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Advances in the aquatic sciences
RESEARCH ARTICLE

Cryptic diversity of the spotted scat Scatophagus argus (Perciformes: Scatophagidae) in the South China Sea: pre- or post-production isolation

Yun-Rong Yan A B C , Kui-Ching Hsu A , Mu-Rong Yi A , Bo Li A , Wei-Kuang Wang D , Bin Kang https://orcid.org/0000-0002-1299-5311 E G and Hung-Du Lin https://orcid.org/0000-0002-2841-1886 F G
+ Author Affiliations
- Author Affiliations

A College of Fisheries, Guangdong Ocean University, 1 Haida Road, Mazhang District, Zhanjiang, Guangdong, 524088, PR China.

B Marine Resources Big Data Center of South China Sea, Southern Marine Science and Engineering Guangdong Laboratory, 3 Wenti Road, Xiashan District, Zhanjiang, Guangdong, 524013, PR China.

C Center of Marine Fisheries Information Technology, Shenzhen Institute of Guangdong Ocean University, 3 BinHai 2nd Road, Dapeng New District, Shenzhen, Guangdong, 518035, PR China.

D Department of Environmental Engineering and Science, Feng Chia University, 100, Wenhwa Road, Seatwen, Taichung, 407, Taiwan.

E College of Fisheries, Ocean University of China, Qingdao, 5 Yushan Road, Shinan District, 266003, PR China.

F The Affiliated School of National Tainan First Senior High School, 1, Sec. 1, Mintzu Road, Tainan, 701, Taiwan.

G Corresponding authors. Email: varicorhinus@hotmail.com; binkang@163.com

Marine and Freshwater Research 71(12) 1640-1650 https://doi.org/10.1071/MF19337
Submitted: 23 October 2019  Accepted: 14 May 2020   Published: 15 July 2020

Abstract

The population genetic structure and historical demography of the spotted scat Scatophagus argus along the coast of the South China Sea were examined on the basis of a 1141-bp segment of the mitochondrial DNA cytochrome b gene to resolve difficulties in artificial breeding in Taiwan. In all, 213 samples were collected from 15 locations, and 75 haplotypes were obtained. The haplotypes were divided into two sympatric lineages. The genetic distance between these two lineages was 2.55%. The observed genetic structures are the result of complex interactions of historical events and oceanographic currents. During glaciations, sea level fluctuations played major roles in isolation, and changes in environmental factors affected diversification. The observed genetic patterns imply that these two lineages are not only genetically distinct, but also ecologically distinct populations. Such divergence may contribute to the development of reproductive isolation. These results suggest the existence of cryptic species within S. argus. We considered it possible that many populations from Taiwan Island were introduced from South-east Asia and that the populations in the Gulf of Tonkin originated from these introduced populations from Taiwan. This study offers important resources for the further study of conservation genetics, hybridisation and speciation.

Additional keywords: demography, north-west Pacific Ocean, phylogeography, refugium, reproductive isolation, sympatric populations.


References

Blum, S. D. (1989). Biogeography of Chaetodontidae: an analysis of allopatry among closely related species. Environmental Biology of Fishes 25, 9–31.
Biogeography of Chaetodontidae: an analysis of allopatry among closely related species.Crossref | GoogleScholarGoogle Scholar |

Chiang, T. Y., Lin, H. D., Shao, K. T., and Hsu, K. C. (2010). Multiple factors have shaped the phylogeography of Chinese spiny loach (Cobitis sinensis) in Taiwan as inferred from mitochondrial DNA variation. Journal of Fish Biology 76, 1173–1189.
Multiple factors have shaped the phylogeography of Chinese spiny loach (Cobitis sinensis) in Taiwan as inferred from mitochondrial DNA variation.Crossref | GoogleScholarGoogle Scholar | 20409169PubMed |

Chiang, T. Y., Chen, Y. Y., Lee, T. W., Hsu, K. C., Lin, F. J., Wang, W. K., and Lin, H. D. (2017). Comparative phylogeography of two codistributed endemic cyprinids in southeastern Taiwan. Biochemical Systematics and Ecology 70, 283–290.
Comparative phylogeography of two codistributed endemic cyprinids in southeastern Taiwan.Crossref | GoogleScholarGoogle Scholar |

