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Different speciation processes in a cryptobenthic reef fish from the Western Tropical Atlantic

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Abstract

The saddled blenny Malacoctenus triangulatus is a widely distributed species of cryptobenthic reef fish that occurs from the Caribbean to southeastern Brazil, including the oceanic islands. Subtle morphological differences have been observed between populations, suggesting some degree of structuring along its distribution, especially between insular and coastal environments. In this study, we conducted phylogeographic analyses of M. triangulatus based on mitochondrial (cytochrome oxidase I and cytochrome b) and nuclear (rhodopsin) genes, including sequences of M. brunoi, a closely related species endemic to the oceanic islands of southeastern Brazil. Three highly structured lineages were identified within the M. triangulatus complex: one restricted to the Caribbean province probably isolated by the Amazon barrier, and two in the Brazilian province, one in the northeastern oceanic islands (NOI) and another along the coast (including M. brunoi). This result indicates that divergent evolutionary processes have driven the evolution of the saddled benny in the Tropical Southwestern Atlantic: an ancient isolation of the NOI lineage during the Neogene and a recent ecological speciation event in the southeastern oceanic islands, which were connected to the coast during Pleistocene marine regressions. Together, these results provide insights on the evolutionary patterns and oceanographic barriers in the Western Tropical Atlantic.

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References

  • Ahmadia, G. N., L. J. Sheard, F. L. Pezold & D. J. Smith, 2012. Cryptobenthic fish assemblages across the coral reef-seagrass continuum in SE Sulawesi, Indonesia. Aquatic Biology 16: 125–135.

    Article  Google Scholar 

  • Almeida, F. F. M., 2006. Ilhas oceânicas brasileiras e suas relações com a tectônica atlântica. Terræ Didatica 2: 3–18.

    Article  Google Scholar 

  • Anderson, A. B., A. Carvalho-Filho, R. A. Morais, L. T. Nunes, J. P. A. Quimbayo & S. R. Floeter, 2015. Brazilian tropical fishes in their southern limit of distribution: checklist of Santa Catarina’s rocky reef ichthyofauna, remarks and new records. Checklist 11: 1688.

    Article  Google Scholar 

  • Barroso, R., M. Klautau, A. M. Solé-Cava & P. C. Paiva, 2010. Eurythoe complanata (Polychaeta: amphinomidae), the ‘cosmopolitan’ fireworm, consists of at least three cryptic species. Marine Biology 157: 59–80.

    Article  Google Scholar 

  • Bernal, M. A. & L. A. Rocha, 2011. Acanthurus tractus Poey, 1860, a valid western Atlantic species of surgeonfish (Teleostei, Acanthuridae), distinct from Acanthurus bahianus Castelnau, 1855. Zootaxa 2905: 63–68.

    Article  Google Scholar 

  • Bickford, D., D. J. Lohman, N. S. Sodhi, P. K. L. Ng, R. Meier, K. Winker, K. K. Ingram & I. Das, 2007. Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22: 148–155.

    Article  PubMed  Google Scholar 

  • Brandl, S. J., C. H. R. Goatley, D. R. Bellwood & L. Tornabene, 2018. The hidden half: ecology and evolution of cryptobenthic fishes on coral reefs. Biological Reviews. https://doi.org/10.1111/brv.12423.

    Article  PubMed  Google Scholar 

  • Brogan, M. W., 1994. Distribution and retention of larval fishes near reefs in the Gulf of California. Marine Ecology Progress Series 115: 1–13.

    Article  Google Scholar 

  • Campos, C. E. C., M. B. Silva, S. G. Targino, J. C. Sá-Oliveira & A. S. Araújo, 2007. Simbiose de limpeza de Thalassoma noronhanum (Boulenger, 1890) (Labridae) na Reserva Biológica do Atol das Rocas, Rio Grande do Norte, Brasil. Revista de Etologia 8(2): 63–70.

    Google Scholar 

  • Clement, M., Q. Snell, P. Walke, D. Posada & K. Crandall, 2002. TCS: estimating gene genealogies. Proceeding 16th International Parallel Distributed Processing Symposium p. 184.

  • Cowen, R. K. & S. Sponaugle, 2009. Larval dispersal and marine population connectivity. Annual Review of Marine Science 1(1): 443–446.

