Conservation Genetics

, Volume 16, Issue 4, pp 811–822 | Cite as

Incorporating historical and ecological genetic data for leopard grouper (Mycteroperca rosacea) into marine reserve design in the Gulf of California

  • Alexis M. Jackson
  • Adrian Munguía-Vega
  • Ricardo Beldade
  • Brad E. Erisman
  • Giacomo Bernardi
Research Article


Effective design of marine reserves for use in fisheries management and conservation requires a clear understanding of patterns of larval transport and sink-source dynamics between populations, as well as a clear understanding of population demography. Mitochondrial and nuclear markers were analyzed to investigate potential mechanisms impacting connectivity among and the demographic history of subpopulations of a commercially important species in the Gulf of California, the leopard grouper (Mycteroperca rosacea). Demographic history and connectivity analyses included a coalescent analysis, estimating neutrality indices, estimating global and pairwise F’ST, ΦST, or G’’ST, and a priori methodologies to identify genetically distinct units and barriers to dispersal. Average, long-term connectivity between geographic regions in the Gulf was also estimated. Divergence of mitochondrial lineages of leopard grouper dated to the late Pleistocene, with deep-water islands serving as demographically stable populations that may have acted as sources for new populations during periods of climate variability. Additionally, we observed genetically distinct units of leopard grouper in the Gulf, particularly between peninsular and mainland sites, as well as asymmetrical migration between the northern and central Gulf. Observed patterns of genetic differentiation are likely attributed to complex asymmetrical oceanographic currents and local larval retention. Based on our genetic findings and current fishing pressure in certain regions, we recommend implementing small, upstream no-take zones in the areas east of Isla Ángel de la Guarda, around Isla San Lorenzo and Isla San Esteban, and north of Isla Tiburón, that would enhance connectivity among subpopulations, preserve sites with high genetic diversity, and benefit fisheries downstream of these sites.


Leopard grouper Mycteroperca rosacea Gulf of California Connectivity Conservation genetics Marine reserves Fisheries management 



Sample collection and lab work was funded by National Geographic (Grant #8928-11), The David and Lucile Foundation (Grant #2008-32210), a UC-HBCU Initiative Grant, a Mia J. Tegner memorial research Grant, Ecology Project International, CenTread, the Dr. Earl H. Myers and Ethel M. Myers Oceanographic and Marine Biology Trust, FCT (SFRH/BPD/26901/2006) and the Friends of Long Marine Lab. We would like to acknowledge Peggy Turk Boyer, Caroline Downton, Jorge Torre, Tad Pfister, Rene Loiaza, Ivan Martinez, Angeles Cruz, Mario Rojo, Kimberly Tenggardjaja, Eva Salas, Gary Longo, Emmett Ziegler and Ana Liedke for their logistical assistance and assistance with acquiring samples. Scientific collection permits were acquired from SAGARPA (No. DGOPA.09151.260809.2885 and DAPA/2/020511/01197). This is a scientific contribution to the PANGAS project (Pesca Artesanal del Norte Golfo de California—Ambiente y Sociedad).

Supplementary material

10592_2015_702_MOESM1_ESM.doc (349 kb)
Supplementary material 1 (DOC 349 kb)


