Abstract
In the Indo-Pacific area, the Caribbean region and West Africa, insular systems are colonised by particular Gobiids of the Sicydiinae subfamily. These species spawn in freshwater, the free embryos drift downstream to the sea where they undergo a planktonic phase, before returning to rivers to grow and reproduce; an amphidromous lifestyle. These gobies are the biggest contributors to the diversity of fish communities in insular systems and have the highest levels of endemism, yet their phylogeny has not been explored before with molecular data. To understand the phylogeny and the biogeography of this subfamily, sequences from the mitochondrial 16S rDNA and cytochrome oxidase I and from the nuclear rhodopsin gene were obtained for 50 Sicydiinae specimens of seven genera. Our results support the monophyly of the subfamily and of all the genera except Sicyopus, which is polyphyletic. Five major clades were identified within this subfamily. One clade clusters Sicyopterus and Sicydium as sister genera, one contains the genus Stiphodon split into two different groups, two other clades include only Sicyopus (Smilosicyopus) and Cotylopus, respectively, and the last clade groups Akihito, Lentipes and Sicyopus (Sicyopus). As a result, the subgenus Smilosicyopus is elevated herein as a genus. A molecular dating approach helps the interpretation of these phylogenetic results in terms of amphidromy and biogeographical events that have allowed the Sicydiinae to colonise the Indo-Pacific, West African and Caribbean islands.
Similar content being viewed by others
References
Akihito (1986) Some morphological characters considered to be important in gobiid phylogeny. In: Uyeno T, Arai R, Taniuchi T, Matsuura K (eds) Indo-Pacific fish biology: proceedings of the second international conference on Indo-Pacific fishes. Ichthyological Society of Japan, Tokyo, pp 629–639
Akihito IwataA, Kobayashi T, Ikeo K, Imanishi T, Ono H, Umehara Y, Hamamatsu C, Sugiyama K, Ikeda Y, Sakamoto K, Fumihito A, Ohno S, Gojobori T (2000) Evolutionary aspects of gobioid fishes based upon a phylogenetic analysis of mitochondrial cytochrome b genes. Gene 259:5–15
Aoyama J, Tsukamoto K, Nishida M (2001) Molecular phylogeny and evolution of the fresh-water Eel, genus Anguilla. Mol Phylogenet Evol 20(3):450–459
Arai T, Limbong D, Otake T, Tsukamoto K (2001) Recruitment mechanisms of tropical eels Anguilla spp., and implications for the evolution of oceanic migration in the genus Anguilla. Mar Ecol Prog Ser 216:253–264
Barriel V (1994) Phylogénies moléculaires et insertions-délétions de nucléotides. C R Acad Sci Paris 317:693–701
Bell KNI (1999) An overview of goby-fry fisheries. Naga Manila 22(4):30–36
Berrebi P, Galewski T, Keith P (2006) Sicyopterus “lagocephalus”, a unique widespread taxon confirmed by mtDNA sequences. Mol Phylogenet Evol 40:903–904
Birdsong RS, Murdy EO, Pezold FL (1988) A study of the vertebral column and median fin osteology in gobioid fishes with comments on gobioid relationships. Bull Mar Sci 42:172–214
Bowen BW, Bass AL, Rocha LA, Grant WS, Robertson DR (2001) Phylogeography of the trumpetfish (Aulostomus spp): ring species complex on a global scale. Evolution 55:1029–1039
Briggs JC (1974) Marine zoogeography, McGraw Hill, New-York
Chen WJ, Bonillo C, Lecointre G (2003) Repeatability of clades as a criterion of reliability: a case study for molecular phylogeny of Acanthomorpha (Teleostei) with larger number of taxa. Mol Phylogenet Evol 26:262–288
Drummond AJ, Rambaut A (2007) BEAST: bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214
Felsenstein J, Kishino H (1993) Is there something wrong with the bootstrap on phylogenies? A reply to Hillis and Bull. Syst Biol 42(2):193–200
