Genome-wide SNP analyses reveal population structure of Portunus pelagicus along Vietnam coastline

English version

Autoři: Binh Thuy Dang ^aff001; Muhammad Arifur Rahman ^aff001; Sang Quang Tran ^aff001; Henrik Glenner ^aff003
Působiště autorů: Department of Biology, Institute for Biotechnology and Environment, Nha Trang University, Nha Trang City, Vietnam ^aff001; Department of Graduate Studies, Nha Trang University, Nha Trang City, Vietnam ^aff002; Department of Biological Sciences, University of Bergen, Bergen, Norway ^aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0224473

Souhrn

The blue swimming crab (Portunus pelagicus Linnaeus, 1758) is one of the commercially exploited crab fishery resources in Vietnam. This is the first study to provide a broad survey of genetic diversity, population structure and migration patterns of P. pelagicus along the Vietnamese coastline. The crab samples were collected from northern, central and southern Vietnam. Here, we used a panel of single nucleotide polymorphisms (SNPs) generated from restriction site-associated DNA sequencing (RADseq). After removing 32 outlier loci, 306 putatively neutral SNPs from 96 individuals were used to assess fine-scale population structure of blue swimming crab. The mean observed heterozygosity (Ho) and expected heterozygosity (He) per locus was 0.196 and 0.223, respectively. Pairwise Fst and hierarchical AMOVA supported significant differentiation of central and northern from southern populations (P<0.01). Population structure analyses revealed that P. pelagicus in the south is a separate fisheries unit from the north and center. Contemporary migration patterns supported high migration between northern and central populations and restricted genetic exchange within the southern population. In contrast, historic gene flow provides strong evidence for single panmictic population. The results are useful for understanding current status of P. pelagicus in the wild under an environment changing due to natural and anthropogenic stresses, with implications for fisheries management.

Klíčová slova:

Animal migration – Crabs – Gene flow – Genetic loci – Inbreeding – Population genetics – Swimming – Vietnam

Zdroje

1. Tran TD. Major issues of coastal environment in Vietnam and orientation for protection. In: Hong PN, editor. The role of mangrove and coral reef ecosystems. Publisher: Agriculture Publishing House, Hanoi; 2006. pp. 1–16.

2. Saito Y, Huy D Van, Tateishi M, Thanh TD, Nguyen VL, Ta TKO. Regimes of human and climate impacts on coastal changes in Vietnam. Reg Environ Chang. 2004;4: 49–62. doi: 10.1007/s10113-003-0062-7

3. Van Ninh P, Quynh DN, Lanh V Van, Viet Lien N. Geostrophic and drift current in the South China Sea, Area IV : Vietnamese waters. SEAFDEC Semin Fish Resour South Chins Sea, Area IV Vietnamese Waters. 2000; 365–373.

4. Pasuya MF, Peter BN, MDA H., Omar KM. Sea surface current in the Gulf of Thailand based on nineteen years altimetric data and GPS tracked drifting buoy. Geomatic & Geospatial Technology Conference. 2016. p. 8.

5. Schmidt-Thomé P, Nguyen TH, Pham TL, Jarva J, Nuottimäki K. Climate change adaptation measures in Vietnam. Springer Briefs Earth Sci. 2015; 7–16. doi: 10.1007/978-3-319-12346-2

6. Hoegh-Guldberg O, Bruno JF. The impact of climate change on the world’s marine ecosystems. Science (80-). 2010;328: 1523–1528. doi: 10.1126/science.1189930

7. Kangas MI. Synopsis of the biology and exploitation of the blue swimmer crab, Portunus pelagicus Linnaeus, in Western Australia. Fish. Res. Rep. Fish. West. Aust. 2000.

8. Banks R, Banks R, Holt T. Assessment report for Vietnamese: Blue swimming crab tangle net fishery (Portunus pelagicus), Kien Giang province. 2009.