  1. Aburto-Oropeza O, Sala E, Paredes G, Mendoza A, Ballesteros E (2007) Predictability of reef fish recruitment in a highly variable nursery habitat. Ecology 88(9):2220–2228PubMedCrossRefGoogle Scholar
  2. Alcala AC, Russ GR (1990) A direct test of the effects of protective management on abundance and yield of tropical marine resources. J Conseil 47(1):40–47CrossRefGoogle Scholar
  3. Avise JC (2004) Molecular markers, natural history and evolution. Sinauer Associates, SunderlandGoogle Scholar
  4. Beerli P, Felsenstein J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152(2):763–773PubMedCentralPubMedGoogle Scholar
  5. Beldade R, Jackson AM, Cudney-Bueno R, Raimondi PT, Bernardi G (2014) Genetic structure among spawning aggregations of the gulf coney Hyporthodus acanthistius. Mar Ecol Prog Ser 499:193–201CrossRefGoogle Scholar
  6. Bernardi G, Findley L, Rocha-Olivares A (2003) Vicariance and dispersal across Baja California in disjunct marine fish populations. Evolution 57(7):1599–1609PubMedCrossRefGoogle Scholar
  7. Burgess SC, Nickols KJ, Griesemer CD, Barnett LAK, Dedrick AG, Satterhwaite EV, Yamane L, Morgan SG, White JW, Botsford LW (2013) Beyond connectivity: how empirical methods can quantify population persistence to improve marine protected area design. Ecol Appl 24:257–270CrossRefGoogle Scholar
  8. Campana MG, Hunt HV, Jones H, White J (2011) Corrsieve: software for summarizing and evaluating structure output. Mol Ecol Resour 11:349–352PubMedCrossRefGoogle Scholar
  9. Carvajal MA, Ezcurra E, Robles A (2004) The Gulf of California: natural resource concerns and the pursuit of a vision. In: Glover K, Earle S (eds) Defying ocean’s end. An agenda for action. Island Press, Washington, pp 105–124Google Scholar
  10. Cinti A, Shaw W, Cudney-Bueno R, Rojo M (2009) The unintended consequences of formal fisheries policies: social disparities and resource overuse in a major fishing community in the Gulf of California. Mexico. Marine Policy 34(2):328–339CrossRefGoogle Scholar
  11. Cisneros-Mata MA (2010) The importance of fisheries in the Gulf of California and ecosystem-based sustainable co-management for conservation. In: Brusca RC (ed) The Gulf of California biodiversity and conservation. University of Arizona Press and the Arizona-Sonora Desert Museum, Tuscon, pp 119–134Google Scholar
  12. Colin PL, Shapiro DY, Weiler D (1987) Aspects of the reproduction of 2 groupers, Epinephelus guttatus and E.striatus in the West Indies. Bull Mar Sci 40(2):220–230Google Scholar
  13. Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. In: Annual review of marine science, vol 1. Annual Review of marine science. Annual Reviews, Palo Alto, pp 443–466Google Scholar
  14. Craig MT, Graham RT, Torres RA, Hyde JR, Freitas MO, Ferreira BP, Hostim-Silva M, Gerhardinger LC, Bertoncini AA, Robertson DR (2009) How many species of goliath grouper are there? Cryptic genetic divergence in a threatened marine fish and the resurrection of a geopolitical species. Endanger Species Res 7(3):167–174CrossRefGoogle Scholar
  15. Diaz-Uribe JG, Elorduy-Garay JF, Gonzalez-Valdovinos MT (2001) Age and growth of the leopard grouper, Mycteroperca rosacea, in the southern Gulf of California, Mexico. Pac Sci 55(2):171–182CrossRefGoogle Scholar
  16. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29(8):1969–1973PubMedCentralPubMedCrossRefGoogle Scholar
  17. Erisman BE, Buckhorn ML, Hastings PA (2007) Spawning patterns in the leopard grouper, Mycteroperca rosacea, in comparison with other aggregating groupers. Mar Biol (Berlin) 151(5):1849–1861CrossRefGoogle Scholar