Gaither MR, Toonen RJ, Robertson R, Planes S, Bowen BW (2010) Genetic evaluation of marine biogeographical barriers: perspective from two widespread Indo-Pacific snappers (Lutjanus kashmira and Lutjanus fluvus). J Biogeogr 37:133–147
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
Harrison IJ (1989) Specialisation of the Gobioid palatopterygoquadrate complex and its relevance to Gobioid systematics. J Nat Hist 23:325–353
Harrison IJ (1993) The West African sicydiine fishes, with notes on the genus Lentipes (Teleostei: Gobiidae). Ichthyol Explor Fresh 4(3):201–232
Hoese DF, Gill AC (1993) Phylogenetic relationships of Eleotrid fishes (Perciformes: Gobioidei). Bull Mar Sci 52(1):415–440
Iida M, Watanabe S, Tsukamoto K (2009) Life history characteristics of a Sicydiinae Goby in Japan, compared with its relatives and other Amphidromous fishes. Am Fisheries Soc Symposium 69:355–373
Iturralde-Vinent MA, Mac Phee RDE (1999) Paleogeography of Caribbean Region: implications for Cenozoic biogeography. Bull Amer Mus Nat Hist 238:1–95
Jobb G, von Haeseler A, Strimmer K (2004) Treefinder: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4:18
Keith P (2003) Biology and ecology of amphidromous Gobiidae in the Indo-pacific and the Caribbean regions. J Fish Biol 63(4):831–847
Keith P, Lord C (2010a) Tropical freshwater gobies: Amphidromy as a life cycle In:Patzner RA, Van Tassell JL, Kovacic M, Kapoor BG (eds) The Biology of Gobies. Science Publishers Inc, in press)
Keith P, Lord C (2010b) Systematics of Sicydiinae In: Patzner RA, Van Tassell JL, Kovacic M, Kapoor BG (eds) The Biology of Gobies. Science Publishers Inc, (in press)
Keith P, Marquet G (2007) Stiphodon rubromaculatus, a new species of freshwater goby from Futuna island (Teleostei: Gobioidei: Sicydiinae). Cybium 31(1):45–49
Keith P, Watson R, Marquet G (2000) Découverte d’Awaous ocellaris (Broussonet, 1782) (Perciformes, Gobiidae) en Nouvelle-Calédonie et au Vanuatu et conséquences biogéographiques. Cybium 24(4):350–400
Keith P, Watson RE, Marquet G (2004) Sicyopterus aiensis, a new species of freshwater goby from Vanuatu (Teleostei: Gobioidei). Cybium 28(2):111–118
Keith P, Galewski T, Cattaneo-Berrebi G, Hoareau T, Berrebi P (2005a) Ubiquity of Sicyopterus lagocephalus (Teleostei: Gobioidei) and phylogeography of the genus Sicyopterus in the Indo-Pacific area inferred from mitochondrial cytochrome b gene. Mol Phylogenet Evol 37:721–732
Keith P, Hoareau T, Bosc P (2005b) A new species of freshwater goby (Pisces: Teleostei: Gobioidei) from Mayotte island (Comoros) and comments about the genus Cotylopus endemic to Indian Ocean. J Nat Hist 39(17):1395–1405
Keith P, Lord C, Vigneux E (2006a) In vivo observations on postlarval development of freshwater gobies and eleotrids from French Polynesia and New Caledonia. Ichthyol Expl Fresh 17(2):187–191
Keith P, Marquet G, Valade P, Bosc P, Vigneux E (2006b) Atlas des poissons et crustacés d’eau douce des Comores, Mascareignes et Seychelles. Muséum National d’Histoire Naturelle, Patrimoines naturels, Paris, vol 67, 158p
Keith P, Marquet G, Watson RE (2007a) Stiphodon kalfatak, a new species of freshwater goby from Vanuatu (Teleostei: Gobioidei: Sicydiinae). Cybium 31(1):33–37
Keith P, Marquet G, Watson RE (2007b) Akihito futuna, a new species of freshwater goby from the South Pacific (Teleostei: Gobioidei: Sicydiinae). Cybium 31(4):471–476
Keith P, Hoareau T, Lord C, Ah-Yane O, Gimmoneau G, Robinet T, Valade P (2008) Characterisation of post-larval to juvenile stages, metamorphosis, and recruitment of an amphidromous goby, Sicyopterus lagocephalus (Pallas, 1767) (Teleostei: Gobiidae: Sicydiinae). Mar Fresh Res 59(10):876–889
