Scientia Marina, Vol 79, No 4 (2015)

Mitochondrial DNA evidences reflect an incipient population structure in Atlantic goliath grouper (Epinephelus itajara, Epinephelidae) in Brazil

Júnio S. Damasceno
Programa de Pós-graduação em Oceanografia Ambiental, Departamento de Oceanografia e Ecologia, Base Oceanográfica, UFES - Universidade Federal do Espírito Santo - Laboratório de Genética da Conservação, Programa de Pós-graduação em Zoologia de Vertebrados, PUCMINAS - Pontifícia Universidade Católica de Minas Gerais, Brazil

Raquel Siccha-Ramirez
Laboratório de Biologia e Genética de Peixes, Departamento de Morfologia, Instituto de Biociências de Botucatu, UNESP, Universidade Estadual Paulista - Laboratorio Costero de Tumbes, Instituto del Mar del Perú, IMARPE, Brazil

Millke J.A. Morales
Laboratório de Biologia e Genética de Peixes, Departamento de Morfologia, Instituto de Biociências de Botucatu, UNESP, Universidade Estadual Paulista, Brazil

Claudio Oliveira
Laboratório de Biologia e Genética de Peixes, Departamento de Morfologia, Instituto de Biociências de Botucatu, UNESP, Universidade Estadual Paulista, Brazil

Rodrigo A. Torres
Laboratório de Genômica Evolutiva e Ambiental, Departamento de Zoologia, Universidade Federal de Pernambuco, Brazil

Edvaldo N. Costa
Centro de Pesquisa e Conservação da Biodiversidade do Nordeste, CEPENE/ICMBio, Brazil

Gláucia C. Silva-Oliveira
Laboratório de Evolução, Instituto de Estudos Costeiros, Campus Universitário de Bragança, UFPA, Universidade Federal do Pará, Brazil

Marcelo Vallinoto
Laboratório de Evolução, Instituto de Estudos Costeiros, Campus Universitário de Bragança, UFPA, Universidade Federal do Pará - InBIO/CIBIO - Centro de Investigação em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, Universidade do Porto, Brazil

Leonardo F. Machado
Departamento de Ciências Agrárias e Biológicas, UFES, Universidade Federal do Espírito Santo, Brazil

Vander C. Tosta
Departamento de Ciências Agrárias e Biológicas, UFES, Universidade Federal do Espírito Santo, Brazil

Ana Paula C. Farro
Departamento de Ciências Agrárias e Biológicas, UFES, Universidade Federal do Espírito Santo, Brazil

Maurício Hostim-Silva
Departamento de Ciências Agrárias e Biológicas, UFES, Universidade Federal do Espírito Santo, Brazil


The Atlantic goliath grouper is a critically endangered species that inhabits estuarine and reef environments and is threatened primarily by fishing activities and habitat destruction. Despite the urgent need for protection, its genetic conservation status remains unknown. The aim of the present study was to evaluate the gene flow among the populations of the species along the coast of Brazil based on the control region of the mitochondrial DNA. The results indicate low haplotype diversity (0.40-0.86) and very low nucleotide diversity (0.1-0.5%). They also show that the genetic diversity of the species varies considerably along the coast and that this finding may be especially important for the identification of priority areas for its conservation. The population analyses indicate a low but significant degree of genetic structuring (ΦST =0.111), probably due to the occurrence of rare haplotypes at some locations, although the genetic differentiation between sites was not correlated with geographic distance (r=0.0501; p=0.7719), and the shared haplotypes indicate that gene flow occurs among all locations along the Brazilian coast. The results of the pairwise FST indicate a high degree of genetic differentiation between locations. The incipient population structuring detected in the present study is not related systematically to the geological or physical features of the Brazilian coast. The complex interaction of fluctuations in sea level, marine currents, and the reproductive characteristics of the species hampers the identification of the specific role of each of these processes in the gene flow dynamics of the population units of the Atlantic goliath grouper. The low overall levels of genetic diversity, the pairwise FST values and the significant population structuring among groups (ΦCT) identified in the present study all reinforce the critically endangered status of the species and are inconsistent with the presence of a single, panmictic population of groupers on the Brazilian coast. The results of this study suggest that, though it may be incipient, the observed genetic structuring must be taken into account in order to prevent potential problems, such as outbreeding depression, in the management of wild stocks.


