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Marine Biology

, Volume 152, Issue 3, pp 645–655 | Cite as

Evidence for restricted gene flow over small spatial scales in a marine snapping shrimp Alpheus angulosus

  • Lauren M. Mathews
Research Article

Abstract

Despite the apparent absence of geographic barriers, connectivity among marine populations may be restricted by, for example, ecological or behavioral mechanisms. In such cases, populations may show genetic differentiation even over relatively small spatial scales. Here, mitochondrial sequence data from the cytochrome oxidase I (COI) gene and seven polymorphic microsatellite markers were used to investigate fine geographic scale population genetic structure in the snapping shrimp Alpheus angulosus, a member of the A. armillatus species complex, from collections in Florida, Jamaica, and Puerto Rico carried out from 1999 to 2005. The COI data showed a deep divergence that separated these samples into two mitochondrial clades, but this divergence was not supported by the microsatellite data. The COI data reflect past population divergence not reflected in extant population structure on the whole genome level. The microsatellite data also revealed evidence for moderate population structure between populations as close as ∼10 km, and no evidence for isolation by distance, as divergences between near populations were at least as strong as those between more broadly separated populations. Overall, these data suggest a role for restricted gene flow between populations, though the mechanisms that reduce gene flow in this taxon remain unknown.

Keywords

Pelagic Larva Chord Distance Pelagic Larval Duration Marine Taxon Phylogeographic Break 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

I am grateful to the Tropical Research Laboratory, the Discovery Bay Marine Laboratory, and the Bermuda Biological Station for Research for logistic support, and to the government of Bermuda (permit no. SP050601) and to the National Environment and Planning Agency of Jamaica for granting me permission to collect and export snapping shrimp. I thank L. Houle and W. Durgin for technical assistance in the laboratory.

