Abstract
To investigate population differentiation in a comparative and historical context, segments of the mitochondrial cytochrome c oxidase subunit I gene and the control region were sequenced in Panulirus argus from nine sites along approximately 1,500 km of the Northern Caribbean Sea (n = 326) and analyzed with respect to available panulirid data. A mismatch analysis and Fu’s FS test uncovered a signature of historical population expansion around the time of the Last Glacial Maximum. Significant population structure was not detected in the area. The data supported a hypothesis of panmixia resulting from ongoing larval transport by ocean currents and historical population expansion. Despite high intraspecific divergence levels at COI within Panulirus argus and several other Panulirus species, genetic species identification through DNA barcoding was feasible using either a modified distance threshold or a character-based approach.
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References
Bandelt H, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Benzie JA, Ballment E, Forbes AT, Demetriades NT, Sugama K, Haryanti MoriaS (2002) Mitochondrial DNA variation in Indo-Pacific populations of the giant tiger prawn, Penaeus monodon. Mol Ecol 11:2553–2569
Bohonak AJ (1999) Dispersal, gene flow and population structure. Quart Rev Bio 74:21–45
Bradbury IR, Snelgrove PVR (2001) Contrasting larval transport in demersal fish and benthic invertebrates : the role of behavior and advective processes in determining spatial pattern. Canad J Fish Aquat Sci 58:811–823
Brasher D, Ovenden JR, White RWG (1992) Mitochondrial DNA variation and phylogenetic relationships of Jasus spp. (Decopoda: Palinuridae). J Zool Lond 227:1–16
Butler MJ, Cowen R, Paris C, Matsuda K, Goldstein J (2008) Long PLDs, Larval Behavior, and Connectivity in Spiny Lobster. 11th International Coral Reef Symposium. Ft. Lauderdale, USA, p 123
Cannas R, Cau A, Deiana AM, Salvadori S, Tagliavini J (2006) Discrimination between the Mediterranean spiny lobsters Palinurus elephas and P. mauritanicus (Crustacea: Decapoda) by mitochondrial sequence analysis. Hydrobiologia 557:1–4
Chow S, Suzuki N, Imai H, Yoshimura T (2006) Molecular species identification of spiny lobster phyllosoma larvae of the genus Panulirus from the northwestern Pacific. Mar Biotechnol 8:260–267
Cochrane KL, Chakalall B (2001) The spiny lobster fishery in the WECAFC region—an approach to responsible fisheries management. Mar Freshwater Res 52:1623–1631
Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Annual Review of Marine Science 1:443–466
Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527
Crow JF, Aoki K (1984) Group selection for a polygenic behavioral trait: estimating the degree of population subdivision. Proc Natl Acad Sci USA 81:6073–6077
DeSalle R, Egan MG, Siddall M (2005) The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philos Trans R Soc Lond B Biol Sci 360:1905–1916
Diniz FM, Maclean N, Paterson IG, Bentzen P (2004) Polymorphic tetranucleotide microsatellite markers in the Caribbean spiny lobster, Panulirus argus. Mol Ecol Notes 4:327–329
Diniz FM, Maclean N, Ogawa M, Cintra IHA, Bentzen P (2005) The hypervariable domain of the mitochondrial control region in Atlantic spiny lobsters and its potential as a marker for investigating phylogeographic structuring. Mar Biotechnol 7:462–473
Doherty PJ, Planes S, Mather P (1995) Gene flow and larval duration in seven species of fish from the Great Barrier Reef. Ecology 76:2373–2391
Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581
Ehrhardt NE, Fitchett MD (2010) Dependence of recruitment on parent stock of the spiny lobster, Panulirus argus, in Florida. Fish Oceanog 19:434–447
Emerson BC (2007) Alarm bells for the molecular clock? No support for Ho et al’.s model of time-dependent molecular rate estimates. Syst Biol 56:337–345
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
FAO (2006) National reports presented at the fifth regional workshop on the assessment and management of the Caribbean Spiny Lobster, FAO, Rome