critically endangered species; gene flow; genetic diversity; marine fish; western Atlantic Ocean

Full Text:



Aboim M.A., Menezes G.M., Schlitt T., et al. 2005. Genetic structure and history of populations of the deep-sea fish Helicolenus dactylopterus (Delaroche, 1809) inferred from mtDNA sequence analysis. Mol. Ecol. 14: 1343-1354. PMid:15813775

Aljanabi S.M., Martinez I. 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res. 25: 4692-4693. PMid:9358185 PMCid:PMC147078

Allendorf F.W., Phelps S.R. 1981. Use of allelic frequencies to describe population structure. Can. J. Fish Aquat. Sci. 38: 1507-1514.

Andrade A.C.S., Dominguez J.M.L., Martin L., et al. 2003. Quaternary evolution of the Caravelas strandplain — Southern Bahia State—Brazil. An. Acad. Bras. Ciênc. 75: 357-382.

Arz H.W., Pätzold J., Wefer G. 1998. Correlated millennial-scale changes in surface hydrography and terrigenous sediment yield inferred from last-glacial marine deposits off northeastern Brazil. Quat. Res. 50: 157-166.

Ayres M., Ayres Jr. M., Ayres D.L., et al. 2007. BioEstat. Versão 5.3, Sociedade Civil Mamirauá, MCT – CNPq, Belém, Pará, Brasil.

Barrett J.C., Fry B., Maller J., et al. 2005. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21: 263-265. PMid:15297300

Behling H., Arz H.W., Pätzold J., et al. 2000. Late Quaternary vegetational and climate dynamics in northeastern Brazil, inferences from marine core GeoB 3104-1. Quat. Sci. Rev. 19: 981-994.

Behling H., Cohen M.C.L., Lara R.J. 2001. Studies on Holocene mangrove ecosystem dynamics of the Bragança Peninsula in north-eastern Pará, Brazil. Palaeogeogr. Palaeocl. Palaeoecol. 167: 225-242.

Benevides E.A., Vallinoto M., Filho A.F., et al. 2014. When physical oceanography meets population genetics: the case study of the genetic/evolutionary discontinuity in the endangered Goliath grouper (Epinephelus itajara; Perciformes: Epinephelidae) with comments on the conservation of the species. Biochem. Sys. Ecol. 56: 255-266.

Bittencourt A.C.S.P., Dominguez J.M.L., Martin L., et al. 2000. Patterns of sediment dispersion coastwise the State of Bahia-Brazil. An. Acad. Bras. Cienc. 72: 21-33.

Bullock L.H., Murphy M.D., Godcharles M.F., et al. 1992. Age, growth, and reproduction of jewfish Epinephelus itajara in the eastern Gulf of Mexico. Fish. Bull. 90: 243-249.

Castro A.L.F., Stewart B.S., Wilson S.G., et al. 2007. Population genetic structure of Earth's largest fish, the whale shark (Rhincodon typus). Mol. Ecol. 16: 5183-5192. PMid:18092992

Chen S., Liu T., Li Z., et al. 2008. Genetic population structuring and demographic history of red spotted grouper (Epinephelus akaara) in South and East China Sea. Afr. J. Biotechnol. 7: 3554-3562.

Cohen M.C.L., Souza-Filho P.W., Lara, R.L., et al. 2005. A model of Holocene mangrove development and relative sea-level changes on the Bragança Peninsula (northern Brazil). Wetl. Ecol. Manag. 13: 433-443.

Coleman F.C., Koenig C.C. 2010. The Effects of Fishing, Climate Change, and Other Anthropogenic Disturbances on Red Grouper and Other Reef Fishes in the Gulf of Mexico. Integr. Comp. Biol. 50 (2): 201-212. PMid:21558199

Coleman F.C., Scanlon K.M., Koenig C.C. 2011. Groupers on the Edge: Shelf Edge Spawning Habitat in and Around Marine Reserves of the Northeastern Gulf of Mexico. Prof. Geogr. 63(4): 1-19.

Craig M.T., Hastings P.A. 2007. A molecular phylogeny of the groupers of the subfamily Epinephelinae with a revised classification of the tribe Epinephelini. Ichthyol. Res. 54: 1-17.

