Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Phylogeographic structuring of the amphidromous shrimp Atya scabra (Crustacea, Decapoda, Atyidae) unveiled by range-wide mitochondrial DNA sampling

Caio M. C. A. Oliveira A , Mariana Terossi https://orcid.org/0000-0002-6860-7883 A B and Fernando L. Mantelatto https://orcid.org/0000-0002-8497-187X A C
+ Author Affiliations
- Author Affiliations

A Laboratory of Bioecology and Crustacean Systematics (LBSC), Department of Biology, Faculty of Phylosophy, Sciences and Letters at Ribeirão Preto (FFCLRP), University of São Paulo (USP), Bandeirantes Avenue 3900, 14040-901, Ribeirão Preto, SP, Brazil.

B Present address: Laboratory of Carcinology, Department of Zoology, Institute of Biosciences, Federal University of Rio Grande do Sul (UFRGS), Bento Gonçalves Avenue 9500, Agronomia, 91501-970, Porto Alegre, RS, Brazil.

C Corresponding author. Email: flmantel@usp.br

Marine and Freshwater Research 70(8) 1078-1093 https://doi.org/10.1071/MF18272
Submitted: 18 August 2017  Accepted: 9 December 2018   Published: 21 February 2019

Abstract

Species with biological traits favourable to long-distance marine larval dispersal might show a phylogeographic structuring over broad regions, even when they are genetically connected within smaller scales. Here, we evaluated this hypothesis by using the widespread amphidromous shrimp Atya scabra, predicting a genetic discontinuity across biogeographical barriers throughout the Western Gulf of Mexico (WGM), Caribbean Sea (CS), south-western Atlantic (SWA) and eastern Atlantic (EA). Using cytochrome oxidase subunit 1 (COI) and 16S ribosomal unit (16S) gene fragments, we did a phylogeographic assessment and genetic characterisation with Bayesian clustering, AMOVA, haplotype networks and demographic analyses. As predicted, three discrete genetic groups, corresponding to the regions WGM, CS and EA, were uncovered by COI, as well an unpredicted SWA+CS group. The 16S fragment detected a low genetic variation, probably owing to a recent lineage differentiation, which was estimated by the COI molecular clock. We evaluated the role of the biological traits of A. scabra, as well as the consequences of Panama Isthmus closure and Pleistocene glaciation cycles in the lineage isolation of WGM and EA, as well as the genetic connectivity shown within regions and between CS and SWA. Our results highlighted that amphidromous species genetically connected over large scales should be genetically characterised in their wide distribution to provide more comprehensive systematics and to assist decision-making in biological conservation.

Additional keywords: amphidromy, Atlantic Ocean, biogeography, Caridea, COI, cytochrome oxidase I, genetic diversity, marine larval dispersal, phylogeography, ribosomal subunit 16S.


References

Abrunhosa, F. A., and Moura, M. G. (1988). O completo desenvolvimento larval do camarão Atya scabra (Leach) (Crustacea: Decapoda: Atyidae), cultivado em laboratório. Arquivo Ciências do Mar 27, 127–146.

Almeida, A. O., Mossolin, E. C., and Luz, R. J. (2010). Reproductive biology of the freshwater shrimp Atya scabra (Leach, 1815) (Crustacea: Atyidae) in Ilhéus, Bahia, Brazil. Zoological Studies 49, 243–252.

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 |

Avise, J. C. (2000). ‘Phylogeography: the History and Formation of Species.’ (Harvard University Press: Cambridge, MA, USA.)

Bauer, R. T. (2013). Amphidromy in shrimps: a life cycle between rivers and the sea. Latin American Journal of Aquatic Research 41, 633–650.
Amphidromy in shrimps: a life cycle between rivers and the sea.Crossref | GoogleScholarGoogle Scholar |

Beheregaray, L. B. (2008). Twenty years of phylogeography: the state of the field and the challenges for the southern hemisphere. Molecular Ecology 17, 3754–3774.
| 18627447PubMed |

Bohonak, A. J., and Jenkins, D. G. (2003). Ecological and evolutionary significance of dispersal by freshwater invertebrates. Ecology Letters 6, 783–796.
Ecological and evolutionary significance of dispersal by freshwater invertebrates.Crossref | GoogleScholarGoogle Scholar |

Bracken, H. D., De Grave, S., and Felder, D. L. (2009). Phylogeny of the Infraorder Caridea based on mitochondrial and nuclear genes (Crustacea: Decapoda). In ‘Crustacean Issues, Vol. 18. Decapod Crustacean Phylogenetics’. (Eds J. W. Martin, K. A. Crandall, and D. L. Felder.) pp. 281–305. (Taylor and Francis/CRC Press: Boca Raton, FL, USA.)