Keith P, Lord C, Marquet G, Kalfatak D (2009) Biodiversity and biogeography of amphidromous fishes from New Caledonia, a comparison to Vanuatu. Zoologica Neocaledonica 7. Biodiversity studies in New Caledonia. Mem Mus natl Hist nat 198:175–183
Kuroki M, Aoyama J, Wouthuyzen S, Sumardhiharga K, Miller MJ, Tsukamoto K (2007) Age and growth of Anguilla bicolor bicolor leptocephali in the eastern Indian Ocean. J Fish Biol 70:538–550
Lewis PO (2001) A likelihood approach to estimating phylogeny from discrete 750 morphological character data. Syst Biol 50:913–925
Lord C, Keith P (2006) Threatened fishes of the world: Protogobius attiti (Watson and Pöllabauer, 1998) (Rhyacichthyidae). Env Biol Fishes 77:101–102
Lord C, Keith P (2008) Threatened fishes of the world: Sicyopterus sarasini Weber & De Beaufort (Gobiidae). Env Biol Fishes 83(2):169–170
Lord C, Brun C, Hautecoeur M, Keith P (2010) Comparison of the duration of the marine larval phase estimated by otolith microstructural analysis of three amphidromous Sicyopterus species (Gobiidae: Sicydiinae) from Vanuatu and New Caledonia: insights on endemism. Ecol Fresh Fish 19:26–38
Maddison WP, Maddison DR (2009) Mesquite: a modular system for evolutionary analysis. Version 2:7
McDowall RM (2007) On amphidromy, a distinct form of diadromy in aquatic organisms. Fish Fisheries 8(1):1–13
McDowall RM (2009a) Early hatch: a strategy for safe downstream larval transport in amphidromous gobies. Rev Fish Biol Fisheries 19:1–8
McDowall RM (2009b) Why be amphidromous: expatrial dispersal and the place of source and sink population dynamics? Rev Fish Biol Fisheries, published on line: 30 June 2009
Mukai H (1992) Biogeography of the tropical seagrasses in the western Pacific. Aus J Mar Fresh Res 44:1–17
Murphy CA, Cowan JH (2007) Production, marine larval retention or dispersal, and recruitment of Amphidromous Hawaiian Gobioids: issues and implications. In: Evenhuis NL, Fizsimons JM (eds) Biology of Hawaiian streams and estuaries. Bish Mus Bull Cult Envir Stud 3:63–74
Muss A, Robertson DR, Stepien CA, Wirtz P, Bowen BW (2001) Phylogeography of Ophioblennius: the role of ocean currents and geography in reef fish evolution. Evolution 55:561–572
Nelson JS (2006) Fishes of the world. John Wiley & Sons, Inc. p. 600
Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala
Palumbi SR (1996a) Nucleic Acids II: The Polymerised Chain Reaction. In: Hillis DM, Moritz C, Mable BK (eds) Molecular Systematics, Sinauer Associates Inc, pp 205–247
Palumbi SR (1996b) What can molecular genetics contribute to marine biogeography? An urchin’s tale. J Exp Mar Biol Ecol 203:75–92
Pandolfi JM (1992) Successive isolation rather than evolutionary centres for the origination of the Indo-Pacific reef corals. J Biogeogr 19:593–609
Parenti LR (1991) Ocean basins and the biogeography of freshwater fishes. Aust Syst Bot 4:137–149
Parenti LR, Maciolek JA (1993) New sicydiine gobies from Ponape and Palau, Micronesia, with comments on the systematics of the subfamily Sicydiinae (Teleostei: Gobiidae). Bull Mar Sci 53:945–972
Parenti LR, Thomas KR (1998) Pharyngeal jaw morphology and homology in Sicydiine gobies (Teleostei: Gobiidae) and allies. J Morphology 237:257–274
Pezold F (1993) Evidence for a monophyletic Gobiinae. Copeia 3:634–643
Pezold F, Iwamoto T, Harrison IJ (2006) Multivariate analysis of sicydiines of São Tomé & Príncipe with redescription of Sicydium brevifile and S. bustamantei (Teleostei: Gobiidae) and a key to west African sicydiines. The California Academy of Sciences Gulf of Guinea Expedition (2201). V Proc Calif Acad Sci (Ser. 4) 57 (34):965–980
Planes S (1993) Genetic differentiation in relation to restricted larval dispersal of the convict surgeonfish Acanthurus triostegus in French Polynesia. Mar Ecol Prog Ser 98:237–246
