Abstract
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.
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Akihito P, Meguro K (1980) On the six species of the genus Bathygobius found in Japan. Jpn J Ichthyol 27:215–236
Alfaro ME, Santini F, Brck CD (2007) Do reefs drive diversification in marine Teleosts? Evidence from the pufferfishes and their allies (order Tetraodontiformes). Evolution 61:2104–2126
Amores A, Giles V, Thode G (1990) Adaptive character of a Robertsonian fusion in chromosomes of the fish Gobius paganellus (Pisces, Perciformes). Heredity 65:151–155
Arai R, Sawada Y (1974) Chromosomes of Japanese gobioid fishes. Bull Nat Sci Mus Tokyo 17:97–105
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 2008:1–22
Barrett RDH, Hebert PDN (2005) Identifying spiders through DNA barcodes. Can J Zool 83:481–491
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 5–32
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 93:228–233
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
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 79:266–271
Carvalho-Filho A (1992) Peixes: costa brasileira. São Paulo, Ed. Marca D’Água, p 304
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 25:231–244
Cheverud JM (1989) A comparative analysis of morphological variation patterns in the papionins. Evolution 43:1737–1747
Collar DC, Wainwright PC, Alfaro ME (2008) Integrated diversification of locomotion and feeding in labrid fishes. Biol Lett 4:84–86
Dayrat B (2005) Towards integrative taxonomy. Biol J Linn Soc 85:407–415
Doebley J, Stec A (1993) Inheritance of the morphological differences between maize and teosinte: comparison of results for two F2 populations. Genetics 134:559–570
Fraser RH, Currie DJ (1996) The species richness-energy hypothesis in a system where historical factors are thought to prevail: coral reefs. Am Nat 148:138–159
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 34:397–423
Galetti PM Jr, Aguilar CT, Molina WF (2000) An overview on marine fish cytogenetics. Hydrobiologia 420:55–62
Galvão TB, Bertollo LAC, Molina WF (2011) Chromosomal complements of some Atlantic Blennioidei and Gobioidei species (Perciformes). Comp Cytogenet 5:259–275
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 Diego
Ginsburg I (1947) American species and subspecies of Bathygobius, with a demonstration of a suggested modified system of nomenclature. J Wash Acad Sci 37:275–284
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 37:563–575
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hebert PDN, Cywinska A, Ball SL, Waard JR (2003a) Biological identifications through DNA barcodes. Proc R Soc B Biol Sci 270:313–321
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 270:96–99
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 36:1014–1015
Huyse T, Houdt JV, Volckaert FA (2004) Paleoclimatic history and vicariant speciation in the “sand goby” group (Gobiidae, Teleostei). Mol Phylogenet Evol 32:324–336
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Klingenberg CP (2011) MORPHOJ: an integrated software package for geometric morphometrics. Mol Eco Res 11:353–357
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 275–296
Levan A, Fredga K, Sandeberg AA (1964) Nomenclature for centromeric position on chromosomes. Hereditas 52:201–220
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 320:211–223
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 43:63–70
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 142:197–203
Lingo ME, Szedlmayer ST (2006) The influence of habitat complexity on reef fish communities in the northeastern Gulf of Mexico. Environ Biol Fish 76:71–80
Mandrioli M, Manicardi GC, Machella N, Caputo V (2001) Molecular and cytogenetic analysis of the goby Gobius niger (Teleostei, Gobiidae). Genetica 110:73–78
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 23:817–823
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 7:683–692
Miller PJ, Smith RM (1989) The West African species of Bathygobius (Teleostei: Gobiidae) and their affinities. J Zool 218:277–318
Miller PJ, Stefanni S (2001) The eastern Pacific species of Bathygobius (Perciformes: Gobiidae). Rev Biol Trop 1:141–156