Briggs, J. C. (1995). ‘Global Biogeography.’ (Elsevier: Amsterdam, Netherlands.)

Castelin, M., Feutry, P., Hautecoeur, M., Marquet, G., Wowor, D., Zimmermann, G., and Keith, P. (2013). New insight on population genetic connectivity of widespread amphidromous prawn Macrobrachium lar (Fabricius, 1798) (Crustacea: Decapoda: Palaemonidae). Marine Biology 160, 1395–1406.
New insight on population genetic connectivity of widespread amphidromous prawn Macrobrachium lar (Fabricius, 1798) (Crustacea: Decapoda: Palaemonidae).Crossref | GoogleScholarGoogle Scholar |

Chace, F. A., and Hobbs, H. H. (1969). The freshwater and terrestrial decapod crustaceans of the West Indies with special reference to Dominica. United States National Museum Bulletin 292, 1–258.
The freshwater and terrestrial decapod crustaceans of the West Indies with special reference to Dominica.Crossref | GoogleScholarGoogle Scholar |

Chenoweth, S. F., and Hughes, J. M. (2003). Speciation and phylogeography in Caridina indistincta, a complex of freshwater shrimps from Australian heathland streams. Marine and Freshwater Research 54, 807–812.
Speciation and phylogeography in Caridina indistincta, a complex of freshwater shrimps from Australian heathland streams.Crossref | GoogleScholarGoogle Scholar |

Claremont, M., Williams, S. T., Barraclough, T. G., and Reid, D. G. (2011). The geographic scale of speciation in a marine snail with high dispersal potential. Journal of Biogeography 38, 1016–1032.
The geographic scale of speciation in a marine snail with high dispersal potential.Crossref | GoogleScholarGoogle Scholar |

Clement, M., Posada, D., and Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
TCS: a computer program to estimate gene genealogies.Crossref | GoogleScholarGoogle Scholar | 11050560PubMed |

Cook, B. D., Baker, A. M., Page, T. J., Grant, S. C., Fawcett, J. H., Hurwood, D. A., and Hughes, J. M. (2006). Biogeographic history of an Australian freshwater shrimp, Paratya australiensis (Atyidae): the role life history transition in phylogeographic diversification. Molecular Ecology 15, 1083–1093.
Biogeographic history of an Australian freshwater shrimp, Paratya australiensis (Atyidae): the role life history transition in phylogeographic diversification.Crossref | GoogleScholarGoogle Scholar | 16599968PubMed |

Cook, B. D., Pringle, C. M., and Hughes, J. M. (2008). Molecular evidence for sequential colonization and taxon cycling in freshwater shrimp on a Caribbean island. Molecular Ecology 17, 1066–1075.
Molecular evidence for sequential colonization and taxon cycling in freshwater shrimp on a Caribbean island.Crossref | GoogleScholarGoogle Scholar | 18261048PubMed |

Cook, B. D., Bernays, S., Pringle, C. M., and Hughes, J. M. (2009). Marine dispersal determines the genetic population structure of stream fauna of Puerto Rico: evidence for island scale population recovery processes. Journal of the North American Benthological Society 28, 709–718.
Marine dispersal determines the genetic population structure of stream fauna of Puerto Rico: evidence for island scale population recovery processes.Crossref | GoogleScholarGoogle Scholar |

Cook, B. D., Page, T. J., and Hughes, J. M. (2012). Phylogeography of related diadromous species in continental and island settings, and a comparison of their potential and realized dispersal patterns. Journal of Biogeography 39, 421–430.
Phylogeography of related diadromous species in continental and island settings, and a comparison of their potential and realized dispersal patterns.Crossref | GoogleScholarGoogle Scholar |

Corander, J., Waldmann, P., and Sillanpää, M. J. (2003). Bayesian analysis of genetic differentiation between populations. Genetics 163, 367–374.
| 12586722PubMed |

Corander, J., Marttinen, P., Sirén, J., and Tang, J. (2008). Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9, 539.
Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations.Crossref | GoogleScholarGoogle Scholar | 19087322PubMed |

Cossey, S. P. J., Nieuwenhuise, D. V., Davis, J., Rosenfeld, J. H., and Pindell, J. (2016). Compelling evidence from eastern Mexico for a Late Paleocene/Early Eocene isolation, drawdown, and refill of the Gulf of Mexico. Interpretation 4, SC63–SC80.
Compelling evidence from eastern Mexico for a Late Paleocene/Early Eocene isolation, drawdown, and refill of the Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |

Cowen, R. K., and Sponaugle, S. (2009). Larval dispersal and marine population connectivity. Annual Review of Marine Science 1, 443–466.
Larval dispersal and marine population connectivity.Crossref | GoogleScholarGoogle Scholar | 21141044PubMed |

Crandall, E. D., Taffel, J. R., and Barber, P. H. (2010). High gene flow due to pelagic larval dispersal among South Pacific archipelagos in two amphidromous gastropods (Neritomorpha: Neritidae). Heredity 104, 563–572.
High gene flow due to pelagic larval dispersal among South Pacific archipelagos in two amphidromous gastropods (Neritomorpha: Neritidae).Crossref | GoogleScholarGoogle Scholar | 19844268PubMed |

Cruz-Soltero, S., and Alston, D. E. (1992). Status report on research with Atya lanipes and A. scabra in Puerto Rico. Proceedings of the Forty-Four Annual Gulf and Caribbean Fisheries Institute Charleston 42, 387–398.

Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 22847109PubMed |

De Grave, S., Villalobos, J., Mantelatto, F. L., and Alvarez, F. (2013). Atya scabra. In ‘The IUCN Red List of Threatened Species 2013’, version 2015.2. e.T197895A107024088. (International Union for Conservation of Nature and Natural Resources.) Available at http://www.iucnredlist.org/details/197895/0 [Verified 31 August 2015].

DeBiasse, M. B., Richards, V. P., Shivji, M. S., and Hellberg, M. E. (2016). Shared phylogeographical breaks in a Caribbean coral reef sponge and its invertebrate commensals. Journal of Biogeography 43, 2136–2146.
Shared phylogeographical breaks in a Caribbean coral reef sponge and its invertebrate commensals.Crossref | GoogleScholarGoogle Scholar |

Dennenmoser, S., Thiel, M., and Schubart, C. D. (2010). High genetic variability with no apparent geographic structuring in the mtDNA of the amphidromous river shrimp Cryphiops caementarius (Decapoda: Palaemonidae) in northern-central Chile. Journal of Crustacean Biology 30, 762–766.
High genetic variability with no apparent geographic structuring in the mtDNA of the amphidromous river shrimp Cryphiops caementarius (Decapoda: Palaemonidae) in northern-central Chile.Crossref | GoogleScholarGoogle Scholar |

Drummond, A. J., and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
BEAST: Bayesian evolutionary analysis by sampling trees.Crossref | GoogleScholarGoogle Scholar | 17996036PubMed |

Drummond, A. J., Rambaut, A., Shapiro, B., and Pybus, O. G. (2005). Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution 22, 1185–1192.
Bayesian coalescent inference of past population dynamics from molecular sequences.Crossref | GoogleScholarGoogle Scholar | 15703244PubMed |

Excoffier, L., and Lischer, H. E. L. (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.
Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar | 21565059PubMed |

Excoffier, L., Smouse, P. E., and Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.
| 1644282PubMed |

Figueiredo, J., Hoorn, C., van der Ven, P., and Soares, E. (2009). Late Miocene onset of the Amazon River and the Amazon deep-sea fan: evidence from the Foz do Amazonas. Basin Geology 37, 619–622.
Late Miocene onset of the Amazon River and the Amazon deep-sea fan: evidence from the Foz do Amazonas.Crossref | GoogleScholarGoogle Scholar |

Floeter, S. R., Rocha, L. A., Robertson, D. R., Joyeux, J. C., Smith-Vaniz, W. F., Wirtz, P., Edwards, A. J., Barreiros, J. P., Ferreira, C. E. L., Gasparini, J. L., Brito, A., Falcon, J. M., Bowen, B. W., and Bernardi, G. (2008). Atlantic reef fish biogeography and evolution. Journal of Biogeography 35, 22–47.

Fu, Y. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.
| 9335623PubMed |

Fujita, S., Zenimoto, K., Iguchi, A., Kai, Y., Ueno, M., and Yamashita, S. (2016). Comparative phylogeography to test for predictions of marine larval dispersal in three amphidromous shrimps. Marine Ecology Progress Series 560, 105–120.
Comparative phylogeography to test for predictions of marine larval dispersal in three amphidromous shrimps.Crossref | GoogleScholarGoogle Scholar |

Galvão, R., and Bueno, S. L. S. (2000). Population structure and reproductive biology of the Camacuto shrimp, Atya scabra (Decapoda, Caridea, Atyidae), from São Sebastião, Brazil. In ‘Crustacean Issues 12. The Biodiversity Crisis and Crustacea’. (Ed. J. C. V. Klein.) pp. 291–299. (Taylor and Francis/CRC Press: Boca Raton, FL, USA.)