9. Kunsook C, Gajaseni N, Paphavasit N. A stock assessment of the blue swimming crab Portunus pelagicus (Linnaeus, 1758) for sustainable management in Kung Krabaen Bay, Gulf of Thailand. Trop Life Sci Res. 2014;25: 41–59.

10. Lai JCY, Ng PKL, Davie PJF. A revision of the Portunus pelagicus (Linnaeus, 1758) species complex (Crustacea: Brachyura: Portunidae), with the recognition of four species. Raffles Bull Zool. 2010;58: 199–237.

11. Ha VV, Nhan TH, Cuong T Van, Doan NS. Stock and fishery assessment report of blue swimming crab Portunus pelagicus (Linnaeus, 1758) in Kien Giang waters, Viet Nam. Report for WWF and WASEP. 2014.

12. Canan T, Irem Y. Reproductive biology of the blue swimming crab, Portunus segnis (Forskal, 1775) in Yumurtalık Cove, North-eastern Mediterranean, Turkey. Mediterr Mar Sci. 2017;18: 424–432. http://dx.doi.org/10.12681/mms.13789

13. Ernawati TRI, Sumiono B, Madduppa H. Reproductive ecology, spawning potential, and breeding season of blue swimming crab (Portunidae: Portunus pelagicus) in Java Sea, Indonesia. Biodiversitas. 2017;18: 1705–1713. doi: 10.13057/biodiv/d180451

14. Zairion, Wardiatno Y, Fahrudin A. Sexual maturity, reproductive pattern and spawning female population of the blue swimming crab, Portunus pelagicus (Brachyura: Portunidae) in East Lampung Coastal Waters, Indonesia. Indian J Sci Technol. 2015;8: 596. doi: 10.17485/ijst/2015/v8i6/69368

15. Bryars SR, Havenhand JN. Temporal and spatial distribution and abundance of blue swimmer crab (Portunus pelagicus) larvae in a temperate gulf. Mar Freshw Res. 2004;55: 809–818. doi: 10.1071/MF04045

16. Bryars S. Larval Dispersal of the Blue Swimmer Crab, Portunus Pelagicus (Linnaeus) (Crustacea:Decapoda: Portunidae), in South Australia. Flinders University of South Australia. 1997.

17. Kemnaren DD, Zarion, Kamal MM, Wardiatno Y. Abundance and spatial distribution of blue swimming crab (Portunus pelagicus) larvae during east monsoon in the East Lampung waters, Indonesia. Biodiversitas J Biol Divers. 2018;19: 1326–1333. doi: 10.13057/biodiv/d190420

18. Macale AMB, Alcantara SG, Nieves PM. Density distribution of blue crab (Portunus pelagicus) larvae with implications to the lying-in concept of stock enhancement. Kuroshio Sci. 2017;11: 54–62.

19. Svane I, Hooper G. Blue Swimmer Crab (Portunus pelagicus) Fishery. Fishery Assessment Report to PIRSA for the Blue Crab Fishery Management Committee. 2004.

20. VASEP. Vietnam is the leading supplier of fresh blue swimming crab to Japan. Vietnam Association of Seafood Exporters and Producers report, 09/2013. [http://www.seafood.vasep.com.vn/Daily-News/378_8240/Vietnam-is-the-leading-supplier-of-fresh-blue-swimming-crab-to-Japan.htm]. 2013.

21. FAO. Species Fact Sheets Portunus pelagicus (Linnaeus, 1758) Fisheries. Fisheries and Aquaculture Department. 2016.

22. Ha VV, Nhan TH, Cuong TV, Doan NS. Stock and fishery assessment report of blue swimming crab Portunus pelagicus (Linnaeus, 1758) in Kien Giang waters, Viet Nam. 2015.

23. Seafood Watch Consulting Researcher. Blue swimming crab Vietnam and Gulf of Thailand Bottom gillnet, Pots, Set gillnet, Traps. 2018.