Mittelbach GG, Osenberg CW, Wainwright PC (1992) Variation in resource abundance affects diet and feeding morphology in the pumpkinseed sunfish (Lepomis gibbosus). Oecologia 90:8–13
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 9:1807–1814
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 86:1801–1812
Moreira-Filho O, Bertollo LAC (1991) Astyanax scabripinnis (Pisces, Characidae): a species complex. Rev Bras Gen 14:331–357
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 16:513–530
Munday PL, Herwerden LV, Dudgeon CL (2004) Evidence for sympatric speciation by host shift in the sea. Curr Biol 14:1498–1504
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
Nelson JS (2006) Fishes of the world, 4th edn. Willey, New Jersey
Peters KM (1983) Larval and early juvenile development of the frillfin goby, Bathygobius soporator (Perciformes: Gobiidae). Northeast Gulf Sci 6:137–153
Pinkel D, Straume T, Gray JW (1986) Cytogenetic analysis using quantitative, high-sensivity, fluorescence hybridization. Proc Natl Acad Sci USA 83:2934–2938
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 35:63–70
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 2006:51–61
Rivera J, Currie DC (2009) Identification of Neartic Black flies using DNA barcodes (Diptera: Simuliidae). Mol Ecol 9:224–236
Rocha LA (2003) Patterns of distribution and processes of speciation in Brazilian reef fishes. J Biogeogr 30:1161–1171
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 44:325–345
Rohlf FJ (2010a) tpsDig, Version 2.16. Departament of Ecology and Evolution, State University of New York, New York
Rohlf FJ (2010b) tpsUtil, version 1.46. Departament of Ecology and Evolution, State University of New York, New York
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 8:983–986
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetics trees. Mol Biol Evol 4:406–425
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Could Spring Harbor Laboratory Press, New York
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 2:205–208
Sazima I, Gasparini JL, Moura RL (1998) Gramma brasiliensis, a new basslet from the western South Atlantic (Perciformes: Grammatidae). Aqua J Ichthyol Aquat Biol 3:39–43
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 60:229–235
Sperling FAH, Hickey DA (1994) Mitochondrial DNA sequence variation in the Spruce budworm species complex (Choristoneura: Lepidoptera). Mol Biol Evol 11:656–665
Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol 30:2725–2729
Tavolga W (1953) Spawning and embryonic development in the gobiid fish, Bathygobius soporator. Anat Rec 117:427–460
Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109
Taylor MS, Hellberg ME (2005) Marine radiations at small geographic scales: speciation in Neotropical reef gobies (Elacatinus). Evolution 59:374–385
Thode G, Martinez G, Ruiz JL, Lopez JR (1988) Complex chromosomal polymorphism in Gobius fallax (Gobiidae, Perciformes). Genetica 76:65–71
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 24:4876–4882
Tornabene L, Pezold F (2011) Phylogenetic analysis of Western Atlantic Bathygobius (Teleostei: Gobiidae). Zootaxa 3042:27–36
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 16:141–170
Vasil’ev VP, Grigoryan KA (1993) Karyology of the Gobiidae. J Ichthyol 33:1–16
Walker JA (1997) Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus (Gasterosteidae) body shape. Biol J Linn Soc 61:3–50
Webb CJ (1986) Karyology of the Indo-Pacific Parioglossus raoi (Herre) (Teleostei: Gobioidei) from Fiji. Aust J Marine Freshw Res 37:347–351
Wells JD, Paper T, Sperling FAH (2001) DNA-based identification and molecular systematics of forensically important Sarcophagidae (Diptera). J Forensic Sci 46:1098–1102
Werner EE (1977) Species packing and niche complementarity in three sunfishes. Am Nat 111:553–579
Acknowledgments
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.
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Lima-Filho, P.A., Rosa, R.S., Souza, A.S. et al. Evolutionary diversification of Western Atlantic Bathygobius species based on cytogenetic, morphologic and DNA barcode data. Rev Fish Biol Fisheries 26, 109–121 (2016). https://doi.org/10.1007/s11160-015-9411-0
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DOI: https://doi.org/10.1007/s11160-015-9411-0