Marine Biology

, Volume 161, Issue 5, pp 1113–1126 | Cite as

Complex genetic structure of a euryhaline marine fish in temporarily open/closed estuaries from the wider Gulf of Aden

  • Edouard Lavergne
  • Isabelle Calvès
  • Anne Leila Meistertzheim
  • Grégory Charrier
  • Uwe Zajonz
  • Jean Laroche
Original Paper

Abstract

Temporarily open/closed estuaries (TOCEs) are major ecosystems of the Indian Ocean coastal zones. Their functioning is tightly linked to climatic events such as monsoons and storms, and their mouth can close up for prolonged and variable periods of time, thus limiting their connectivity with the marine environment. Two types of genetic markers (i.e., mitochondrial cytochrome c oxidase I (COI) gene and microsatellites) were used to assess the genetic structure of 288 individuals of Terapon jarbua, a widely distributed fish species in the wider Gulf of Aden. Firstly, the hypothesis of panmixia was tested. Then, alternative hypotheses were investigated to explain the population genetic structure of T. jarbua: could it be shaped by (1) regional biogeographic barriers (i.e., Socotra Island vs. mainland Yemen) and/or (2) the particular functioning of TOCEs in relation to the species life cycle and particular physical ocean parameters? On one hand, the polymorphism of the COI inferred (1) a high haplotype diversity and a reduced nucleotide diversity over the whole data set and (2) a “star-like” shape of the haplotype network, thus suggesting a population expansion after local extinctions during the Pleistocene glaciations. On a second hand, the genotyping of eight microsatellites showed a significant genetic differentiation between T. jarbua populations in the wider Gulf of Aden (FST = 0.035, p < 0.01), and thus, the panmixia hypothesis was rejected. Analyses of molecular variance results did not show any significant structure between Socotra Island and mainland Yemen and thus did not support the role of biogeographic barriers in structuring T. jarbua populations. Significant multi-locus deficits in heterozygotes at particular locations displaying high levels of FIS were recorded. It was suggested that a possible Wahlund effect took place in those TOCEs which could gather several cohorts of larvae stemming from different marine subpopulations over the sampled area. The present study emphasized the uniqueness of each TOCE as a potential reservoir of biodiversity and the urgent need for a better conservation program of those estuaries in the region, in order to avoid habitat fragmentation and permanent closure of those nursery areas by human activities.

Supplementary material

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Supplementary material 1 (DOCX 80 kb)
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Supplementary material 2 (DOCX 38 kb)
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Supplementary material 3 (EPS 51 kb)
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Supplementary material 4 (EPS 58 kb)

References

  1. Avise JC (2004) Molecular markers, natural history, and evolution. Sinauer Associates, SunderlandGoogle Scholar
  2. Baker AM, Hughes JM, Dean JC, Bunn SE (2004) Mitochondrial DNA reveals phylogenetic structuring and cryptic diversity in Australian freshwater macroinvertebrate assemblages. Mar Freshw Res 55(6):629–640. doi:10.1071/MF04050 CrossRefGoogle Scholar
  3. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX v.4.05. Logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier, FranceGoogle Scholar
