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Systematics, phylogeny and biogeography
RESEARCH ARTICLE

A tree money grows on: the first inclusive molecular phylogeny of the economically important pink shrimp (Decapoda : Farfantepenaeus) reveals cryptic diversity

Laura Timm A D , Joan A. Browder B , Shaina Simon A , Thomas L. Jackson B , Ian C. Zink B C and Heather D. Bracken-Grissom A
+ Author Affiliations
- Author Affiliations

A Florida International University, Biscayne Bay Campus, 3000 NE 151st Street, Miami, FL 33181, USA.

B NOAA National Marine Fisheries Service, Southeast Fisheries Science Center, 75 Virginia Beach Drive, Miami, FL 33149, USA.

C University of Miami RSMAS CIMAS, 4600 Rickenbacker Causeway, Miami, FL 33149, USA.

D Corresponding author. Email: ltimm004@fiu.edu

Invertebrate Systematics 33(2) 488-500 https://doi.org/10.1071/IS18044
Submitted: 19 May 2018  Accepted: 7 November 2018   Published: 11 April 2019

Abstract

Species of Farfantepenaeus support economically important shrimp fisheries throughout the Western Hemisphere, necessitating proper fisheries management. To be effective, species management should be informed of the potential presence of cryptic species and of the evolutionary forces driving biodiversity. This is best accomplished through a robust phylogenetic framework and evidence-based species delimitation. This study represents the first comprehensive molecular phylogeny and species delimitation analyses of shrimps belonging to the genus Farfantepenaeus. Targeting three mitochondrial genes (12S, 16S, and COI), gene trees and a phylogeny for the genus were inferred using maximum likelihood and Bayesian approaches. In general, the phylogenetic relationships inferred here largely agree with those recovered from morphological data, including the most recent designation of F. isabelae as sister to F. subtilis. Molecular divergence was found between northern and southern populations of F. brasiliensis, suggesting the existence of unrecognised subspecies. However, previous recognition of F. duorarum and F. notialis as two distinct species was not supported by this study. The phylogeny inferred here also uncovers a phylogeographic signal of latitudinal speciation in the genus. The study presented here provides valuable insight into the evolutionary history of Farfantepenaeus, improving our ability to effectively manage these economically important species.

Additional keywords: fisheries management, genetics, penaeid.


References

Arreguin-Sanchez, F. (1999). Age and growth estimation for the White Shrimp, Penaeus setiferus, from the offshore fishery of the Northwestern Gulf of Mexico. Proceedings of the 45th Gulf and Caribbean Fisheries Institute, 146–159.

Arreguin-Sanchez, F., Zetina-Rejon, M., and Ramírez-Rodríguez, M. (2008). Exploring ecosystem-based harvesting strategies to recover the collapsed pink shrimp (Farfantepenaeus duorarum) fishery in the southern Gulf of Mexico. Ecological Modelling 214, 83–94.

Avise, J. C. (1992). Molecular population structure and the biogeographic history of a regional fauna: a case history with lessons for conservation biology. Oikos 63, 62–76.
Molecular population structure and the biogeographic history of a regional fauna: a case history with lessons for conservation biology.Crossref | GoogleScholarGoogle Scholar |

Ayre, D. J., Minchinton, T. E., and Perrin, C. (2009). Does life history predict past and current connectivity for rocky intertidal invertebrates across a marine biogeographic barrier? Molecular Ecology 18, 1887–1903.
Does life history predict past and current connectivity for rocky intertidal invertebrates across a marine biogeographic barrier?Crossref | GoogleScholarGoogle Scholar | 19434808PubMed |

Baldwin, J. D., Bass, A. L., Bowen, B. W., and Clark, W. H. (1998). Molecular phylogeny and biogeography of the marine shrimp Penaeus. Molecular Phylogenetics and Evolution 10, 399–407.
Molecular phylogeny and biogeography of the marine shrimp Penaeus.Crossref | GoogleScholarGoogle Scholar | 10051392PubMed |

Bernatchez, L. (1995). A role for molecular systematics in defining evolutionarily significant units in fishes. In ‘Evolution and the Aquatic Ecosystem: Defining Unique Units in Population Conservation’. (Ed. Nielsen, J. L.) pp. 114-132. (American Fisheries Society: Bethesda, Maryland.)