References

  1. Avise JC (1992) Molecular population structure and the biogeographic history of a regional fauna: a case history with lessons for conservation biology. Oikos 63:62–76CrossRefGoogle Scholar
  2. Ball AO, Chapman RW (2003) Population genetic analysis of white shrimp, Litopenaeus setiferus, using microsatellite genetic markers. Mol Ecol 12:2319–2330CrossRefGoogle Scholar
  3. Baums IB, Miller MW, Hellberg ME (2005) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390CrossRefGoogle Scholar
  4. Bay LK, Crozier RH, Caley MJ (2006) The relationship between population genetic structure and pelagic larval duration in coral reef fishes on the Great Barrier Reef. Mar Biol 149:1247–1256CrossRefGoogle Scholar
  5. Bilodeau AL, Felder DL, Neigel JE (2005) Population structure at two geographic scales in the burrowing crustacean Callichirus islagrande (Decapoda, Thalassinidea): historical and contemporary barriers to planktonic dispersal. Evolution 59:2125–2138CrossRefGoogle Scholar
  6. Bowen BW, Bass AL, Muss A, Carlin J, Robertson DR (2006) Phylogeography of two Atlantic squirrelfishes (Family Holocentridae): exploring links between pelagic larval duration and population connectivity. Mar Biol 149:899–913CrossRefGoogle Scholar
  7. Briggs JC (1974) Marine zoogeography. McGraw-Hill, New YorkGoogle Scholar
  8. Bruce AJ (1999) Alpheus sorror, a new snapping shrimp cryptospecies from Sri Lanka (Crustacea: Decapoda: Alpheidae). Raffles Bull Zool 47:453–463Google Scholar
  9. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Am J Hum Genet 19:233–257PubMedPubMedCentralGoogle Scholar
  10. Chace FA (1972) The shrimps of the Smithsonian-Bredin Caribbean expeditions with a summary of the West Indian shallow water species (Crustacea: Decapoda: Natantia). Smithson Contrib Zool 98:1–179Google Scholar
  11. Chace FA (1988) The caridean shrimps (Crustacea: Decapoda) of the Albatross Philippine expedition, 1907–1910, Part 5: family Alpheidae. Smithson Contrib Zool 466:1–99Google Scholar
  12. Collin R (2001) The effects of mode of development on phylogeography and population structure of North Atlantic Crepidula (Gastropoda: Calyptraeidae). Mol Ecol 10:2249–2262CrossRefGoogle Scholar
  13. Cowen RK, Lwiza KMM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Science 287:857–859CrossRefGoogle Scholar
  14. Dennis GD, Smith-Vaniz WF, Colin PL, Hensley DA, McGhee MA (2005) Shore fishes from islands of the Mona Passage, Greater Antilles with comments on their zoogeography. Caribb J Sci 41:716–743Google Scholar
  15. Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169CrossRefGoogle Scholar
  16. Doherty PJ, Planes S, Mather P (1995) Gene flow and larval duration in seven species of fish from the Great Barrier Reef. Ecology 76:2373–2391CrossRefGoogle Scholar
  17. Duffy JE (2003) The ecology and evolution of eusociality in sponge-dwelling shrimp. In: Kikuchi T, Higashi S, Azuma N (eds) Genes, behaviors and evolution of social insects. Hokkaido University Press, Sapporo, pp 217–254Google Scholar
  18. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50CrossRefGoogle Scholar
  19. Felder DL, Staton JL (1994) Genetic differentiation in the Gulf-Atlantic species complexes of Sesarma and Uca (Crustacea: Decapoda: Brachyura). J Crustacean Biol 14:191–209CrossRefGoogle Scholar
  20. Garoia F, Guarniero I, Ramšak A, Ungaro N, Landi M, Piccinetti C, Mannini P, Tinti F (2004) Microsatellite DNA variation reveals high gene flow and panmictic populations in the Adriatic shared stocks of the European squid and cuttlefish (Cephalopoda). Heredity 93:166–174CrossRefGoogle Scholar
  21. Gutiérrez-Rodríguez C, Lasker HR (2004) Microsatellite variation reveals high levels of genetic variability and population structure in the gorgonian coral Pseudopterogorgia elisabethae across the Bahamas. Mol Ecol 13:2211–2221CrossRefGoogle Scholar
  22. Hedgecock D (1994) Does variance in reproductive success limit effective population size of marine organisms? In: Beaumont A (eds) Genetics and evolution of aquatic organisms. Chapman and Hall, London, pp 122–134Google Scholar
  23. Hoffman EA, Kolm N, Berglund A, Arguello JR, Jones AG (2005) Genetic structure in the coral-reef-associated Banggai cardinalfish, Pterapogon kauderni. Mol Ecol 14:1367–1375CrossRefGoogle Scholar
