Skip to main content

Advertisement

SpringerLink
Log in

Small-scale genetic connectivity of bicolor damselfish (Stegastes partitus) recruits in Mexican Caribbean reefs

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

The analysis of genetic similarities among marine populations is a key method for use in connectivity studies intended to provide information for management strategies. The present study aimed at assessing the connectivity levels of subpopulations of bicolor damselfish (Stegastes partitus) recruits at a small scale (~200 km) among four reefs in the Mexican Caribbean. Samples were collected from 13 sites nested in two Marine Parks (Cozumel and Xcalak), one Biosphere Reserve (Chinchorro Bank) and one unprotected area (Mahahual). A total of 713 samples were genetically characterized by means of seven microsatellite DNA markers and were analyzed on a hierarchical basis. A strong genetic structure was detected among sites with a weak but significant genetic structure among reefs, the combination of which has not been reported in previous studies. These results appear to be related to a “sweepstake-chance effect” combined with oceanographic factors. An isolation by distance test, in addition to a hierarchical Bayesian method, revealed that neither distance among sites and reefs nor any of 10 environmental factors tested could be used to explain the genetic differences observed. The results suggest that conservation strategies for S. partitus based on local scales are likely to be effective.

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

References

  • Almada-Villela PC, Sale PF, Gold-Bouchot G, Kjerfve B (2003) Manual of methods for the MBRS synoptic monitoring program. Selected methods for monitoring physical and biological parameters for use in the Mesoamerican region. Mesoamerican Barrier Reef Systems project (MBRS), Belize City

  • Almany GR, Berumen ML, Thorrold SR, Planes S, Jones GP (2007) Local replenishment of coral reef fish populations in a marine reserve. Science 316:742–744

    Article  CAS  PubMed  Google Scholar 

  • Arias-González JE, Legendre P, Rodríguez-Zaragoza FA (2008) Scaling up beta diversity on Caribbean coral reefs. J Exp Mar Biol Ecol 366:28–36

    Article  Google Scholar 

  • Arnaud-Haond S, Vonau V, Rouxel C, Bonhomme F, Prou J, Goyard E, Boudry P (2008) Genetic structure at different spatial scales in the pearl oyster (Pinctada margaritifera cumingii) in French Polynesian lagoons: beware of sampling strategy and genetic patchiness. Mar Biol 155:147–157

    Article  Google Scholar 

  • Aronson RB, Edmunds PJ, Precht WF, Swanson DW, Levitan DR (1994) Large-scale, long-term monitoring of Caribbean coral reefs: simple, quick, inexpensive techniques. Atoll Res Bull 421:1–19

    Google Scholar 

  • Bekkevold D, André C, Dahlgren TG, Clausen LAW, Torstensen E, Mosegaard H, Carvalho GR, Christensen TB, Norlinder E, Ruzzante DE (2005) Environmental correlates of population differentiation in Atlantic herring. Evolution 59:2656–2668

    PubMed  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) Genetix 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier France. http://www.genetix.univ-montp2.fr/genetix/genetix.htm

  • Bell LJ, Moyer JT, Numachi K (1982) Morphological and genetic variation in Japanese populations of the anemonefish Amphiprion clarkii. Mar Biol 72:99–108

    Article  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. The Annals of Statistics 29:1165–1188

    Article  Google Scholar 

  • Beukers JS, Jones GP (1997) Habitat complexity modifies the impact of piscivores on a coral reef fish population. Oecologia 114:50–59

    Article  Google Scholar 

  • Bohonak AJ (2002) IBD (isolation by distance): a program for analyses of isolation by distance. J Hered 93:153–154. http://www.bio.sdsu.edu/pub/andy/IBD.html

    Google Scholar 

  • Bryja J, Charbonnel N, Berthier K, Galan M, Cosson JF (2007) Density-related changes in selection pattern for major histocompatibility complex genes in fluctuating populations of voles. Mol Ecol 16:5084–5097

    Article  CAS  PubMed  Google Scholar 

  • Cervigón F (1993) Los peces marinos de Venezuela. Vol 2. Fundación científica Los Roques, Caracas

    Google Scholar 

  • Cetina P, Candela J, Sheinbaum J, Ochoa J, Badan A (2006) Circulation along the Mexican Caribbean coast. J Geophys Res 111:C08021. doi:10.1029/2005JC003056

  • Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631. http://www.ensam.inra.fr/URLB/

  • Cowen RK, Castro LR (1994) Relation of coral reef fish larval distributions to island scale circulation around Barbados, West Indies. Bull Mar Sci 54:228–244

    Google Scholar 

  • Cowen RK, Sponaugle S (2009) Laval dispersal and marine population connectivity. Annu Rev Mar Sci 1:446–466