Burukovsky, R. N. (1972). Nekotorye voprosy sistematiki i rasprostraneniya krevetok roda Penaeus. In ‘Rybokhozyaistvennyeissledovaniya v Atlanticheskom Okeane’. (Ed. T. AtlantNIRO) Vol. 2, pp. 3–21. (Kalingrad.)

Burukovsky, R. N. (1997). Selection of a type species for Farfantepenaeus Burukovsky (Crustacea: Decapoda: Penaeidae). Proceedings of the Biological Society of Washington 110, 154.

Charuau, A., and Die, D. (2000). The fishery for brown shrimp (Penaeus subtilis) in French Guiana. In: FAO Western Central Atlantic Fishery Commission. Report of the third Workshop on the Assessment of Shrimp and Groundfish Fisheries on the Brazil-Guianas Shelf. FAO Fisheries Report No. 628, 53-71.

Cowen, R. K., Paris, C. B., and Srinivasan, A. (2006). Scaling of connectivity in marine populations. Science 311, 522–527.
Scaling of connectivity in marine populations.Crossref | GoogleScholarGoogle Scholar | 16357224PubMed |

Crandall, K. A., Bininda-Emonds, O. R. R., Mace, G. M., and Wayne, R. K. (2000). Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution 15, 290–295.
Considering evolutionary processes in conservation biology.Crossref | GoogleScholarGoogle Scholar |

Cunningham, C. W., Blackstone, N. W., and Buss, L. W. (1992). Evolution of king crabs from hermit crab ancestors. Nature 355, 539–542.
Evolution of king crabs from hermit crab ancestors.Crossref | GoogleScholarGoogle Scholar | 1741031PubMed |

D’Incao, F., Delevedove, G., Maggioni, D., and Maggioni, R. (1998). Evidência genética da presença de Farfantepenaeus paulensis (Pérez Farfante, 1967) no litoral nordeste do Brasil (Decapoda: Penaeidae). Nauplius 6, 129–137.

Dall, W., Hill, B. J., Rothlisberg, P. C., and Staples, D. J. (1990). The biology of Penaeidae. In ‘Advances in Marine Biology’, vol. 27. (Ed. Blaxter, J. H. S., and Southward, A. J.) pp. 1-489. (Academic Press: London.)

Desalle, R. (2006). Species discovery versus species identification in DNA barcoding efforts: response to Rubinoff. Conservation Biology 20, 1545–1547.
Species discovery versus species identification in DNA barcoding efforts: response to Rubinoff.Crossref | GoogleScholarGoogle Scholar | 17002772PubMed |

Ditty, J. G., and Alvarado Bremer, J. R. (2011). Species discrimination of postlarvae and early juvenile brown shrimp (Farfantepenaeus aztecus) and pink shrimp (F. duorarum) (Decapoda: Penaeidae): coupling molecular genetics and comparative morphology to identify early life stages. Journal of Crustacean Biology 31, 126–137.
Species discrimination of postlarvae and early juvenile brown shrimp (Farfantepenaeus aztecus) and pink shrimp (F. duorarum) (Decapoda: Penaeidae): coupling molecular genetics and comparative morphology to identify early life stages.Crossref | GoogleScholarGoogle Scholar |

Frankel, O. H. (1974). Genetic conservation: our evolutionary responsibility. Genetics 78, 53–65.
| 17248668PubMed |

García-Machado, E., Pempera, M., Dennebouy, N., Oliva-Suarez, M., Mounolou, J. C., and Monnerot, M. (1999). Mitochondrial genes collectively suggest the paraphyly of Crustacea with respect to Insecta. Journal of Molecular Evolution 49, 142–149.
Mitochondrial genes collectively suggest the paraphyly of Crustacea with respect to Insecta.Crossref | GoogleScholarGoogle Scholar | 10368442PubMed |

