Reviews in Fish Biology and Fisheries

, Volume 26, Issue 1, pp 109–121 | Cite as

Evolutionary diversification of Western Atlantic Bathygobius species based on cytogenetic, morphologic and DNA barcode data

  • Paulo Augusto Lima-Filho
  • Ricardo de Souza Rosa
  • Allyson de Santos de Souza
  • Gideão Wagner Werneck Félix da Costa
  • Claudio de Oliveira
  • Wagner Franco MolinaEmail author
Research Paper


A number of fish groups, such as Gobiidae, are highly diversified and taxonomically complex. Extensive efforts are necessary to elucidate their cryptic diversity, since questions often arise about the phylogenetic aspects of new species. Clarifications about the diversity and phylogeny of the Bathygobius species from the southwestern Atlantic are particularly needed. Evidence has been accumulating on the Brazilian coast regarding the possible presence of new species while doubts remain about the taxonomic status of others. The taxonomic identification of some species of Bathygobius has been problematic, given their generally conservative external morphology, and several species are recognized as cryptic. This situation hinders understanding the real diversity in this taxon. Taken together, genetic, cytogenetic and morphometric analyses have been effective in identifying new species of this genus. Here we describe the karyotypic features and morphological patterns of three Western South Atlantic species of Bathygobius. Furthermore, its cytochrome c oxidase I (COI) gene sequences were compared with those of species from Central America, North America and the Caribbean. The broad analyses performed demonstrated an unsuspected diversity, leading to the identification of an un-described new species (Bathygobius sp.2) and the geographic redefinition of another, Bathygobius sp.1, undoubtedly a branch of B. geminatus, hitherto inaccurately identified as B. mystacium on the coast of Brazil.


Biodiversity Karyotype evolution Geometric morphometrics COI 



The authors thank CNPq (Proc. 556793/2009-9), INCT “Marine Sciences” and FAPESB (565054/2010-4 and 8936/2011) for financial support; CAPES for the scholarship granted to GWWFC and ASS, CNPq (Proc. 309879/2013-2) for the research grant to RSR, and ICMBio SISBIO (licenses 19135-1, 27027-2 and 131360-1) for permits to collect specimens. We are also grateful to José Lima de Figueiredo and Oswaldo Oiakawa (MZUSP) for the loan of specimens, to João Eduardo Pereira de Freitas (UFC) for making available specimens he collected, and to Jose Garcia Jr. for taxonomic identification of specimens.


  1. Akihito P, Meguro K (1980) On the six species of the genus Bathygobius found in Japan. Jpn J Ichthyol 27:215–236Google Scholar
  2. Alfaro ME, Santini F, Brck CD (2007) Do reefs drive diversification in marine Teleosts? Evidence from the pufferfishes and their allies (order Tetraodontiformes). Evolution 61:2104–2126CrossRefPubMedGoogle Scholar
  3. Amores A, Giles V, Thode G (1990) Adaptive character of a Robertsonian fusion in chromosomes of the fish Gobius paganellus (Pisces, Perciformes). Heredity 65:151–155CrossRefGoogle Scholar
  4. Arai R, Sawada Y (1974) Chromosomes of Japanese gobioid fishes. Bull Nat Sci Mus Tokyo 17:97–105Google Scholar
  5. Baldwin CC, Mounts JH, Smith DG, Weigt LA (2009) Genetic identification and color descriptions of early life-history stages of Belizean Phaeoptyx and Astrapogon (Teleostei: Apogonidae) with comments on identification of adult Phaeoptyx. Zootaxa 2008:1–22Google Scholar