  18. Erisman B, Mascarenas I, Paredes G, de Mitcheson YS, Aburto-Oropeza O, Hastings P (2010) Seasonal, annual, and long-term trends in commercial fisheries for aggregating reef fishes in the Gulf of California, Mexico. Fish Res 106(3):279–288CrossRefGoogle Scholar
  19. 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(2):479–491PubMedCentralPubMedGoogle Scholar
  20. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50Google Scholar
  21. Ezcurra E (2002) Ecological Conservation. In: Case TJ, Cody ML, Ezcurra E (eds) A new island biogeography of the Sea of Cortés. Oxford Press, New York, pp 417–444Google Scholar
  22. Fraser CI, Thiel M, Spencer HG, Waters JM (2010) Contemporary habitat discontinuity and historic glacial ice drive genetic divergence in Chilean kelp. Bmc Evol Biol 10:203PubMedCentralPubMedCrossRefGoogle Scholar
  23. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147(2):915–925PubMedCentralPubMedGoogle Scholar
  24. Gaines SD, White C, Carr MH, Palumbi SR (2010) Designing marine reserve networks for both conservation and fisheries management. Proc Natl Acad Sci USA 107:18286–18293PubMedCentralPubMedCrossRefGoogle Scholar
  25. Halpern BS, Warner RR (2002) Marine reserves have rapid and lasting effects. Ecol Lett 5(3):361–366CrossRefGoogle Scholar
  26. Hartl DL, Clark AG (2007) Principles of population genetics, 4th edn. Sinauer Associates, SunderlandGoogle Scholar
  27. Hedgecock D, Barber PH, Edmands S (2007) Genetic approaches to measuring connectivity. Oceanography 20(3):70–79CrossRefGoogle Scholar
  28. Hurtado LA, Mateos M, Santamaria CA (2010) Phylogeography of supralittoral rocky intertidal Ligia Isopods in the Pacific region from Central California to Central Mexico. PLoS ONE 5(7):1–13CrossRefGoogle Scholar
  29. Iacchei M, Ben-Horin T, Selkoe KA, Bird CE, Garcia-Rodríguez FJ, Toonen RJ (2013) Combined analyses of kinship and FST suggest potential drivers of chaotic genetic patchiness in high gene-flow populations. Mol Ecol 22:3476–3494PubMedCentralPubMedCrossRefGoogle Scholar
  30. Jackson AM, Munguía-Vega A, Lain AS, Stokes SA, Williams AJ, Bernardi G (2013) Isolation and characterization of fifteen microsatellite loci in Leopard grouper (Mycteroperca rosacea) via 454 pyrosequencing. Conserv Genet Resour 1:185–187Google Scholar
  31. Johansson ML, Banks MA, Glunt KD, Hassel-Finnegan HM, Buonaccorsi VP (2008) Influence of habitat discontinuity, geographical distance, and oceanography on fine-scale population genetic structure of copper rockfish (Sebastes caurinus). Mol Ecol 17(13):3051–3061PubMedCrossRefGoogle Scholar
  32. Levin LA (2006) Recent progress in understanding larval dispersal: new directions and digressions. Integr Comp Biol 46(3):282–297PubMedCrossRefGoogle Scholar
  33. Lluch-Cota SE, Aragon-Noriega EA, Arreguin-Sanchez F, Aurioles-Gamboa D, Bautista-Romero JJ, Brusca RC, Cervantes-Duarte R, Cortes-Altamirano R, Del-Monte-Luna P, Esquivel-Herrera A, Fernandez G, Hendrickx ME, Hernandez-Vazquez S, Herrera-Cervantes H, Kahru M, Lavin M, Lluch-Belda D, Lluch-Cota DB, Lopez-Martinez J, Marinone SG, Nevarez-Martinez MO, Ortega-Garcia S, Palacios-Castro E, Pares-Sierra A, Ponce-Diaz G, Ramirez-Rodriguez M, Salinas-Zavala CA, Schwartzlose RA, Sierra-Beltran AP (2007) The Gulf of California: review of ecosystem status and sustainability challenges. Prog Oceanogr 73(1):1–26CrossRefGoogle Scholar
  34. Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 19:3038–3051PubMedCrossRefGoogle Scholar
  35. Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76(2):173–190PubMedCrossRefGoogle Scholar
  36. Marinone SG (2003) A three-dimensional model of the mean and seasonal circulation of the Gulf of California. J Geophys Res 108:(C10)Google Scholar