García-Machado, E., Robainas, A., Espinosa, G., Oliva, M., Páez, J., Verdecia, N., and Monnerot, M. (2001). Allozyme and mitochondrial DNA variation in Cuban populations of the shrimp Farfantepenaeus notialis (Crustacea: Decapoda). Marine Biology 138, 701–707.
Allozyme and mitochondrial DNA variation in Cuban populations of the shrimp Farfantepenaeus notialis (Crustacea: Decapoda).Crossref | GoogleScholarGoogle Scholar |

García-Machado, E., Ulmo-Díaz, G., Castellanos-Gell, J., and Casane, D. (2018). Patterns of population connectivity in marine organisms of Cuba. Bulletin of Marine Science 94, 1–20.

Gusmão, J., Lazoski, C., and Sole-Cava, A. M. (2000). A new species of Penaeus (Crustacea: Penaeidae) revealed by allozyme and cytochrome oxidase I analyses. Marine Biology 137, 435–446.
A new species of Penaeus (Crustacea: Penaeidae) revealed by allozyme and cytochrome oxidase I analyses.Crossref | GoogleScholarGoogle Scholar |

Hebert, P. D. N., Stoeckle, M. Y., Zemlak, T. S., and Francis, C. M. (2004). Identification of birds through DNA barcodes. PLoS Biology 2, e312.
Identification of birds through DNA barcodes.Crossref | GoogleScholarGoogle Scholar |

Huelsenbeck, J. P., and Ronquist, F. (2001). MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
MrBayes: Bayesian inference of phylogenetic trees.Crossref | GoogleScholarGoogle Scholar | 11524383PubMed |

Hultgren, K., Hurt, C., and Anker, A. (2014). Phylogenetic relationships within the snapping shrimp genus Synalpheus (Decapoda: Alpheidae). Molecular Phylogenetics and Evolution 77, 116–125.
Phylogenetic relationships within the snapping shrimp genus Synalpheus (Decapoda: Alpheidae).Crossref | GoogleScholarGoogle Scholar | 24680914PubMed |

Katoh, K., and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.
MAFFT multiple sequence alignment software version 7: improvements in performance and usability.Crossref | GoogleScholarGoogle Scholar | 23329690PubMed |

Lande, R., and Shannon, S. (1996). The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50, 434–437.
The role of genetic variation in adaptation and population persistence in a changing environment.Crossref | GoogleScholarGoogle Scholar | 28568879PubMed |

Lanfear, R., Calcott, B., Ho, S. Y. W., and Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 22319168PubMed |

Lavery, S., Chan, T. Y., Tam, Y. K., and Chu, K. H. (2004). Phylogenetic relationships and evolutionary history of the shrimp genus Penaeus s.l. derived from mitochondrial DNA. Molecular Phylogenetics and Evolution 31, 39–49.
Phylogenetic relationships and evolutionary history of the shrimp genus Penaeus s.l. derived from mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 15019607PubMed |

Lee, M. S. Y. (2004). The molecularisation of taxonomy. Invertebrate Systematics 18, 1–6.
The molecularisation of taxonomy.Crossref | GoogleScholarGoogle Scholar |

Leitre, Jr., N. O., and Petrere, Jr., M. P. (2006). Growth and mortalities of the pink shrimp Farfantepenaeus brasiliensis Latreille, 1970 and F. paulensis Pérez-Farfante, 1967 in southeast Brazil. Brazilian Journal of Biology 66, 523–536.

Maggioni, D. (1996). Caracterização de algumas espécies do gênero Penaeus do litoral brasileiro através de eletroenfonque. Nauplius 4, 129–137.