Planes S, Galzin R (1997) New perspectives in biogeography of coral reef fish in the Pacific using phylogeography and population genetics approaches. Vie Milieu 47(4):375–380
Radtke RL, Kinzie RA (1996) Evidence of a marine larval stage in endemic Hawaiian stream gobies from isolated high-elevation localities. Trans Am Fish Soc 125:613–621
Radtke RL, Kinzie RA, Folsom SD (1988) Age at recruitment of Hawaiian freshwater gobies. Envir Biol Fishes 23:205–213
Rambaut A (2008) Fig Tree v.1.1.2. Institute of Evolutionary biology, University of Endinburgh, England
Rambaut A, Drummond AJ (2007) Tracer v1.4, Available from http://beast.bio.ed.ac.uk/Tracer
Robinet T, Feunteun E, Réveillac E, Keith P, Marquet G, Olivier JM, Valade P (2007) Eel community structure, fluvial recruitment of Anguilla marmorata and indication for a weak local production of spawners from rivers of Réunion and Mauritius islands. Envir Biol Fishes 78:93–105
Rocha LA, Robertson RD, Rocha CR, Tassell JL, Craig MT, Bowen BW (2005) Recent invasion of the tropical Atlantic by an Indo-Pacific coral reef fish. Mol Ecol 14(13):3921–3928
Rosen BR (1988) Progress, problems and patterns in the biogeography of reef corals and other tropical marine organisms. Helg Meer 42:269–301
Sakai H, Nakamura M (1979) Two new species of freshwater gobies (Gobiidae: Sicydiaphiinae) from Ishigaki Island, Japan. Jap J Ichthyol 26:43–54
Shafer DJ (1998) Evaluation of periodic and a periodic otolith microchemistry a nd somatic-otolith scaling for use in retrospective life history analysis of a tropical marine goby, Bathygobius coalitus. Mar Ecol Prog Ser 199:217–229
Shen KN, Tzeng WN (2002) Formation of a metamorphosis check in otolith of the amphidromous goby Sicyopterus japonicus. Mar Ecol Prog Ser 228:205–211
Springer VG (1982) Pacific plate Biogeography with Secial Reference to Shorefishes. Smiths Contrib Zool 367:1–182
Stoddart DR (1992) Biogeography of the Tropical Pacific. Pacific Sci 46:276–293
Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (* and Other Methods), 4. Sinauer Associates, Sunderland, MA
Thacker C (2003) Molecular phylogeny of the gobioid fishes. Mol Phylogenet Evol 26:354–368
Thacker C (2009) Phylogeny of Gobioidei and placement within Acanthomorpha, with a new classification and investigation of diversification and character evolution. Copeia 1:93–104
Tsukamoto K, Aoyama J (1998) Evolution of freshwater eels of the genus Anguilla: a probable scenario. Env Biol Fishes 52:139–148
Valade P, Lord C, Bosc P, Iida M, Tsukamoto K, Keith P (2009) Early life history and description of larval stages of an amphidromous goby, Sicyopterus lagocephalus (Pallas 1767) (Teleostei: Gobiidae: Sicydiinae). Cybium 33(4):309–319
Veron JEN (1995) Corals in space and time. The biogeography and evolution of the Scleractinia. University of New South Wales Press, Sydney
Victor BC (1986) Delayed metamorphosis with reduced larval growth in a coral reef fish (Thalassoma bifasciatum). Can J Fisheries Aquat Sci 43(6):1208–1213
Victor BC, Wellington GM (2000) Endemism and pelagic larval duration of reef fishes in the eastern Pacific Ocean. Mar Ecol Prog Ser 205:241–248
Wallace CC, Pandolfi JM, Ross R, Cronin TM (1989) Indo-Pacific coral biogeography: a case study from the Acropora selago group. Aust Biogeo 4:199–210
Wang HY, Tsai MP, Dean J, Lee SC (2001) Molecular phylogeny of Gobiod fishes (Perciformes:Gobioidei) based on mitochondrial 12 s rRNA sequences. Mol Phylogenet Evol 20(3):390–408
Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Phil Trans R Soc B 360(1462):1847–1857
Watson RE (1995) Review of the freshwater goby genus Cotylopus (Pisces, Teleostei, Gobiidae, Sicydiinae). Ichthyol Expl Fresh 6(1):61–70
