Skip to main content
SpringerLink
Log in

Population structure and genetic variation of lane snapper (Lutjanus synagris) in the northern Gulf of Mexico

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Lane snappers (Lutjanus synagris), sampled from eight localities in the northern Gulf of Mexico (Gulf) and one locality along the Atlantic coast of Florida, were assayed for allelic variation at 14 nuclear-encoded microsatellites and for sequence variation in a 590 base-pair fragment of the mitochondrially encoded ND-4 gene (mtDNA). Significant heterogeneity among the nine localities in both microsatellite allele and genotype distributions and mtDNA haplotype distributions was indicated by exact tests and by analysis of molecular variance (AMOVA). Exact tests between pairs of localities and spatial analysis of molecular variance (SAMOVA) for both microsatellites and mtDNA revealed two genetically distinct groups: a Western Group that included six localities from the northwestern and northcentral Gulf and an Eastern Group that included three localities, one from the west coast of Florida, one from the Florida Keys, and one from the east (Atlantic) coast of Florida. The between-groups component of molecular variance was significant for both microsatellites (ΦCT = 0.016, P = 0.009) and mtDNA (ΦCT = 0.208, P = 0.010). Exact tests between pairs of localities within each group and spatial autocorrelation analysis did not reveal genetic heterogeneity or an isolation-by-distance effect among localities within either group. MtDNA haplotype diversity was significantly less (P < 0.0001) in the Western Group than in the Eastern Group; microsatellite allelic richness and gene diversity also were significantly less in the Western Group (P = 0.015 and 0.013, respectively). The difference in genetic variability between the two groups may reflect reduced effective population size in the Western Group and/or asymmetric rates of genetic migration. The relative difference in variability between the two groups was substantially greater in mtDNA and may reflect one or more mtDNA selective sweeps; tests of neutrality of the mtDNA data were consistent with this possibility. Bayesian analysis of genetic demography indicated that both groups have experienced a historical decline in effective population size, with the decline being greater in the Western Group. Maximum-likelihood analysis of microsatellite data indicated significant asymmetry in average, long-term migration rates between the two groups, with roughly twofold greater migration from the Western Group to the Eastern Group. The difference in mtDNA variability and the order-of-magnitude difference in genetic divergence between mtDNA and microsatellites may reflect different demographic events affecting mtDNA disproportionately and/or a sexual and/or spatial bias in gene flow and dispersal. The spatial discontinuity among lane snappers in the region corresponds to a known zone of vicariance in other marine species. The evidence of two genetically distinct groupings (stocks) has implications for management of lane snapper resources in the northern Gulf.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allen GR (1985) Snappers of the world: an annotated catalogue of lutjanid species known to date. FAO Fish. Synopsis (125) vol 6, 208 p

  • Arevalo E, Davis S, Sites J Jr (1994) Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloporus grammicus complex (Phrynosomatidae) in Central Mexico. Syst Biol 43:387–418

    Article  Google Scholar 

  • Bagley MJ, Geller JB (1998) Characterization of microsatellite loci in vermillion snapper Rhomboplites aurorubens (Percoidei: Lutjanidae). Mol Ecol Notes 7:1089–1090

    CAS  Google Scholar 

  • Baughman JL (1950) Random notes on Texas fishes, part I. Texas J Sci 1:117–138

    Google Scholar 

  • Bazin E, Glémin S, Galtier N (2006) Population size does not influence mitochondrial genetic diversity in animals. Science 312:570–572

    Article  CAS  PubMed  Google Scholar 

  • Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond B 263:1619–1626

    Article  Google Scholar 

  • Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bert TM (1986) Speciation in western Atlantic stone crabs (genus Menippe): the role of geological processes and climatic events in the formation and distribution of species. Mar Biol 93:157–170

    Article  Google Scholar 

  • Bielawski JP, Gold JR (2002) Mutation patterns of mitochondrial H- and L-strand DNA in closely related cyprinid fishes. Genetics 161:1589–1597

    CAS  PubMed  PubMed Central  Google Scholar 

  • Birky CW, Fuerst P, Maruyama T (1989) Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics 121:613–627

    PubMed  Google Scholar 

  • Bortone SA, Williams JL (1986) Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (South Florida): gray, lane, mutton, and yellowtail snappers. Biol. Rep. 82(11.52) TR EL-82-4. Coastal Ecology Group, U.S. Army Corps of Engineers and National Coastal Ecosystems Team, U.S. Dept. Interior. Available at http://www.nwrc.usgs.gov/wdb/pub/species_profiles/82_11-052.pdf)