Maggioni, R., Rogers, A. D., Maclean, N., and D’Incao, F. (2001). Molecular phylogeny of western Atlantic Farfantepenaeus and Litopenaeus shrimp based on mitochondrial 16S partial sequences. Molecular Phylogenetics and Evolution 18, 66–73.
Molecular phylogeny of western Atlantic Farfantepenaeus and Litopenaeus shrimp based on mitochondrial 16S partial sequences.Crossref | GoogleScholarGoogle Scholar | 11161743PubMed |

May-Kú, M. A., and Ordóñez-López, U. (2006). Spatial patterns of density and size structure of penaeid shrimps Farfantepenaeus brasiliensis and Farfantepenaeus notialis in a hypersaline lagoon in the Yucatán Peninsula, Mexico. Bulletin of Marine Science 79, 259–271.

Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA 1, 1–8.

Moritz, C. (2002). Strategies to protect biological diversity and the evolutionary processes that sustain it. Systematic Biology 51, 238–254.
Strategies to protect biological diversity and the evolutionary processes that sustain it.Crossref | GoogleScholarGoogle Scholar | 12028731PubMed |

Moritz, C., and Cicero, C. (2004). DNA barcoding: promise and pitfalls. PLoS Biology 2, e354.
DNA barcoding: promise and pitfalls.Crossref | GoogleScholarGoogle Scholar | 15486587PubMed |

Mulley, J. C., and Latter, B. D. H. (1980). Genetic variation and evolutionary relationships within a group of thirteen species of penaeid prawns. Evolution 34, 904–916.
Genetic variation and evolutionary relationships within a group of thirteen species of penaeid prawns.Crossref | GoogleScholarGoogle Scholar | 28581142PubMed |

Nelson, K., and Hedgecock, D. (1980). Enzyme polymorphism and adaptive strategy in the decapod Crustacea. American Naturalist 116, 238–280.
Enzyme polymorphism and adaptive strategy in the decapod Crustacea.Crossref | GoogleScholarGoogle Scholar |

Pérez-Castañeda, R., and Defeo, O. (2000). Population structure of the penaeid shrimp Farfantepenaeus notialis in its new range. Bulletin of Marine Science 67, 1069–1074.

Pérez-Farfante, I. (1967). A new species and two new subspecies of shrimp of the genus Penaeus from western Atlantic. Proceedings of the Biological Society of Washington 80, 83–100.

Pérez-Farfante, I. (1969). Western Atlantic shrimps of the genus Penaeus. U.S. Fish and Wildlife Service Fishery Bulletin 67, 461–591.

Pérez-Farfante, I. (1970a). Características diagnósticas de los juveniles de Penaeus aztecus subtilis, P. duorarum notialis y P. brasiliensis (Crustacea, Decapoda, Penaeidae). Separatas Memorias Sociedad de Ciencias Naturales La Salle 30, 159–182.

Pérez-Farfante, I. (1970b). Claves ilustradas para la identificación de los camarones comerciales de la América Latina. Folleto No. 1605.

Pérez-Farfante, I. (1970c). Diagnostic characters of juveniles of the shrimps Penaeus aztecus aztecus, P. duorarum duorarum, and P. brasiliensis (Crustacea, Decapoda, Penaeidae). Special Scientific Report, Fisheries no. 599. US Fish and Wildlife Service, Washington, DC.

Pérez-Farfante, I. (1988). Illustrated key to the penaeoid shrimps of commerce in the Americas. NOAA Technical Report 64. US Department of Commerce, Washington, DC.

Pérez-Farfante, I., and Kensley, B. F. (1997). Penaeoid and sergestoid shrimps and prawns of the world: keys and diagnoses for the families and genera. Editions Du Museum National d’Histoire Naturelle 175, 1–233.

Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
jModelTest: phylogenetic model averaging.Crossref | GoogleScholarGoogle Scholar | 18397919PubMed |

Puillandre, N., Lambert, A., Brouillet, S., and Achaz, G. (2012). ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.
ABGD, Automatic Barcode Gap Discovery for primary species delimitation.Crossref | GoogleScholarGoogle Scholar | 21883587PubMed |

Rambaut, A. (2012). ‘FigTree v1.4.’ (University of Edinburgh: Edinburgh.)

