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Fine-scale genetic structuring, divergent selection, and conservation prospects for the overexploited crab (Cardisoma guanhumi) in tropical mangroves from North-eastern Brazil

Published online by Cambridge University Press:  19 January 2016

D.J. Gama-Maia  and
R.A. Torres
D.J. Gama-Maia*
Affiliation:
Programa de Pós-graduação em Genética, Departamento de Genética, Centro de Ciências Biológicas, Universidade Federal de Pernambuco, Recife, PE, Brazil Laboratório de Genômica Evolutiva e Ambiental, Universidade Federal de Pernambuco, Centro de Ciências Biológicas, Departamento de Zoologia, Av. Professor Nelson Chaves s/n, Cidade Universitaria, Recife 50670-420, Brazil
R.A. Torres
Affiliation:
Laboratório de Genômica Evolutiva e Ambiental, Universidade Federal de Pernambuco, Centro de Ciências Biológicas, Departamento de Zoologia, Av. Professor Nelson Chaves s/n, Cidade Universitaria, Recife 50670-420, Brazil
*
Correspondence should be addressed to:D.J. Gama-Maia, Programa de Pós-graduação em Genética, Departamento de Genética, Centro de Ciências Biológicas, Universidade Federal de Pernambuco, Recife, PE, Brazil email: [email protected]
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Abstract

Popularly known as blue land crab, Cardisoma guanhumi is heavily exploited as food and considered as an important economic resource in Brazil. In recent decades, the species has experienced a sharp population decline by the loss and/or degradation of its natural habitat and overfishing. The present study aimed to investigate the genetic variation and connectivity among 154 specimens of C. guanhumi sampled along the coast of Pernambuco in five different levels of tropical mangroves conservation. Nine ISSR primers were used for assessing the genetic variation of the species. The genetic diversity observed in C. guanhumi was high reinforcing the condition of a resilient species, indicating a good conservation status of this resource in Pernambuco. The hypothesis of panmixia was rejected in favour of a heterogeneous distribution of the genotypes of C. guanhumi (ФST = 0.19) despite the high gene flow observed in the study region. Such difference could be attributed to the candidate loci being under positive selection and differentially distributed between the geographic regions assessed. The genetic structure showed a pattern of fine-scale genetic structuring better fitted to a model of selection-mediated geographic cline. Cluster analysis and candidate loci under positive selection suggested that the populations of C. guanhumi in the North-central and South coasts of Pernambuco might be different management units and must be managed independently. In conclusion, exhaustion of natural stocks upon which fishing is totally dependent will lead to serious ecological and sociocultural impacts.

Keywords

Inter simple sequences repeatgene flowgenomic divergencepositive selectionCrustacea
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 96 , Issue 8 , December 2016 , pp. 1677 - 1686
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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References

