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Lack of mtDNA and morphological differentiation between two acorn barnacles Tetraclita japonica and T. formosana differing in parietes colours and geographical distribution

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Abstract

Tetraclita japonica and T. formosana are common intertidal barnacles with similar morphology, which leads to uncertainty in their species status. In the present study, we try to elucidate the taxonomic status of the two taxa using morphology and mitochondrial control region and cytochrome c oxidase subunit I (COI) sequences of the barnacles in their distribution range. The two taxa were found to be morphologically similar; a diagnostic difference between them was only observed in the colour of the parietes and opercular plates. Little genetic differentiation was detected in the control region and COI (ΦCT < 0.025 for both markers) between two taxa, but differentiation was found between the southern (Taiwan and Hong Kong) and northern (Japan) populations of T. japonica/T. formosana, which might be the result of isolation by distance and upwelling in summer. Our data suggest that the two presently recognized species probably represent two colour morphotypes of the same species exhibiting different geographical distribution. T. japonica is abundant in Japan and southeast coast of China, whereas T. formosana is only abundant in Taiwan. The heterogeneous environment might exert a divergent selection pressure leading to asymmetric distribution of the two colour morphotypes. The different colours might be a result of either phenotypic plasticity adaptive to environmental variables or genetic hitchhiking of local adaptive genotypes.

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References

  • Achituv Y, Borut A (1975) Temperature and water relation in Tetraclita squamosa rufotincta Pilsbry Cirripedia from the Gulf of Elat (Red Sea). In: Barnes H (ed) Proc 9th Europ Mar Biol Symp, Aberdeen University Press, Aberdeen, pp 95–108

    Google Scholar 

  • Achituv Y, Mizrahi L (1987) Allozyme differences between tidal levels in Tetraclita squamosa from the Red Sea. J Exp Mar Biol Ecol 108:181–189

    Article  Google Scholar 

  • Albertson RC, Markert JA, Danley PD, Kocher TD (1999) Phylogeny of a rapidly evolving clade: the cichlid fishes of Lake Malawi, East Africa. Proc Natl Acad Sci USA 96:5107–5110

    Article  CAS  Google Scholar 

  • Appelbaum L, Achituv Y, Mokady O (2002) Speciation and the establishment of zonation in an intertidal barnacle: specific settlement vs. selection. Mol Ecol 11:1731–1737

    Article  CAS  Google Scholar 

  • Bernardi G, Vagelli A (2004) Population structure in Banggai cardinalfish, Pterapogon kauderni, a coral reef species lacking a pelagic larval phase. Mar Biol 145:803–810

    Google Scholar 

  • Bonin A, Taberlet P, Miaud C, Pompanon F (2006) Explorative genome scan to detect candidate loci for adaptation along a gradient of altitude in the common frog (Rana temporaria). Mol Biol Evol 23:773–783

    Article  CAS  Google Scholar 

  • Campell D, Bernatchez L (2004) Generic scan using AFLP markers as a means to assess the role of divergent selection in the divergence of sympatric whitefish ecotypes. Mol Biol Evol 21:945–956

    Article  Google Scholar 

  • Chan BKK (2001) Studies on Tetraclita squamosa and Tetraclita japonica I: adult morphology. J Crustacean Biol 21:616–630

    Article  Google Scholar 

  • Chan BKK (2003) Studies on Tetraclita squamosa and Tetraclita japonica II: larval morphology and development. J Crustacean Biol 23:522–547

    Article  Google Scholar 

  • Chan BKK, Hung OS (2005) Cirral length of the acorn barnacle Tetraclita japonica: effect of wave exposure and tidal height. J Crustacean Biol 25:329–332

    Article  Google Scholar 

  • Chan BKK, Tsang LM, Chu KH (2006a) Morphological and genetic differentiation of Tetraclita squamosa (Crustacea, Cirripedia) in East Asia and description of a new species of Tetraclita. Zool Scr (in press)

  • Chan BKK, Morritt D, Depirro M, Leung KMY, Williams GA (2006b) Summer mortality: impacts on the distribution and abundance of the barnacle Tetraclita japonica on tropical shores. Mar Ecol Prog Ser (in press)