    Article  PubMed  Google Scholar 

  • Cowman, P. & D. R. Bellwood, 2011. Coral reefs as drivers of cladogenesis: expanding coral reefs, cryptic extinction events, and the development of biodiversity hotspots. Journal of Evolutionary Biology 24: 2543–2562.

    Article  CAS  PubMed  Google Scholar 

  • Depczynski, M. & D. R. Bellwood, 2003. The role of cryptobenthic reef fishes in coral reef trophodynamics. Marine Ecology Progress Series 256: 183–191.

    Article  Google Scholar 

  • Drummond, A. J., M. A. Suchard, D. Xie & A. Rambaut, 2012. Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29: 1969–1973.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Excoffier, L. & H. E. L. Lischer, 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.

    Article  PubMed  Google Scholar 

  • Feitoza, B. M., R. S. Rosa & L. A. Rocha, 2005. Ecology and zoogeography of deep reef fishes in northeastern Brazil. Bulletin of Marine Science 76(3): 725–742.

    Google Scholar 

  • Floeter, S. R., R. Z. P. Guimarães, L. A. Rocha, C. E. L. Ferreira, C. A. Rangel & J. L. Gasparini, 2001. Geographic variation in reef-fish assemblages along the Brazilian coast. Global Ecology and Biogeography 10: 423–431.

    Article  Google Scholar 

  • Floeter, S. R., L. A. Rocha, D. R. Robertson, J. C. Joyeux, W. F. Smith-Vaniz, P. Wirtz, A. J. Edwards, J. P. Barreiros, C. E. L. Ferreira, J. L. Gasparini, A. Brito, J. M. Falcón, B. W. Bowen & G. Bernard, 2008. Atlantic reef fish biogeography and evolution. Journal of Biogeography 35(1): 22–47.

    Google Scholar 

  • Greenfield, D. W., 1979. A review of the Western Atlantic Starksia ocellata: complex (Pisces: Clinidae) with the description of two new species and proposal of superspecies status. Fieldiana Zoology 73(2): 9–48.

    Google Scholar 

  • Greenfield, D. W., 1988. A review of the Lythrypnus mowbrayi complex (Pisces: Gobiidae), with a description of a new species. Copeia 1988(2): 460–470.

    Article  Google Scholar 

  • Guillot, G., F. Mortier & A. Estoup, 2005. Geneland: a computer package for landscape genetics. Molecular Ecology Notes 5: 712–715.

    Article  CAS  Google Scholar 

  • Guimarães, R. Z. P., G. W. Nunan & J. L. Gasparini, 2010. Malacoctenus brunoi sp. n. (Blennioidei: Labrisomidae), a new scaled-blenny from Trindade Island, off Brazil. Zootaxa 2567: 50–56.

    Article  Google Scholar 

  • Hohenlohe, L. A., 2004. Limits to gene flow in marine animals with planktonic larvae: models of Littorina species around Point Conception, california. Biological Journal of Linnean Society 82: 169–187.

    Article  Google Scholar 

  • Hoorn, C., F. P. Wesselingh, H. ter Steege, M. A. Bermudez, A. Mora, J. Sevink, I. Sanmartín, A. Sanchez-Meseguer, C. L. Anderson, J. P. Figueiredo, C. Jaramillo, D. Riff, F. R. Negri, H. Hooghiemstra, J. Lundberg, T. Stadler, T. Särkinen & A. Antonelli, 2010. Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330: 927–931.

    Article  CAS  PubMed  Google Scholar 

  • Lastrucci, N. S., L. T. Nunes, A. Lindner & S. R. Floeter, 2018. An updated phylogeny of the redlip blenny genus Ophioblennius. Journal of Fish Biology 93(2): 411–414.

    Article  PubMed  Google Scholar 

  • Leigh, J. W. & D. Bryant, 2015. PopART: full-feature software for haplotype network construction. Methods Ecology Evolution 6(9): 1110–1116.

    Article  Google Scholar 

  • Librado, P. & J. Rozas, 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.

    Article  CAS  PubMed  Google Scholar 

  • Ludt, W. B. & L. A. Rocha, 2015. Shifting seas: the impacts of Pleistocene sea-level fluctuations on the evolution of tropical marine taxa. Journal Biogeography 42: 25–38.

