Atlantic Ocean. African Journal of Marine Science 34, 425–430.Google Scholar
Molnar, P (2008) Closing of the Central American Seaway and the Ice Age: a critical review. Paleoceanography 23, PA2201.Google Scholar
Moore, WS (1995) Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution 49, 718–726.Google Scholar
Ortman, BD, Bucklin, A, Pages, F and Youngbluth, M (2010) DNA barcoding the Medusozoa using mtCOI. Deep Sea Research Part II: Topical Studies in Oceanography 57, 2148–2156.Google Scholar
Patarnello, T, Volckaert, FAMJ and Castilho, R (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Molecular Ecology 16, 4426–4444.Google Scholar
Piraino, S, Aglieri, G, Martell, L, Mazzoldi, C, Melli, V, Milisenda, G, Scorrano, S and Boero, F (2014) Pelagia benovici sp. nov. (Cnidaria, Scyphozoa): a new jellyfish in the Mediterranean Sea. Zootaxa 3794, 455–468.Google Scholar
Rambaut, A and Drummond, AJ (2009) TRACER: MCMC Trace Analysis Tool Version v1.5.0. Oxford: Oxford University Press.Google Scholar
Rogers, AR and Harpending, H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552–569.Google Scholar
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.Google Scholar
Schroth, W, Jarms, G, Streit, B and Schierwater, B (2002) Speciation and phylogeography in the cosmopolitan marine moon jelly, Aurelia sp. BMC Evolutionary Biology 2, 1–10.Google Scholar
Shearer, TL, Van Oppen, MJH, Romano, SL and Wörheide, G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Molecular Ecology 11, 2475–2487.Google Scholar
Slatkin, M and Hudson, RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129, 555–562.Google Scholar
Stopar, K, Ramšak, A, Trontelj, P and Malej, A (2010) Lack of genetic structure in the jellyfish Pelagia noctiluca (Cnidaria: Scyphozoa: Semaeostomeae) across European Seas. Molecular Phylogenetics and Evolution 57, 417–428.Google Scholar
Straehler-Pohl, I and Jarms, G (2010) Identification key for young ephyrae: a first step for early detection of jellyfish blooms. Hydrobiologia 645, 3–21.Google Scholar
Tronolone, VB, Morandini, AC and Migotto, AE (2002) On the occurrence of scyphozoan ephyrae (Cnidaria, Scyphozoa, Semaeostomeae and Rhizostomeae) in the southeastern Brazilian coast. Biota Neotropica 2, 1–18.Google Scholar
Van Iten, H, Leme, JM, Marques, AC and Simões, MG (2013) Alternative interpretations of some earliest Ediacaran fossils from China. Acta Palaeontologica Polonica 58, 111–113.Google Scholar
Van Iten, H, Marques, AC, Leme, JM, Pacheco, MLAF and Simões, MG (2014) Origin and early diversification of the phylum Cnidaria Verrill: major developments in the analysis of the taxon's Proterozoic and earliest Cambrian history. Palaeontology 57, 677–690.Google Scholar
Van Iten, H, Leme, JM, Pacheco, MLAF, Simões, MG, Fairchild, TR, Rodrigues, F, Galante, D, Boggiani, PC and Marques, AC (2016) Origin and early diversification of phylum Cnidaria: key macrofossils from the Ediacaran system of North and South America. In Goffredo, S and Dubinsky, Z (eds), The Cnidaria, Past, Present and Future. Dordrecht: Springer, pp. 31–40.Google Scholar
Vawter, AT, Rosenblatt, RH and Gorman, GC (1980) Genetic divergence among fishes of the eastern Pacific and the Caribbean: support for the molecular clock. Evolution 34, 705–711.Google Scholar
Waters, JM, Rowe, DL, Apte, S, King, TM, Wallis, GP, Anderson, L, Norris, RJ, Craw, D and Burridge, CP (2007) Geological dates and molecular rates: rapid divergence of rivers and their biotas. Systematic Biology 56, 271–282.Google Scholar
Young, GA and Hagadorn, JW (2010) The fossil record of cnidarian medusae. Palaeoworld 19, 212–221.Google Scholar
Yule, GU (1925) A mathematical theory of evolution, based on the conclusions of Dr J.C. Willis, F.R.S. Philosophical Transactions of the Royal Society, B: Biological Sciences 213, 21–87.Google Scholar
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