Grant, W. S., and Bowen, B. W. (1998). Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. The Journal of Heredity 89, 415–426.
Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation.Crossref | GoogleScholarGoogle Scholar |

Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.

Harrison, J. S. (2004). Evolution, biogeography, and the utility of mitochondrial 16S and COI genes in phylogenetic analysis of the crab genus Austinixa (Decapoda: Pinnotheridae). Molecular Phylogenetics and Evolution 30, 743–754.
Evolution, biogeography, and the utility of mitochondrial 16S and COI genes in phylogenetic analysis of the crab genus Austinixa (Decapoda: Pinnotheridae).Crossref | GoogleScholarGoogle Scholar | 15012952PubMed |

Haug, G. H., and Tiedemann, R. (1998). Effect of the formation of the Isthmus of Panama on Atlantic Ocean thermohaline circulation. Nature 393, 673–676.
Effect of the formation of the Isthmus of Panama on Atlantic Ocean thermohaline circulation.Crossref | GoogleScholarGoogle 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, 273–290.

Hernández-Vergara, M. P., and Jiménez–Rojo, S. (2008). Desarrollo larval y supervivencia de Atya scabra (Crustacea: Decapoda: Atyidae), a diferentes salinidades de cultivo. Ciencia Pesquera 16, 17–24.

Herrera-Correal, J., Mossolin, E. C., Wehrtmann, I. S., and Mantelatto, F. L. (2013). Reproductive aspects of the caridean shrimp Atya scabra (Leach, 1815) (Decapoda: Atyidae) in São Sebastião Island, southwestern Atlantic, Brazil. Latin American Journal of Aquatic Research 41, 676–684.
Reproductive aspects of the caridean shrimp Atya scabra (Leach, 1815) (Decapoda: Atyidae) in São Sebastião Island, southwestern Atlantic, Brazil.Crossref | GoogleScholarGoogle Scholar |

Hewitt, G. (2000). The genetic legacy of the Quaternary ice ages. Nature 405, 907–913.
The genetic legacy of the Quaternary ice ages.Crossref | GoogleScholarGoogle Scholar | 10879524PubMed |

Hewitt, G. M. (2004). Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 359, 183–195.
Genetic consequences of climatic oscillations in the Quaternary.Crossref | GoogleScholarGoogle Scholar | 15101575PubMed |

Hidaka, H., and Kano, Y. (2014). Morphological and genetic variation between the japanes populations of the amphidromous snail Stenomelania crenulata (Cerithioidea: Thiaridae). Zoological Science 31, 593–602.
Morphological and genetic variation between the japanes populations of the amphidromous snail Stenomelania crenulata (Cerithioidea: Thiaridae).Crossref | GoogleScholarGoogle Scholar | 25186931PubMed |

Hobbs, H. H., and Hart, C. W. (1982). The shrimp genus Atya (Decapoda: Atyidae). Smithsonian Contributions to Zoology 364, 1–143.
The shrimp genus Atya (Decapoda: Atyidae).Crossref | GoogleScholarGoogle Scholar |

Holthuis, L. B. (1959). The Crustacea Decapoda of Suriname (Dutch Guiana). Zoölogische Verhandelingen 44, 1–296.

Hoorn, C., Wesselingh, F. P., ter Steege, H., Bermudez, M. A., Mora, A., Sevink, J., Sanmartín, I., Sanchez-Meseguer, A., Anderson, C. L., Figueiredo, J. P., Jaramillo, C., Riff, D., Negri, F. R., Hooghiemstra, H., Lundberg, J., Stadler, T., Särkinen, T., and Antonelli, A. (2010). Amazonia through time: andean uplift, climate change, landscape evolution, and biodiversity. Science 330, 927.
Amazonia through time: andean uplift, climate change, landscape evolution, and biodiversity.Crossref | GoogleScholarGoogle Scholar | 21071659PubMed |

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 |

Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Mentjies, P., and Drummond, A. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.
Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar | 22543367PubMed |

Kimura, N. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.
A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences.Crossref | GoogleScholarGoogle Scholar |

Knowlton, N., and Weigt, L. A. (1998). New dates and new rates for divergence across the Isthmus of Panama. Proceedings of the Royal Society of London – B. Biological Sciences 265, 2257–2263.
New dates and new rates for divergence across the Isthmus of Panama.Crossref | GoogleScholarGoogle Scholar |

Knowlton, N., Weigt, L. A., Solórzano, L. A., Mills, D. K., and Bermingham, E. (1993). Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the isthmus of Panama. Science 260, 1629–1632.
Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the isthmus of Panama.Crossref | GoogleScholarGoogle Scholar | 8503007PubMed |