  6. Barrett RDH, Hebert PDN (2005) Identifying spiders through DNA barcodes. Can J Zool 83:481–491CrossRefGoogle Scholar
  7. Bellwood DR, Wainwright PC (2002) The history and biogeography of fishes on coral reefs. In: Sale PF (ed) Coral reef fishes. Academic Press, San Diego, pp 5–32CrossRefGoogle Scholar
  8. Bertollo LAC, Oliveira C, Molina WF, Margarido VP, Fontes MS, Pastori MC, Falcão JN, Fenocchio AS (2004) Chromosome evolution in the erythrinid fish, Erythrinus erythrinus (Teleostei: Characiformes). Heredity 93:228–233CrossRefPubMedGoogle Scholar
  9. Betancur-R R, Broughton RE, Wiley EO, Carpenter K, López JA, Li C, Holcroft NI, Arcila D, Sanciangco M, Cureton II JC, Zhang F, Buser T, Campbell MA, Ballesteros JA, Roa-Varon A, Willis S, Borden WC, Rowley T, Reneau PC, Hough DJ, Lu G, Grande T, Arratia G, Ortí G (2013) The tree of life and a new classification of bony fishes. PLOS Curr Tree Life. doi: 10.1371/currents.tol.53ba26640df0ccaee75bb165c8c26288 Google Scholar
  10. Caputo V, Marchegiani F, Sorice M, Olmo E (1997) Heterochromatin heterogeneity and chromosome variability in four species of gobiid fishes (Perciformes: Gobiidae). Cytogenet Cell Genet 79:266–271CrossRefPubMedGoogle Scholar
  11. Carvalho-Filho A (1992) Peixes: costa brasileira. São Paulo, Ed. Marca D’Água, p 304Google Scholar
  12. Castro JP, Moura MO, Moreira-Filho O, Shibatta AO, Santos MH, Nogaroto V, Vicari MR, Almeida MC, Artoni RF (2014) Diversity of the Astyanax scabripinnis species complex (Teleostei: Characidae) in the Atlantic Forest, Brazil: species limits and evolutionary inferences. Rev Fish Biol Fish 25:231–244CrossRefGoogle Scholar
  13. Cheverud JM (1989) A comparative analysis of morphological variation patterns in the papionins. Evolution 43:1737–1747CrossRefGoogle Scholar
  14. Collar DC, Wainwright PC, Alfaro ME (2008) Integrated diversification of locomotion and feeding in labrid fishes. Biol Lett 4:84–86PubMedCentralCrossRefPubMedGoogle Scholar
  15. Dayrat B (2005) Towards integrative taxonomy. Biol J Linn Soc 85:407–415CrossRefGoogle Scholar
  16. Doebley J, Stec A (1993) Inheritance of the morphological differences between maize and teosinte: comparison of results for two F2 populations. Genetics 134:559–570PubMedCentralPubMedGoogle Scholar
  17. Fraser RH, Currie DJ (1996) The species richness-energy hypothesis in a system where historical factors are thought to prevail: coral reefs. Am Nat 148:138–159CrossRefGoogle Scholar
  18. Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Evol Syst 34:397–423CrossRefGoogle Scholar
  19. Galetti PM Jr, Aguilar CT, Molina WF (2000) An overview on marine fish cytogenetics. Hydrobiologia 420:55–62CrossRefGoogle Scholar
  20. Galvão TB, Bertollo LAC, Molina WF (2011) Chromosomal complements of some Atlantic Blennioidei and Gobioidei species (Perciformes). Comp Cytogenet 5:259–275PubMedCentralCrossRefPubMedGoogle Scholar
  21. Gibson RN, Yoshiyama RM (1999) Intertidal fish communities, pp 264–296. In: Horn MH, Martin KLM, Chotkowski MA (eds) Intertidal fishes: life in two worlds. Academic Press, San DiegoGoogle Scholar
  22. Ginsburg I (1947) American species and subspecies of Bathygobius, with a demonstration of a suggested modified system of nomenclature. J Wash Acad Sci 37:275–284Google Scholar