REFERENCES

Abrunhosa, F.A., do Nascimento Mendes, L., de Brito, L.T., de Oliveira, Y.S., Ogawa, C.Y. and Ogawa, M. (2000) Cultivo do Caranguejo Terrestre Cardisoma guanhumi (Latreille, 1825) do Ovo ao Estágio Juvenil. Revista Científica de Produção Animal 2, 190–197.Google Scholar
Agência Estadual de Meio Ambiente do Estado de Pernambuco (CPRH/PE) (2010) Monitoramento de Bacias Hidrográficas. Available from: http://www.cprh.pe.gov.br/monitoramento/bacias_hidrograficas/39709%3B52052%3B1702%3B0%3B0.asp.Google Scholar
Allendorf, F.W., England, P.R., Luikart, G., Ritchie, P.A. and Ryman, N. (2008) Genetic effects of harvest on wild animal populations. Trends in Ecology and Evolution 23, 327–337.Google Scholar
Allendorf, F.W., Luikart, G.H. and Aitken, S.N. (2007) Conservation and the genetics of populations. Oxford: Blackwell Publishing.Google Scholar
Almeida, F.S., Fungaro, M.H.P. and Sodré, L.M.K. (2001) RAPD and isozyme analysis of genetic variability in three allied species of catfish (Siluriformes: Pimelodidae) from the Tibagi River. Brazil Journal of Zoology 253, 113–120.Google Scholar
Amaral, A.C.Z. and Jablonski, S. (2005) Conservação da biodiversidade marinha e costeira no Brasil. Megadiversidade 1, 43–51.Google Scholar
Antao, T. and Beaumont, M.A. (2011) Mcheza: a workbench to detect selection using dominant markers. Bioinformatics 27, 1717–1718.CrossRefGoogle ScholarPubMed
Ayres, M., Ayres-Júnior, M., Ayres, D.L. and Santos, A.A. (2007) BIOESTAT – Aplicações estatísticas nas áreas das ciências biomédicas. Belém, PA: Ong Mamiraua.Google Scholar
Barboza, R.S.L., Neumann-Leitão, S., Barboza, M.S.L. and Batista-Leite, L.D.M.A. (2008) ‘Fui no mangue catar lixo, pegar caranguejo, conversar com o urubu’: Estudo socioeconômico dos catadores de caranguejo no litoral norte de Pernambuco. Revista Brasileira de Engenharia de Pesca 3, 117–134.Google Scholar
Benevides, E.A., Vallinoto, M.N.S., Fetter Filho, A.F.H., de Souza, J.R.B., Silva-Oliveira, G., Freitas, M.O., Ferreira, B.P., Hostim-Silva, M., Bertoncini, A.A., Blanchardi, F. and Torres, R.A. (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. Biochemical Systematics and Ecology 56, 255–266.Google Scholar
Bilton, D.T., Paula, J. and Bishop, J.D.D. (2002) Dispersal, genetic differentiation and speciation in estuarine organisms. Estuarine, Coastal and Shelf Science 55, 937–952.Google Scholar
Botelho, E.R.O., Santos, M.F. and Souza, J.R.B. (2001) Aspectos populacionais do guaiamum, Cardisoma guanhumi Latreille, 1825, do estuário do Rio Una (Pernambuco Brasil). Boletim Técnico Científico, CEPENE 9, 123–146.Google Scholar
Britto, F.B., Mendes, D.S.F., Ogawa, M., Cintra, I.H.A. and Diniz, F.M. (2011) Single primer-based DNA amplification as a suitable and low-cost tool for assessing genetic diversity in mangrove crabs. Genetics and Molecular Research 10, 4084–4092.Google Scholar
Case, R.A.J., Hutchinson, W.F., Hauser, L., Van Oosterhout, C. and Carvalho, G.R. (2005) Macro-and micro-geographic variation in pantophysin (Pan I) allele frequencies in NE Atlantic cod Gadus morhua . Marine Ecology Progress Series 301, 267–278.Google Scholar
Chowdhury, U., Tanti, B., Rethy, P. and Gajurel, P.R. (2014) Analysis of genetic diversity of certain species of piper using RAPD-based molecular markers. Applied Biochemistry and Biotechnology 174, 168–173.Google Scholar
Clarke, K.R. and Gorley, R.N. (2006) Primer v6: user manual/tutorial. Plymouth: PRIMER-E.Google Scholar
Cooke, G.M., Chao, N.L. and Beheregaray, L.B. (2012) Natural selection in the water: freshwater invasion and adaptation by water colour in the Amazonian pufferfish. Journal of Evolutionary Biology 25, 1305–1320.CrossRefGoogle ScholarPubMed
Cooke, G.M., Landguth, E.L. and Beheregaray, L.B. (2014) Riverscape genetics identifies replicated ecological divergence across an Amazonian ecotone. Evolution 68, 1947–1960.Google Scholar
Costlow, J.D. Jr and Bookhout, C.G. (1968a) The complete larval development of the land-crab, Cardisoma guanhumi Latreille in the laboratory (Brachyura, Gecarcinidae). Crustaceana (Suppl.) 2, 259–270.Google Scholar
Costlow, J.D. Jr and Bookhout, C.G. (1968b) The effect of environmental factors on development of the land-grab, Cardisoma guanhumi Latreille. American Zoologist 8, 399–410.Google Scholar
Duarte, M.S., Maia-lima, F.A. and Molina, W.F. (2008) Interpopulational morphological analyses and fluctuating asymmetry in the brackish crab Cardisoma guanhumi Latreille (Decapoda, Gecarcinidae), on the Brazilian Northeast coastline. Pan-American Journal of Aquatic Sciences 3, 294–303.Google Scholar