  24. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755CrossRefGoogle Scholar
  25. Jones GP, Milicich MJ, Emslie MJ, Lunow C (1999) Self-recruitment in a coral reef fish population. Nature 402:802–804CrossRefGoogle Scholar
  26. Knowlton N, Keller BD (1985) Two more species of alpheid shrimps associated with the Caribbean sea anemones Bartholomea annulata and Heteractis lucida. Bull Mar Sci 37:893–904Google Scholar
  27. Knowlton N, Weigt LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proc R Soc Ser B 265:2257–2263CrossRefGoogle Scholar
  28. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163CrossRefGoogle Scholar
  29. Lessios HA, Robertson DR (2006) Crossing the impassable: genetic connections in 20 reef fishes across the eastern Pacific barrier. Proc R Soc Ser B 273:2201–2208CrossRefGoogle Scholar
  30. Lessios HA, Kessing BD, Pearse JS (2001) Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55:955–975CrossRefGoogle Scholar
  31. Macdonald KS, Rios R, Duffy JE (2006) Biodiversity, host specificity, and dominance by eusocial species among sponge-dwelling alpheid shrimp on the Belize barrier reef. Divers Distrib 12:165–178CrossRefGoogle Scholar
  32. Maier E, Tollrian R, Rinkevich B, Nürnberger B (2005) Isolation by distance in the scleractinian coral Seriatopora hystrixfrom the Red Sea. Mar Biol 147:1109–1120CrossRefGoogle Scholar
  33. Mathews LM (2002) Tests of the mate-guarding hypothesis for social monogamy: does population density, sex ratio, or female synchrony affect behavior of male snapping shrimp (Alpheus angulatus)? Behav Ecol Sociobiol 51:426–432CrossRefGoogle Scholar
  34. Mathews LM (2006a) Cryptic biodiversity and phylogeographic patterns in a snapping shrimp species complex. Mol Ecol 15:4049–4063CrossRefGoogle Scholar
  35. Mathews LM (2006b) Variable microsatellite markers for a snapping shrimp (Alpheus armillatus) species complex. Mol Ecol Notes.  doi:10.1111/j.1471-8286.2006.01623.x CrossRefGoogle Scholar
  36. McClure MR (1995) Alpheus angulatus, a new species of snapping shrimp from the Gulf of Mexico and the northwestern Atlantic, with a redescription of A. heterochaelis Say 1818 (Decapoda: Caridea: Alpheidae). Proc Biol Soc Wash 108:84–97Google Scholar
  37. McClure MR (2002) Revised nomenclature of Alpheus angulatus McClure, 1995 (Decapoda: Caridea: Alpheidae). Proc Biol Soc Wash 115:368–370Google Scholar
  38. McClure MR, Greenbaum IF (1994) Biochemical variation in Alpheus (Decapoda, Caridea, Alpheidae) from the coast of Texas: evidence for cryptic species. Southwest Nat 39:63–66CrossRefGoogle Scholar
  39. McMillen-Jackson ALM, Bert TM (2003) Disparate patterns of population genetic structure and population history in two sympatric penaeid shrimp species (Farfantepenaeus aztecus and Litopenaeus setiferus) in the eastern United States. Mol Ecol 12:2895–2905CrossRefGoogle Scholar
  40. Moberg PE, Burton RS (2000) Genetic heterogeneity among adult and recruit red sea urchins, Strongylocentrotus franciscanus. Mar Biol 136:773–784CrossRefGoogle Scholar
  41. Muss A, Robertson DR, Stepien CA, Wirtz P, Bowen BW (2001) Phylogeography of Ophioblennius: the role of ocean currents and geography in reef fish evolution. Evolution 55:561–572CrossRefGoogle Scholar
  42. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  43. Nylander JAA (2004) MrModeltest (version 2.2). Program distributed by the author. Evolutionary Biology Centre, Uppsala UniversityGoogle Scholar
  44. Palumbi SR, Martin A, Romano S, McMillan WO, Stice L (1991) The simple fool’s guide to PCR: a collection of PCR protocols, version 2. University of Hawaii, HonoluluGoogle Scholar
  45. Papadopoulos LN, Peijnenburg KTCA, Luttikhuizen PC (2005) Phylogeography of the calanoid copepods Calanus helgolandicus and C. euxinus suggests Pleistocene divergences between Atlantic, Mediterranean, and Black Sea populations. Mar Biol 147:1353–1365CrossRefGoogle Scholar
  46. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  47. Raymond M, Rousset F (1995) Genepop (version 1.2)—population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  48. Richardson PL (2005) Caribbean Current and eddies as observed by surface drifters Deep Sea Res II 52:429–463CrossRefGoogle Scholar