  23. Gold JR, Li YC, Shipley NS, Powers PK (1990) Improved methods for working with fish chromosomes with a review of metaphase chromosome banding. J Fish Biol 37:563–575CrossRefGoogle Scholar
  24. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  25. Hebert PDN, Cywinska A, Ball SL, Waard JR (2003a) Biological identifications through DNA barcodes. Proc R Soc B Biol Sci 270:313–321CrossRefGoogle Scholar
  26. Hebert PDN, Ratnasingham S, Waard JR (2003b) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond Ser B Biol Sci 270:96–99CrossRefGoogle Scholar
  27. Howell WM, Black DA (1980) Controlled silver staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method. Cell Mol Life Sci 36:1014–1015CrossRefGoogle Scholar
  28. Huyse T, Houdt JV, Volckaert FA (2004) Paleoclimatic history and vicariant speciation in the “sand goby” group (Gobiidae, Teleostei). Mol Phylogenet Evol 32:324–336CrossRefPubMedGoogle Scholar
  29. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMedGoogle Scholar
  30. Klingenberg CP (2011) MORPHOJ: an integrated software package for geometric morphometrics. Mol Eco Res 11:353–357CrossRefGoogle Scholar
  31. Larson A (1998) The comparison of morphological and molecular data in phylogenetic systematics. In: DeSalle R, Schierwater B (eds) Molecular approaches to ecology and evolution. Birkhäuser Verlag, Basel, pp 275–296CrossRefGoogle Scholar
  32. Levan A, Fredga K, Sandeberg AA (1964) Nomenclature for centromeric position on chromosomes. Hereditas 52:201–220CrossRefGoogle Scholar
  33. Lima D, Freitas JEP, Araújo ME, Solé-Cava AM (2005) Genetic detection of cryptic species in the frillfin goby Bathygobius soporator. J Exp Mar Biol Ecol 320:211–223CrossRefGoogle Scholar
  34. Lima-Filho PA, Cioffi MB, Bertollo LAC, Molina WF (2012) Karyoevolution and morphological divergences in Atlantic populations of the frillfin goby Bathygobius soporator (Gobiidae, Perciformes). J Exp Mar Biol Ecol 43:63–70CrossRefGoogle Scholar
  35. Lima-Filho PA, Bertollo LAC, Cioffi MB, Costa GWWF, Molina WF (2014) Karyotype divergence and spreading of 5S rDNA sequences between Genomes of Two Species: Darter and Emerald Gobies (Ctenogobius, Gobiidae). Cytogenet Genome Res 142:197–203PubMedGoogle Scholar
  36. Lingo ME, Szedlmayer ST (2006) The influence of habitat complexity on reef fish communities in the northeastern Gulf of Mexico. Environ Biol Fish 76:71–80CrossRefGoogle Scholar
  37. Mandrioli M, Manicardi GC, Machella N, Caputo V (2001) Molecular and cytogenetic analysis of the goby Gobius niger (Teleostei, Gobiidae). Genetica 110:73–78CrossRefGoogle Scholar
  38. Mendes LF (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. Rev Bras Zool 23:817–823CrossRefGoogle Scholar
  39. Mérona B, Mol J, Vigouroux R, Chaves PT (2009) Phenotypic plasticity in fish life-history traits in two neotropical reservoirs: Petit-Saut Reservoir in French Guiana and Brokopondo Reservoir in Suriname. Neotrop Ichthyol 7:683–692CrossRefGoogle Scholar
  40. Miller PJ, Smith RM (1989) The West African species of Bathygobius (Teleostei: Gobiidae) and their affinities. J Zool 218:277–318CrossRefGoogle Scholar
  41. Miller PJ, Stefanni S (2001) The eastern Pacific species of Bathygobius (Perciformes: Gobiidae). Rev Biol Trop 1:141–156Google Scholar
  42. Mittelbach GG, Osenberg CW, Wainwright PC (1992) Variation in resource abundance affects diet and feeding morphology in the pumpkinseed sunfish (Lepomis gibbosus). Oecologia 90:8–13CrossRefGoogle Scholar