Craig M.T., Hastings P.A., Pondella D.J., et al. 2006. Phylogeography of the flag cabrilla Epinephelus labriformis (Serranidae): implications for the biogeography of the Tropical Eastern Pacific and the early stages of speciation in a marine shore fish. J. Biogeogr. 33: 969-979.

Craig M.T., Graham R.T., Torres R.A., et al. 2009. How many species of goliath grouper are there Cryptic genetic divergence in a threatened marine fish and the resurrection of a geopolitical species. Endang. Species Res. 7: 167-174.

Craig M.T., Sadovy de Mitcheson Y.J., Heemstra P.C. 2012. Groupers of the World: A Field and Market Guide, CRC Press. 424 pp.

Cunha I.M.C., Souza, A.S., Dias Jr. E.A., et al. 2014. Genetic Multipartitions Based on D-Loop Sequences and Chromosomal Patterns in Brown Chromis, Chromis multilineata (Pomacentridae), in the Western Atlantic. Hindawi BioMed Research International. Article ID 254698, 11 pp.

Drew J.A, Barber P.H. 2012. Comparative Phylogeography in Fijian Coral Reef Fishes: A Multi-Taxa Approach towards Marine Reserve Design. PLoS ONE 7(10): e47710. PMid:23118892 PMCid:PMC3484158

Drummond A.J., Ashton B., Cheung M., et al. 2009. Geneious v4. 7, Available from

Dupanloup I., Schneider S., Excoffier L. 2002. A simulated annealing approach to define the genetic structure of populations. Mol. Ecol. 11(12): 2571-2581. PMid:12453240

Edgar R.C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32(5): 1792-1797. PMid:15034147 PMCid:PMC390337

Eklund A.M., Schull J. 2001. A stepwise approach to investigate the movement patterns and habitat utilization of goliath grouper, Epinephelus itajara, using conventional tagging, acoustic telemetry and satellite tracking. In: Sibert J.R. and Nielsen J.L. (eds) Electronic tagging and tracking in marine fisheries. Springer-Verlag, New York. pp. 189-216.

Excoffier L., Laval L.G., Schneider S. 2005. Arlequin ver. 3.5: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1: 47-50. PMCid:PMC2658868

Frias-Torres S. 2006. Habitat Use of Juvenile Goliath Grouper Epinephelus itajara in the Florida Keys, USA. Endang. Species Res. 1: 1-6.

Giglio V.J., Adelir-Alves J., Gerhardinger L.C., et al. 2014. Habitat use and abundance of goliath grouper Epinephelus itajara in Brazil: a participative survey. Neotrop. Ichthyol. 12(4): 803-810.

Grant W.S., Bowen B.W. 1998. Shallow population histories in deep evolutionary lineages of marine fishes: Insights from sardines and anchovies and lessons for conservation. J. Hered. 89: 415-426.

Hébert C., Danzman R.G., Jones M.W., et al. 2000. Hydrography and population genetic structure in brook charr (Salvelinus fontinalis, Mitchill) from eastern Canada. Mol. Ecol. 9: 971-982. PMid:10886659

Hobbs J-P.A., Herwerden L.V., Jerry D.R., et al. 2013. High Genetic Diversity in Geographically Remote Populations of Endemic and Widespread Coral Reef Angelfishes (genus: Centropyge). Diversity 5: 39-50.

Ingvarsson P.K. 2004. Population subdivision and the Hudson-Kreitman-Aguade test: testing for deviations from the neutral model in organelle genomes. Genet. Res. 83: 31-39. PMid:15125064

IUCN. 2015. The IUCN (International Union for Conservation of Nature) Red List of Threatened Species. Version 2015.2. Downloaded on 27 July 2015.

Ji Y-Q., Wu D-D., Wu G-S., et al. 2011. Multi-Locus Analysis Reveals A Different Pattern of Genetic Diversity for Mitochondrial and Nuclear DNA between Wild and Domestic Pigs in East Asia. PLoS ONE 6(10): e26416. PMid:22065995 PMCid:PMC3204973

Koenig C.C., Coleman F.C., Eklund A.M., et al. 2007. Mangroves as Essential Nursery Habitat for Goliath grouper (Epinephelus itajara). Bull. Mar. Sci. 80(3): 567-586.