  4. Borkenhagen K, Esmaeili HR, Mohsenzadeh S, Shahryari F, Gholamifard A (2011) The molecular systematics of the Carasobarbus species from Iran and adjacent areas, with comments on Carasobarbus albus (Heckel, 1843). Environ Biol Fishes 91(3):327–335. doi:10.1007/s10641-011-9787-1 CrossRefGoogle Scholar
  5. Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5(3):453–455. doi:10.1046/j.1365-294X.1996.00098.x CrossRefGoogle Scholar
  6. Calvès I, Lavergne E, Meistertzheim AL, Charrier G, Cabral H, Guinand B, Quiniou L, Laroche J (2013) Genetic structure of European flounder Platichthys flesus: effects of both the southern limit of the species’ range and chemical stress. Mar Ecol Prog Ser 472:257–273. doi:10.3354/meps09797 CrossRefGoogle Scholar
  7. Carr MH, Reed DC (1993) Conceptual issues relevant to marine harvest refuges: examples from temperate reef fishes. Can J Fish Aquat Sci 50(9):2019–2028. doi:10.1139/f93-226 CrossRefGoogle Scholar
  8. Cavalli-Sforza LL, Edwards AW (1967) Phylogenetic analysis. Models and estimation procedures. Am J Hum Genet 19:233–257Google Scholar
  9. Chang EH, Menezes M, Meyer NC, Cucci RA, Vervoort VS, Schwartz CE, Smith RJ (2004) Branchio-oto-renal syndrome: the mutation spectrum in EYA1 and its phenotypic consequences. Hum Mutat 23(6):582–589. doi:10.1002/humu.20048 CrossRefGoogle Scholar
  10. Chapius MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24(3):621–631. doi:10.1093/molbev/msl191 CrossRefGoogle Scholar
  11. Chapuis MP, Estoup A (2006) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24(3):621–631. doi:10.1093/molbev/msl191 CrossRefGoogle Scholar
  12. Charrier G, Chenel T, Durand J, Girard M, Quiniou L, Laroche J (2006) Discrepancies in phylogeographical patterns of two European anglerfishes (Lophius budegassa and Lophius piscatorius). Mol Phylogenet Evol 38(3):742–754. doi:10.1016/j.ympev.2005.08.002 CrossRefGoogle Scholar
  13. Clement M, Posada D, Crandall KA (2000) TCS. A computer program to estimate gene genealogies. Mol Ecol 9(10):1657–1660. doi:10.1046/j.1365-294x.2000.01020.x CrossRefGoogle Scholar
  14. Corlett RT (2010) Invasive aliens on tropical East Asian islands. Biodivers Conserv 19(2):411–423. doi:10.1007/s10531-009-9624-4 CrossRefGoogle Scholar
  15. Cowley PD, Whitfield AK (2001) Ichthyofaunal characteristics of a typical temporarily open/closed estuary on the south east coast of South Africa. Ichthyol Bull 71:1–17Google Scholar
  16. Craig MT, Eble JA, Bowen BW, Robertson DR (2007) High genetic connectivity across the Indian and Pacific Oceans in the reef fish Myripristis berndti (Holocentridae). Mar Ecol Prog Ser 334:245–254. doi:10.3354/meps334245 CrossRefGoogle Scholar
  17. Crandall KA, Templeton AR, Sing CF (1994) Intraspecific phylogenetics: problems and solutions. In: Scotland RW, Siebert DJ, Williams DM (eds) Models in phylogeny reconstruction. Published for the Systematics Association by Clarendon Press; Oxford University Press, Oxford, pp 273–297. 0198548249 Google Scholar
  18. Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10:556–557. doi:10.1111/j.1755-0998.2009.02801.x CrossRefGoogle Scholar
  19. Currie RJ, Fisher AE, Hargreaves PM (1973) Arabian sea upwelling. In: Zeitzschel B, Gerlach SA (eds) The biology of the Indian Ocean. Springer, Berlin, pp 37–52CrossRefGoogle Scholar
  20. Dalmasso A, Fontanella E, Piatti P, Civera T, Secchi C, Bottero M (2007) Identification of four tuna species by means of real-time PCR and melting curve analysis. Vet Res Commun 31(S1):355–357. doi:10.1007/s11259-007-0036-1 CrossRefGoogle Scholar
  21. Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc Ser B (Methodol) 39(1):1–38Google Scholar