    Article  Google Scholar 

  • Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527

    Article  CAS  PubMed  Google Scholar 

  • Cowen RK, Lwiza KMM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Science 287:857–859

    Article  CAS  PubMed  Google Scholar 

  • Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504–509

    Article  CAS  PubMed  Google Scholar 

  • Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J Royal Stat Soc. Series B (Methodological) 39:1–38

    Google Scholar 

  • 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. http://anthro.unige.ch/software/arlequin/

  • Fauvelot C, Planes S (2002) Understanding origins of present-day genetic structure in marine fish: biologically or historically driven patterns? Mar Biol 141:773–788

    Article  Google Scholar 

  • Foll M, Gaggiotti O (2006) Identifying the environmental factors that determine the genetic structure of populations. Genetics 174:875–891. http://www-leca.ujf-grenoble.fr/logiciels.htm

    Google Scholar 

  • Frisch AJ, Ulstrup KE, Hobbs JA (2007) The effects of clove oil on coral: an experimental evaluation using Pocillopora damicornis (Linnaeus). J Exp Mar Biol Ecol 345:101–109

    Article  CAS  Google Scholar 

  • Gaggiotti OE, Bekkevold D, Jørgensen HBH, Foll M, Carvalho GR, Andre C, Ruzzante DE (2009) Disentangling the effects of evolutionary, demographic, and environmental factors influencing genetic structure of natural populations: Atlantic herring as a case study. Evolution 63:2939–2951

    Article  PubMed  Google Scholar 

  • Grimaldi MC, Crouau-Roy B (1997) Microsatellite allelic homoplasy due to variable flanking sequences. J Mol Evol 44:336–340

    Article  CAS  PubMed  Google Scholar 

  • Haney RA, Silliman BR, Rand DM (2007) A multi-locus assessment of connectivity and historical demography in the bluehead wrasse (Thalassoma bifasciatum). Heredity 98:294–302

    Article  CAS  PubMed  Google Scholar 

  • Hedgecock D (1994) Does variance in reproductive success limit effective population size of marine organisms? In: Beaumont A (ed) Genetics and evolution of aquatic organisms. Chapman and Hall, London, pp 122–134

    Google Scholar 

  • Hedgecock D, Barber PH, Edmands S (2007) Genetic approaches to measuring connectivity. Oceanography 20:70–79

    Google Scholar 

  • Hepburn RI, Sale PF, Dixon B, Heath DD (2009) Genetic structure of juvenile cohorts of bicolor damselfish (Stegastes partitus) along the Mesoamerican barrier reef: chaos through time. Coral Reefs 28:277–288

    Article  Google Scholar 

  • Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263

    Article  Google Scholar 

  • Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314. http://www.r-project.org

  • Jones GP, Planes S, Thorrold SR (2005) Coral reef fish larvae settle close to home. Curr Biol 15:1314–1318

    Article  CAS  PubMed  Google Scholar 

  • Jones GP, Milicich MJ, Emslie MJ, Lunow C (1999) Self-recruitment in a coral reef fish population. Nature 402:802–804

    Article  CAS  Google Scholar 

  • Jones GP, Almany GR, Russ GR, Sale PF, Steneck RS, van Oppen MJH, Willis BL (2009) Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28:307–325

    Article  Google Scholar 

  • Jones ME, Barber PH (2005) Characterization of microsatellite loci for the detection of temporal genetic shifts within a single cohort of the brown demoiselle, Neopomacentrus filamentosus. Mol Ecol Notes 5:834–836

    Article  CAS  Google Scholar 

  • Jordán E, Martin E (1987) Chinchorro: morphology and composition of a Caribbean atoll. Atoll Res Bull 310:1–27

    Google Scholar 

  • Jordan MA, Snell HL (2008) Historical fragmentation of islands and genetic drift in populations of Galápagos lava lizards (Microlophus albemarlensis complex). Mol Ecol 17:1224–1237

    Article  CAS  PubMed  Google Scholar 

  • Jørgensen HBH, Hansen MM, Bekkevold D, Ruzzante DE, Loeschcke V (2005) Marine landscapes and population genetic structure of herring (Clupea harengus L.) in the Baltic Sea. Mol Ecol 14:3219–3234

    Article  PubMed  Google Scholar 

  • Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv Genet 5:539–543

    Article  CAS  Google Scholar 

  • Kalinowski ST (2005) HP-Rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189. http://www.montana.edu/kalinowski/Software/HPRare.htm

  • Kittlein MJ, Gaggiotti OE (2008) Interactions between environmental factors can hide isolation by distance patterns: a case study of Ctenomys rionegrensis in Uruguay. Proc R Soc B 275:2633–2638

    Article  PubMed  Google Scholar 

  • Lacson JM (1992) Minimal genetic variation among samples of six species of coral reef fishes collected at La Parguera, Puerto Rico, and Discovery Bay, Jamaica. Mar Biol 112:327–331