Eimanifar, A. and Wink, M. (2013) Fine-scale population genetic structure in Artemia urmiana (Günther, 1890) based on mtDNA sequences and ISSR genomic fingerprinting. Organisms Diversity and Evolution 13, 1–13.Google Scholar
Excoffier, L. and Lischer, H.E. (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.CrossRefGoogle ScholarPubMed
Excoffier, L., Smouse, P. and Quattro, J. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.Google Scholar
Fernández, M.V., Maltagliati, F., Pannacciulli, F.G. and Roldán, M.I. (2011) Analysis of genetic variability in Aristaeomorpha foliacea (Crustacea, Aristeidae) using DNA-ISSR (Inter Simple Sequence Repeats) markers. Comptes Rendus Biologies 334, 705–712.Google Scholar
Ferreira, B.P. and Maida, M. (2006) Monitoramento dos recifes de coral do Brasil: situação atual e perspectivas. Brasília-DF: MMA/SBF.Google Scholar
Ferreira, E.M., Mourão, J.S., Rocha, P.D., Nascimento, D.M. and Bezerra, D.M.M.S.Q. (2009) Folk classification of the crabs and swimming crabs (Crustacea –Brachyura) of the Mamanguape river estuary, Northeastern Brazil. Journal of Ethnobiology and Ethnomedicine 5, 22.Google Scholar
Firmo, A.M., Tognella, M.M., Silva, S.R., Barboza, R.R. and Alves, R.R. (2012) Capture and commercialization of blue land crabs. Journal of Ethnobiology and Ethnomedicine 8, 12.Google Scholar
Forsee, R.A. and Albrecht, M. (2012) Population estimation and site fidelity of the land crab Cardisoma guanhumi (Decapoda: Brachyura: Gecarcinidae) on Vieques Island, Puerto Rico. Journal of Crustacean Biology 32, 435–442.Google Scholar
Frankham, R., Ballou, J.D. and Briscoe, D.A. (2004) Fundamentos de Genética da Conservação. Ribeirão Preto, SP: SBG (Sociedade Brasileira de Genética), 262 pp.Google Scholar
Galli, O.B., Fujimoto, R.Y. and Abrunhosa, F.A. (2012) Acute toxicity of sodium metabisulphite in larvae and post-larvae of the land crab, Cardisoma guanhumi . Bulletin of Environmental Contamination and Toxicology 89, 274–280.Google Scholar
Gifford, C.A. (1962) Some observations on the general biology of the land crab, Cardisoma guanhumi (Latreille), in south Florida. Biological Bulletin 123, 207–223.Google Scholar
Google Inc. (2013) Google Earth. Mountain View, CA: Google.Google Scholar
Govender, Y., Sabat, A.M. and Cuevas, E. (2008) Effects of land-use/land-cover changes on land crab, Cardisoma guanhumi, abundance in Puerto Rico. Journal of Tropical Ecology 24, 417–423.CrossRefGoogle Scholar
Hartl, D.L. and Clark, A.G. (2010) Princípios de genética de populações, 4th edn. São Paulo: Artmed, 659 pp.Google Scholar
Hellberg, M.E., Burton, R.S., Neigel, J.E. and Palumbi, S.R. (2002) Genetic assessment of connectivity among marine populations. Bulletin of Marine Science 70(Suppl. 1), 273–290.Google Scholar
Instituto brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) (2014) Lista das Espécies da Fauna Brasileira ameaçadas de Extinção. Anexo à: Instrução normativa no. 445 de 17 de dezembro de 2014. Ministério do Meio Ambiente, Brasília.Google Scholar
Laikre, L., Palm, S. and Ryman, N. (2005) Genetic population structure of fishes: implications for coastal zone management. AMBIO: A Journal of the Human Environment 34, 111–119.Google Scholar
Luikart, G., England, P.R., Tallmon, D., Jordan, S. and Taberlet, P. (2003) The power and promise of population genomics: from genotyping to genome typing. Nature Reviews Genetics 4, 981–994.Google Scholar
Moritz, C. (1994) Defining ‘Evolutionary Significant Units’ for conservation. Trends in Ecology and Evolution 9, 373–375.Google Scholar
Moritz, C. (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Systematic Biology 51, 238–254.Google Scholar
Nei, M. (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590.Google Scholar
Nelson, M.F. and Anderson, N.O. (2013) How many marker loci are necessary? Analysis of dominant marker data sets using two popular population genetic algorithms. Ecology and Evolution 3, 3455–3470.Google Scholar
Nosil, P., Funk, D.J. and Ortiz-Barrientos, D. (2009) Divergent selection and heterogeneous genomic divergence. Molecular Ecology 18, 375–402.Google Scholar
Oliveira-Neto, J.F., Batista, E., Metri, R. and Metri, C.B. (2014) Local distribution and abundance of Cardisoma guanhumi Latreille, 1928 (Brachyura: Gecarcinidae) in southern Brazil. Brazilian Journal of Biology 74, 1–7.Google Scholar