Kumar S., Subramanian S. 2002. Mutation rates in mammalian genomes. Proc. Natl. Acad. Sci. USA 99: 803-808. PMid:11792858 PMCid:PMC117386

Leipe T., Knoppers B., Marone E., et al. 1999. Suspended matter transport in coral reef waters of the Abrolhos Bank, Brazil. Geo-Marine Letters 19(3): 186-195.

Librado P., Rosas J. 2009. DnaSP v.5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452. PMid:19346325

Mann D.A., Locascio J.V., Coleman F.C., et al. 2008. Goliath grouper Epinephelus itajara sound production and movement patterns on aggregation sites. Endang. Species Res. 7: 229-236.

McClenachan L. 2009. Historical declines of goliath grouper populations in South Florida, USA. Endang. Species Res. 7: 175-181.

Mora C., Sale P.F. 2002. Are populations of coral reef fishes open or closed? Trends Ecol. Evol. 17: 422-428.

Moura A., Shukla J. 1981. On the dynamics of droughts in northeast Brazil: Observations, theory and numerical experiments with a general circulation model. J. Atmos. Sci. 38: 2653-2675.<2653:OTDODI>2.0.CO;2

Nonaka R.H., Matsuura Y., Suzuki K. 2000. Seasonal variation in larval fi sh assemblages in relation to oceanographic conditions in the Abrolhos Bank region off eastern Brazil. Fish. Bull. 98: 767-784.

Ostellari L., Bargelloni L., Penzo E., et al. 1996. Optimization of single-strand conformation polymorphism and sequence analysis of the mitochondrial control region in Pagellus bogaraveo (Sparidae, Teleostei): rationalized tools in fish population biology. Anim. Genet. 27: 423-427. PMid:9022158

Palumbi S.R. 2003. Population Genetics, Demographic Connectivity, and the Design of Marine Reserves. Ecol. Appl. 13(1, Suppl.): 146-158.[0146:PGDCAT]2.0.CO;2

Palumbi S.R., Baker C.S. 1994. Contrasting Population Structure from Nuclear Intron Sequences and mtDNA of Humpback Whales. Mol. Biol. Evol. 11(3): 246-435.

Pesole G., Gissi C., De Chirico A., et al. 1999. Nucleotide substitution rate of mammalian mitochondrial genomes. J. Mol. Evol. 48: 427-434. PMid:10079281

Pina-Amargós F., González-Sansón G. 2009. Movement patterns of goliath grouper Epinephelus itajara around southeast Cuba: implications for conservation. Endang. Species Res. 7: 243-247.

Portnoy D.S., Hollenbeck C.M., Renshaw M.A., et al. 2013. Does mating behaviour affect connectivity in marine fishes? Comparative population genetics of two protogynous groupers (Family Serranidae). Mol. Ecol. 22: 301-313. PMid:23189927

Rivera M.A., Kelley C.D., Roderic G.K. 2004. Subtle population genetic structure in the Hawaiian grouper, Epinephelus quernus (Serranidae) as revealed by mitochondrial DNA analyses. Biol. J. Linnean Soc. 81: 449-468.

Sadovy Y., Eklund A.M. 1999. Synopsis of biological information on the Nassau grouper, Epinephelus striatus, (Bloch 1792), and the jewfish, E. itajara (Lichtenstein 1822). NOAA Technical Report, NMFS 146, and FAO Fisheries Synopsis 157. 65 pp.

Sanger F., Air G.M., Barrell B.G., et al. 1977. Nucleotide sequence of bacteriophage φX174 DNA. Nature 265: 687-695. PMid:870828

Schaeffer-Novelli Y., Cintron-Molero G., Adaime R.R. 1990. Variability of mangrove ecosystems along the brazilian coast. Estuaries 13(2): 201-218.

Seyoum S., Tringali M.D., Barthel B.L., et al. 2013. Isolation and characterization of 29 polymorphic microsatellite markers for the endangered Atlantic goliath grouper (Epinephelus itajara), and the Pacific goliath grouper (E. quinquefasciatus). Conservation Genet. Resour. 5: 729-732.