  • Brown-Gladden JG, Ferguson MM, Friesen MK, Clayton JW (1999) Population structure of North American beluga whales (Delphinapterus leucas) based on nuclear DNA microsatellite variation and contrasted with the population structure revealed by mitochondrial DNA variation. Mol Ecol 8:347–363

    Article  Google Scholar 

  • Buonaccorsi VP, Reece KS, Morgan LW, Graves JE (1999) Geographic distribution of molecular variance within the blue marlin (Makaira nigricans): a hierarchical analysis of allozyme, single-copy nuclear DNA, and mitochondrial DNA markers. Evolution 53:568–579

    CAS  PubMed  Google Scholar 

  • Cano JM, Mäkinen HS, Merilä J (2008) Genetic evidence for male-biased dispersal in the three-spined stickleback (Gasterosteus aculeatus). Mol Ecol 17:3234–3242

    Article  CAS  PubMed  Google Scholar 

  • Carvalho GR, Hauser L (1995) Molecular genetics and the stock concept in fisheries. In: Carvalho GR, Pitcher TJ (eds) Molecular genetics in fisheries. Chapman and Hall, London, pp 55–80

    Chapter  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  PubMed  Google Scholar 

  • Dahlberg MD (1970) Atlantic and Gulf menhadens, genus Brevoortia (Pisces: Clupeidae). Bull Florida State Mus 15:91–162

    Google Scholar 

  • Dowling TE, Minckley WL, Marsh PC, Goldstein ES (1996) Mitochondrial DNA variability in the endangered razorback sucker (Xyrauchen texanus): analysis of hatchery stocks and implications for captive propagation. Conserv Biol 10:120–127

    Article  Google Scholar 

  • Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581

    Article  CAS  PubMed  Google Scholar 

  • El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among population of the argan tree (Argania spinosa (L.) Skeels) endemic to Morocco. Theor Appl Genet 92:832–839

    Article  CAS  PubMed  Google Scholar 

  • Ferguson A, Taggart JB, Prodöhl PA, McMeel O, Thompson C, Stone C, McGinnity P, Hynes RA (1995) The application of molecular markers to the study and conservation of fish populations, with special reference to Salmo. J Fish Biol 47(Suppl A):103–126

    Article  CAS  Google Scholar 

  • FitzSimmons NN, Limpus CJ, Norman JA, Goldizen AR, Mille JD, Moritz C (1997) Philopatry of male marine turtles inferred from mitochondrial DNA markers. Proc Natl Acad Sci USA 94:8912–8917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking, and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fu Y-X, Li W-H (1993) Statistical tests of neutral mutations. Genetics 133:693–709

    CAS  PubMed  PubMed Central  Google Scholar 

  • FWRI (Fish and Wildlife Research Institute) (2006) Lane snapper, Lutjanus synagris. Florida Fish and Wildlife Conservation Commission. Available at http://research.myfwc.com/engine/download_redirection_process.asp?file=Lane_snapper.pdfandobjid=5284anddltype=article

  • Gemmell NJ, Metcalf VJ, Allendorf FW (2004) Mother’s curse: the effect of mtDNA on individual fitness and population viability. TREE 19:238–244

    PubMed  Google Scholar 

  • Gillespie JH (2000) Genetic drift in an infinite population. The pseudohitchhiking model. Genetics 155:909–919

    CAS  PubMed  PubMed Central  Google Scholar 

  • GMFMC (Gulf of Mexico Fishery Management Council) (2005) Final amendment 24 to the reef fish fishery management plan for reef fish resources in the Gulf of Mexico including environmental assessment. Regulatory impact review, and initial regulatory flexibility analysis. Available at http://www.gulfcouncil.org/Beta/GMFMCWeb/downloads/Amend24Final-105.pdf

  • Gold JR, Pak E, Richardson LR (2001) Microsatellite variation among red snapper (Lutjanus campechanus) from the Gulf of Mexico. Mar Biotechnol 3:293–304

    Article  CAS  Google Scholar 

  • Gold JR, Saillant E, Ebelt ND, Lem S (2009) Conservation genetics of gray snapper (Lutjanus griseus) in U.S. waters of the northern Gulf of Mexico and western Atlantic Ocean. Copeia 2009:277–286