Oliveira-Neto, J.F., Pie, M.R., Chammas, M.A., Ostrensky, A. and Boerger, W.A. (2008) Phylogeography of the blue land crab, Cardisoma guanhumi (Decapoda: Gecarnicidae) along the Brazilian coast. Journal of the Marine Biological Association of the United Kingdom 88, 1417–1423.Google Scholar
Ovenden, J.R., Berry, O., Welch, D.J., Buckworth, R.C. and Dichmont, C.M. (2013) Ocean's eleven: a critical evaluation of the role of population, evolutionary and molecular genetics in the management of wild fisheries. Fish and Fisheries 16, 125–159.Google Scholar
Palsbøll, P.J., Berube, M. and Allendorf, F.W. (2007) Identification of management units using population genetic data. Trends in Ecology and Evolution 22, 11–16.Google Scholar
Pampoulie, C., Ruzzante, D.E., Chosson, V., Jörundsdóttir, T.D., Taylor, L., Thorsteinsson, V. and Marteinsdóttir, G. (2006) The genetic structure of Atlantic cod (Gadus morhua) around Iceland: insight from microsatellites, the Pan I locus, and tagging experiments. Canadian Journal of Fisheries and Aquatic Sciences 63, 2660–2674.Google Scholar
Pannacciulli, F.G., Manetti, G. and Maltagliati, F. (2009) Genetic diversity in two barnacle species, Chthamalus stellatus and Tesseropora atlantica (Crustacea, Cirripedia), with diferent larval dispersal modes in the archipelago of the Azores. Marine Biology 156, 2441–2450.Google Scholar
Pinder, A.W. and Smits, A.W. (1993) The burrow microhabitat of the land crab Cardisoma guanhumi: respiratory/ionic conditions and physiological responses of crabs to hypercapnia. Physiological Zoology 66, 216–236.CrossRefGoogle Scholar
Pritchard, J.K., Wen, W. and Falush, D. (2003) Documentation for STRUCTURE software: version 2.Google Scholar
Rodríguez-Fourquet, C. and Sabat, A.M. (2009) Effect of harvesting, vegetation structure and composition on the abundance and demography of the land crab Cardisoma guanhumi in Puerto Rico. Wetlands Ecology and Management 17, 627–640.Google Scholar
Sambrook, J. and Russell, D.W. (2001) Molecular cloning: a laboratory manual, 3rd edn. New York, NY: Cold Spring Harbor Laboratory.Google Scholar
Schulz, H.K., Smietana, P. and Schulz, R. (2004) Assessment of DNA variations of the Noble Crayfish (Astacus astacus L.) in Germany and Poland using Inter-simple sequence repeats (ISSRs). Bulletin français de la pêche et de la pisciculture 372–373–387–399.Google Scholar
Sexton, J.P., Hangartner, S.B. and Hoffmann, A.A. (2014) Genetic isolation by environment or distance: which pattern of gene flow is most common? Evolution 68, 1–15.CrossRefGoogle ScholarPubMed
Shafer, A.B.A. and Wolf, J.B.W. (2013) Widespread evidence for incipient ecological speciation: a meta-analysis of isolation-by-ecology. Ecology Letters 16, 940–950.Google Scholar
Shinozaki-Mendes, R.A., Silva, J.R.F., Santander-Neto, J. and Hazin, F.H.V. (2013) Reproductive biology of the land crab Cardisoma guanhumi (Decapoda: Gecarcinidae) in north-eastern Brazil. Journal of the Marine Biological Association of the United Kingdom 93, 761–768.Google Scholar
Sokal, R.R. and Rohlf, F.J. (1981) Biometry: the principles and practice of statistics in biological research. New York, NY: Freeman.Google Scholar
Statsoft Inc. (2004) Statistica 7.0.Google Scholar
Ungherese, G., Mengoni, A., Somigli, S., Baroni, D., Focardi, S. and Ugolini, A. (2010) Relationship between heavy metals pollution and genetic diversity in Mediterranean populations of the sandhopper Talitrus saltator (Montagu) (Crustacea, Amphipoda). Environmental Pollution 158, 1638–1643.Google Scholar
Vasemägi, A., Nilsson, J. and Primmer, C.R. (2005) Expressed sequence tag-linked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in Atlantic salmon (Salmo salar L.). Molecular Biology and Evolution 22, 1067–1076.Google Scholar
Ward, R.D., Skibinski, D.O. and Woodwark, M. (1992) Protein heterozygosity, protein structure, and taxonomic differentiation. Evolutionary Biology 26, 73–159.Google Scholar
Wolcott, D.L. and Wolcott, T.G. (1987) Nitrogen limitation in the herbivorous land crab Cardisoma guanhumi . Physiological Zoology 60, 262–268.Google Scholar
Wright, S. (1943) Isolation by distance. Genetics 28, 114.Google Scholar
Yeh, F.C., Yang, R.C. and Boyle, T. (1999) PopGene Version 131: Microsoft Window-based freeware for population genetic analysis. Edmonton: University of Alberta and Centre for International Forestry Research, 11–23.Google Scholar