Abdelwaheb Ben Othmen, Mohamed Abhary, Temim Deli, Zouhour Ouanes, Noura Alhuwaiti, Najet Dimassi, Lamjed Mansour. Lack of mitochondrial genetic structure in the endangered giant clam populations of Tridacna maxima (Bivalvia: Cardiidae: Tridacninae) across the Saudi Arabian coast[J]. Acta Oceanologica Sinica, 2020, 39(2): 28-37. doi: 10.1007/s13131-020-1547-7
Citation: Abdelwaheb Ben Othmen, Mohamed Abhary, Temim Deli, Zouhour Ouanes, Noura Alhuwaiti, Najet Dimassi, Lamjed Mansour. Lack of mitochondrial genetic structure in the endangered giant clam populations of Tridacna maxima (Bivalvia: Cardiidae: Tridacninae) across the Saudi Arabian coast[J]. Acta Oceanologica Sinica, 2020, 39(2): 28-37. doi: 10.1007/s13131-020-1547-7

Lack of mitochondrial genetic structure in the endangered giant clam populations of Tridacna maxima (Bivalvia: Cardiidae: Tridacninae) across the Saudi Arabian coast

doi: 10.1007/s13131-020-1547-7
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  • Corresponding author: E-mail: temimdeli@yahoo.co.uk
  • Received Date: 2019-05-10
  • Accepted Date: 2019-06-24
  • Available Online: 2020-04-21
  • Publish Date: 2020-02-25
  • The present investigation focuses on population genetic structure analysis of the endangered giant clam species Tridacna maxima across part of the Red Sea, with the main aim of assessing the influence of postulated potential barriers to gene flow (i.e., particular oceanographic features and marked environmental heterogeneity) on genetic connectivity among populations of this poorly dispersive bivalve species. For this purpose, a total of 44 specimens of T. maxima were collected from five sampling locations along the Saudi Arabian coast and examined for genetic variability at the considerably variable mitochondrial gene cytochrome c oxidase I (COI). Our results revealed lack of population subdivision and phylogeographic structure across the surveyed geographic spectrum, suggesting that neither the short pelagic larval dispersal nor the various postulated barriers to gene flow in the Red Sea can trigger the onset of marked genetic differentiation in T. maxima. Furthermore, the discerned shallow COI haplotype genealogy (exhibiting high haplotype diversity and low nucleotide diversity), associated with recent demographic and spatial expansion events, can be considered as residual effect of a recent evolutionary history of the species in the Red Sea.
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  • [1]
    Ahmed Mohamed N, Yu Qian, Chanfi M I, et al. 2016. Genetic diversity and population differentiation of small giant clam Tridacna maxima in Comoros islands assessed by microsatellite markers. SpringerPlus, 5(1): 1852. doi: 10.1186/s40064-016-3513-6
    [2]
    Andréfouët S, Van Wynsberge S, Fauvelot C, et al. 2014. Significance of new records of Tridacna squamosa Lamarck, 1819, in the Tuamotu and Gambier Archipelagos (French Polynesia). Molluscan Research, 34(4): 277–284. doi: 10.1080/13235818.2014.940662
    [3]
    Benzie J A H, Williams S T. 1992a. Genetic structure of giant clam (Tridacna maxima) populations from reefs in the Western Coral Sea. Coral Reefs, 11(3): 135–141. doi: 10.1007/BF00255467
    [4]
    Benzie J A H, Williams S T. 1992b. No genetic differentiation of giant clam (Tridacna gigas) populations in the Great Barrier Reef, Australia. Marine Biology, 113(3): 373–377. doi: 10.1007/BF00349161
    [5]
    Clement M, Posada D, Crandall K A. 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9(10): 1657–1660. doi: 10.1046/j.1365-294x.2000.01020.x
    [6]
    DeBoer T S, Naguit M R A, Erdmann M V, et al. 2014a. Concordance between phylogeographic and biogeographic boundaries in the Coral Triangle: conservation implications based on comparative analyses of multiple giant clam species. Bulletin of Marine Science, 90(1): 277–300. doi: 10.5343/bms.2013.1003