  • Chu KH, Li CP, Tam YK, Lavery S (2003) Application of mitochondrial control region in population genetic studies of the shrimp Penaeus. Mol Ecol Notes 3:120–122

    Article  CAS  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  Google Scholar 

  • Darwin C (1854) A monograph of the sub-class Cirripedia: the Balanidae, the Verrucidae etc. Ray Society, London

  • 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 86:991–1000

    Google Scholar 

  • Excoffier L, Laval LG, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    Article  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz RA, Vrijenhoek RC (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  Google Scholar 

  • Garm A (2004) Revising the definition of setae from the mouth apparatus of seven species of decapod crustaceans. J Morph 260:85–100

    Article  Google Scholar 

  • Hasegawa T, Yamaguchi T, Kojima S, Ohta S (1996) Phylogenetic analysis among three species of intertidal barnacles of the genus Tetraclita (Cirripedia: Balanomorpha) by nucleotide sequences of a mitochondrial gene. Benthos Res 51:33–39

    Article  Google Scholar 

  • Hiro F (1939) Studies on the cirripedian fauna of Japan IV: cirripedes of Formosa (Taiwan) with some geographical and ecological remarks on the littoral forms. Mem Coll Sci Kyoto Imp Univ B 15:245–284

    Google Scholar 

  • Ishizaka J, Fukushima H, Kishino M, Saino T, Takahashi M (1992) Phytoplankton pigment distributions in regional upwelling around the Izu Peninsula detected by coastal zone colour scanner on May 1982. J Oceanogr 48:305–327

    Article  CAS  Google Scholar 

  • Ito T, Kaneko A, Furukawa H, Gohda N, Koterayama W (1995) A structure of the Kuroshio and its related upwelling on the East China Sea Shelf slope. J Oceanogr 51:267–278

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420:73–90

    Article  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  CAS  Google Scholar 

  • Lee HJ, Chao SY (2003) A climatological description of circulation in and around the East China Sea. Deep-Sea Res II 50:1065–1084

    Article  Google Scholar 

  • Lively CM (1986) Predator-induced shell dimorphism in the acorn barnacle Cthtamalus anisopoma. Evolution 40:232–242

    Article  Google Scholar 

  • Moran P, Kornfield I (1993) Retention of ancestral polymorphism in the Mbuna species flock (Teleostei: Cichlidae) of Lake Malawi. Mol Biol Evol 10:1015–1029

    CAS  Google Scholar 

  • Mokady O, Loya Y, Achituv Y, Geffen E, Graur D, Rozenblatt S, Brickner I (1999) Speciation versus phenotypic plasticity in coral inhabiting barnacles: Darwin’s observations in an ecological context. J Mol Evol 49:367–375

    Article  CAS  Google Scholar 

  • Mokady O, Mizrahi L, Perl-Treves R, Achituv Y (2000) The different morphs of Chthamalus anisopoma: a phenotypic response? Direct molecular evidence. J Exp Mar Biol Ecol 243:295–304

    Article  CAS  Google Scholar 

  • Newman WA, Ross A (1976) Revision of the balanomorph barnacles; including a catalogue of the species. Mem San Diego Soc Nat Hist 9:1–108

    Google Scholar 

  • Palumbi SR, Cirpiano F, Hare MP (2001) Predicting nuclear coalescence from mitochondrial data: the three-times rule. Evolution 55:859–868

    Article  CAS  Google Scholar 

  • Parker A, Kornfield I (1997) Evolution of the mitochondrial DNA control region in the Mbuna (Cichlidae) species flock of Lake Malawai, East Africa. J Mol Evol 45:70–83

    Article  CAS  Google Scholar 

  • Pilsbry HA (1916) The sessile barnacles (Cirripedia) contained in the collection of the US National Museum: including a monograph of the American species. US Natl Mus Bull 93:241–353

    Google Scholar 

  • Ross A (1969) Studies on the Tetraclitidae (Cirripedia: Thoracica): revision of Tetraclita. Trans San Diego Soc Nat Hist 15:237–251