Farmer MW, Ward JA, Luckhurst BE (1989) Development of spiny lobster (Panulirus argus) phyllosoma larvae in the plankton near Bermuda. Proceedings of the 39th Gulf and Carib Fish Inst 39:289–301
Felsenstein J (2007) PHYLIP (Phylogeny Inference Package) Department of Genome Sciences. University of Washington, Seattle, Washington
FindModel (2010) http://www.hiv.lanl.gov/content/sequence/findmodel/findmodel.html
Fu Y-X (1997) Statistical tests of neutrality against population growth, hitchhiking and background selection. Genetics 147:915–925
García-Rodríguez FJ, Perez-Enriquez R (2006) Genetic differentiation of the California spiny lobster Panulirus interruptus (Randall, 1840) along the west coast of the Baja California Peninsula, Mexico. Mar Biol 148:621–629
García-Rodríguez FJ, Ponce-Díaz G, Muñoz-García I, González-Armas R, Perez-Enriquez R (2008) Mitochondrial DNA markers to identify commercial spiny lobster species (Panulirus spp.) from the Pacific coast of Mexico: an application on phyllosoma larvae. Fish Bull 106:204–212
Glaholt R, Seeb J (1992) Preliminary investigation into the origin of the spiny lobster, Panulirus argus (Latreille, 1804), population of Belize, Central America (Decapoda, Palinuridea). Crustaceana 62:159–165
Goldstein J, Matsuda H, Takenouchi T, Butler IV MJ (2008) The complete development of larval Caribbean spiny lobster Panulirus argus (Latreille, 1804) in culture. J Crustac Biol 28:306–327
Gopal K, Tolley KA, Groeneveld JC, Matthee CA (2006) Mitochondrial DNA variation in spiny lobster Palinurus delagoae suggests genetically structured populations in the south-western Indian Ocean. Mar Ecol Prog Ser 319:191–198
Grant WS, Waples RS (2000) Spatial and temporal scales of genetic variability in marine and anadromous species: implications for fisheries oceanography. In: Harrison PJ, Parsons TR (eds) Fisheries Oceanography: An Integrative Approach to Fisheries Ecology and Management. Blackwell Science, Oxford, pp 63–93
Groeneveld JC, Griffiths CL, Van Dalsen AP (2006) A new species of spiny lobster Palinurus barbarae (Decapoda, Palinuridae) from Walters Shoals on the Madagascar Ridge. Crustaceana 79:821–833
Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600
Harpending HC, Sherry ST, Rogers AR, Stoneking M (1993) Genetic structure of ancient human populations. Curr Anthr 34:483–496
Hately J, Sleeter TD (1993) A biochemical genetic investigation of spiny lobster (Panulirus argus) stock replenishment in Bermuda. Bull Mar Sci 53:993–1008
Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc Roy Soc Lond B 270:313–321
Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Nat Acad Sci USA 101:14812–14817
Hellberg ME, Burton RS, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Bull Mar Sci 70(Suppl):273–290
Inoue N, Watanabe H, Kojima S, Sekiguchi H (2007) Population structure of Japanese spiny lobster Panulirus japonicus inferred by nucleotide sequence analysis of mitochondrial COI gene. Fish Sci 73:550–556
IV ButlerMJ, Herrnkind WF (2000) Puerulus and juvenile ecology. In: Phillips BF, Kittaka J (eds) Spiny Lobsters: Fisheries and Culture, 2nd edn. Blackwell Scientific, Oxford, pp 276–301
Jensen J, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genetics 6:13
Ketmaier V, Argano R, Caccone A (2003) Phylogeography and molecular rates of subterranean aquatic Stenasellid Isopods with a peri-Tyrrhenian distribution. Mol Ecol 12:547–555
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
Lambeck K, Esat TM, Potter EK (2002) Links between climate and sea levels for the past three million years. Nature 419:199–206
Leis JM (2006) Are larvae of demersal fishes plankton or nekton? Adv Mar Biol 51(2006):57–141
Levin LA (2006) Recent progress in understanding larval dispersal: new directions and digressions. Integrative and Comparative Biology 46:282–297
Lipcius RN, Eggleston DB (2000) Ecology and Fishery Biology of Spiny Lobsters. In: Phillips BF, Kittaka J (eds) Spiny Lobsters: Fisheries and Culture, 2nd edn edn. Blackwell Scientific, Oxford, pp 1–41
Lipcius RN, Stockhausen WT, Eggleston DB, Marshall LS Jr, Hickey B (1997) Hydrodynamic decoupling of recruitment, habitat quality and adult abundance in the Caribbean spiny lobster: source–sink dynamics? Mar Freshw Res 48:807–816