    [7]
    DeBoer T S, Naguit M R A, Erdmann M V, et al. 2014b. Concordant phylogenetic patterns inferred from mitochondrial and microsatellite DNA in the giant clam Tridacna crocea. Bulletin of Marine Science, 90(1): 301–329. doi: 10.5343/bms.2013.1002
    [8]
    DeBoer T S, Subia M D, Erdmann M V, et al. 2008. Phylogeography and limited genetic connectivity in the endangered boring giant clam across the Coral Triangle. Conservation Biology, 22(5): 1255–1266. doi: 10.1111/j.1523-1739.2008.00983.x
    [9]
    Deli T, Ben Attia M H, Zitari-Chatti R, et al. 2017. Genetic and morphological divergence in the purple sea urchin Paracentrotus lividus (Echinodermata, Echinoidea) across the African Mediterranean coast. Acta Oceanologica Sinica, 36(12): 52–66. doi: 10.1007/s13131-017-1090-3
    [10]
    Deli T, Ben Mohamed A, Ben Attia M H, et al. 2019. High genetic connectivity among morphologically differentiated populations of the black sea urchin Arbacia lixula (Echinoidea: Arbacioida) across the central African Mediterranean coast. Marine Biodiversity, 49(2): 603–620. doi: 10.1007/s12526-017-0832-y
    [11]
    Deli T, Chatti N, Said K, et al. 2016. Concordant patterns of mtDNA and nuclear phylogeographic structure reveal Pleistocene vicariant event in the green crab Carcinus aestuarii across the Siculo-Tunisian Strait. Mediterranean Marine Science, 17(2): 533–551. doi: 10.12681/mms.1562
    [12]
    Deli T, Kalkan E, Karhan S Ü, et al. 2018. Parapatric genetic divergence among deep evolutionary lineages in the Mediterranean green crab, Carcinus aestuarii (Brachyura, Portunoidea, Carcinidae), accounts for a sharp phylogeographic break in the Eastern Mediterranean. BMC Evolutionary Biology, 18(1): 53. doi: 10.1186/s12862-018-1167-4
    [13]
    DiBattista J D, Berumen M L, Gaither M R, et al. 2013. After continents divide: comparative phylogeography of reef fishes from the Red Sea and Indian Ocean. Journal of Biogeography, 40(6): 1170–1181. doi: 10.1111/jbi.12068
    [14]
    DiBattista J D, Roberts M B, Bouwmeester J, et al. 2016. A review of contemporary patterns of endemism for shallow water reef fauna in the Red Sea. Journal of Biogeography, 43(3): 423–439. doi: 10.1111/jbi.12649
    [15]
    Drummond A J, Rambaut A, Shapiro B, et al. 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution, 22(5): 1185–1192. doi: 10.1093/molbev/msi103
    [16]
    Drummond A J, Suchard M A, Xie Dong, et al. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29(8): 1969–1973. doi: 10.1093/molbev/mss075
    [17]
    Excoffier L. 2004. Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Molecular Ecology, 13(4): 853–864. doi: 10.1046/j.1365-294X.2003.02004.x
    [18]
    Excoffier L, Laval G, Schneider S. 2007. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1: 47–50
    [19]
    Excoffier L, Smouse P E, Quattro J M. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131(2): 479–491
    [20]
    Fratini S, Ragionieri L, Deli T, et al. 2016. Unravelling population genetic structure with mitochondrial DNA in a notional panmictic coastal crab species: sample size makes the difference. BMC Evolutionary Biology, 16(1): 150. doi: 10.1186/s12862-016-0720-2
    [21]
    Fratini S, Vannini M. 2002. Genetic differentiation in the mud crab Scylla serrata (Decapoda: Portunidae) within the Indian Ocean. Journal of Experimental Marine Biology and Ecology, 272(1): 103–116. doi: 10.1016/S0022-0981(02)00052-7
    [22]
    Froukh T, Kochzius M. 2008. Species boundaries and evolutionary lineages in the blue green damselfishes Chromis viridis and Chromis atripectoralis (Pomacentridae). Journal of Fish Biology, 72(2): 451–457. doi: 10.1111/j.1095-8649.2007.01746.x
    [23]
    Fu Yunxin. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147(2): 915–925
    [24]