  49. Rocha LA, Bass AL, Robertson DR, Bowen BW (2002) Adult habitat preferences, larval dispersal, and the comparative phylogeography of three Atlantic surgeonfishes (Teleostei: Acanthuridae). Mol Ecol 11:243–252CrossRefGoogle Scholar
  50. Rocha LA, Robertson DR, Roman J, Bowen BW (2005) Ecological speciation in tropical reef fishes. Proc R Soc Ser B 272:573–579CrossRefGoogle Scholar
  51. Riginos C, Victor BC (2001) BC Larval spatial distributions and other early life-history characteristics predict genetic differentiation in eastern Pacific blennioid fishes. Proc R Soc Ser B 268:1931–1936CrossRefGoogle Scholar
  52. Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629CrossRefGoogle Scholar
  53. Stamatis C, Triantafyllidis A, Moutou KA, Mamuris Z (2004) Mitochondrial DNA variation in northeast Atlantic and Mediterranean populations of Norway lobster, Nephrops norvegicus. Mol Ecol 13:1377–1390CrossRefGoogle Scholar
  54. Sunnocks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15:199–203CrossRefGoogle Scholar
  55. Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402:799–802CrossRefGoogle Scholar
  56. Swearer SE, Shima JS, Hellberg ME, Thorrold SR, Jones GP, Robertson DR, Morgan SG, Selkoe KA, Ruiz GM, Warner RR (2002) Evidence of self-recruitment in demersal marine populations. Bull Mar Sci S70:251–271Google Scholar
  57. Swofford DL (2003) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4.0B10. Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  58. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  59. Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109CrossRefGoogle Scholar
  60. Taylor MS, Hellberg ME (2006) Comparative phylogeography in a genus of coral reef fishes: biogeographic and genetic concordance in the Caribbean. Mol Ecol 15:695–707CrossRefGoogle Scholar
  61. Thompson AR, Thacker CE, Shaw EY (2005) Phylogeography of marine mutualists: parallel patterns of genetic structure between obligate goby and shrimp partners. Mol Ecol 14:3557–3572CrossRefGoogle Scholar
  62. Todd CD, Lambert WJ, Thorpe JP (1998) The genetic structure of intertidal populations of two species of nudibranch molluscs with planktotrophic and pelagic lecithotrophic larval stages: are pelagic larvae ‘‘for’’ dispersal? J Exp Mar Biol Ecol 228:1–28CrossRefGoogle Scholar
  63. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  64. Vitalis R, Dawson K, Boursot P, Belkhir K (2003) DetSel 1.0: a computer program to detect markers responding to selection. J Hered 94:429–431CrossRefGoogle Scholar
  65. Warner RR, Cowen RK (2002) Local retention of production in marine populations: Evidence, mechanisms, and consequences. Bull Mar Sci 70:245–249Google Scholar
  66. Watts PC, Thorpe JP (2006) Influence of contrasting larval developmental types upon the population-genetic structure of cheilostome bryozoans. Mar Biol 149:1093–1101CrossRefGoogle Scholar
  67. Wehrtmann IS, Albornoz L (2002) Evidence of different reproductive traits in the transisthmian sister species, Alpheus saxidomus and A. simus (Decapoda, Caridea, Alpheidae): description of the first postembryonic stage Mar Biol 140:605–612CrossRefGoogle Scholar
  68. Williams ST, Knowlton N (2001) Mitochondrial pseudogenes are pervasive and often insidious in the snapping shrimp genus Alpheus. Mol Biol Evol 18:1484–1493CrossRefGoogle Scholar
  69. Williams ST, Knowlton N, Weigt LA, Jara JA (2001) Evidence for three major clades within the snapping shrimp genus Alpheus inferred from nuclear and mitochondrial gene sequence data. Mol Phylogenet Evol 20:375–389CrossRefGoogle Scholar
  70. Williams ST, Jara J, Gomez E, Knowlton N (2002) The marine Indo-West Pacific break: contrasting the resolving power of mitochondrial and nuclear genes. Integr Comp Biol 42:941–952CrossRefGoogle Scholar
  71. Williamson DI (1969) Names of larvae in the Decapoda and Euphausiacea. Crustaceana 16:210–213CrossRefGoogle Scholar
  72. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159PubMedPubMedCentralGoogle Scholar
  73. Young AM, Torres C, Mack JE, Cunningham CW (2002) Morphological and genetic evidence for vicariance and refugium in Atlantic and Gulf of Mexico populations of the hermit crab Pagurus longicarpus. Mar Biol 140:1059–1066CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Department of BiologyWorcester Polytechnic InstituteWorcesterUSA

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