Chiu, Y. W., Bor, H., Kuo, P. H., Hsu, K. C., Tan, M. S., Wang, W. K., and Lin, H. D. (2017). Origins of Semisulcospira libertina (Gastropoda: Semisulcospiridae) in Taiwan. Mitochondrial DNA – A. DNA Mapping, Sequencing, and Analysis 28, 518–525.
Origins of Semisulcospira libertina (Gastropoda: Semisulcospiridae) in Taiwan.Crossref | GoogleScholarGoogle Scholar |

Clark, P., Dyke, A., Shakun, J., Carlson, A., Clark, J., Wohlfarth, B., Mitrovica, J., Hostetler, S., and McCabe, M. (2009). The last glacial maximum. Science 325, 710–714.
The last glacial maximum.Crossref | GoogleScholarGoogle Scholar | 19661421PubMed |

Coyne, J. A., and Orr, H. A. (2004). ‘Speciation.’ (Sinauer Associates: Sunderland, MA, USA.)

Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772–772.
jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 22847109PubMed |

Delrieu-Trottin, E., Mona, S., Maynard, J., Neglia, V., Veuille, M., and Planes, S. (2017). Population expansions dominate demographic histories of endemic and widespread Pacific reef fishes. Scientific Reports 7, 40519.
Population expansions dominate demographic histories of endemic and widespread Pacific reef fishes.Crossref | GoogleScholarGoogle Scholar | 28091580PubMed |

Dowling, T. E., Tibbets, C. A., Minckley, W. L., and Smith, G. R. (2002). Evolutionary relationships of the plagopterins (Teleostei: Cyprinidae) from cytochrome b sequences. Copeia 2002, 665–678.
Evolutionary relationships of the plagopterins (Teleostei: Cyprinidae) from cytochrome b sequences.Crossref | GoogleScholarGoogle Scholar |

Excoffier, L., and Lischer, H. E. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar | 21565059PubMed |

Fu, Y. X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.
| 9335623PubMed |

Gupta, S. (2016). An overview on morphology, biology, and culture of spotted scat Scatophagus argus (Linnaeus 1766). Reviews in Fisheries Science & Aquaculture 24, 203–212.
An overview on morphology, biology, and culture of spotted scat Scatophagus argus (Linnaeus 1766).Crossref | GoogleScholarGoogle Scholar |

Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium 41, 95–98.

Herbert, T. D., Schuffert, J. D., Andreasen, D., Heusser, L., Lyle, M., Mix, A., Ravelo, A. C., Stott, L. D., and Herguera, J. C. (2001). Collapse of the California Current during glacial maxima linked to climate change on the land. Science 293, 71–76.
Collapse of the California Current during glacial maxima linked to climate change on the land.Crossref | GoogleScholarGoogle Scholar | 11441174PubMed |

Hsu, K. C., Shih, N. Z., Ni, I. H., and Shao, K. T. (2009). Speciation and population structure of three Trichiurus species based on mitochondrial DNA. Zoological Studies (Taipei, Taiwan) 48, 835–849.

Jenkins, T. L., Castilho, R., and Stevens, J. R. (2018). Meta-analysis of northeast Atlantic marine taxa shows contrasting phylogeographic patterns following post-LGM expansions. PeerJ 6, e5684.
Meta-analysis of northeast Atlantic marine taxa shows contrasting phylogeographic patterns following post-LGM expansions.Crossref | GoogleScholarGoogle Scholar | 30280047PubMed |

Jukes, T. H., and Cantor, C. R. (1969). Evolution of protein molecules. In ‘Mammalian Protein Metabolism’. (Ed. H. N. Monro.) pp. 21–132. (Academic Press: New York, NY, USA.)

Lan, G. B., Yan, B., Liao, S. M., Luo, Y., and Xie, R. Z. (2005). Biology of spotted scat Scatophagus argus: a review. Fisheries Science 24, 39–41.