  22. DeVantier L, De’ath G, Klaus R, Al-Moghrabi S, Abdulaziz M, Reinicke GB, Cheung C (2004) Reef-building corals and coral communities of the Socotra Archipelago, a zoogeographic “crossroads” in the Arabian Sea. Fauna Arab 20:117–168Google Scholar
  23. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2011) Geneious v.5.4. http://www.geneious.com
  24. Duran S, Palacin C, Becerro MA, Turon X, Giribet G (2004) Genetic diversity and population structure of the commercially harvested sea urchin Paracentrotus lividus (Echinodermata, Echinoidea). Mol Ecol 13(11):3317–3328. doi:10.1111/j.1365-294X.2004.02338.x CrossRefGoogle Scholar
  25. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14(8):2611–2620. doi:10.1111/j.1365-294X.2005.02553.x CrossRefGoogle Scholar
  26. Excoffier L, Lischer HEL (2010) Arlequin suite v. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10(3):564–567. doi:10.1111/j.1755-0998.2010.02847.x CrossRefGoogle Scholar
  27. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131(2):479–491Google Scholar
  28. Forsskål P (1775) Descriptiones animalium avium, amphibiorum, piscium, insectorum, vermium; quae in itinere orientali observavit. Copenhagen, MölleriGoogle Scholar
  29. Fratini S, Vannini M (2002) Genetic differentiation in the mud crab Scylla serrata (Decapoda: Portunidae) within the Indian Ocean. J Exp Mar Biol Ecol 272(1):103–116. doi:10.1016/S0022-0981(02)00052-7 CrossRefGoogle Scholar
  30. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147(2):915–925Google Scholar
  31. Gaither MR, Toonen RJ, Robertson DR, Planes S, Bowen BW (2010) Genetic evaluation of marine biogeographical barriers: perspectives from two widespread Indo-Pacific snappers (Lutjanus kasmira and Lutjanus fulvus). J Biogeogr 37(1):133–147. doi:10.1111/j.1365-2699.2009.02188.x CrossRefGoogle Scholar
  32. Gill AC (2004) Revision of the Indo-Pacific dottyback fish subfamily Pseudochrominae (Perciformes: Pseudochromidae). South African Institute for Aquatic Biodiversity, Grahamstown, South Africa. 0-86810-399-3 Google Scholar
  33. Gill AC, Kemp JM (2002) Widespread Indo-Pacific shore-fish species: a challenge for taxonomists, biogeographers, ecologists, and fishery and conservation managers. Environ Biol Fishes 65(2):165–174. doi:10.1023/A:1020044616889 CrossRefGoogle Scholar
  34. Gill AC, Zajonz U (2011) Pseudochromine and pseudoplesiopine dottyback fishes from the Socotra Archipelago, Indian Ocean, with descriptions of two new species of Pseudochromis Rüppell (Perciformes: Pseudochromidae). Zootaxa 3106:1–23Google Scholar
  35. Glynn PW (1993) Monsoonal upwelling and episodic Acanthaster predation as probable controls of coral reef distribution and community structure in Oman, Indian Ocean. Atoll Res Bull 379:1–66CrossRefGoogle Scholar
  36. Golani D, Appelbaum-Golani B (2010) First record of the Indo-Pacific fish the Jarbua terapon (Terapon jarbua) (Osteichthyes: Terapontidae) in the Mediterranean with remarks on the wide geographical distribution of this species. Sci Mar 74(4):717–720. doi:10.3989/scimar.2010.74n4717 CrossRefGoogle Scholar
  37. Gower JC (1966) Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53(3–4):325–338. doi:10.1093/biomet/53.3-4.325 CrossRefGoogle Scholar
  38. Grant WS, Waples RS (2000) Spatial and temporal scales of genetic variability in marine and anadromous species. Implications for fisheries oceanography. In: Harrison PJ, Parsons TR (eds) Fisheries oceanography. An integrative approach to fisheries ecology and management. Blackwell Science, Oxford, pp 61–93Google Scholar
  39. Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48(2):361–372CrossRefGoogle Scholar