    Article  Google Scholar 

  • Machado, L. F., J. S. Damasceno, A. A. Bertoncini, V. C. Tosta, A. P. C. Farro, M. Hostim-Silva & C. Oliveira, 2017. Population genetic structure and demographic history of the spadefish Chaetodipterus faber (Ephippidae) from Southwestern Atlantic. Journal of Experimental Marine Biology and Ecology 487: 45–52.

    Article  Google Scholar 

  • Mattos, G., V. C. Seixas & P. C. Paiva, 2018. Comparative phylogeography and genetic connectivity of two crustacean species with contrasting life histories on South Atlantic sandy beaches. Hydrobiologia 823: 1–12.

    Article  Google Scholar 

  • Mendes, L. F., 2006. História natural dos amborés e peixes-macaco (Actinopterygii, Blennioidei, Gobioidei) do Parque Nacional Marinho do Arquipélago de Fernando de Noronha, sob um enfoque comportamental. Revista Brasileira de Zoologia 23(3): 817–823.

    Article  Google Scholar 

  • Moura, R. L., G. M. Amado-Filho, F. C. Moraes, P. S. Brasileiro, P. S. Salomon, M. M. Mahiques, A. C. Bastos, M. G. Almeida, J. M. Silva Jr., B. F. Araujo, F. P. Brito, T. P. Rangel, B. C. Oliveira, R. G. Bahia, R. P. Paranhos, R. J. Dias, E. Siegle, A. G. Figueiredo Jr., R. C. Pereira, C. V. Leal, E. Hajdu, N. E. Asp, G. B. Gregoracci, S. Neumann-Leitão, P. L. Yager, R. B. Francini-Filho, A. Fróes, M. Campeão, B. S. Silva, A. P. Moreira, L. Oliveira, A. C. Soares, L. Araujo, N. L. Oliveira, J. B. Teixeira, R. A. Valle, C. C. Thompson, C. E. Rezende & F. L. Thompson, 2016. An extensive reef system at the Amazon River mouth. Science Advances 2: e1501252.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nei, M. & S. Kumar, 2000. Molecular Evolution and Phylogenetics. Oxford University Press, Oxford, UK.

    Google Scholar 

  • Neves, J. M. M., S. M. Q. Lima, L. F. Mendes, R. A. Torres, R. J. Pereira & T. Mott, 2016. Population structure of the rockpool blenny Entomacrodus vomerinus shows source-sink dynamics among Ecoregions in the tropical Southwestern Atlantic. PLoS ONE 11(6): e0157472.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinheiro, H. T., G. Bernardi, T. Simon, J. C. Joyeux, R. M. Macieira, J. L. Gasparini, C. Rocha & L. A. Rocha, 2017. Island biogeography of marine organisms. Nature 549: 82–85.

    Article  CAS  PubMed  Google Scholar 

  • Pinheiro, H. T., L. A. RochA, R. M. Macieira, A. Carvalho-Filho, A. B. Anderson, M. G. Bender, F. Di Dario, C. E. L. Ferreira, J. Figueiredo-Filho, R. Francini-Filho, J. L. Gasparini, J. C. Joyeux, O. J. Luiz, M. M. Mincarone, R. L. Moura, J. A. C. C. Nunes, J. P. Quimbayo, R. S. Rosa, C. L. S. Sampaio, I. Sazima, T. Simon, D. A. Vila-Nova & S. R. Floeter, 2018. South-western Atlantic reef fishes: zoogeographical patterns and ecological drivers reveal a secondary biodiversity centre in the Atlantic Ocean. Diversity and Distributions 24: 951–965.

    Article  Google Scholar 

  • Puillandre, N., A. Lambert, S. Brouillet & G. Achaz, 2012. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21: 1864–1877.

    Article  CAS  PubMed  Google Scholar 

  • Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.

    Article  CAS  PubMed  Google Scholar 

  • Rambaut, A., A. J. Drummond, D. Xie, G. Baele & M. A. Suchard, 2018. Tracer v1.7. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67(5): 901–904.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ritchie, A. M., N. Lo & S. Y. Ho, 2016. The impact of the tree prior on molecular dating of data sets containing a mixture of inter-and intraspecies sampling. Systematic Biology 66: 413–425.

    Google Scholar 

  • Rocha, L. A., 2003. Patterns of distribution and processes of speciation in Brazilian reef fishes. Journal of Biogeography 30: 1161–1171.