Watson RE (1999) Two new subgenera of Sicyopus, with a redescription of Sicyopus zosterophorum (Teleostei: Gobioidei: Sicydiinae). Aqua J Ichthyol Aquat Biol 3:93–104
Watson RE (2000) Sicydium from the Dominican Republic with description of a new species (Teleostei: Gobiidae). Stutt Beitr Naturk (A) Biol 608(31):1–31
Watson RE, Marquet G, Pöllabauer C (2000) New Caledonia Fish Species of the genus Sicyopterus (Teleostei: Gobiodei: Sicydiinae). Aqua J Ichthyol Aquat biol 4(1):5–34
Watson RE, Keith P, Marquet G (2001) Sicyopus (Smilosicyopus) chloe, a new species of freshwater goby from New Caledonia (Teleostei: Gobioidei: Sicydiinae). Cybium 25(1):41–52
Watson RE, Keith P, Marquet G (2002) Lentipes kaaea, a new species of freshwater goby from New Caledonia (Teleostei: Gobioidei: Sicydiinae). Bull Fr Pêche Piscic 364:173–185
Watson RE, Keith P, Marquet G (2005) Stiphodon sapphirinus, a new species of freshwater goby from New Caledonia (Teleostei: Gobioidei: Sicydiinae). Cybium 29(4):339–345
Watson RE, Keith P, Marquet G (2007) Akihito vanuatu, a new genus and new species of freshwater goby from the South Pacific (Teleostei: Gobioidei: Sicydiinae). Cybium 31(3):341–349
Wellington GM, Victor BC (1989) Planktonic larval duration of one hundred species of Pacific and Atlantic damselfishes (Pomacentridae). Mar Biol 101:557–567
Wilson DT, McCormick MI (1999) Microstructure of settlement-marks in the otolith of tropical reef fishes. Mar Biol 134:29–410
Winnepenninckx B, Backeljau T, Wachter RD (1993) Extraction of high molecular weight DNA from molluscs. T. I. G. 9:407
Yamasaki N, Maeda K, Tachihara K (2007) Pelagic larval duration and morphology at recruitment of Stiphodon percopterygionus (Gobiidae: Sicydiinae). Raffles Bull Zool Suppl 14:209–214
Acknowledgments
Firstly, we would like to thank all the partners that have financially supported this work: the New Caledonian Government and the Muséum National d’Histoire Naturelle of Paris (PPF Structure et Evolution des Ecosystèmes and Leg Prevost) for C. Lord’s PhD fellowship; the BIONEOCAL ANR and the “Fondation de France”. We also thank the Vanuatu Environment Unit (D. Kalfatak) and the New Caledonian North and South Provinces (J-J. Cassan, J. Manauté and C. Méresse) for allowing sampling (permit No 1224-08/PS). This work was supported by the ‘Consortium National de Recherche en Génomique’, and the ‘Service de Systématique Moléculaire’ of the Muséum National d’Histoire Naturelle (IFR 101). It is part of the agreement number 2005/67 between the Genoscope and the Muséum national d’Histoire naturelle on the project ‘Macrophylogeny of life’ directed by G. Lecointre. This study was made possible with the assistance for sampling expeditions or with the help of many colleagues working in all the areas studied: G. Marquet, E. Vigneux, J. Keith, D. Kalfatak, D. Labrousse, C. Flouhr, I. Yahaya, R. Galzin, A. Jenkins, P. Lim, K. Maeda, Dr Mukai, D. Monti, F. Pezold, G. Ségura, J. Atherton, R. Nari, C. Butin, S. Lavoué, P. Valade and P. Bosc. Finally, we want to extend our thanks to D. Lord, native English speaker, for rereading this manuscript. This paper was improved by the comments of B. Santer and two anonymous reviewers.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. I. Taylor.
An erratum to this article can be found at http://dx.doi.org/10.1007/s00227-010-1603-5
Rights and permissions
About this article
Cite this article
Keith, P., Lord, C., Lorion, J. et al. Phylogeny and biogeography of Sicydiinae (Teleostei: Gobiidae) inferred from mitochondrial and nuclear genes. Mar Biol 158, 311–326 (2011). https://doi.org/10.1007/s00227-010-1560-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-010-1560-z