24. Berger AM, Goethel DR, Lynch PD, Quinn II T, Mormede S, McKenzie J, et al. Space oddity: The mission for spatial integration. Can J Fish Aquat Sci. 2017;74: 1698–1716. doi: 10.1139/cjfas-2017-0150

25. Kerr LA, Hintzen NT, Cadrin SX, Clausen LW, Dickey-Collas M, Goethel DR, et al. Lessons learned from practical approaches to reconcile mismatches between biological population structure and stock units of marine fish. ICES J Mar Sci. 2017;74: 1708–1722. doi: 10.1093/icesjms/fsw188

26. Kritzer JP, Liu OR. Fishery management strategies for addressing complex spatial structure in marine fish stocks. In: Cadrin S. X., Kerr SM L. A., editor. Stock identification methods: Applications in Ffshery science. Second Edi. Academic Press, San Diego, California; 2014. pp. 29–57. doi: 10.1016/B978-0-12-397003-9.00003–5

27. Reiss H, Hoarau G, Dickey-Collas M, Wolff WJ. Genetic population structure of marine fish: Mismatch between biological and fisheries management units. Fish Fish. 2009;10: 361–395. doi: 10.1111/j.1467-2979.2008.00324.x

28. Cimmaruta R, Scialanca F, Luccioli F, Nascetti G. Genetic diversity and environmental stress in Italian populations of the cyprinodont fish Aphanius fasciatus. Oceanol Acta. 2003;26: 101–110. doi: 10.1016/S0399-1784(02)01234-3

29. Dao HT, Smith-keune C, Wolanski E, Jones CM. Oceanographic currents and local ecological knowledge indicate, and genetics does not refute, a Contemporary pattern of larval dispersal for The ornate spiny lobster, Panulirus ornatus in the South-East Asian Archipelago. PLoS One. 2015;10: 1–19. 110.1371/journal.pone.0124568

30. Dang BT, Vu QHD, Biesack EE, Doan T V., Truong OT, Tran TL, et al. Population genomics of the peripheral freshwater fish Polynemus melanochir (Perciformes, Polynemidae) in a changing Mekong Delta. Conserv Genet. 2019; doi: 10.1007/s10592-019-01157-5

31. Truelove NK, Kough AS, Behringer DC, Paris CB, Box SJ, Preziosi RF, et al. Biophysical connectivity explains population genetic structure in a highly dispersive marine species. Coral Reefs. Springer Berlin Heidelberg; 2017;36: 233–244. doi: 10.1007/s00338-016-1516-y

32. Nehemia A, Kochzius M. Reduced genetic diversity and alteration of gene flow in a fiddler crab due to mangrove degradation. PLoS One. 2017;12: 1–20. doi: 10.1371/journal.pone.0182987

33. Puritz JB, Toonen RJ. Coastal pollution limits pelagic larval dispersal. Nat Commun. Nature Publishing Group; 2011;2: 226–228. doi: 10.1038/ncomms1238 21407192

34. Hamilton PB, Cowx IG, Oleksiak MF, Griffiths AM, Grahn M, Stevens JR, et al. Population-level consequences for wild fish exposed to sublethal concentrations of chemicals–a critical review. FFish Fish. 2016;17: 545–566. doi: 10.1111/faf.12125

35. Kenchington EL. The effects of fishing on species and genetic diversity. In: Sinclair M, Valdimarson G, editors. Responsible fisheries in the marine ecosystem. CAB International, Wallingford, Oxon, UK; 2003. pp. 253–272. doi: 10.1079/9780851996332.0235

36. Smith P. Genetic diversity of marine fisheries resources: possible impacts of fishing. FAO Fisheries Technical paper No. 344. Rome, FAO. 1994.