Liu, J. Y. (2013). Status of marine biodiversity of the China Seas. PLoS One 8, e50719.
Status of marine biodiversity of the China Seas.Crossref | GoogleScholarGoogle Scholar | 24265671PubMed |

Liu, J. X., Gao, T. X., Yokogawa, K., and Zhang, Y. P. (2006). Differential population structuring and demographic history of two closely related fish species, Japanese sea bass (Lateolabrax japonicus) and spotted sea bass (Lateolabrax maculatus) in Northwestern Pacific. Molecular Phylogenetics and Evolution 39, 799–811.
Differential population structuring and demographic history of two closely related fish species, Japanese sea bass (Lateolabrax japonicus) and spotted sea bass (Lateolabrax maculatus) in Northwestern Pacific.Crossref | GoogleScholarGoogle Scholar | 16503171PubMed |

Liu, J. Y., Brown, C. L., and Yang, T. B. (2009). Population genetic structure and historical demography of grey mullet, Mugil cephalus, along the coast of China, inferred by analysis of the mitochondrial control region. Biochemical Systematics and Ecology 37, 556–566.
Population genetic structure and historical demography of grey mullet, Mugil cephalus, along the coast of China, inferred by analysis of the mitochondrial control region.Crossref | GoogleScholarGoogle Scholar |

Liu, J. X., Taterenkov, A., Beacham, T. D., Gorbachev, V., Wildes, S., and Avise, J. C. (2011). Effects of Pleistocene climatic fluctuations on the phylogeographic and demographic histories of Pacific herring (Clupea pallasii). Molecular Ecology 20, 3879–3893.
Effects of Pleistocene climatic fluctuations on the phylogeographic and demographic histories of Pacific herring (Clupea pallasii).Crossref | GoogleScholarGoogle Scholar | 21824211PubMed |

Nei, M., and Tajima, F. (1983). Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data. Genetics 105, 207–217.
| 6311668PubMed |

Ni, G., Li, Q., Kong, L., and Yu, H. (2014). Comparative phylogeography in marginal seas of the northwestern Pacific. Molecular Ecology 23, 534–548.
Comparative phylogeography in marginal seas of the northwestern Pacific.Crossref | GoogleScholarGoogle Scholar | 24600706PubMed |

Pons, O., and Petit, R. J. (1996). Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144, 1237–1245.
| 8913764PubMed |

Qiu, F., Li, H., Lin, H., Ding, S., and Miyamoto, M. M. (2016). Phylogeography of the inshore fish, Bostrychus sinensis, along the Pacific coastline of China. Molecular Phylogenetics and Evolution 96, 112–117.
Phylogeography of the inshore fish, Bostrychus sinensis, along the Pacific coastline of China.Crossref | GoogleScholarGoogle Scholar | 26732489PubMed |

Qu, M., Tang, W., Liu, Q., Wang, D., and Ding, S. (2018). Genetic diversity within grouper species and a method for interspecific hybrid identification using DNA barcoding and RYR3 marker. Molecular Phylogenetics and Evolution 121, 46–51.
Genetic diversity within grouper species and a method for interspecific hybrid identification using DNA barcoding and RYR3 marker.Crossref | GoogleScholarGoogle Scholar | 29294404PubMed |

Rogers, A. R., and Harpending, H. (1992). Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552–569.
Population growth makes waves in the distribution of pairwise genetic differences.Crossref | GoogleScholarGoogle Scholar | 1316531PubMed |

Rozas, J., Sanchez-DelBarrio, J. C., Messeguer, X., and Rozas, R. (2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.
DnaSP, DNA polymorphism analyses by the coalescent and other methods.Crossref | GoogleScholarGoogle Scholar | 14668244PubMed |

Sevilla, R. G., Diez, A., Norén, M., Mouchel, O., Jérôme, M., Verrez-Bagnis, V., van Pelt, H., Favre-Krey, L., Krey, G., The FishTrace Consortium Bautista, J. M. (2007). Primers and polymerase chain reaction conditions for DNA barcoding teleost fish based on the mitochondrial cytochrome b and nuclear rhodopsin genes. Molecular Ecology Notes 7, 730–734.
Primers and polymerase chain reaction conditions for DNA barcoding teleost fish based on the mitochondrial cytochrome b and nuclear rhodopsin genes.Crossref | GoogleScholarGoogle Scholar |

Shen, K. N., Jamandre, B. W., Hsu, C. C., Tzeng, W. N., and Durand, J. D. (2011). Plio-Pleistocene sea level and temperature fluctuations in the northwestern Pacific promoted speciation in the globally-distributed flathead mullet Mugil cephalus. BMC Evolutionary Biology 11, 83.
Plio-Pleistocene sea level and temperature fluctuations in the northwestern Pacific promoted speciation in the globally-distributed flathead mullet Mugil cephalus.Crossref | GoogleScholarGoogle Scholar | 21450111PubMed |