  40. Harold AS, Winterbottom R, Munday PL, Chapman RW (2008) Phylogenetic relationships of Indo-Pacific coral gobies of the genus Gobiodon (Teleostei Gobiidae), based on morphological and molecular data. Bull Mar Sci 82(1):119–136Google Scholar
  41. Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66(4):591–600Google Scholar
  42. Harrison TD, Whitfield AK (1995) Fish community structure in three temporarily open/closed estuaries on the Natal coast. Ichthyol Bull 64:1–80Google Scholar
  43. He L, Zhang A, Zhu C, Weese D, Qiao Z (2011) Phylogeography of the mud crab (Scylla serrata) in the Indo-West Pacific reappraised from mitochondrial molecular and oceanographic clues: transoceanic dispersal and coastal sequential colonization. Mar Ecol 32(1):52–64. doi:10.1111/j.1439-0485.2010.00406.x CrossRefGoogle Scholar
  44. Hoarau G, Rijnsdorp AD, Van der Veer HW, Stam WT, Olsen JL (2002) Population structure of plaice (Pleuronectes platessa L.) in northern Europe: microsatellites revealed large-scale spatial and temporal homogeneity. Mol Ecol 11(7):1165–1176. doi:10.1046/j.1365-294X.2002.01515.x CrossRefGoogle Scholar
  45. Hoareau TB, Bosc P, Valade P, Berrebi P (2007) Gene flow and genetic structure of Sicyopterus lagocephalus in the South-western Indian Ocean, assessed by intron-length polymorphism. J Exp Mar Biol Ecol 349(2):223–234. doi:10.1016/j.jembe.2007.05.015 CrossRefGoogle Scholar
  46. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9(5):1322–1332. doi:10.1111/j.1755-0998.2009.02591.x CrossRefGoogle Scholar
  47. Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5(3):299–314Google Scholar
  48. Ivanova NV, Dewaard JR, Hebert PDN (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol Ecol Notes 6(4):998–1002. doi:10.1111/j.1471-8286.2006.01428.x CrossRefGoogle Scholar
  49. Jakobsson M, Edge MD, Rosenberg NA (2013) The relationship between FST and the frequency of the most frequent allele. Genetics 193(2):515–528. doi:10.1534/genetics.112.144758 CrossRefGoogle Scholar
  50. Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17(18):4015–4026. doi:10.1111/j.1365-294X.2008.03887.x CrossRefGoogle Scholar
  51. Jost L (2009) D vs. GST: response to Heller and Siegismund (2009) and Ryman and Leimar (2009). Mol Ecol 18(10):2088–2091. doi:10.1111/j.1365-294X.2009.04186.x CrossRefGoogle Scholar
  52. Kemp JM (1998) Zoogeography of the coral reef fishes of the Socotra Archipelago. J Biogeogr 25(5):919–933. doi:10.1046/j.1365-2699.1998.00249.x CrossRefGoogle Scholar
  53. Klaus R, Turner JR (2004) The marine biotopes of the Socotra Island Group. Fauna Arab 20:45–115Google Scholar
  54. Klausewitz W, Nielsen JG (1965) On Forsskål’s collection in the Zoological Museum of Copenhagen. Spolia Zoolgical Museum Hauniensis, Copenhagen, pp 1–29Google Scholar
  55. Lakra WS, Verma MS, Goswami M, Lal KK, Mohindra V, Punia P, Gopalakrishnan A, Singh KV, Ward RD, Hebert PDN (2011) DNA barcoding Indian marine fishes. Mol Ecol Resour 11(1):60–71. doi:10.1111/j.1755-0998.2010.02894.x CrossRefGoogle Scholar
  56. Lavergne E (2012) Estuarine fish biodiversity of Socotra Island (North-Western Indian Ocean): from the community to the functioning of Terapon jarbua populations. Ph.D. thesis, University of Western Brittany, France. http://tel.archives-ouvertes.fr/tel-00806383
  57. Lavergne E, Calvès I, Zajonz U, Laroche J (2011) Isolation and characterization of nine microsatellite loci of Terapon jarbua (Forsskål, 1775) from Socotra Island (Gulf of Aden) using multiplex PCR. Electronic supplement to Agostini et al. Permanent Genetic Resources added to Molecular Ecology Resources Database 1 October 2010–2030 November 2010. Mol Ecol Resour 11(2): 418–421. 10.1111/j.1755-0998.2010.02970.x