37. Hutchings JA RJ. Marine fish population collapses: consequences for recovery and extinction risk. Bioscience. 2004;54: 297–309. doi: 10.1641/0006-3568(2004)054[0297:MFPCCF]2.0.CO;2

38. Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE. Double digest RADseq: An inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One. 2012;7. doi: 10.1371/journal.pone.0037135

39. Al-Breiki RD, Kjeldsen SR, Afzal H, Al Hinai MS, Zenger KR, Jerry DR, et al. Genome-wide SNP analyses reveal high gene flow and signatures of local adaptation among the scalloped spiny lobster (Panulirus homarus) along the Omani coastline. BMC Genomics. BMC Genomics; 2018;19: 1DUMMY. doi: 10.1186/s12864-018-5044-8

40. Vigouroux R, Roussel J-M, Lassalle G, Longin G, Rinaldo R, Barloy D, et al. A cost-and-time effective procedure to develop SNP markers for multiple species: A support for community genetics. Methods Ecol Evol. 2018;9: 1959–1974. doi: 10.1111/2041-210x.13034

41. Etter PD, Selker EU, Currey MC, Cresko WA, Baird NA, Atwood TS, et al. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One. 2008;3: e3376. doi: 10.1371/journal.pone.0003376 18852878

42. Wang S, Meyer E, Mckay JK, Matz M V. 2b-RAD: A simple and flexible method for genome-wide genotyping. Nat Methods. 2012;9: 808–810. doi: 10.1038/nmeth.2023 22609625

43. Bird CE, Andrews KR, Fernandez-Silva I, Forsman ZH, Toonen RJ, Puritz JB, et al. ezRAD: a simplified method for genomic genotyping in non-model organisms. PeerJ. 2013;1: e203. doi: 10.7717/peerj.203 24282669

44. Yap ES, Sezmis E, Chaplin JA, Potter IC, Spencer PBS. Isolation and characterization of microsatellite loci in Portunus pelagicus (Crustacea: Portunidae). Mol Ecol Notes. 2002;2: 30–32. doi: 10.1046/j.1471-8286.2002.00136.x

45. Sezmiş E. The population genetic structure of Portunus pelagicus in Australian waters. Ph.D thesis, Murdoch University, Australia. 2004.

46. Klinbunga S, Khetpu K, Khamnamtong B, Menasveta P. Genetic heterogeneity of the blue swimming crab (Portunus pelagicus) in Thailand determined by AFLP analysis. Biochem Genet. 2007;45: 725–736. doi: 10.1007/s10528-007-9110-1 17879155

47. Klinbunga S, Yuvanatemiya V, Wongphayak S, Khetpu K, Menasveta P, Khamnamtong B. Genetic population differentiation of the blue swimming crab Portunus pelagicus (Portunidae) in Thai waters revealed by RAPD analysis. Genet Mol Res. 2010;9: 1615–1624. doi: 10.4238/vol9-3gmr886 20730713

48. Ren G, Miao G, Ma C, Lu J, Yang X, Ma H. Genetic structure and historical demography of the blue swimming crab (Portunus pelagicus) from southeastern sea of China based on mitochondrial COI gene. Mitochondrial DNA Part A DNA Mapping, Seq Anal. Informa UK Ltd.; 2018;29: 192–198. doi: 10.1080/24701394.2016.1261855

49. Sienes PMQ, Willette DA, Romena LR, Alvior CG, Estacion JS, Malay MCD. Genetic diversity and the discovery of a putative cryptic species within a valued crab fishery, Portunus pelagicus (Linnaeus 1758), in the Philippines. Philipp Sci Lett. 2014;7: 317–323.