Stelkens, R. B., Schmid, C., and Seehausen, O. (2015). Hybrid breakdown in cichlid fish. PLoS One 10, e0127207.
Hybrid breakdown in cichlid fish.Crossref | GoogleScholarGoogle Scholar | 25996870PubMed |

Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.
| 2513255PubMed |

Tamura, K., and 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, 512–52610.1093/OXFORDJOURNALS.MOLBEV.A040023

Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
MEGA6: molecular evolutionary genetics analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 24132122PubMed |

Templeton, A. R. (1993). The ‘Eve’ hypotheses: a genetic critique and reanalysis. American Anthropologist 95, 51–72.
The ‘Eve’ hypotheses: a genetic critique and reanalysis.Crossref | GoogleScholarGoogle Scholar |

Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.
The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.Crossref | GoogleScholarGoogle Scholar | 9396791PubMed |

Walter, G. M., Wilkinson, M. J., James, M. E., Richards, T. J., Aguirre, J. D., and Ortiz-Barrientos, D. (2016). Diversification across a heterogenous landscape. Evolution 70, 1979–1992.
Diversification across a heterogenous landscape.Crossref | GoogleScholarGoogle Scholar | 27436057PubMed |

Wang, P. (1999). Response of western Pacific marginal seas to glacial cycles: paleoceanographic and sedimentological features. Marine Geology 156, 5–39.
Response of western Pacific marginal seas to glacial cycles: paleoceanographic and sedimentological features.Crossref | GoogleScholarGoogle Scholar |

Wang, J., Tsang, L. M., and Dong, Y. W. (2015). Causations of phylogeographic barrier of some rocky shore species along the Chinese coastline. BMC Evolutionary Biology 15, 114.
Causations of phylogeographic barrier of some rocky shore species along the Chinese coastline.Crossref | GoogleScholarGoogle Scholar | 26071894PubMed |

Yang, J. Q., Hsu, K. C., Liu, Z. Z., Su, L. W., Kuo, P. H., Tang, W. Q., and Lin, H. D. (2016). The population history of Garra orientalis (Teleostei: Cyprinidae) using mitochondrial DNA and microsatellite data with approximate Bayesian computation. BMC Evolutionary Biology 16, 73.
The population history of Garra orientalis (Teleostei: Cyprinidae) using mitochondrial DNA and microsatellite data with approximate Bayesian computation.Crossref | GoogleScholarGoogle Scholar | 27068356PubMed |

Yang, Y., Li, J., Yang, S., Li, X., Fang, L., Zhong, C., Duke, N., Zhou, R., and Shi, S. (2017). Effects of Pleistocene sea-level fluctuations on mangrove population dynamics: a less from Sonneratia alba. BMC Evolutionary Biology 17, 22.
Effects of Pleistocene sea-level fluctuations on mangrove population dynamics: a less from Sonneratia alba.Crossref | GoogleScholarGoogle Scholar | 28100168PubMed |

Yang, W., Chen, H. P., Jiang, D. N., Deng, S. P., Wu, T. L., Zhu, C. H., and Li, G. L. (2018). An overview on biology and artificial propagation and culture in the spotted scat Scatophagus argus. Journal of Biology 35, 104–108.

Young, M. K., Mckelvey, K. S., Pilgrim, K. L., and Schwartz, M. K. (2013). DNA barcoding at riverscape scales: assessing biodiversity among fishes of the genus Cottus (Teleostei) in northern Rocky Mountain streams. Molecular Ecology Resources 13, 583–595.
DNA barcoding at riverscape scales: assessing biodiversity among fishes of the genus Cottus (Teleostei) in northern Rocky Mountain streams.Crossref | GoogleScholarGoogle Scholar | 23496857PubMed |

Zhao, J., Hsu, K. C., Luo, J. Z., Wang, C. H., Chan, B. P., Li, J., Kuo, P. H., and Lin, H. D. (2018). Genetic diversity and population history of Tanichthys albonubes (Teleostei: Cyprinidae): implications for conservation. Aquatic Conservation 28, 422–434.
Genetic diversity and population history of Tanichthys albonubes (Teleostei: Cyprinidae): implications for conservation.Crossref | GoogleScholarGoogle Scholar |