  37. Marinone SG (2012) Seasonal surface connectivity in the Gulf of California. Estuar Coast Shelf Sci 100:133–141CrossRefGoogle Scholar
  38. Meirmans PG, Hedrick PW (2011) Assessing population structure: f-ST and related measures. Mol Ecol Resour 11(1):5–18PubMedCrossRefGoogle Scholar
  39. Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4(4):792–794CrossRefGoogle Scholar
  40. Milana V, Franchini P, Sola L, Angiulli E, Rossi AR (2012) Genetic structure in lagoons: the effects of habitat discontinuity and low dispersal ability on populations of Atherina boyeri. Mar Biol 159(2):399–411CrossRefGoogle Scholar
  41. Moreno-Báez M (2010) Mapping human dimensions of small-scale fisheries in the northern Gulf of California, Mexico. University of Arizona, TusconGoogle Scholar
  42. Moreno-Baez M, Cudney-Bueno R, Orr BJ, Shaw W, Pfister T, Torre-Cosio J, Loaiza R, Rojo M (2012) Integrating the spatial and temporal dimensions of sishing activities for management in the Northern Gulf of California, Mexico. Ocean Coast Manag 55:111–127CrossRefGoogle Scholar
  43. Munguía-Vega A, Jackson AM, Marinone SG, Erisman B, Moreno-Baez M, Giron-Nava A, Pfister T, Aburto-Oropeza O, Torre J (2014) Asymmetric connectivity of spawning aggregations of a commercially important marine fish using a multidisciplinary approach. PeerJ 2:e511PubMedCentralPubMedCrossRefGoogle Scholar
  44. Munguía-Vega A, Leyva-Valencia I, Lluch-Cota D, Cruz-Hernandez P (In press) Genetic structure of cortes geoduck clam panopea globosa dall 1898 from the Mexican Northwest. J Shellfish Res (special issue)Google Scholar
  45. Palumbi SR, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR, Version 2.0. Privately published document, Honolulu, HIGoogle Scholar
  46. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290PubMedCrossRefGoogle Scholar
  47. Pearse DE, Crandall KA (2004) Beyond F-ST: analysis of population genetic data for conservation. Conserv Genet 5(5):585–602CrossRefGoogle Scholar
  48. Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855CrossRefGoogle Scholar
  49. Pfeiler E, Hurtado LA, Knowles LL, Torre-Cosio J, Bourillon-Moreno L, Marquez-Farias JF, Montemayor-Lopez G (2005) Population genetics of the swimming crab Callinectes bellicosus (Brachyura : Portunidae) from the eastern Pacific Ocean. Mar Biol 146(3):559–569CrossRefGoogle Scholar
  50. Pfeiler E, Watts T, Pugh J, van der Heiden AM (2008) Speciation and demographic history of the Cortez bonefish, Albula sp A (Albuliformes : Albulidae), in the Gulf of California inferred from mitochondrial DNA. J Fish Biol 73(2):382–394CrossRefGoogle Scholar
  51. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256PubMedCrossRefGoogle Scholar
  52. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959PubMedCentralPubMedGoogle Scholar
  53. Rife AN, Erisman B, Sanchez A, Aburto-Oropeza O (2013) When good intentions are not enough. Insights on networks of “paper park” marine protected areas. Conserv Lett 6:200–212CrossRefGoogle Scholar
  54. Riginos C (2005) Cryptic vicariance in Gulf of California fishes parallels vicariant patterns found in Baja California mammals and reptiles. Evolution 59(12):2678–2690PubMedCrossRefGoogle Scholar
  55. Riginos C, Nachman MW (2001) Population subdivision in marine environments: the contributions of biogeography, geographical distance and discontinuous habitat to genetic differentiation in a blennioid fish, Axoclinus nigricaudus. Mol Ecol 10(6):1439–1453PubMedCrossRefGoogle Scholar
  56. Roberts CM (1995) Rapid buildup of fish biomass in a Caribbean marine reserve. Conserv Biol 9(4):815–826CrossRefGoogle Scholar