    Garcia-Cisneros A, Palacín C, Ben Khadra Y, et al. 2016. Low genetic diversity and recent demographic expansion in the red starfish Echinaster sepositus (Retzius 1816). Scientific Reports, 6(1): 33269. doi: 10.1038/srep33269
    [25]
    Gilbert A, Planes S, Andréfouët S, et al. 2007. First observation of the giant clam Tridacna squamosa in French Polynesia: a species range extension. Coral Reefs, 26(2): 229. doi: 10.1007/s00338-007-0218-x
    [26]
    Giles E C, Saenz-Agudelo P, Hussey N E, et al. 2015. Exploring seascape genetics and kinship in the reef sponge Stylissa carteri in the Red Sea. Ecology and Evolution, 5(13): 2487–2502. doi: 10.1002/ece3.1511
    [27]
    Grant W S. 2015. Problems and cautions with sequence mismatch analysis and Bayesian Skyline Plots to infer historical demography. Journal of Heredity, 106(4): 333–346. doi: 10.1093/jhered/esv020
    [28]
    Grant W S, Spies I B, Canino M F. 2006. Biogeographic evidence for selection on mitochondrial DNA in North Pacific walleye pollock Theragra chalcogramma. Journal of Heredity, 97(6): 571–580. doi: 10.1093/jhered/esl033
    [29]
    Grulois D, Tiavouane J, Dumas P P, et al. 2015. Isolation and characterization of fifteen microsatellite loci for the giant clam Tridacna maxima. Conservation Genetics Resources, 7(1): 73–75. doi: 10.1007/s12686-014-0290-9
    [30]
    Hall T A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41: 95–98
    [31]
    Harpending H C. 1994. Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology, 66(4): 591–600
    [32]
    Hasegawa M, Kishino H, Yano T A. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22(2): 160–174. doi: 10.1007/BF02101694
    [33]
    Hudson R R. 1990. Gene genealogies and the coalescent process. In: Futuyama D, Antonovics J, eds. Oxford surveys in Evolutionary Biology. Oxford: Oxford University Press, 1–44
    [34]
    Hui Min, Kraemer W E, Seidel C, et al. 2016. Comparative genetic population structure of three endangered giant clams (Cardiidae: Tridacna species) throughout the Indo-West Pacific: implications for divergence, connectivity and conservation. Journal of Molluscan Studies, 82(3): 403–414. doi: 10.1093/mollus/eyw001
    [35]
    Hunter R L, Halanych K M. 2010. Phylogeography of the Antarctic planktotrophic brittle star Ophionotus victoriae reveals genetic structure inconsistent with early life history. Marine Biology, 157(8): 1693–1704. doi: 10.1007/s00227-010-1443-3
    [36]
    Iacchei M, Gaither M R, Bowen B W, et al. 2016. Testing dispersal limits in the sea: range-wide phylogeography of the pronghorn spiny lobster Panulirus penicillatus. Journal of Biogeography, 43(5): 1032–1044. doi: 10.1111/jbi.12689
    [37]
    Juinio-Meñez M A, Magsino R M, Ravago-Gotanco R, et al. 2003. Genetic structure of Linckia laevigata and Tridacna crocea populations in the Palawan shelf and shoal reefs. Marine Biology, 142(4): 717–726. doi: 10.1007/s00227-002-0998-z
    [38]
    Klausewitz W. 1989. Evolutionary history and zoogeography of the Red Sea ichthyofauna. Fauna of Saudi Arabia, 10: 310–337
    [39]
    Kochzius M, Nuryanto A. 2008. Strong genetic population structure in the boring giant clam, Tridacna crocea, across the Indo-Malay Archipelago: implications related to evolutionary processes and connectivity. Molecular Ecology, 17(17): 3775–3787. doi: 10.1111/j.1365-294X.2008.03803.x
    [40]
    Kumar S, Stecher G, Tamura K. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7): 1870–1874. doi: 10.1093/molbev/msw054
    [41]
    Kürten B, Al-Aidaroos A M, Struck U, et al. 2014. Influence of environmental gradients on C and N stable isotope ratios in coral reef biota of the Red Sea, Saudi Arabia. Journal of Sea Research, 85: 379–394. doi: 10.1016/j.seares.2013.07.008
    [42]
    Laurent V, Planes S, Salvat B. 2002. High variability of genetic pattern in giant clam (Tridacna maxima) populations within French Polynesia. Biological Journal of the Linnean Society, 77(2): 221–231. doi: 10.1046/j.1095-8312.2002.00106.x