  43. Molina WF, Alves DEO, Araújo WC, Martinez PA, Silva MFM, Costa GWWF (2010) Performance of human immunostimulating agents in the improvement of fish cytogenetic preparations. Genet Mol Res 9:1807–1814CrossRefPubMedGoogle Scholar
  44. Molina WF, Martinez PA, Bertollo LAC, Bidau CJ (2014) Preferential accumulation of sex and Bs chromosomes in biarmed karyotypes by meiotic drive and rates of chromosomal changes in fishes. An Acad Bras Cienc 86:1801–1812CrossRefPubMedGoogle Scholar
  45. Moreira-Filho O, Bertollo LAC (1991) Astyanax scabripinnis (Pisces, Characidae): a species complex. Rev Bras Gen 14:331–357Google Scholar
  46. Moura R, Gasparini J, Sazima I (1999) New records and range extensions of reef fishes in the western south Atlantic, with comments on reef fish distribution along the Brazilian coast. Rev Bras Zool 16:513–530CrossRefGoogle Scholar
  47. Munday PL, Herwerden LV, Dudgeon CL (2004) Evidence for sympatric speciation by host shift in the sea. Curr Biol 14:1498–1504CrossRefPubMedGoogle Scholar
  48. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New YorkGoogle Scholar
  49. Nelson JS (2006) Fishes of the world, 4th edn. Willey, New JerseyGoogle Scholar
  50. Peters KM (1983) Larval and early juvenile development of the frillfin goby, Bathygobius soporator (Perciformes: Gobiidae). Northeast Gulf Sci 6:137–153Google Scholar
  51. Pinkel D, Straume T, Gray JW (1986) Cytogenetic analysis using quantitative, high-sensivity, fluorescence hybridization. Proc Natl Acad Sci USA 83:2934–2938PubMedCentralCrossRefPubMedGoogle Scholar
  52. Piorski NM, Alves JR, Machado MRD, Correia MMV (2005) Alimentação e ecomorfologia de duas espécies de piranhas (Characiformes: Characidae) do lago de Viana, Maranhão, Brasil. Acta Amazon 35:63–70CrossRefGoogle Scholar
  53. Rangel CA, Mendes LF (2009) Review of blenniid fishes from Fernando de Noronha Archipelago, Brazil, with description of a new species of Scartella (Teleostei: Blenniidae). Zootaxa 2006:51–61Google Scholar
  54. Rivera J, Currie DC (2009) Identification of Neartic Black flies using DNA barcodes (Diptera: Simuliidae). Mol Ecol 9:224–236CrossRefGoogle Scholar
  55. Rocha LA (2003) Patterns of distribution and processes of speciation in Brazilian reef fishes. J Biogeogr 30:1161–1171CrossRefGoogle Scholar
  56. Roe AD, Sperling FAH (2007) Patterns of evolution of mitochondrial cytochrome c oxidase I and II DNA and implications for DNA barcoding. Mol Phylogenet Evol 44:325–345CrossRefPubMedGoogle Scholar
  57. Rohlf FJ (2010a) tpsDig, Version 2.16. Departament of Ecology and Evolution, State University of New York, New YorkGoogle Scholar
  58. Rohlf FJ (2010b) tpsUtil, version 1.46. Departament of Ecology and Evolution, State University of New York, New YorkGoogle Scholar
  59. Rosa RS, Moura RL (1997) Visual assessment of reef fish community structure in Atol das Rocas Biological Reserve, off northeastern Brazil. Proc 8th Int Coral Reef Symp 8:983–986Google Scholar
  60. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetics trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  61. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Could Spring Harbor Laboratory Press, New YorkGoogle Scholar
  62. Sampaio CLS, Nunes JACC, Mendes LF (2004) Acyrtus pauciradiatus, a new species of clingfish (Teleostei: Gobiesocidae) from Fernando de Noronha Archipelago, Penambuco state, Notheastern Brazil. Neotrop Ichthyol 2:205–208CrossRefGoogle Scholar