    Article  Google Scholar 

  • Lacson JM, Morizot DC (1991) Temporal genetic variation in subpopulations of bicolor damselfish (Stegastes partitus) inhabiting coral reefs in the Florida Keys. Mar Biol 110:353–357

    Article  Google Scholar 

  • Lacson JM, Riccardi VM, Calhoun SW, Morizot DC (1989) Genetic differentiation of bicolor damselfish (Eupomacentrus partitus) populations in the Florida Keys. Mar Biol 103:445–451

    Article  Google Scholar 

  • Leis JM, McCormick MI (2002) The biology, behavior, and ecology of the pelagic, larval stage of coral reef fishes. In: Sale PF (ed) Coral reef fishes. Dynamics and diversity in a complex ecosystem. Academic Press, San Diego, pp 171–199

    Google Scholar 

  • Lesser MP (2004) Experimental biology of coral reef ecosystems. J Exp Mar Biol Ecol 300:217–252

    Article  Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283–292

    Article  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed  Google Scholar 

  • Nemeth RS (1998) The effect of natural variation in substrate architecture on the survival of juvenile bicolor damselfish. Environ Biol Fish 53:129–141

    Article  Google Scholar 

  • Ospina-Guerrero SP, Landinez-García RM, Rodríguez-Castro DJ, Arango R, Márquez E (2008) Genetic connectivity of Stegastes partitus in the South Caribbean evidenced by microsatellite analysis. Cienc Mar 34:155–163

    Google Scholar 

  • Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572

    Article  Google Scholar 

  • Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158

    Article  Google Scholar 

  • Pandolfi JM (2002) Coral community dynamics at multiple scales. Coral Reefs 21:13–23

    Google Scholar 

  • Paris CB, Cowen RK (2004) Direct evidence of a biophysical retention mechanism for coral reef fish larvae. Limnol Oceanogr 49:1964–1979

    Article  Google Scholar 

  • Planes S (1993) Genetic differentiation in relation to restricted larval dispersal of the convict surgeonfish Acanthurus triostegus in French Polynesia. Mar Ecol Prog Ser 98:237–246

    Article  Google Scholar 

  • Planes S, Bonhomme F, Galzin R (1993) Genetic structure of Dascyllus aruanus populations in French Polynesia. Mar Biol 117:665–674

    Article  Google Scholar 

  • Planes S, Parroni M, Chauvet C (1998) Evidence of limited gene flow in three species of coral reef fishes in the lagoon of New Caledonia. Mar Biol 130:361–368

    Article  Google Scholar 

  • Planes S, Jones GP, Thorrold SR (2009) Larval dispersal connects fish populations in a network of marine protected areas. Proc Natl Acad Sci USA 106:5693–5697

    Article  CAS  PubMed  Google Scholar 

  • Purcell JFH, Cowen RK, Hughes CR, Williams DA (2006) Weak genetic structure indicates strong dispersal limits: a tale of two coral reef fish. Proc R Soc B 273:1483–1490

    Article  CAS  PubMed  Google Scholar 

  • Purcell JFH, Cowen RK, Hughes CR, Williams DA (2009) Population structure in a common Caribbean coral-reef fish: implications for larval dispersal and early life-history traits. J Fish Biol 74:403–417

    Article  CAS  PubMed  Google Scholar 

  • Roberts CM (1997) Connectivity and management of Caribbean coral reefs. Science 278:1454–1457

    Article  CAS  PubMed  Google Scholar 

  • Robertson DR, Green DG, Victor BC (1988) Temporal coupling of production and recruitment of larvae of a Caribbean reef fish. Ecology 69:370–381

    Article  Google Scholar 

  • Rodríguez-Zaragoza FA, Arias-González JE (2008) Additive diversity partitioning of reef fishes across multiple spatial scales. Caribb J Sci 44:90–101

    Google Scholar 

  • Rousset F (2004) Genetic structure and selection in subdivided populations. Princeton University, Princeton

    Google Scholar 

  • Ruiz-Zárate MA, Arias-González JE (2004) Spatial study of juvenile corals in the Northern region of the Mesoamerican Barrier Reef System (MBRS). Coral Reefs 23:584–594

    Google Scholar 

  • Sale PF (2004) Connectivity, recruitment variation, and the structure of reef fish communities. Integr Comp Biol 44:390–399

    Article  Google Scholar 

  • Sale PF, Guy JA, Steel WJ (1994) Ecological structure of assemblages of coral reef fishes on isolated patch reefs. Oecologia 98:83–99

    Article  Google Scholar 

  • Selkoe KA, Gaines SD, Caselle JE, Warner RR (2006) Current shifts and kin aggregation explain genetic patchiness in fish recruits. Ecology 87:3082–3094