    [43]
    Layton K K S, Martel A L, Hebert P D N. 2014. Patterns of DNA barcode variation in Canadian marine Molluscs. PLoS One, 9(4): e95003. doi: 10.1371/journal.pone.0095003
    [44]
    Librado P, Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25(11): 1451–1452. doi: 10.1093/bioinformatics/btp187
    [45]
    Lobel P S, Robinson A R. 1986. Transport and entrapment of fish larvae by ocean mesoscale eddies and currents in Hawaiian waters. Deep Sea Research Part A. Oceanographic Research Papers, 33(4): 483–500
    [46]
    Lucas J S. 1988. Giant clams: description, distribution and life history. In: Copland J W, Lucas J S, ed. Giant Clams in Asia and the Pacific. Vol 9. Canbera: ACIAR Monograph, 21–33
    [47]
    Macaranas J M, Ablan C A, Pante M J R, et al. 1992. Genetic structure of giant clam (Tridacna derasa) populations from reefs in the Indo-Pacific. Marine Biology, 113(2): 231–238
    [48]
    Maggs C A, Castilho R, Foltz D, et al. 2008. Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology, 89(sp11): S108–S122. doi: 10.1890/08-0257.1
    [49]
    Nanninga G B, Saenz-Agudelo P, Manica A, et al. 2014. Environmental gradients predict the genetic population structure of a coral reef fish in the Red Sea. Molecular Ecology, 23(3): 591–602. doi: 10.1111/mec.12623
    [50]
    Nei M. 1987. Molecular Evolutionary Genetics. New York: Columbia University Press, 512
    [51]
    Nikula R, Väinölä R. 2003. Phylogeography of Cerastoderma glaucum (Bivalvia: Cardiidae) across Europe: a major break in the Eastern Mediterranean. Marine Biology, 143(2): 339–350. doi: 10.1007/s00227-003-1088-6
    [52]
    Nuryanto A, Kochzius M. 2009. Highly restricted gene flow and deep evolutionary lineages in the giant clam Tridacna maxima. Coral Reefs, 28(3): 607–619. doi: 10.1007/s00338-009-0483-y
    [53]
    Pannacciulli F G, Maltagliati F, de Guttry C, et al. 2017. Phylogeography on the rocks: the contribution of current and historical factors in shaping the genetic structure of Chthamalus montagui (Crustacea, Cirripedia). PLoS One, 12(6): e0178287. doi: 10.1371/journal.pone.0178287
    [54]
    Patarnello T, Volckaert F A M J, Castilho R. 2007. Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break?. Molecular Ecology, 16(21): 4426–4444. doi: 10.1111/j.1365-294X.2007.03477.x
    [55]
    Penant G, Aurelle D, Feral J P, et al. 2013. Planktonic larvae do not ensure gene flow in the edible sea urchin Paracentrotus lividus. Marine Ecology Progress Series, 480: 155–170. doi: 10.3354/meps10194
    [56]
    Petit R J, Hampe A, Cheddadi R. 2005. Climate changes and tree phylogeography in the Mediterranean. Taxon, 54(4): 877–885. doi: 10.2307/25065568
    [57]
    Pineda J, Hare J A, Sponaugle S. 2007. Larval transport and dispersal in the coastal ocean and consequences for population connectivity. Oceanography, 20(3): 22–39. doi: 10.5670/oceanog.2007.27
    [58]
    Pons O, Petit R J. 1995. Estimation, variance and optimal sampling of gene diversity. Theoretical and Applied Genetics, 90(3–4): 462–470. doi: 10.1007/BF00221991
    [59]
    Pons O, Petit R J. 1996. Measuring and testing genetic differentiation with ordered Versus unordered alleles. Genetics, 144(3): 1237–1245
    [60]
    Posada D, Crandall K A. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics, 14(9): 817–818. doi: 10.1093/bioinformatics/14.9.817
    [61]
    Raitsos D E, Pradhan Y, Brewin R J W, et al. 2013. Remote sensing the phytoplankton seasonal succession of the Red Sea. PLoS One, 8(6): e64909. doi: 10.1371/journal.pone.0064909
    [62]
    Rambaut A. 2012. FigTree v 1.4.0. Institute of Evolutionary Biology, University of Edinburg. http//tree.bio.ed.ac.uk/software/figtree [2012–10–08/2013–02–15]
    [63]
    Rambaut A, Drummond A J. 2009. Tracer v 1.5. Institute of Evolutionary Biology, University of Edinburg. http//beast.bio.ed.ac.uk/Tracer [2009–11–30/2012–12–05]