  63. Sazima I, Gasparini JL, Moura RL (1998) Gramma brasiliensis, a new basslet from the western South Atlantic (Perciformes: Grammatidae). Aqua J Ichthyol Aquat Biol 3:39–43Google Scholar
  64. Sola L, Iaselli V, Rossi AR, Rasch EM, Monaco PJ (1992) Cytogenetics of bisexual/unisexual species of Poecilia. II analysis of heterochromatin and nucleolar organizer regions in Poecilia mexicana by C-banding and DAPI, quinacrine, chromomycin A3 and silver staining. Cytogenet Cell Genet 60:229–235CrossRefPubMedGoogle Scholar
  65. Sperling FAH, Hickey DA (1994) Mitochondrial DNA sequence variation in the Spruce budworm species complex (Choristoneura: Lepidoptera). Mol Biol Evol 11:656–665PubMedGoogle Scholar
  66. Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306CrossRefPubMedGoogle Scholar
  67. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol 30:2725–2729PubMedCentralCrossRefPubMedGoogle Scholar
  68. Tavolga W (1953) Spawning and embryonic development in the gobiid fish, Bathygobius soporator. Anat Rec 117:427–460CrossRefGoogle Scholar
  69. Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109CrossRefPubMedGoogle Scholar
  70. Taylor MS, Hellberg ME (2005) Marine radiations at small geographic scales: speciation in Neotropical reef gobies (Elacatinus). Evolution 59:374–385PubMedGoogle Scholar
  71. Thode G, Martinez G, Ruiz JL, Lopez JR (1988) Complex chromosomal polymorphism in Gobius fallax (Gobiidae, Perciformes). Genetica 76:65–71CrossRefGoogle Scholar
  72. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  73. Tornabene L, Pezold F (2011) Phylogenetic analysis of Western Atlantic Bathygobius (Teleostei: Gobiidae). Zootaxa 3042:27–36Google Scholar
  74. Tornabene L, Baldwin CC, Weigt LA, Pezold F (2010) Exploring the diversity of western Atlantic Bathygobius (Teleostei: Gobiidae) with cytochrome c oxidase-I, with descriptions of two new species. Aqua J Ichthyol Aquat Biol 16:141–170Google Scholar
  75. Vasil’ev VP, Grigoryan KA (1993) Karyology of the Gobiidae. J Ichthyol 33:1–16Google Scholar
  76. Walker JA (1997) Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus (Gasterosteidae) body shape. Biol J Linn Soc 61:3–50Google Scholar
  77. Webb CJ (1986) Karyology of the Indo-Pacific Parioglossus raoi (Herre) (Teleostei: Gobioidei) from Fiji. Aust J Marine Freshw Res 37:347–351CrossRefGoogle Scholar
  78. Wells JD, Paper T, Sperling FAH (2001) DNA-based identification and molecular systematics of forensically important Sarcophagidae (Diptera). J Forensic Sci 46:1098–1102PubMedGoogle Scholar
  79. Werner EE (1977) Species packing and niche complementarity in three sunfishes. Am Nat 111:553–579CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Paulo Augusto Lima-Filho
    • 1
    • 4
  • Ricardo de Souza Rosa
    • 2
  • Allyson de Santos de Souza
    • 1
  • Gideão Wagner Werneck Félix da Costa
    • 1
  • Claudio de Oliveira
    • 3
  • Wagner Franco Molina
    • 1
    Email author
  1. 1.Departamento de Biologia Celular e Genética, Centro de BiociênciasUniversidade Federal do Rio Grande do NorteNatalBrazil
  2. 2.Departamento de Sistemática e Ecologia, CCENUniversidade Federal da ParaíbaJoão PessoaBrazil
  3. 3.Departamento de Morfologia, Instituto de BiociênciasUniversidade Estadual Paulista (UNESP)BotucatuBrazil
  4. 4.Instituto Federal de EducaçãoCiência e Tecnologia do Rio Grande do NorteMacauBrazil

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