Lipcius RN, Stockhausen WT, Eggleston DB (2001) Marine reserves for Caribbean spiny lobster: empirical evaluation and theoretical metapopulation recruitment dynamics. Mar Freshw Res 52:1589–1598
Lyons W (1980) Possible sources of Florida’s spiny lobster population. Proc Gulf Carib Fish Inst 33:253–266
Maddison D, Maddison WP (2002) MacClade: Analysis of phylogeny and character evolution. Sinauer Associates, Sunderland, MA
Marko PB (2004) ‘What’s larvae got to do with it?’ Disparate patterns of post-glacial population structure in two benthic marine gastropods with identical dispersal potential. Mol Ecol 13:597–611
McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654
McMillen-Jackson A, Bert TM (2004) Genetic diversity in the mtDNA control region and population structure in the pink shrimp Farfantepenaeus duorarum. J Crustac Biol 24:101–109
Naro-Maciel E, Becker JH, Lima EHSM, Marcovaldi MA, DeSalle R (2007) Testing dispersal hypotheses in foraging green sea turtles of Brazil. J Hered 98:29–39
Naylor E (2006) Orientation and navigation in coastal and estuarine zooplankton. Mar Freshw Behav Phys 39:13–24
Nei M (1987) Molecular Evolutionary Genetics, Columbia University Press, New York
Ogawa M, Oliveira GM, Sezaki K, Watabe S, Hashimoto K (1991) Genetic variations in three species of spiny lobsters, Panulirus argus, Panulirus laevicauda and Panulirus japonicus. Revta Investnes Mar, Habana 12:39–44
Ovenden J, Brasher DJ, White RWG (1992) Mitochondrial DNA analyses of the red rock lobster Jasus edwardsii supports an apparent absence of population subdivision throughout Australasia. Mar Biol 112:319–326
Palero F, Abello P, Macpherson E, Gristina M, Pascual M (2008) Phylogeography of the European spiny lobster (Palinurus elephas): Influence of current oceanographical features and historical processes. Mol Phylogenet Evol 48:708–717
Palero F, Crandall KA, Abello P, Macpherson E, Pascual M (2009) Phylogenetic relationships between spiny, slipper and coral lobsters (Crustacea, Decapoda, Achelata). Mol Phylogenet Evol 50:152–162
Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158
Palumbi S (2004) Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Ann Rev Env Res 29:31–68
Perez-Enriquez R, Vega A, Avila S, Sandoval JL (2001) Population genetics of red spiny lobster (Panulirus interruptus) along the Baja California Peninsula, Mexico. Mar Freshw Res 52:1541–1549
Pollock D (1990) Palaeoceanography and speciation in the spiny lobster genus Jasus. Bull Mar Sci 46:387–405
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818
Ptacek MB, Sarver SK, Childress MJ, Herrnkind WF (2001) Molecular phylogeny of the spiny lobster genus Panulirus (Decapoda: Palinuridae). Mar Freshw Res 52:1037–1047
Rach J, DeSalle R, Sarkar IN, Schierwater B, Hadrys H (2008) Character-based DNA barcoding allows discrimination of genera, species and populations in Odonata. Proc Roy Soc Lond B 275:237–247
Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100
Ratnasingham S, Hebert PD (2007) Bold: the barcode of life data system (http://www.barcodinglife.org). Mol Ecol Notes 7:355–364
Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283
Roberts CM (1997) Connectivity and management of Caribbean coral reefs. Science 278:1454–1457
Rozas J (2009) DNA sequence polymorphism analysis using DnaSP. Methods Mol Biol 537:337–350
Sarkar I, Thornton J, Planet PJ, Schierwater B, DeSalle R (2002) A systematic method for classification of novel homeoboxes. Mol Phyl Evol 24:388–399
Sarver S, Silberman JD, Walsh PJ (1998) Mitochondrial DNA sequence evidence supporting the recognition of two subspecies or species of the Florida spiny lobster Panulirus argus. J Crustac Biol 18:177–186
Sarver S, Wilson D, Walsh PJ (2000) The occurrence of the provisional Brazilian subspecies of spiny lobster—Panulirus argus westonii—in Florida waters. Fish Bull 98:870–873
Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089
Silberman JD, Sarver SK, Walsh PJ (1994a) Mitochondrial DNA variation and population structure in the spiny lobster, Panulirus argus. Mar Biol 120:601–608