  58. Lavergne E, Zajonz U, Sellin L (2013) Length-weight relationships of Terapon jarbua (Forsskål, 1775) from the North-Western Indian Ocean including Socotra Island. J Appl Ichthyol 29(1):274–277. doi:10.1111/j.1439-0426.2012.02018.x CrossRefGoogle Scholar
  59. Liu JX, Tatarenkov A, Beacham TD, Gorbachev V, Wildes S, Avise JC (2011) Effects of Pleistocene climatic fluctuations on the phylogeographic and demographic histories of Pacific herring (Clupea pallasii). Mol Ecol 20(18):3879–3893. doi:10.1111/j.1365-294X.2011.05213.x CrossRefGoogle Scholar
  60. Malewski T, Draber-Mońko A, Pomorski J, Łoś M, Bogdanowicz W (2010) Identification of forensically important blowfly species (Diptera: Calliphoridae) by high-resolution melting PCR analysis. Int J Leg Med 124(4):277–285. doi:10.1007/s00414-009-0396-x CrossRefGoogle Scholar
  61. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27(2 Part 1):209–220Google Scholar
  62. Meistertzheim AL, Calvès I, Artigaud S, Friedman CS, Paillard C, Laroche J, Ferec C (2012) High resolution melting analysis for fast and cheap polymorphism screening of marine populations. Protoc Exch. doi:10.1038/protex.2012.015 Google Scholar
  63. Miu TC, Lee SC, Tzeng WN (1990) Reproductive biology of Terapon jarbua from the estuary of Tamshui River. J Fish Soc Taiwan 17(1):9–20Google Scholar
  64. Moran M (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100(2):403–405. doi:10.1034/j.1600-0706.2003.12010.x CrossRefGoogle Scholar
  65. Morant P, Quinn N (1999) Influence of man and management of South African estuaries. In: Allanson BR, Baird D (eds) Estuaries of South Africa. Cambridge University Press, Cambridge, pp 289–321CrossRefGoogle Scholar
  66. Nielsen JG (1974) Fish types in the Zoological Museum of Copenhagen. University of Copenhagen, Denmark, p 115Google Scholar
  67. Nielsen EE, Nielsen PH, Meldrup D, Hansen MM (2004) Genetic population structure of turbot (Scophthalmus maximus L.) supports the presence of multiple hybrid zones for marine fishes in the transition zone between the Baltic Sea and the North Sea. Mol Ecol 13(3):585–595. doi:10.1046/j.1365-294X.2004.02097.x CrossRefGoogle Scholar
  68. Nielsen EE, Hansen MM, Meldrup D (2006) Evidence of microsatellite hitch-hiking selection in Atlantic cod (Gadus morhua L.): implications for inferring population structure in nonmodel organisms. Mol Ecol 15(11):3219–3229. doi:10.1111/j.1365-294X.2006.03025.x CrossRefGoogle Scholar
  69. Nielsen EE, Hemmer-Hansen J, Larsen PF, Bekkevold D (2009) Population genomics of marine fishes: identifying adaptive variation in space and time. Mol Ecol 18(15):3128–3150. doi:10.1111/j.1365-294X.2009.04272.x CrossRefGoogle Scholar
  70. O’Connell M, Wright JM (1997) Microsatellite DNA in fishes. Rev Fish Biol Fish 7(3):331–363. doi:10.1023/A:1018443912945 CrossRefGoogle Scholar
  71. Perissinotto R, Stretch DD, Whitfield AK, Adams JB, Forbes AT, Demetriades NT (2010) Temporarily open/closed estuaries in South Africa. Nova Science, New York, pp 978–1616684129Google Scholar
  72. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256. doi:10.1093/molbev/msn083 CrossRefGoogle Scholar
  73. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959Google Scholar
  74. Pulch H (2010) Autökologie und Populationsbiologie des endemischen Zwergbarsches Pseudochromis „sp.“(Perciformes: Pseudochromidae) vom Sokotra-Archipel. Diploma Thesis (M.Sc.), Goethe University, Frankfurt am Main, GermanyGoogle Scholar
  75. Raventos N, Macpherson E (2001) Planktonic larval duration and settlement marks on the otoliths of Mediterranean littoral fishes. Mar Biol 138(6):1115–1120. doi:10.1007/s002270000535 CrossRefGoogle Scholar