Redfield, J. A., Hedgecock, D., Nelson, K., and Salini, J. P. (1980). Low heterozygosity in tropical marine crustaceans of Australia and the trophic stability hypothesis. Marine Biology Letters 1, 303–313.

Robainas-Barcia, A., Blanco, G., Sánchez, J. A., Monnerot, M., Solignac, M., and García-Machado, E. (2008). Spatiotemporal genetic differentiation of Cuban natural populations of the pink shrimp Farfantepenaeus notialis. Genetica 133, 283–294.
Spatiotemporal genetic differentiation of Cuban natural populations of the pink shrimp Farfantepenaeus notialis.Crossref | GoogleScholarGoogle Scholar | 17934785PubMed |

Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 12912839PubMed |

Ryder, O. A. (1986). Species conservation and systematics: the dilemma of subspecies. Trends in Ecology & Evolution 1, 9–10.
Species conservation and systematics: the dilemma of subspecies.Crossref | GoogleScholarGoogle Scholar |

Salini, J. (1987). Genetic variation and population subdivison in the greentail prawn Metapenaeus bennettae (Racek & Dall). Marine and Freshwater Research 38, 339–349.
Genetic variation and population subdivison in the greentail prawn Metapenaeus bennettae (Racek & Dall).Crossref | GoogleScholarGoogle Scholar |

Schubart, C. D., Cuesta, J. A., Diesel, R., and Felder, D. L. (2000). Molecular phylogeny, taxonomy, and evolution of nonmarine lineages within the American grapsoid crabs (Crustacea: Brachyura). Molecular Phylogenetics and Evolution 15, 179–190.
Molecular phylogeny, taxonomy, and evolution of nonmarine lineages within the American grapsoid crabs (Crustacea: Brachyura).Crossref | GoogleScholarGoogle Scholar | 10837150PubMed |

Sheperd, D., and Ehrhardt, N.M. (2000). Assessments of shrimp fisheries of Guyana. In: FAO Western Central Atlantic Fishery Commission. Report of the third Workshop on the Assessment of Shrimp and Groundfish Fisheries on the Brazil-Guianas Shelf. FAO Fisheries Report No. 628, 105–171.

Sheridan, P. F., Patella, F. J., Baxter, N., and Emiliani, D. A. (1987). Movements of brown shrimp, Penaeus aztecus, and pink shrimp, Penaeus duorarum, relative to the United-States-Mexico border in the western Gulf of Mexico. Marine Fisheries Review 49, 14–19.

Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar | 16928733PubMed |

Stillman, J. H., and Reeb, C. A. (2001). Molecular phylogeny of eastern Pacific porcelain crabs, genera Petrolisthes and Pachycheles, based on the mtDNA 16S rDNA sequence: phylogeographic and systematic implications. Molecular Phylogenetics and Evolution 19, 236–245.
Molecular phylogeny of eastern Pacific porcelain crabs, genera Petrolisthes and Pachycheles, based on the mtDNA 16S rDNA sequence: phylogeographic and systematic implications.Crossref | GoogleScholarGoogle Scholar | 11341806PubMed |

Sunden, S. L. F., and Davis, S. K. (1991). Evaluation of genetic variation in a domestic population of Penaeus vannamei (Boone): a comparison with three natural populations. Aquaculture 97, 131–142.
Evaluation of genetic variation in a domestic population of Penaeus vannamei (Boone): a comparison with three natural populations.Crossref | GoogleScholarGoogle Scholar |

Tam, Y. K., and Chu, K. H. (1993). Electrophoretic study on the phylogenetic relationships of some species of Penaeus and Metapenaeus (Decapoda: Penaeidae) from the South China Sea. Journal of Coastal Research 13, 697–705.

Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 24132122PubMed |

Tavares, M. (2002). Shrimps. In: Carpenter, K. E., Ed. The Living Marine Resources of the Western Central Atlantic Vol. 1: Introduction, molluscs, crustaceans, hagfishes, sharks, batoid fishes and chimaeras. FAO Species Identification Guide for Fishery Purposes and American Society of Ichthyologists and Herpetologists Special Publication No. 5. 251–291.

Tavares, C., and Gusmão, J. (2016). Description of a new Penaeidae (Decapoda: Dendrobranchiata) species, Farfantepenaeus isabelae sp. nov. Zootaxa 4171, 505–516.
Description of a new Penaeidae (Decapoda: Dendrobranchiata) species, Farfantepenaeus isabelae sp. nov.Crossref | GoogleScholarGoogle Scholar | 27701214PubMed |

Teodoro, S. S. A., Terossi, M., Mantelatto, F. L., and Costa, R. C. (2016). Discordance in the identification of juvenile pink shrimp (Farfantepenaeus brasiliensis and F. paulensis: Family Penaeidae): an integrative approach using morphology, morphometry and barcoding. Fisheries Research 183, 244–253.
Discordance in the identification of juvenile pink shrimp (Farfantepenaeus brasiliensis and F. paulensis: Family Penaeidae): an integrative approach using morphology, morphometry and barcoding.Crossref | GoogleScholarGoogle Scholar |

Timm, L. E., and Bracken-Grissom, H. D. (2015). The forest for the trees: evaluating molecular phylogenies with an emphasis on higher-level Decapoda. Journal of Crustacean Biology 35, 577–592.
The forest for the trees: evaluating molecular phylogenies with an emphasis on higher-level Decapoda.Crossref | GoogleScholarGoogle Scholar |

Timm, L. E., Simon, S., and Bracken-Grissom, H. D. (2018). Mitochondrial DNA sequence alignments for phylogenetic analysis of the shrimp genus Farfantepenaeus. Deep-Pelagic Nekton Dynamics of the Gulf of Mexico (DEEPEND) Consortium. Gulf of Mexico Research Initiative Information and Data Cooperative (GRIIDC), Harte Research Institute, Texas A&M University – Corpus Christi. 10.7266/n7-9yq3-3177.

Voloch, C. M., Freire, P. R., and Russo, C. A. M. (2005). Molecular phylogeny of penaeid shrimps inferred from two mitochondrial markers. Genetics and Molecular Research 4, 668–674.
| 16475111PubMed |

Waples, R. S. (1991). Pacific salmon, Oncorhynchus spp., and the definition of “species” under the Endangered Species Act. Marine Fisheries Review 53, 11–22.

Wiens, J. (2005). Can incomplete taxa rescue phylogenetic analyses from long-branch attraction? Systematic Biology 54, 731–742.
Can incomplete taxa rescue phylogenetic analyses from long-branch attraction?Crossref | GoogleScholarGoogle Scholar | 16243761PubMed |

Wiens, J. (2006). Missing data and the design of phylogenetic analyses. Journal of Biomedical Informatics 39, 34–42.
Missing data and the design of phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 15922672PubMed |

Witt, J., Threlhoff, D. L., and Hebert, P. D. N. (2006). DNA barcoding reveals extraordinary cryptic diversity in an amphipod genus: implications for desert spring conservation. Molecular Ecology 15, 3073–3082.
DNA barcoding reveals extraordinary cryptic diversity in an amphipod genus: implications for desert spring conservation.Crossref | GoogleScholarGoogle Scholar | 16911222PubMed |

Young, A. M., Torres, C., Mack, J. E., and Cunningham, C. W. (2002). Morphological and genetic evidence for vicariance and refugium in Atlantic and Gulf of Mexico populations of the hermit crab Pagurus longicarpus. Marine Biology 140, 1059–1066.
Morphological and genetic evidence for vicariance and refugium in Atlantic and Gulf of Mexico populations of the hermit crab Pagurus longicarpus.Crossref | GoogleScholarGoogle Scholar |