  57. Roberts CM, Bohnsack JA, Gell F, Hawkins JP, Goodridge R (2001) Effects of marine reserves on adjacent fisheries. Science 294(5548):1920–1923PubMedCrossRefGoogle Scholar
  58. Roberts CM, McClean CJ, Veron JEN, Hawkins JP, Allen GR, McAllister DE, Mittermeier CG, Schueler FW, Spalding M, Wells F, Vynne C, Werner TB (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295(5558):1280–1284PubMedCrossRefGoogle Scholar
  59. Ryman N, Palm S (2006) POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol Ecol 6:600–602CrossRefGoogle Scholar
  60. Sala E, Aburto-Oropeza O, Paredes G, Parra I, Barrera JC, Dayton PK (2002) A general model for designing networks of marine reserves. Science 298(5600):1991–1993PubMedCrossRefGoogle Scholar
  61. Sale PF, Cowen RK, Danilowicz BS, Jones GP, Kritzer JP, Lindeman KC, Planes S, Polunin NVC, Russ GR, Sadovy YJ, Steneck RS (2005) Critical science gaps impede use of no-take fishery reserves. Trends Ecol Evol 20(2):74–80PubMedCrossRefGoogle Scholar
  62. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: a laboratory manual second edition vols. 1, 2, and 3. In: molecular cloning: a laboratory manual, second edition, vols. 1, 2 and 3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New YorkGoogle Scholar
  63. Soria G, Munguia-Vega A, Marinone SG, Moreno-Baez M, Martinez-Tovar I, Cudney-Bueno R (2012) Linking bio-oceanography and population genetics to assess larval connectivity. Mar Ecol Prog Ser 463:159–175CrossRefGoogle Scholar
  64. Soria G, Torre-Cosio J, Munguia-Vega A, Marinone SG, Lavín MF, Cinti A, Moreno-Báez M (2014) Dynamic connectivity patterns from an insular marine protected area in the Gulf of California. J Mar Syst 129:248–258CrossRefGoogle Scholar
  65. Starr RM, Sala E, Ballesteros E, Zabala M (2007) Spatial dynamics of the Nassau grouper Epinephelus striatus in a Caribbean atoll. Mar Ecol Prog Ser 343:239–249CrossRefGoogle Scholar
  66. Thomson DA, Findley LT, Kerstitch AN (2000) Reef fishes of the Sea of Cortez. University of Texas Press, AustinGoogle Scholar
  67. Tinhan T, Erisman B, Aburto-Oropeza O, Weaver A, Vazquez-Arce D, Lowe C (2014) Residency and seasonal movements in Lutjanus argentiventris and Mycteroperca rosacea at Los Islotes Reserve, Gulf of California. Marine Ecology Progress Series in pressGoogle Scholar
  68. Turk-Boyer P, Morzaria-Luna HN, Martinez I, Downton-Hoffmann C, Munguia-Vega A (2014) Ecosystem-based fisheries management of a biological corridor along the Northern Sonora Coastline (NE Gulf of California). In: Amezcua F, Bellgraph B (eds) Fisheries management of Mexican and Central American Estuaries, Estuaries of the World. Springer Science, Berlin, pp 125–154Google Scholar
  69. 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(3):535–538CrossRefGoogle Scholar
  70. Walker BW (1960) The distribution and affinities of the marine fish fauna of the Gulf of California. Syst Zool 9(3):123–133CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Alexis M. Jackson
    • 1
  • Adrian Munguía-Vega
    • 2
    • 3
  • Ricardo Beldade
    • 1
    • 4
    • 5
  • Brad E. Erisman
    • 6
  • Giacomo Bernardi
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of California Santa CruzSanta CruzUSA
  2. 2.PANGAS Science CoordinationComunidad y Biodiversidad A.C.GuaymasMexico
  3. 3.Conservation Genetics Laboratory, School of Natural Resources & The EnvironmentUniversity of ArizonaTucsonUSA
  4. 4.USR 3278 CRIOBE, CNRS EPHECBETM de l’Université de PerpignanPerpignan CedexFrance
  5. 5.Centro de OceanografiaUniversidade de LisboaLisbonPortugal
  6. 6.Marine Science InstituteUniversity of Texas at AustinPort AransasUSA

Personalised recommendations