  76. Raymond M, Rousset F (1995) Genepop v. 1.2—population genetics software for exact tests and ecumenicism. J Hered 86(3):248–249Google Scholar
  77. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43(1):223–225. doi:10.2307/2409177 CrossRefGoogle Scholar
  78. Rogers AR, Harpending HC (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9(3):552–569Google Scholar
  79. Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8(1):103–106. doi:10.1111/j.1471-8286.2007.01931.x CrossRefGoogle Scholar
  80. Ryman N, Utter F, Laikre L (1995) Protection of intraspecific biodiversity of exploited fishes. Rev Fish Biol Fish 5(4):417–446. doi:10.1007/BF01103814 CrossRefGoogle Scholar
  81. Scholte P, De Geest P (2010) The climate of Socotra Island (Yemen): a first-time assessment of the timing of the monsoon wind reversal and its influence on precipitation and vegetation patterns. J Arid Environ 74(11):1507–1515. doi:10.1016/j.jaridenv.2010.05.017 CrossRefGoogle Scholar
  82. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18(2):233–234. doi:10.1038/72708 CrossRefGoogle Scholar
  83. Shadbolt AB, Ragai R (2010) Effects of habitat fragmentation on the movement patterns and dispersal ability of the brown spiny rat (Maxomys rajah) in the Planted Forest Zone of Sarawak, Eastern Malaysia. Biodivers Conserv 19(2):531–541. doi:10.1007/s10531-009-9729-9 CrossRefGoogle Scholar
  84. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139(1):457–462Google Scholar
  85. Slatkin M, Hudson R (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129(2):555–562Google Scholar
  86. Storey JD (2002) A direct approach to false discovery rates. J R Stat Soc Ser B (Stat Methodol) 64(3):479–498. doi:10.1111/1467-9868.00346 CrossRefGoogle Scholar
  87. Storey JD (2003) The positive false discovery rate: a Bayesian interpretation and the q-value. Ann Stat 31(6):2013–2035. doi:10.1214/aos/1074290335 CrossRefGoogle Scholar
  88. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595Google Scholar
  89. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526Google Scholar
  90. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132(2):619–633Google Scholar
  91. Van Damme K, Banfield L (2011) Past and present human impacts on the biodiversity of Socotra Island (Yemen): implications for future conservation. Zool Middle East Suppl 3:31–88CrossRefGoogle Scholar
  92. Van Niekerk L (2007) Hydrodynamics. In: Whitfield AK, Bate GC (eds) A review of information on temporarily open/closed estuaries in the warm and cool temperate biogeographic regions of South Africa, with particular emphasis on the influence of river flow on these systems. Report No. 1581/1/07, Water Research Commission, Gezina, South Africa, pp 1–20Google Scholar
  93. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4(3):535–538. doi:10.1111/j.1471-8286.2004.00684.x CrossRefGoogle Scholar
  94. Vari RP (1978) The terapon perches (Percoidei, Teraponidae): a cladistic analysis and taxonomic revision. Bull Am Mus Nat Hist 159(5):175–340Google Scholar
  95. Victor BC (1986) Duration of the planktonic larval stage of one hundred species of Pacific and Atlantic wrasses (family Labridae). Mar Biol 90(3):317–326. doi:10.1007/BF00428555 CrossRefGoogle Scholar
  96. Visram S, Yang MC, Pillay RM, Said S, Henriksson O, Grahn M, Chen CA (2010) Genetic connectivity and historical demography of the blue barred parrotfish (Scarus ghobban) in the western Indian Ocean. Mar Biol 157(7):1475–1487. doi:10.1007/s00227-010-1422-8 CrossRefGoogle Scholar
  97. Wahlund S (1928) Zusammensetzung von Populationen und Korrelationserscheinungen vom Standpunkt der Vererbungslehre aus betrachtet. Hereditas 11(1):65–106. doi:10.1111/j.1601-5223.1928.tb02483.x CrossRefGoogle Scholar