    Article  Google Scholar 

  • Ross A (1999) Studies on the Tetraclitidae (Cirripedia: Balanomorpha); new species of Tetraclita from the Red Sea. Pak J Mar Sci 8:41–53

    Google Scholar 

  • Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16:372–380

    Article  CAS  Google Scholar 

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:652–701

    Article  Google Scholar 

  • Sotka EE, Wares JP, Barth JA, Grosberg RK, Palumbi SR (2004) Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula. Mol Ecol 13:2143–2156

    Article  CAS  Google Scholar 

  • Southward AJ, Crisp DJ (1963) Barnacles of European waters. Catalogue of main marine fouling organisms Vol 1: barnacles. Organization for Economic Co-operation and Development, Paris

  • Swofford DL (2000) PAUP*: phylogenetic analysis using parsimony (*and other methods), ver 4. Sinauer, Sunderland, MA

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Proc Natl Acad Sci USA 22:4673–4680

    CAS  Google Scholar 

  • Tsoi KH, Wang ZY, Chu KH (2005) Genetic divergence between two morphologically similar varieties of the kuruma shrimp Penaeus japonicus. Mar Biol 147:367–379

    Article  CAS  Google Scholar 

  • Wares JP (2001) Patterns of speciation inferred from mitochondrial DNA in North American Chthamalus (Cirripedia: Balanomorpha: Chthamaloidea). Mol Phylogenet Evol 18:104–116

    Article  CAS  Google Scholar 

  • Wilding CS, Butlin RK, Grahame J (2001) Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. J Evol Biol 14:611–619

    Article  CAS  Google Scholar 

  • Yamaguchi Y (1987) Changes in the barnacle fauna since the Miocene and the infraspecific structure of Tetraclita in Japan (Cirripedia: Balanomorpha). Bull Mar Sci 41:337–350

    Google Scholar 

  • Zardus JD, Hadfield MG (2005) Multiple origins and incursions of the Atlantic barnacle Chthamalus proteus in the Pacific. Mol Ecol 14:3719–3733

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Mr. A. Murata (Natural History Museum and Institute, Chiba) for assistance in field work in Kominato, Prof. T. Yamaguchi and Dr. Romanus Prabrowo (Chiba University, Japan) for assistance in field work and providing specimens in Kurosaki, Prof. M. Yamaguchi (University of Ryukyus, Okinawa) for assistance in field collection in Okinawa, Dr. Ming Liu (HKU) for field work assistance in Xiamen and Ms. Damgy Chan (HKU) for the collection in Hong Kong. The work described in this paper was substantially supported by a grant from the Research Grants Council, Hong Kong (Project no. HKU7597/05M), and a grant from the National Science Council, Taiwan (NSC 95-2621-B-001-014). The authors also thank the Agriculture, Fisheries and Conservation Department of the Hong Kong SAR Government for permission to collect Tetraclita in the Cape d’Aguilar Marine Reserve. The experiments complied with the current laws of HKSAR and Taiwan.

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Authors and Affiliations

  1. Department of Biology, The Chinese University of Hong Kong, Shatin, Hong Kong

    L. M. Tsang, K. Y. Ma & K. H. Chu

  2. Research Centre for Biodiversity, Academia Sinica, Taipei, 115, Taiwan

    Benny K. K. Chan & C.-H. Hsu

  3. Department of Ecology and Biodiversity, The Swire Institute of Marine Science, The University of Hong Kong, Pokfulam Road, Hong Kong

    Benny K. K. Chan

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  1. L. M. Tsang
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  2. Benny K. K. Chan
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  3. K. Y. Ma
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  5. K. H. Chu
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Correspondence to K. H. Chu.

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Communicated by S. Nishida, Tokyo.

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Tsang, L.M., Chan, B.K.K., Ma, K.Y. et al. Lack of mtDNA and morphological differentiation between two acorn barnacles Tetraclita japonica and T. formosana differing in parietes colours and geographical distribution. Mar Biol 151, 147–155 (2007). https://doi.org/10.1007/s00227-006-0460-8

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