    Article  Google Scholar 

  • Goudet J (1995) F-STAT, a computer program to calculate F-Statistics. J Hered 86:485–486

    Article  Google Scholar 

  • Graham WM (1998) First report of Carybdea alata var. grandis (Reynaud 1830) (Cnidaria: Cubozoa) from the Gulf of Mexico. Gulf Mexico Sci 1998:28–30

    Google Scholar 

  • Gulland JA (1965) Fish stock assessment: a manual of basic methods. Wiley, NY

    Google Scholar 

  • Guo S, Thompson E (1992) Performing the exact test of Hardy–Weinberg proportion from multiple alleles. Biometrics 48:361–372

    Article  CAS  PubMed  Google Scholar 

  • Heath DD, Buch C, Kelly J, Atagi DY (2002) Temporal change in genetic structure and effective population size in steelhead trout (Onchorynchus mykiss). Mol Ecol 11:197–214

    Article  CAS  PubMed  Google Scholar 

  • Herke SW, Foltz DW (2002) Phylogepgraphy of two squid (Loligo pealei and L. plei) in the Gulf of Mexico and northwestern Atlantic Ocean. Mar Biol 140:103–115

    Article  CAS  Google Scholar 

  • Hilborn R (1985) Apparent stock-recruitment relationships in mixed stock fisheries. Can J Fish Aquat Sci 42:718–723

    Article  Google Scholar 

  • Huh OK, Wiseman WJ, Rouse LJ (1981) Intrusion of Loop Current waters onto the West Florida continental shelf. J Geophys Res 86:4186–4192

    Article  Google Scholar 

  • Johnson DR, Perry HM, Graham WM (2004) Using nowcast model currents to explore transport of non-indigenous jellyfish into the Gulf of Mexico. Mar Ecol Prog Ser 305:139–146

    Article  Google Scholar 

  • Kauer MO, Dieringer D, Schlötterer C (2003) A microsatellite variability screen for positive selection associated with the “Out of Africa” habitat expansion of Drosophila melanogaster. Genetics 165:1137–1148

    CAS  PubMed  PubMed Central  Google Scholar 

  • Luckhurst BE, Dean JM, Reichert M (2000) Age, growth and reproduction of the lane snapper Lutjanus synagris (Pisces: Lutjanidae) at Bermuda. Mar Ecol Prog Ser 203:255–261

    Article  Google Scholar 

  • Manooch CS III, Mason DL (1984) Age, growth, and mortality of lane snapper from southern Florida. NE Gulf Sci 7:109–115

    Google Scholar 

  • McClure MR, McEachran JD (1992) Hybridization between Prionotus alatus and P. parapatus in the northern Gulf of Mexico. Copeia 1992:1039–1046

    Article  Google Scholar 

  • Meiklejohn CD, Montooth KL, Rand DM (2007) Positive and negative selection on the mitochondrial genome. Trends Genet 23:259–263

    Article  CAS  PubMed  Google Scholar 

  • Nowlin WD, McLellan HJ (1967) A characterization of the Gulf of Mexico waters in winter. J Mar Res 25:29–59

    Google Scholar 

  • Nunney L, Elam D (1994) Estimating the effective population size of conserved populations. Conserv Biol 8:175–184

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Ruibal M, Lindenmayer DB (2003) Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution 57:1182–1195

    Article  PubMed  Google Scholar 

  • Pruett CL, Saillant E, Gold JR (2005) Historical population demography of red snapper (Lutjanus campechanus) from the northern Gulf of mexico based on analysis of sequences of mitochondrial DNA. Mar Biol 147:593–602

    Article  CAS  Google Scholar 

  • Prugnolle F, de Meeus T (2002) Inferring sex-biased dispersal from population genetic tools: a review. Heredity 88:161–165

    Article  CAS  PubMed  Google Scholar 

  • Rand DM (2001) The units of selection on mitochondrial DNA. Annu Rev Ecol Syst 32:415–449

    Article  Google Scholar 

  • Rassmann K, Tautz D, Trillmich F, Gliddon C (1997) The microevolution of the Galápagos marine iguana Amblyrhynchus cristatus assessed by nuclear and mitochondrial genetic analysis. Mol Ecol 6:437–452

    Article  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) Genepop (version 2.1): Population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Article  Google Scholar 