    Article  Google Scholar 

  • Rocha, L. A., 2004. Mitochondrial DNA and color pattern variation in three western Atlantic Halichoeres (Labridae), with the revalidation of two species. Copeia 2004(4): 770–782.

    Article  Google Scholar 

  • Rocha, L. A. & I. L. Rosa, 1999. New species of Haemulon (Teleostei: Haemulidae) from the Northeastern Brazilian Coast. Copeia 1999(2): 447–452.

    Article  Google Scholar 

  • Rocha, L. A., C. R. Rocha, D. R. Robertson & B. W. Bowen, 2008. Comparative phylogeography of Atlantic reef fishes indicates both origin and accumulation of diversity in the Caribbean. BMC Evolutionary Biology 8: 157.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodríguez-Rey, G. T., R. G. Hartnoll & A. M. Solé-Cava, 2016. Genetic structure and diversity of the island-restricted endangered land crab, Johngarthia lagostoma (H. Milne Edwards, 1837). Journal of Experimental Marine Biology and Ecology 474: 204–209.

    Article  CAS  Google Scholar 

  • Rodríguez-Rey, G. T., A. Carvalho Filho, M. E. Araújo & A. M. Solé-Cava, 2017. Evolutionary history of Bathygobius (Perciformes: Gobiidae) in the Atlantic biogeographic provinces: a new endemic species and old mitochondrial lineages. Zoological Journal of the Linnean Society 182(2): 360–384.

    Article  Google Scholar 

  • Santos, S., T. Hrbek, I. P. Farias, H. Schneider & I. Sampaio, 2006. Population genetic structuring of the king weakfish, Macrodon ancylodon (Sciaenidae), in Atlantic coastal waters of South America: deep genetic divergence without morphological change. Molecular Ecology 15: 4361–4373.

    Article  CAS  PubMed  Google Scholar 

  • Sazima, I., R. L. Moura & R. S. Rosa, 1997. Elacatinus figaro sp. n. (Perciformes: Gobiidae), a new cleaner goby from the coast of Brazil. Aqua. Journal of Ichthyology and Aquatic Biology 2(3): 33–38.

    Google Scholar 

  • Sevilla, R. G., A. Diez, M. Norén, O. Mouchel, M. Jérôme, V. Verrez-Bagnis, H. V. Pelt, L. Favre-Krey, G. Krey, T. F. Consortium & J. M. Bautista, 2007. Primers and polymerase chain reaction conditions for DNA barcoding teleost fish based on the mitochondrial cytochrome b and nuclear rhodopsin genes. Molecular Ecology Notes 7: 730–734.

    Article  CAS  Google Scholar 

  • Souza, A. S., E. A. Dias Jr., P. M. Galetti Jr., E. G. Machado, M. Pichorim & W. F. Molina, 2015. Wide- range genetic connectivity of Coney, Cephalopholis fulva (Epinephelidae), through oceanic islands and continental Brazilian coast. Anais da Academia Brasileira de Ciências 87(1): 121–136.

    Article  PubMed  Google Scholar 

  • Spalding, M. D., H. E. Fox, G. R. Allen, N. Davidson, Z. A. Ferdaña, M. Finlayson, B. S. Halpern, M. A. Jorge, A. Lombana, S. A. Lourie, K. D. Martin, E. McManus, J. Molnar, C. A. Recchia & J. Robertson, 2007. Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57(7): 573–583.

    Article  Google Scholar 

  • Springer, V. G., 1959. Systematics and zoogeography of the clinid fishes of the subtribe Labrisomini Hubbs. Publication of the Institute of Marine Science, University of Texas 5: 417–492.

    Google Scholar 

  • Springer, V. G. & M. F. Gomon, 1975. Variation in the western Atlantic clinid fish Malacoctenus triangulatus with a revidsed key to the Atlantic species of Malacoctenus. Smithsonian Contributions to Zoology 200: 1–11.

    Google Scholar 

  • Stephens, M., N. J. Smith & P. Donnelly, 2001. A new statistical method for haplotype reconstruction from population data. The American Journal of Human Genetics 68: 978–989.

    Article  CAS  PubMed  Google Scholar 

  • Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor, M. S. & M. E. Hellberg, 2005. Marine radiations at small geographic scales: speciation in neotropical reef gobies (Elacatinus). Evolution 59: 374–385.