Laurenzano, C., Costa, T. M., and Schubart, C. D. (2016). Contrasting patterns of clinal genetic diversity and potential colonization pathways in two species of western Atlantic fiddler crabs. PLoS One 11, e0166518.
Contrasting patterns of clinal genetic diversity and potential colonization pathways in two species of western Atlantic fiddler crabs.Crossref | GoogleScholarGoogle Scholar | 27861598PubMed |

Librado, P., and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.
DnaSP v5: a software for comprehensive analysis of DNA polymorphism data.Crossref | GoogleScholarGoogle Scholar | 19346325PubMed |

Lorán-Núñez, R. M., Valdez-Guzmán, A. J., and Martínez-Isunza, F. R. (2009). Estudio biologico-pesquero del ‘burro’ Atya scabra em el río Los Pescados y río Actopan, Veracruz, México. Ciencia Pesquera 17, 5–16.

Lord, C., Lorion, J., Dettai, A., Watanabe, S., Tsukamoto, K., Cruaud, C., and Keith, P. (2012). From endemism to widespread distribution: phylogeography of three amphidromous Sicyopterus species (Teleostei: Gobioidei: Sicydiinae). Marine Ecology Progress Series 455, 269–285.
From endemism to widespread distribution: phylogeography of three amphidromous Sicyopterus species (Teleostei: Gobioidei: Sicydiinae).Crossref | GoogleScholarGoogle Scholar |

Ludt, W. B., and Rocha, L. A. (2015). Shifting seas: the impacts of Pleistocene sea-level fluctuations on the evolution of tropical marine taxa. Journal of Biogeography 42, 25–38.
Shifting seas: the impacts of Pleistocene sea-level fluctuations on the evolution of tropical marine taxa.Crossref | GoogleScholarGoogle Scholar |

Magalhães, C., and Pereira, G. (2007). Assessment of the decapod crustacean diversity in the Guayana Shield region aiming at conservation decisions. Biota Neotropica 7, 111–124.
Assessment of the decapod crustacean diversity in the Guayana Shield region aiming at conservation decisions.Crossref | GoogleScholarGoogle Scholar |

Mantelatto, F. L., Robles, R., Biagi, R., and Felder, D. L. (2006). Molecular analysis of the taxonomic and distributional status for the hermit crab genera Loxopagurus Forest, 1964 and Isocheles Stimpson, 1858 (Decapoda, Anomura, Diogenidae). Zoosystema 28, 495–506.

Mantelatto, F. L., Torati, L. S., Pileggi, L. G., Mossolin, E. C., Terossi, M., Carvalho, F. L., Rocha, S. S., and Magalhães, C. (2016). Avaliação dos camarões atiídeos (Decapoda: Atyidae). In ‘Livro Vermelho dos Crustáceos do Brasil: Avaliação 2010–2014’. (Eds M. Pinheiro and H. Boos.) Chapter 5, pp. 93–102. (Sociedade Brasileira de Carcinologia – SBC: Porto Alegre, RS, Brazil.)

Matzen da Silva, J., Creer, S., dos Santos, A., Costa, A. C., Cunha, M. R., Costa, F. O., and Carvalho, G. R. (2011). Systematic and evolutionary insights derived from mtDNA COI barcode diversity in the Decapoda (Crustacea: Malacostraca). PLoS One 6, e19449.
Systematic and evolutionary insights derived from mtDNA COI barcode diversity in the Decapoda (Crustacea: Malacostraca).Crossref | GoogleScholarGoogle Scholar | 22174780PubMed |

McDowall, R. M. (2007). On amphidromy, a distinct form of diadromy in aquatic organisms. Fish and Fisheries 8, 1–13.
On amphidromy, a distinct form of diadromy in aquatic organisms.Crossref | GoogleScholarGoogle Scholar |

Mercado-Salas, N. F., Morales-Vela, B., Suárez-Morales, E., and Iliffe, T. M. (2013). Conservation status of the inland aquatic crustaceans in the Yucatan Peninsula, Mexico: shortcomings of a protection strategy. Aquatic Conservation 23, 939–951.
Conservation status of the inland aquatic crustaceans in the Yucatan Peninsula, Mexico: shortcomings of a protection strategy.Crossref | GoogleScholarGoogle Scholar |

Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Proceedings of the Gateway Computing Environments Workshop (GCE)’, 14 November 2010, New Orleans, LA, USA. pp. 1–8. (IEEE: New Orleans, LA, USA.)