    Article  PubMed  Google Scholar 

  • Shulman MJ (1998) What can population genetics tell us about dispersal and biogeographic history of coral-reef fishes? Aust J Ecol 23:216–225

    Article  Google Scholar 

  • Shulman MJ, Bermingham E (1995) Early life histories, ocean currents, and the population genetics of Caribbean reef fishes. Evolution 49:897–910

    Article  Google Scholar 

  • Soto I, Andréfouët S, Hu C, Muller-Karger FE, Wall CC, Sheng J, Hatcher BG (2009) Physical connectivity in the Mesoamerican Barrier Reef System inferred from 9 years of ocean color observations. Coral Reefs 28:415–425

    Article  Google Scholar 

  • Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402:799–802

    Article  CAS  Google Scholar 

  • Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109

    Article  CAS  PubMed  Google Scholar 

  • Thériault V, Bernatchez L, Dodson JJ (2007) Mating system and individual reproductive success of sympatric anadromus and resident brook charr, Salvelinus fontinalis, under natural conditions. Behav Ecol Sociobiol 62:51–65

    Article  Google Scholar 

  • Thiessen RJ, Heath DD (2007) Characterization of one trinucleotide and six dinucleotide microsatellite markers in bicolor damselfish, Stegastes partitus, a common coral reef fish. Conserv Genet 8:983–985

    Article  CAS  Google Scholar 

  • Thioulouse J, Chessel D, Dolédec S, Olivier JM (1997) ADE-4: a multivariate analysis and graphical display software. Statistics and Computing 7:75–83

    Article  Google Scholar 

  • Thorrold SR, Jones GP, Hellberg ME, Burton RS, Swearer SE, Neigel JE, Morgan SG, Warner RR (2002) Quantifying larval retention and connectivity in marine populations with artificial and natural markers. Bull Mar Sci 70:291–308

    Google Scholar 

  • Turner TF, Wares JP, Gold JR (2002) Genetic effective size is three orders of magnitude smaller than adult census size in an abundant, estuarine-dependent marine fish (Sciaenops ocellatus). Genetics 162:1329–1339

    PubMed  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Willis DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535-538. http://www.microchecker.hull.ac.uk

    Google Scholar 

  • Weir BS (1996) Genetic data analysis II: methods for discrete population genetic data. Sinauer Associates, Sunderland

    Google Scholar 

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

    Article  Google Scholar 

  • Williams DA, Purcell J, Hughes CR, Cowen RK (2003) Polymorphic microsatellite loci for population studies of the bicolor damselfish, Stegastes partitus (Pomacentridae). Mol Ecol Notes 3:547–549

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This project was supported by Mexican Secretaría de Educación Pública (SEP) and Consejo Nacional de Ciencia y Tecnología (CONACyT) funds. The first author also thanks CONACyT for the PhD scholarship and the World Wildlife Fund (WWF, Russell E. Train Education for Nature Program) for the grant. We thank the Mexican Protected Marine Areas (Chinchorro Bank Biosphere Reserve, Cozumel and Xcalak Marine Parks) for their assistance in the field work and members of the LEEAC laboratory for their help in sample collection. We thank José H. Lara Arenas, Paul Barber, Elizabeth Jones, and Margarita Aguilar Espinosa for advice, discussion, and technical help. Thanks also to the three anonymous reviewers for improving the manuscript.

Author information

Authors and Affiliations

  1. Laboratorio de Ecología de Ecosistemas de Arrecifes Coralinos, Departamento de Recursos del Mar, Centro de Investigación y de Estudios Avanzados del I.P.N.-Unidad Mérida, Ant. Carr. a Progreso km 6, A.P. 73, Cordemex, 97310, Mérida, Yucatán, México

    C. A. Villegas-Sánchez & J. E. Arias-González

  2. Unidad de Bioquímica y Biología Molecular de Plantas, Centro de Investigación Científica de Yucatán, A.C., Calle 43 No. 130, Col. Chuburná de Hidalgo, 97200, Mérida, Yucatán, México

    R. Rivera-Madrid

Authors
  1. C. A. Villegas-Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Rivera-Madrid
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. E. Arias-González
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. E. Arias-González.

Additional information

Communicated by Biology Editor Prof. Philip Munday

Electronic supplementary material

Below is the link to the electronic supplementary material.

(DOC 213 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Villegas-Sánchez, C.A., Rivera-Madrid, R. & Arias-González, J.E. Small-scale genetic connectivity of bicolor damselfish (Stegastes partitus) recruits in Mexican Caribbean reefs. Coral Reefs 29, 1023–1033 (2010). https://doi.org/10.1007/s00338-010-0643-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-010-0643-0

Keywords

Search

Navigation