Silva-Oliveira G.C., Rêgo P.S., Schneider H., et al. 2008. Genetic characterisation of populations of the critically endangered Goliath grouper (Epinephelus itajara, Serranidae) from the Northern Brazilian coast through analyses of mtDNA. Genet. Mol. Biol. 31(4): 988-994.

Silva-Oliveira G.C., Silva A.B.C., Oliveira Y., et al. 2012. New nuclear primers for molecular studies of Epinephelidae fishes. Conservation Genet. Resour. 5: 165-168.

Silva-Oliveira G.C., Silva A.B.C., Blanchard F., et al. 2014. Primers for the amplification of the MHC IIβ chain exon 2 in the Atlantic goliath grouper (Epinephelus itajara). Conservation Genet. Resour. 6: 523-525.

Soutelino R.G., Gangopadhyay A., Silveira I.C.A. 2013. The roles of vertical shear and topography on the eddy formation near the site of origin of the Brazil Current. Cont. Shelf Res. 70: 46-60.

Souza A.S., Dias Júnior E.A., Galetti P.M., et al. 2015. Wide-range genetic connectivity of Coney, Cephalopholis fulva (Epinephelidae), through oceanic islands and continental Brazilian coast. An. Acad. Bras. Cienc. 87(1): 121-136. PMid:25806980

Suguio K., Bittencourt A.C.S.P., Dominguez J.M.L., et al. 1985. Flutuações do nível relativo do mar durante o quaternário superior ao longo do litoral brasileiro e suas implicações na sedimentação costeira. Rev. Bras. Geociênc. 15: 273-286.

Tamura R., Peterson D., Peterson N., et al. 2011. MEGA 5: Molecular Evolutionary Genetics Analysis using Maximum Likehood, Evolutionary Distance and Maximum Parsimony Methods. Mol. Biol. Evol. 28: 2732-2739. PMid:21546353 PMCid:PMC3203626

Tang Q., Liu H., Mayden R., et al. 2006. Comparison of evolutionary rates in the mitochondrial DNA cytochrome b gene and control region and their implications for phylogeny of the Cobitoidea (Teleostei: Cypriniformes). Mol. Phylogenet. Evol. 39: 347-357. PMid:16213167

Teixeira C.E.P., Lessa G.C., Cirano M., et al. 2013. The inner shelf circulation on the Abrolhos Bank, 18°S, Brazil. Cont. Shelf Res. 70: 13-26.

Toews D.P.L., Brelsford A. 2012. The biogeography of mitochondrial and nuclear discordance in animals. Mol. Ecol. 21: 3907-3930. PMid:22738314

Torres R.A., Feitosa R.B., Carvalho D.C., et al. 2013. DNA barcoding approaches for fishing authentication of exploited grouper species including the endangered and legally protected goliath grouper Epinephelus itajara. Sci. Mar. 77(3): 409-418.

Vasconcellos A.V., Vianna P., Paiva P.C., et al. 2008. Genetic and morphometric differences between yellowtail snapper (Ocyurus chrysurus, Lutjanidae) populations of the tropical West Atlantic. Genet. Mol. Biol. 31(1): 308-316.

Wasko A.P., Martins C., Oliveira C., et al. 2003. Non-destructive genetic sampling in fish. An improved method for DNA extraction from fish fins and scales. Hereditas 138: 161-165. PMid:14641478

Wright S. 1951. The genetical structure of populations. Ann. Eugen. 15: 323-354. PMid:24540312

Zabel M., Wagner T., deMenocal P. 2003. Terrigenous signals in sediments from Terrigenous Signals in Sediments of the Low-Latitude Atlantic – Indications to Environmental Variations during the Late Quaternary, Part II: Lithogenic Matter. In: Wefer G., Mulitza S., Ratmeyer V. (eds), The South Atlantic in the Late Quaternary: Reconstruction of Mass Budget and Current Systems, Springer-Verlag, Berlin, Heidelberg, New York. pp. 323-345.

Zhang J., Cai Z., Huang L. 2006. Population genetic structure of crimson snapper Lutjanus erythropterus in East Asia, revealed by analysis of the mitochondrial control region. ICES J. Mar. Sci. 63: 693-704.

Copyright (c) 2015 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

Contact us

Technical support