Muss, A., Robertson, D. R., Stepien, C. A., Wirtz, P., and Bowen, B. W. (2001). Phylogeography of Ophioblennius: the role of ocean currents and geography in reef fish evolution. Evolution 55, 561–572.
Phylogeography of Ophioblennius: the role of ocean currents and geography in reef fish evolution.Crossref | GoogleScholarGoogle Scholar | 11327163PubMed |

Nei, M. (1987). ‘Molecular Evolutionary Genetics.’ (Colombia University Press: New York, NY, USA.)

Nunes, F. L. D., Norris, R. D., and Knowlton, N. (2011). Long distance dispersal and connectivity in amphi-atlantic corals at regional and basin scales. PLoS One 6, e22298.
Long distance dispersal and connectivity in amphi-atlantic corals at regional and basin scales.Crossref | GoogleScholarGoogle Scholar |

O’Dea, A., Lessios, H. A., Coates, A. G., Eytan, R. I., Restrepo-Moreno, S. A., Cione, A. L., Collins, L. S., de Queiroz, A., Farris, D. W., Norris, R. D., Stallard, R. F., Woodburne, M. O., Aguilera, O., Aubry, M., Berggren, W. A., Budd, A. F., Cozzuol, M. A., Coppard, S. E., Duque-Caro, H., Finnegan, S., Gasparini, G. M., Grossman, E. L., Johnson, K. G., Keigwin, L. D., Knowlton, N., Leigh, E. G., Leonard-Pingel, J. S., Marko, P. B., Pyenson, N. D., Rachello-Dolmen, P. G., Soibelzon, E., Soibelzon, L., Todd, J. A., Vermeij, G. J., and Jackson, J. B. C. (2016). Formation of the Isthmus of Panama. Science Advances 2, e1600883.
Formation of the Isthmus of Panama.Crossref | GoogleScholarGoogle Scholar | 27540590PubMed |

Oey, L.-Y., Ezer, T., and Lee, H. C. (2005). Loop Current, rings and related circulation in the Gulf of Mexico: a review of numerical models and future challenges. Geophysical Monograph Series 161, 31–56.

Page, T. J., and Hughes, J. M. (2007). Radically different scales of phylogeographic structuring within cryptic species of freshwater shrimp (Atyidae: Caridina). Limnology and Oceanography 52, 1055–1066.
Radically different scales of phylogeographic structuring within cryptic species of freshwater shrimp (Atyidae: Caridina).Crossref | GoogleScholarGoogle Scholar |

Page, T. J., Cook, B. D., von Rintelen, T., von Rintelen, K., and Hughes, J. M. (2008). Evolutionary relationships of atyid shrimps imply both ancient Caribbean radiations and common marine dispersals. Journal of the North American Benthological Society 27, 68–83.
Evolutionary relationships of atyid shrimps imply both ancient Caribbean radiations and common marine dispersals.Crossref | GoogleScholarGoogle Scholar |

Page, T. J., Torati, L. S., Cook, B. D., Binderup, A., Pringle, C. M., Reuschel, S., Schubart, C. D., and Hughes, J. M. (2013). Invertébrés sans frontières: large scales of connectivity of selected freshwater species among Caribbean Islands. Biotropica 45, 236–244.
Invertébrés sans frontières: large scales of connectivity of selected freshwater species among Caribbean Islands.Crossref | GoogleScholarGoogle Scholar |

Palumbi, S. R., and Benzie, J. (1991). Large mitochondrial DNA differences between morphologically similar penaeid shrimp. Molecular Marine Biology and Biotechnology 1, 27–34.
| 1669002PubMed |

Peterson, R. G., and Stramma, L. (1991). Upper-level circulation in the South Atlantic Ocean Progress in Oceanography 26, 1–73.
Upper-level circulation in the South Atlantic OceanCrossref | GoogleScholarGoogle Scholar |

Pindell, J. (1993). Regional synopsis of Gulf of Mexico and Caribbean evolution. In ‘Mesozoic and Early Cenozoic Development of the Gulf of Mexico and Caribbean Region – a Context for Hydrocarbon Exploration, Society for Sedimentary Geology, volume 13’, Houston, TX, USA. (Eds J. L. Pindell and B. F. Perkins.) pp. 251–274. (SEPM Society for Sedimentary Geology: Houston, TX, USA.)

Pindell, J., and Kennan, L. (2009). Tectonic evolution of the Gulf of Mexico, Caribbean and northern South America in the mantle reference frame: an update. In ‘The Geology and Evolution of the Region between North and South America 328’. (Eds K. James, M. A. Lorente, and J. Pindell.) pp. 1–55. (Geological Society of London Special Publication: London, UK.)

Reid, D. G. (2009). The genus Echinolittorina Habe, 1956 (Gastropoda: Littorinidae) in the western Atlantic Ocean. Zootaxa 2184, 1–103.