    PubMed  Google Scholar 

  • Turchetto-Zolet, A. C., F. Pinheiro, F. Salgueiro & C. Palma-Silva, 2013. Phylogeographical patterns shed light on evolutionary process in South America. Molecular Ecology 22: 1193–1213.

    Article  CAS  PubMed  Google Scholar 

  • Victor, B., 2015. How many coral reef fish species are there? Cryptic diversity and the new molecular taxonomy. In: Mora C, ed. Ecology of Fishes on Coral Reefs. Cambridge: Cambridge University Press, 76–87.

  • Ward, R. D., T. S. Zemlak, B. H. Innes, P. R. Last & P. D. N. Hebert, 2005. DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 360: 1847–1857.

    Article  CAS  Google Scholar 

  • Zhang, J., P. Kapli, P. Pavlidis & A. Stamatakis, 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 2869–2876.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We are grateful to F. Petean, N. Dias, G. Araújo, F. Pupo, T. Leite, F. Lima, and A. Almeida for help during field collections, to R. Noguchi and SISBIOTA–MAR for donating material to the MNRJ fish collection, to M. Gehara for help with analysis, to A. Carvalho Filho and F. Lima for the photos, and to Abudefduf Atividades Subaquáticas and DeepTrip for logistical support during fieldwork. This paper is part of the PhD Thesis of Ricardo Marques Dias at the Biodiversity and Evolutionary Biology Graduate Program at the Federal University of Rio de Janeiro (PPGBBE/UFRJ); RMD is supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Grant Number 132124/2013-0 and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES) Grant Number 2346/2011. PCP is supported by CNPq Grant Number 304321/2017-6. MRB is supported by CNPq Grant Number 305955/2015-2 and also a Grant from “Edital Programa Institucional de Pesquisa nos Acervos da USP.”

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  1. Departamento de Vertebrados, Museu Nacional, Setor de Ictiologia, Universidade Federal do Rio de Janeiro, Quinta da Boa vista, s/n, Rio de Janeiro, RJ, 20940-040, Brazil

    Ricardo M. Dias, Daniel F. Almeida & Marcelo R. Britto

  2. Laboratório de Ictiologia Sistemática e Evolutiva, Departamento de Botânica e Zoologia, Universidade Federal do Rio Grande do Norte, Av. Senador Salgado Filho 3000, Natal, RN, 56078-970, Brazil

    Sergio M. Q. Lima

  3. Laboratório do Oceano, Departamento de Ecologia, Universidade Federal do Rio Grande do Norte, Av. Senador Salgado Filho 3000, Natal, RN, 56078-970, Brazil

    Liana F. Mendes

  4. Laboratório de Polychaeta, Departamento de Zoologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, 21941-902, Brazil

    Ricardo M. Dias & Paulo C. Paiva

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  1. Ricardo M. Dias
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10750_2019_3966_MOESM1_ESM.doc

Supplementary material 1 (DOC 379 kb) Online Resource 1. List of specimens analyzed in this study, including species, biogeographic provinces, major clades recovered in phylogeny analysis, sampling site, geographic coordinates, and sequence accession number. Sequences obtained from GenBank are marked with an * and from BoldSystem with an **

10750_2019_3966_MOESM2_ESM.doc

Supplementary material 2 (DOC 51 kb) Online Resource 2. Molecular parameters of the Malacoctenus triangulatus species complex in the Brazilian provinces for mtDNA (COI and Cytb) and nuDNA (Rho). Parameters include total number of individuals analyzed in each location (N), number of haplotypes (H), number of polymorphic sites (S), haplotype diversity (h), and nucleotide diversity (π)

10750_2019_3966_MOESM3_ESM.doc

Supplementary material 3 (DOC 71 kb) Online Resource 3. Matrix of pairwise genetic distances (p-distance) for cytochrome c oxidase subunit I (COI, A), cytochrome b (Cytb, B), and rhodopsin (Rho, C) sequences of Malacoctenus. N = number of samples

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Dias, R.M., Lima, S.M.Q., Mendes, L.F. et al. Different speciation processes in a cryptobenthic reef fish from the Western Tropical Atlantic. Hydrobiologia 837, 133–147 (2019). https://doi.org/10.1007/s10750-019-3966-z

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