  98. Waldman B, McKinnon JS (1993) Inbreeding and outbreeding in fishes, amphibians and reptiles. In: Thornhill NW (ed) The Natural history of inbreeding and outbreeding. Theoretical and empirical perspectives. University of Chicago Press, Chicago, pp 250–282Google Scholar
  99. Wallace JH, Koh HM, Beckley LE, Bennett B, Blaber SJM, Whitfield AK (1984) South African estuaries and their importance to fishes. S Afr J Sci 80:203–207Google Scholar
  100. Wan QH, Wu H, Fujihara T, Fang SG (2004) Which genetic marker for which conservation genetics issue? Electrophoresis 25(14):2165–2176. doi:10.1002/elps.200305922 CrossRefGoogle Scholar
  101. Wang ZD, Guo YS, Liu XM, Fan YB, Liu CW (2012) DNA barcoding South China Sea fishes. Mitochondrial DNA 23(5):405–410. doi:10(3109/19401736),2012,710204 CrossRefGoogle Scholar
  102. Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89(5):438–450. doi:10.1093/jhered/89.5.438 CrossRefGoogle Scholar
  103. Ward RD, Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos Trans 360(1462):1847–1857. doi:10.1098/rstb2005.1716 CrossRefGoogle Scholar
  104. Weir BS (1996) Genetic data analysis: methods for discrete population genetic data, 2nd edn. Sinauer Associates, SunderlandGoogle Scholar
  105. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38(6):1358–1370. doi:10.2307/2408641 CrossRefGoogle Scholar
  106. Whitfield AK, Blaber SJM (1978) Scale-eating habits of the marine teleost Terapon jarbua (Forsskål, 1775). J Fish Biol 12(1):61–70. doi:10.1111/j.1095-8649.1978.tb04151.x CrossRefGoogle Scholar
  107. Whitfield AK, Bate GC, Adams JB, Cowley PD, Froneman PW, Gama PT, Strydom NA, Taljaard S, Theron AK, Turpie JK, Van Niekerk L, Wooldridge TH (2012) A review of the ecology and management of temporarily open/closed estuaries in South Africa, with particular emphasis on river flow and mouth state as primary drivers of these systems. Afr J Mar Sci 34(2):163–180. doi:10.2989/1814232X.2012.675041 CrossRefGoogle Scholar
  108. Whitlock MC (2011) G’ST and D do not replace FST. Mol Ecol 20:1083–1091. doi:10.1111/j.1365-294X.2010.04996.x CrossRefGoogle Scholar
  109. Winters KL, Herwerden L, Choat JH, Robertson DR (2010) Phylogeography of the Indo-Pacific parrotfish Scarus psittacus: isolation generates distinctive peripheral populations in two oceans. Mar Biol 157(8):1679–1691. doi:10.1007/s00227-010-1442-4 CrossRefGoogle Scholar
  110. Zajonz U, Khalaf MA, Krupp F (2000) Coastal fish assemblages of the Socotra Archipelago. In: Apel M, Krupp F, Hariri KI (eds) Conservation and sustainable use of biodiversity of Socotra Archipelago. Marine Habitat, Biodiversity and Fisheries Surveys and Management. Progress Report of Phase III (UNOPS YEM/96/G32, C-972248). Senckenberg Research Institute, Frankfurt a.M., Germany, pp 127–170Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Edouard Lavergne
    • 1
    • 2
    • 3
  • Isabelle Calvès
    • 3
  • Anne Leila Meistertzheim
    • 4
  • Grégory Charrier
    • 3
  • Uwe Zajonz
    • 1
    • 2
  • Jean Laroche
    • 3
  1. 1.Sektion IchthyologieSenckenberg Forschungsinstitut und NaturmuseumFrankfurt am MainGermany
  2. 2.Biodiversität und Klima Forschungszentrum (BiK-F)Frankfurt am MainGermany
  3. 3.Laboratoire des Sciences de l’Environnement Marin LEMAR, UMR 6539, CNRS/IRD/UBO/IFREMER, Institut Universitaire Européen de la Mer IUEMUniversité de Bretagne OccidentalePlouzanéFrance
  4. 4.Centre de Formation et de Recherche sur l’Environnement Méditerranéen (CEFREM), UMR 5110, CNRS/UPVDUniversité de PerpignanPerpignan CedexFrance

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