Roberts, C. M. (1997). Connectivity and management of Caribbean coral reefs. Science 278, 1454–1457.
Connectivity and management of Caribbean coral reefs.Crossref | GoogleScholarGoogle Scholar | 9367956PubMed |

Robertson, D. R., and Cramer, K. L. (2014). Defining and dividing the greater Caribbean: insights from the biogeography of shorefishes. PLoS One 9, e102918.
Defining and dividing the greater Caribbean: insights from the biogeography of shorefishes.Crossref | GoogleScholarGoogle Scholar | 25054225PubMed |

Rodríguez, G. (1982). Fresh-water shrimps (Crustacea, Decapoda, Natantia) of the Orinoco Basin and the Venezuelan Guayana. Journal of Crustacean Biology 2, 378–391.
Fresh-water shrimps (Crustacea, Decapoda, Natantia) of the Orinoco Basin and the Venezuelan Guayana.Crossref | GoogleScholarGoogle Scholar |

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar | 22357727PubMed |

Rossi, N., and Mantelatto, F. L. (2013). Molecular analysis of the freshwater prawn Macrobrachium olfersii (Decapoda, Palaemonidae) supports the existence of a single species throughout its distribution. PLoS One 8, e54698.
Molecular analysis of the freshwater prawn Macrobrachium olfersii (Decapoda, Palaemonidae) supports the existence of a single species throughout its distribution.Crossref | GoogleScholarGoogle Scholar | 23382941PubMed |

Schmitter-Soto, J. J., Comín, F. A., Escobar-Briones, E., Herrera-Silveira, J., Alcocer, J., Suárez-Morales, E., Elías-Gutiérrez, M., Díaz-Arce, V., Marín, L. E., and Steinich, B. (2002). Hydrogeochemical and biological characteristics of cenotes in the Yucatan Peninsula (SE Mexico). Hydrobiologia 467, 215–228.
Hydrogeochemical and biological characteristics of cenotes in the Yucatan Peninsula (SE Mexico).Crossref | GoogleScholarGoogle Scholar |

Schmitz, W. J., Biggs, D. C., Lugo-Fernandez, A., Oey, L.-Y., and Sturges, W. (2005). A synopsis of the circulation in the Gulf of Mexico and on its continental margins. Geophysical Monograph Series 161, 11–30.

Schneider, B., and Schmittner, A. (2006). Simulating the impact of the Panamanian seaway closure on ocean circulation, marine productivity and nutrient cycling Earth and Planetary Science Letters 246, 367–380.
Simulating the impact of the Panamanian seaway closure on ocean circulation, marine productivity and nutrient cyclingCrossref | GoogleScholarGoogle Scholar |

Schubart, C. D. (2009). Mitochondrial DNA and decapod phylogenies; the importance of pseudogenes and primer optimization.). In ‘Crustacean Issues, Vol. 18, Decapod Crustacean Phylogenetics’. (Eds J. W. Martin, K. A. Crandall, and D. L. Felder.) pp. 45–63. (Taylor and Francis/CRC Press: Boca Raton, FL, USA.)

Schubart, C. D. (2011). Reconstruction of phylogenetic relationships within Grapsidae (Crustacea: Brachyura) and comparison of trans-isthmian versus amphi-Atlantic gene flow based on mtDNA. Zoologischer Anzeiger 250, 472–478.
Reconstruction of phylogenetic relationships within Grapsidae (Crustacea: Brachyura) and comparison of trans-isthmian versus amphi-Atlantic gene flow based on mtDNA.Crossref | GoogleScholarGoogle Scholar |

Schubart, C. D., and Huber, M. G. J. (2006). Genetic comparisons of German populations of the stone crayfish, Austropotamobius torrentium (Crustacea: Astacidae). Bulletin Francais de la Peche et de la Pisciculture 380–381, 1019–1028.
Genetic comparisons of German populations of the stone crayfish, Austropotamobius torrentium (Crustacea: Astacidae).Crossref | GoogleScholarGoogle Scholar |

Shulman, M. J., and Bermingham, E. (1995). Early life histories, ocean currents, and the population genetics of Caribbean reef fishes. Evolution 49, 897–910.
Early life histories, ocean currents, and the population genetics of Caribbean reef fishes.Crossref | GoogleScholarGoogle Scholar | 28564869PubMed |

Silberman, J. D., Sarver, S. K., and Walsh, P. J. (1994). Mitochondrial DNA variation and population structure in the spiny lobster Panulirus argus. Marine Biology 120, 601–608.
Mitochondrial DNA variation and population structure in the spiny lobster Panulirus argus.Crossref | GoogleScholarGoogle Scholar |