50. Chai CJ, Esa Y Bin, Ismail MFS, Kamarudin MS. Population structure of Portunus pelagicus in coastal areas of Malaysia inferred from microsatellites. Zool Stud. 2017;56: 1–12. doi: 10.6620/ZS.2017.56–26

51. Andi IA, Andi T, Andi AH, Yushinta F, Andi P. High genetic variation of Portunus pelagicus from Makassar Straits revealed by RAPD markers and mitochondrial 16S rRNA sequences. African J Biotechnol. 2016;15: 180–190. doi: 10.5897/ajb2015.15045

52. Yang X, You C, Wang S, Miao G, Shi X, Wu Q, et al. Isolation and characterization of 91 single nucleotide polymorphism (SNP) markers for the blue swimming crab (Portunus pelagicus). Conserv Genet Resour. Springer Netherlands; 2017;9: 549–556. doi: 10.1007/s12686-017-0720-6

53. Nguyen TAT, Dang TB, Chau TML. A study of genetic structure of giant clam (Tridacna spp.) (Tridacninae) population in south central and southern Vietnam’s coast. J Biol. 2014;36 (1se): 189–194.

54. Puritz JB, Hollenbeck CM, Gold JR. dDocent : a RADseq, variant-calling pipeline designed for population genomics of non-model organisms. PeerJ. 2014;2: e431. doi: 10.7717/peerj.431 24949246

55. Bolger AM, Lohse M, Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30: 2114–2120. doi: 10.1093/bioinformatics/btu170 24695404

56. Chong Z, Ruan J, Wu CI. Rainbow: An integrated tool for efficient clustering and assembling RAD-seq reads. Bioinformatics. 2012;28: 2732–2737. doi: 10.1093/bioinformatics/bts482 22942077

57. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: Accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012;28: 3150–3152. doi: 10.1093/bioinformatics/bts565 23060610

58. Li W, Godzik A. Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22: 1658–1659. doi: 10.1093/bioinformatics/btl158 16731699

59. Li H, Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25: 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168

60. Li H, Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics. 2010;26: 589–595. doi: 10.1093/bioinformatics/btp698 20080505

61. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Oxford Univ Press 2013. 2013;00: 1–3. doi: 10.1186/s13756-018-0352-y

62. Wysoker A, Fennell T, Marth G, Abecasis G, Ruan J, Li H, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

63. Garrison E, Marth G. Haplotype-based variant detection from short-read sequencing [Internet]. 2012. pp. 1–9. arXiv:1207.3907

64. Banks E, Lunter G, Albers CA, Durbin R, Danecek P, Auton A, et al. The variant call format and VCFtools. Bioinformatics. 2011;27: 2156–2158. doi: 10.1093/bioinformatics/btr330 21653522

65. Foll M, Gaggiotti O. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: A Bayesian perspective. Genetics. 2008;180: 977–993. doi: 10.1534/genetics.108.092221 18780740

66. Benajmini Y, Hochberg Y, Benjamini Y, Hochberg Y. Controlling the False Discovery Rate : A Practical and powerful approach to Multiple Testing. J R Stat Soc B. 1995;57: 289–300. doi: 10.2307/2346101

67. Gregory W., Gregor G. FL and MM. Genetics: Population Genetics. R package version 1.3.8.1.1 [Internet]. 2019. Available: https://cran.r-project.org/package=genetics

68. Kemppainen P, Hlaing T, Walton C, Somboon P, Knight CG, Mahanta J, et al. Linkage disequilibrium network analysis (LDna) gives a global view of chromosomal inversions, local adaptation and geographic structure. Mol Ecol Resour. 2015;15: 1031–1045. doi: 10.1111/1755-0998.12369 25573196

69. Csardi G. NT. The igraph software package for complex network research, InterJournal, Complex Systems 1695. http://igraph.org; 2006.