    [64]
    Ramos-Onsins S E, Rozas J. 2002. Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution, 19(12): 2092–2100. doi: 10.1093/oxfordjournals.molbev.a004034
    [65]
    Reuschel S, Cuesta J A, Schubart C D. 2010. Marine biogeographic boundaries and human introduction along the European coast revealed by phylogeography of the prawn Palaemon elegans. Molecular Phylogenetics and Evolution, 55(3): 765–775. doi: 10.1016/j.ympev.2010.03.021
    [66]
    Richter C, Roa-Quiaoit H, Jantzen C, et al. 2008. Collapse of a new living species of giant clam in the Red Sea. Current Biology, 18(17): 1349–1354. doi: 10.1016/j.cub.2008.07.060
    [67]
    Robitzch V, Banguera-Hinestroza E, Sawall Y, et al. 2015. Absence of genetic differentiation in the coral Pocillopora verrucosa along environmental gradients of the Saudi Arabian Red Sea. Frontiers in Marine Science, 2: 5
    [68]
    Sammarco P W, Andrews J C. 1989. The Helix experiment: differential localized dispersal and recruitment patterns in Great Barrier Reef corals. Limnology and Oceanography, 34(5): 896–912. doi: 10.4319/lo.1989.34.5.0896
    [69]
    Sanna D, Cossu P, Dedola G L, et al. 2013. Mitochondrial DNA reveals genetic structuring of Pinna nobilis across the Mediterranean Sea. PLoS One, 8(6): e67372. doi: 10.1371/journal.pone.0067372
    [70]
    Shau-Hwai A T, Yasin Z B. 1998. The reproductive cycle of Tridacna squamosa and Tridacna maxima at Rengis Island (Tioman Island), Malaysia. Phuket Marine Biological Center Special Publication, 18(1): 107–112
    [71]
    Simon C, Frati F, Beckenbach A, et al. 1994. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America, 87(6): 651–701. doi: 10.1093/aesa/87.6.651
    [72]
    Slatkin M. 1985. Gene flow in natural populations. Annual Review of Ecology and Systematics, 16: 393–430. doi: 10.1146/annurev.es.16.110185.002141
    [73]
    Slatkin M, Barton N H. 1989. A comparison of three indirect methods for estimating average levels of gene flow. Evolution, 43(7): 1349–1368. doi: 10.1111/j.1558-5646.1989.tb02587.x
    [74]
    Sofianos S S, Johns W E, Murray S P. 2002. Heat and freshwater budgets in the Red Sea from direct observations at Bab el Mandeb. Deep Sea Research, 49(7–8): 1323–1340. doi: 10.1016/S0967-0645(01)00164-3
    [75]
    Sofianos S S, Johns W E. 2007. Observations of the summer Red Sea circulation. Journal of Geophysical Research: Oceans, 112(C6): C06025
    [76]
    Soo P, Todd P A. 2014. The behaviour of giant clams (Bivalvia: Cardiidae: Tridacninae). Marine Biology, 161(12): 2699–2717. doi: 10.1007/s00227-014-2545-0
    [77]
    Tajima F. 1983. Evolutionary relationship of DNA sequences in finite populations. Genetics, 105(2): 437–460
    [78]
    Tajima F. 1989. The effect of change in population size on DNA polymorphism. Genetics Society of America, 123(3): 597–601
    [79]
    Tamura K, Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10(3): 512–526
    [80]
    Templeton A R, Crandall K A, Sing C F. 1992. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics, 132(2): 619–633
    [81]
    Weersing K, Toonen R J. 2009. Population genetics, larval dispersal, and connectivity in marine systems. Marine Ecology Progress Series, 393: 1–12. doi: 10.3354/meps08287
    [82]
    Wolanski E, Burrage D, King B. 1989. Trapping and dispersion of coral eggs around Bowden Reef, Great Barrier Reef, following mass coral spawning. Continental Shelf Research, 9(5): 479–496. doi: 10.1016/0278-4343(89)90011-3
    [83]
    Wörheide G, Epp L S, Macis L. 2008. Deep genetic divergences among Indo-Pacific populations of the coral reef sponge Leucetta chagosensis (Leucettidae): founder effects, vicariance, or both?. BMC Evolutionary Biology, 8(1): 24. doi: 10.1186/1471-2148-8-24
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