Spalding, M. D., Fox, H. E., Allen, G. R., Davidson, N., Ferdaña, Z. A., Finlayson, M., Halpern, B. S., Jorge, M. A., Lombana, A., Lourie, S. A., Martin, K. D., Mcmanus, E., Molnar, J., Recchia, C. A., and Robertson, J. (2007). Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57, 573–583.
Marine ecoregions of the world: a bioregionalization of coastal and shelf areas.Crossref | GoogleScholarGoogle Scholar |

Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.Crossref | GoogleScholarGoogle Scholar | 24451623PubMed |

Stamatakis, A., Hoover, P., and Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758–771.
A rapid bootstrap algorithm for the RAxML web servers.Crossref | GoogleScholarGoogle Scholar | 18853362PubMed |

Suárez-Morales, E., and Rivera-Arriaga, E. (1998). Hidrología y fauna acuática de los cenotes de la Península de Yucatán. Revista de la Sociedad Mexicana de Historia Natural 48, 37–47.

Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.
| 2513255PubMed |

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 |

Terossi, M., and Mantelatto, F. L. (2012). Morphological and genetic variability in Hippolyte obliquimanus Dana, 1852 (Decapoda: Caridea: Hippolytidae) from Brazil and the Caribbean Sea. Crustaceana 85, 685–712.
Morphological and genetic variability in Hippolyte obliquimanus Dana, 1852 (Decapoda: Caridea: Hippolytidae) from Brazil and the Caribbean Sea.Crossref | GoogleScholarGoogle Scholar |

Torati, L. S., and Mantelatto, F. L. (2012). Ontogenetic and evolutionary change of external morphology of the neotropical shrimp Potimirim (holthuis, 1954) explained by a molecular phylogeny of the genus. Journal of Crustacean Biology 32, 625–640.
Ontogenetic and evolutionary change of external morphology of the neotropical shrimp Potimirim (holthuis, 1954) explained by a molecular phylogeny of the genus.Crossref | GoogleScholarGoogle Scholar |

Torsvik, T. H., Rousse, S., Labails, C., and Smethurst, M. A. (2009). A new scheme for the opening of the South Atlantic Ocean and the dissection of an Aptian salt basin. Geophysical Journal International 177, 1315–1333.
A new scheme for the opening of the South Atlantic Ocean and the dissection of an Aptian salt basin.Crossref | GoogleScholarGoogle Scholar |

Tourinho, J. L., Solé-Cava, A. M., and Lazoski, C. (2012). Cryptic species within the commercially most important lobster in the tropical Atlantic, the spiny lobster Panulirus argus. Marine Biology 159, 1897–1906.
Cryptic species within the commercially most important lobster in the tropical Atlantic, the spiny lobster Panulirus argus.Crossref | GoogleScholarGoogle Scholar |

Urbano, D. F., De Almeida, R. A. F., and Nobre, P. (2008). Equatorial Undercurrent and North Equatorial Countercurrent at 38°W: a new perspective from direct velocity data. Journal of Geophysical Research 113, C04041.
Equatorial Undercurrent and North Equatorial Countercurrent at 38°W: a new perspective from direct velocity data.Crossref | GoogleScholarGoogle Scholar |

Williams, S., and Knowlton, N. (2001). Mitochondrial pseudogenes are pervasive and often insidious in the snapping shrimp genus Alpheus. Molecular Biology and Evolution 18, 1484–1493.
Mitochondrial pseudogenes are pervasive and often insidious in the snapping shrimp genus Alpheus.Crossref | GoogleScholarGoogle Scholar | 11470839PubMed |

Wood, L. E., De Grave, S., and Daniels, S. R. (2017). Phylogeographic patterning among two codistributed shrimp species (Crustacea: Decapoda: Palaemonidae) reveals high levels of connectivity across biogeographic regions along the South African coast. PLoS One 12, e0173356.
Phylogeographic patterning among two codistributed shrimp species (Crustacea: Decapoda: Palaemonidae) reveals high levels of connectivity across biogeographic regions along the South African coast.Crossref | GoogleScholarGoogle Scholar | 28282399PubMed |

Wunsch, C. (2003). Determining paleoceanographic circulations, with emphasis on the Last Glacial Maximum Quaternary. Scientific Review 22, 371–385.

Zhang, D., and Hewitt, G. M. (1996). Nuclear integrations: challenges for mitochondrial DNA markers. Trends in Ecology & Evolution 11, 247–251.
Nuclear integrations: challenges for mitochondrial DNA markers.Crossref | GoogleScholarGoogle Scholar |