70. Peakall R, Smouse PE. GenALEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics. 2012;28: 2537–2539. doi: 10.1093/bioinformatics/bts460 22820204

71. Meirmans Patrick G., Tienderen VH. GENOTYPE and GENODIVE : two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes. 2004;4: 792–794. doi: 10.1111/j.1471-8286.2004.00770.x

72. Pew J, Muir PH, Wang J, Frasier TR. related: An R package for analysing pairwise relatedness from codominant molecular markers. Mol Ecol Resour. 2015;15: 557–561. doi: 10.1111/1755-0998.12323 25186958

73. Milligan BG. Maximum-likelihood estimation of relatedness. Genetics. 2003;163: 1153–1167. doi: 10.4289/0013-8797-112.1.1 12663552

74. Wang J. Triadic IBD coefficients and applications to estimating pairwise relatedness. Genet Res. 2007;89: 135–153. doi: 10.1017/S0016672307008798 17894908

75. Waples RS, Anderson EC. Purging putative siblings from population genetic data sets: A cautionary view. Mol Ecol. 2017;26: 1211–1224. doi: 10.1111/mec.14022 28099771

76. Excoffier L, Laval G, Schneider S. Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol Bioinforma. 2017;1: 117693430500100. doi: 10.1177/117693430500100003

77. Hubisz MJ, Falush D, Stephens M, Pritchard JK. Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour. 2009;9: 1322–1332. doi: 10.1111/j.1755-0998.2009.02591.x 21564903

78. Daniel Falush MS and JKP. Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics. 2003;164: 1567–1587. 12930761

79. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol Ecol. 2005;14: 2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x 15969739

80. Earl DA, vonHoldt BM. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour. 2012;4: 359–361. doi: 10.1007/s12686-011-9548-7

81. Jombart T, Ahmed I. adegenet 1.3–1: New tools for the analysis of genome-wide SNP data. Bioinformatics. 2011;27: 3070–3071. doi: 10.1093/bioinformatics/btr521 21926124

82. Beerli P, Felsenstein J. Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA. 2001;98: 4563–456. doi: 10.1073/pnas.081068098 11287657

83. Chiucchi JE, Gibbs HL. Similarity of contemporary and historical gene flow among highly fragmented populations of an endangered rattlesnake. Mol Ecol. 2010;19: 5345–5358. doi: 10.1111/j.1365-294X.2010.04860.x 20964755

84. Beerli P. How to use M IGRATE or why are Markov chain Monte Carlo programs difficult to use? Bertorelle G, Bruford MW, Hauffe HC, Rizzoli A, Vernesi (eds) Population genetics for animal conservation. The Cambridge University Press, Cambridge; 2009. pp. 42–79.

85. Sundqvist L, Keenan K, Zackrisson M, Prodöhl P, Kleinhans D. Directional genetic differentiation and relative migration. Ecol Evol. 2016;6: 3461–3475. doi: 10.1002/ece3.2096 27127613

86. Keenan K., McGinnity P., Cross T.F., Crozier W.W., & Prodöhl PA. DiveRsity: An R package for the estimation of population genetics parameters and their associated errors. Methods Ecol Evol. https://CRAN.R-project.org/package=genetics; 2013;4: 782–788. doi: 10.1111/2041-210X.12067

87. Epskamp S, Cramer AOJ, Waldorp LJ, Schmittmann VD, Borsboom D. qgraph : Network visualizations of relationships in psychometric data. J Stat Softw. 2012;48: 1–18. doi: 10.18637/jss.v048.i04

88. Moore JS, Bourret V, Dionne M, Bradbury I, O’Reilly P, Kent M, et al. Conservation genomics of anadromous Atlantic salmon across its North American range: Outlier loci identify the same patterns of population structure as neutral loci. Mol Ecol. 2014;23: 5680–5697. doi: 10.1111/mec.12972 25327895

89. Chen C, Lai Z, Beardsley RC, Xu Q, Lin H, Viet NT. Current separation and upwelling over the southeast shelf of Vietnam in the South China Sea. J Geophys Res. 2012;117: C03033. doi: 10.1029/2011JC007150

90. Morgan SG, Fisher JL, Miller SH, McAfee ST, Largier JL. Nearshore larval retention in a region of strong upwelling and recruitment limitation. Ecology. 2009;90: 3489–3502. doi: 10.1890/08-1550.1 20120816