  • Renshaw MA, Saillant E, Lem S, Berry P, Gold JR (2007) Microsatellite multiplex panels for genetic studies of grey snapper (Lutjanus griseus) and lane snapper (Lutjanus synagris). Fish Bull US 105:436–439

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  PubMed  Google Scholar 

  • Ricker WE (1975) Computation and interpretation of biological statistics of fish populations. Bull Fish Res Bd Canada 191:1–382

    Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messequer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Saillant E, Gold JR (2006) Population structure and variance effective size of red snapper (Lutjanus campechanus) in the northern Gulf of Mexico. Fish Bull US 104:136–148

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Lab Press, New York

    Google Scholar 

  • Schlötterer C (2002) A microsatellite-based multilocus screen for the identification of local selective sweep. Genetics 160:753–763

    PubMed  PubMed Central  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin Ver. 2.0: a software for population genetic data analysis. Genetics &Biometry Laboratory, University of Geneva, Geneva

    Google Scholar 

  • Sinclair M, Anthony VC, Iles TD, O’Boyle RN (1985) Stock assessment problems in Atlantic herring (Clupea harengus) in the northwest Atlantic. Can J Fish Aquat Sci 42:888–898

    Article  Google Scholar 

  • Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573

    Article  PubMed  Google Scholar 

  • SMS (Smithsonian Marine Station) (2007) Lutjanus synagris (lane snapper). Available at http://www.sms.si.edu/irlspec/Lutjan_synagr.htm

  • Stepien C (1995) Population genetic divergence and geographic patterns from DNA sequences: examples from marine and freshwater fishes. Am Fish Soc Symp 17:263–287

    Google Scholar 

  • Storz J, Beaumont MA (2002) Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution 56:154–166

    Article  CAS  PubMed  Google Scholar 

  • Templeton AR, Crandall KA, Sing F (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tester PA, Steidinger KA (1997) Gymnodinium breve red tide blooms: initiation, transport, and consequences of surface circulation. Limnol Oceanogr 42:1039–1051

    Article  Google Scholar 

  • van Oosterhout C, Hutchinson W, Wills D, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    CAS  PubMed  Google Scholar 

  • Wiseman WJ Jr, Dinnel SP (1988) Shelf current near the mouth of the Mississippi River. J Phys Oceanogr 18:1287–1291

    Article  Google Scholar 

Download references

Acknowledgments

We thank the crew of the RV Tommy Munro (Gulf Coast Research Laboratory, University of Southern Mississippi), the scientific team of the baitfish survey (Florida Fish and Wildlife Research Institute), E. Ault, K. Doncaster, M. Murphy, and M. Renshaw for assistance in sampling, E. Carson for assistance in generating Fig. 2, D. Portnoy for helpful comments on an early draft of the manuscript, and L. Causey for assistance with Fig. 3. Thanks also to C. Bradfield and M. Renshaw for assistance in the laboratory. Work was supported in part by the MARFIN Program of the U. S. Department of Commerce (Grant NA04-NMF-4330074), and in part by Texas AgriLIFE Research (Project H-6703). Views expressed in this paper are those of the authors and do not necessarily reflect views of the sponsors. This article is number 66 in the series ‘Genetic Studies in Marine Fishes’ and Contribution Number 165 of the Center for Biosystematics and Biodiversity at Texas A&M University.

Author information

Authors and Affiliations

  1. Center for Biosystematics and Biodiversity, Texas A&M University, College Station, TX, 77843-2258, USA

    S. Karlsson, E. Saillant & J. R. Gold

Authors
  1. S. Karlsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. Saillant
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. R. Gold
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. R. Gold.

Additional information

Communicated by M.I. Taylor.

Appendix

Appendix

See Tables 4 and 5.

Table 4 Summary statistics for 14 nuclear-encoded microsatellites and a 590 base-pair sequence of the mitochondrially encoded ND-4 gene for lane snapper (Lutjanus synagris) sampled from eight localities in the northern Gulf of Mexico and one locality along the east coast of Florida
Full size table
Table 5 Spatial distribution of mtDNA haplotypes among lane snapper (Lutjanus synagris) from eight localities in the Gulf of Mexico and one locality in the Western Atlantic Ocean
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Karlsson, S., Saillant, E. & Gold, J.R. Population structure and genetic variation of lane snapper (Lutjanus synagris) in the northern Gulf of Mexico. Mar Biol 156, 1841–1855 (2009). https://doi.org/10.1007/s00227-009-1217-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-009-1217-y

Keywords

Search

Navigation