Silberman J, Sarver SK, Walsh PJ (1994b) Mitochondrial DNA variation in seasonal cohorts of spiny lobster (Panulirus argus) postlarvae. Mol Mar Biotech 3:165–170
Sims HW, Ingle RM (1967) Caribbean recruitment of Florida’s spiny lobster population. Q J Fla Acad Sci 29:207–242
Steinke D, Vences M, Salzburger W, Meyer A (2005) TaxI—-a software for DNA barcoding using distance methods. Phil Trans Roy Soc Lond B: Biol Sci 360:1975–1980
Stockhausen WT, Lipcius RN (2001) Single large or several small marine reserves for the Caribbean spiny lobster? Mar Freshw Res 52:1605–1614
Stockhausen WT, Lipcius RN, Hickey BH (2000) Joint effects of larval dispersal, population regulation, marine reserve design, and exploitation on production and recruitment in the Caribbean spiny lobster. Bull Mar Sci 66:957–990
Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (and Other Methods). Sinauer associates, Sunderland, Massachusetts
Tajima F (1993) Simple methods for testing molecular clock hypothesis. Genetics 135:599–607
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109
R Development Core Team (2005) R: a language and environment for statistical computing, reference index version 2.2.1. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org
Tolley KA, Groeneveld J, Gopal K, Matthee CA (2005) Panmixia in spiny lobster, Palinurus gilchristi, supports a recent population expansion. Mar Ecol Prog Ser 297:225–231
Viñas J, Bremer JA, Pla C (2004) Phylogeography of the Atlantic bonito (Sarda sarda) in the northern Mediterranean: the combined effects of historical vicariance, population expansion, secondary invasion, and isolation by distance. Mol Phylog Evol 33:32–42
Waples RS (1987) A multispecies approach to the analysis of gene flow in marine shore fishes. Evolution 41:385–400
Warner RR, Cowen RK (2002) Local retention of production in marine populations: evidence, mechanisms and consequences. Bull Mar Sci 70(suppl): 245–249
Weersing K, Toonen RJ (2009) Population genetics, larval dispersal, and connectivity in marine systems. MEPS 393:1–12
Woodson CB, McManus MA (2007) Foraging behavior can influence dispersal of marine organisms. Limnol Oceanogr 52:2701–2709
Yamauchi M, Miya M, Nishida M (2002) Complete mitochondrial DNA sequence of the Japanese spiny lobster, Panulirus japonicus (Crustacea: Decapoda). Gene 295:89–96
Acknowledgments
For samples or unpublished data, we thank Kenny Broad, Kevin Buch, Seinen Chow, Alondra Diaz, Nariaki Inoue, Aurea Rodriguez, Shane K. Sarver, Hideo Sekiguchi, Jeffrey Silberman, Patrick J. Walsh, and K and B EZ Dive in Bimini. Craig Dahlgren, Elizabeth Hemond, Carrie Kappel, and other members of the Bahamas Biocomplexity Project provided additional field assistance. We thank the students funded through NSF’s Research Experience for Undergraduates program, Ballington Kinloch, Catherine Munsch, Anthony Petroso, Caroline Storer, and Matthew Winfield, for laboratory assistance, and Steve Palumbi and Tom Oliver for discussions about this research. We are grateful to Jeffrey Silverman for producing Fig. 1. We thank The Bahamas Department of Marine Resources, the Department of Environment and Coastal Resources in the Turks and Caicos Islands, and the Departamento de Recursos Naturales y Ambientales of Puerto Rico for providing research permits for our work, as well as the School for Field Studies in the Turks and Caicos. E.N.M., K.E.H., and D.R.B. were supported in part by an NSF Biocomplexity in the Environment grant (OCE-0119976) to D.R.B. Additional support was provided by NOAA Grant #NA05SEC4691002, as well as George Amato and the AMNH’s Center for Conservation Genetics, and Eleanor Sterling and the Center for Biodiversity and Conservation.
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Naro-Maciel, E., Reid, B., Holmes, K.E. et al. Mitochondrial DNA sequence variation in spiny lobsters: population expansion, panmixia, and divergence. Mar Biol 158, 2027–2041 (2011). https://doi.org/10.1007/s00227-011-1710-y
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DOI: https://doi.org/10.1007/s00227-011-1710-y