91. Condie S, Condie R. Retention of plankton within ocean eddies. Glob Ecol Biogeogr. 2016;25: 1264–1277. doi: 10.1111/geb.12485

92. Pineda J, Hare J, Sponaugle S. Larval transport and dispersal in the coastal ocean and consequences for population connectivity. Oceanography. 2011;20: 22–39. doi: 10.5670/oceanog.2007.27

93. Hung NN, Delgado JM, Tri VK, Hung LM, Merz B, Bárdossy A, et al. Floodplain hydrology of the mekong delta, Vietnam. Hydrol Process. 2012;26: 674–686. doi: 10.1002/hyp.8183

94. Tri VK. Hydrology and hydraulic infrastructure systems in the Mekong Delta, Vietnam. Renaud F, Kuenzer C The Mekong Delta System Springer Environmental Science and Engineering. Dordrecht: Springer; 2012. pp. 49–81. doi: 10.1007/978-94-007-39-62_3

95. Gonzalez EB, Knutsen H, Jorde PE. Habitat discontinuities separate genetically divergent populations of a rocky shore marine fish. PLoS One. 2016;11. doi: 10.5061/dryad.4g349.Funding

96. Yuhara T, Kawane M, Furota T. Genetic population structure of local populations of the endangered saltmarsh sesarmid crab Clistocoeloma sinense in Japan. PLoS One. 2014;9: 1–9. doi: 10.1371/journal.pone.0084720

97. Ackiss AS, Dang BT, Bird CE, Biesack EE, Chheng P, Phounvisouk L, et al. Cryptic lineages and a population dammed to incipient extinction? Insights into the genetic structure of a Mekong River catfish. J Hered. 535–547. https://doi.org/10.1093/jhered/esz016

98. Aglieri G, Papetti C, Zane L, Milisenda G, Boero F, Piraino S. First evidence of inbreeding, relatedness and chaotic genetic patchiness in the holoplanktonic jellyfish Pelagia noctiluca (Scyphozoa, Cnidaria). PLoS One. 2014;9. doi: 10.1371/journal.pone.0099647

99. Riesgo A, Taboada S, Pérez-Portela R, Melis P, Xavier JR, Blasco G, et al. Genetic diversity, connectivity and gene flow along the distribution of the emblematic Atlanto-Mediterranean sponge Petrosia ficiformis (Haplosclerida, Demospongiae). BMC Evol Biol. BMC Evolutionary Biology; 2019;19: 1–18. doi: 10.1186/s12862-018-1333-8

100. Teske PR, Sandoval-Castillo J, Van Sebille E, Waters J, Beheregaray LB. Oceanography promotes self-recruitment in a planktonic larval disperser. Sci Rep. Nature Publishing Group; 2016;6: 1–8. doi: 10.1038/s41598-016-0001-8

101. Munguía-Vega A, Sáenz-Arroyo A, Greenley AP, Espinoza-Montes JA, Palumbi SR, Rossetto M, et al. Marine reserves help preserve genetic diversity after impacts derived from climate variability: Lessons from the pink abalone in Baja California. Glob Ecol Conserv. Elsevier B.V.; 2015;4: 264–276. doi: 10.1016/j.gecco.2015.07.005

102. Lemopoulos A, Prokkola JM, Uusi-Heikkilä S, Vasemägi A, Huusko A, Hyvärinen P, et al. Comparing RADseq and microsatellites for estimating genetic diversity and relatedness—Implications for brown trout conservation. Ecol Evol. 2019;9: 2106–2120. doi: 10.1002/ece3.4905 30847096

Genome-wide SNP analyses reveal population structure of Portunus pelagicus along Vietnam coastline

Souhrn

Klíčová slova:

Zdroje

PLOS One

Současné pohledy na riziko v parodontologii

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií

Střevní příprava před kolonoskopií

Aktuální možnosti diagnostiky a léčby litiáz