Advertisement

Marine Biodiversity

, Volume 49, Issue 6, pp 2521–2534 | Cite as

Species identification and cryptic diversity in Pampus species as inferred from morphological and molecular characteristics

  • Yuan Li
  • Yongdong Zhou
  • Pengfei Li
  • Tianxiang GaoEmail author
  • Longshan LinEmail author
Original Paper
  • 52 Downloads

Abstract

Pomfret, which are widely distributed throughout the western Pacific and Indian Oceans, are economically important fish species. As their similar external morphological characteristics can inhibit proper species identification, numerous errors exist in the morphological characterization and DNA barcoding data of pomfret. In this study, we extensively sampled pomfret from the Indian and Pacific Oceans. Using the sampled specimens, in combination with morphological assessments, DNA barcoding, and corrected sequences of the mitochondrial cytochrome c oxidase I (COI) gene in GenBank, we attempted to resolve the classification issues surrounding this group. We identified seven valid species in the genus Pampus, of which all seven are distributed in the western Pacific and three are distributed in the Indian Ocean. Pampus argenteus, Pampus cinereus, and Pampus sp. were identified as three valid species with relatively close genetic distances and sharing a common ancestor. Significant variation between Pampus chinensis specimens from the Arabian Sea and the northwestern Pacific suggest a possible species complex. Finally, we provide an identification key to facilitate the identification of pomfret based on the major diagnostic morphological characteristics of six Pampus species collected along the western Pacific coast. On the basis of the reports on the new record of “Pampus argenteus,” we found that the Lessepsian migration of pomfret was likely, with species from the Indian and Pacific Oceans spreading through the Mediterranean Sea into the waters of the eastern Atlantic. Further study is required to clarify the validity of the newly recorded “Pampus argenteus.”

Keywords

DNA barcoding Phylogenetic analysis Species diversity Stromateidae Synonymous species 

Notes

Acknowledgments

The present study could not have been performed without assistance from Dr. Karhoe Loh, Dr. Takashi Yanagimoto, Prof. Weizhong Chen, Prof. Dianrong Sun, and Mr. Long Li in the Pampus specimen collection.

Funding

The study was funded by the National Natural Science Foundation of China (grant number 41776171), the National Programme on Global Change and Air-Sea Interaction (grant number GASI-02-SCS-YDsum/spr/aut and GASI-02-PAC-YDsum/aut), the Bilateral Cooperation of Maritime Affairs (grant number 2200207), the International Science & Technology Cooperation Program of China (grant number 2015DFR30450), the Public Science and Technology Research Funds Projects of Ocean (grant number 201505025), and the Scientific Research Foundation of Third Institute of Oceanography, State Oceanic Administration (grant number 2016010).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities.

Data availability

All data generated or analyzed during this study are included in this published article and its supplementary information files.

Supplementary material

12526_2019_976_MOESM1_ESM.pdf (2.8 mb)
Supplementary Figure 1 (PDF 2892 kb)

References

  1. Abe T, Kosakai T (1964) Notes on an economically important but scientifically little-known silver pomfret, Pampus echinogaster (Pampidae, Teleostei). Jpn J Ichthyol 12(1/2):29–31.  https://doi.org/10.11369/jji1950.12.29 CrossRefGoogle Scholar
  2. Basilewsky S (1855) Ichthyographia Chinae Borealis. Nouveaux Mémoires de la Société Impériale des Naturalistes de Moscou. 10: 215–263Google Scholar
  3. Bassham S, Catchen J, Lescak E, von Hippel FA, Cresko WA (2018) Repeated selection of alternatively adapted haplotypes creates sweeping genomic remodeling in stickleback. Genetics 209(3):921–939.  https://doi.org/10.1534/genetics.117.300610 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Beaufort LF, Chapman WM (1951) The Fishes of the Indo-Australian Archipelago. IX Percomorphi (Concluded). Brill, LeidenGoogle Scholar
  5. Bermingham E, McCafferty SS, Martin AP (1997) Fish biogeography and molecular clocks: perspectives from the Panamanian Isthmus. In: Kocher TD, Stepien CA (eds) Molecular systematics of fishes. Academic Press, San Diego, pp 113–126CrossRefGoogle Scholar
  6. Bleeker P (1852) Bijdrage tot de kennis der Makreelachtige visschen van den Soenda-Molukschen Archipel. Ver Bat Gen 24:1–93Google Scholar
  7. Bloch ME (1795) Naturgeschichte der ausländischen Fische, vol 9. Schlesinger, Berlin, p 192Google Scholar
  8. Bonaparte CL (1837) Iconografia della fauna Italica, per le quattro classi degli animali vertebrati. Tome III, part 2, Pesce, RomaGoogle Scholar
  9. Brawand D, Wagner CE, Li YI, Malinsky M, Keller I, Fan S et al (2014) The genomic substrate for adaptive radiation in African cichlid fish. Nature 513(7518):375.  https://doi.org/10.1038/nature13726 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Chen WT, Ma XH, Shen YJ, Mao YT, He SP (2015) The fish diversity in the upper reaches of the Salween River, Nujiang River, revealed by DNA barcoding. Sci Rep 5:17437.  https://doi.org/10.1038/srep17437 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cheng QT, Zheng BS (1987) Systematic synopsis of Chinese fishes, vol 1. Science Press, BeijingGoogle Scholar
  12. Cui ZX, Liu Y, Li CP, Chu KH (2011) Species delineation in Pampus (Perciformes) and the phylogenetic status of the Stromateoidei based on mitogenomics. Mol Biol Rep 38(2):1103–1114.  https://doi.org/10.1007/s11033-010-0207-y CrossRefPubMedGoogle Scholar
  13. Davis P, Wheeler A (1985) The occurrence of Pampus argenteus (Euphrasen, 1788), (Osteichthyes, Perciformes, Stromateoidei, Stromateidae) in the North Sea. J Fish Biol 26(2):105–109.  https://doi.org/10.1111/j.1095-8649.1985.tb04247.x CrossRefGoogle Scholar
  14. Divya PR, Mohitha C, Rahul GK, Shanis CPR, Basheer VS, Gopalakrishnan A (2017) Molecular based phylogenetic species recognition in the genus Pampus (Perciformes: Stromateidae) reveals hidden diversity in the Indian Ocean. Mol Phylogenet Evol 109:240–245.  https://doi.org/10.1016/j.ympev.2016.12.030 CrossRefPubMedGoogle Scholar
  15. Doiuchi R, Nakabo T (2006) Molecular phylogeny of the stromateoid fishes (Teleostei: Perciformes) inferred from mitochondrial DNA sequences and compared with morphology-based hypotheses. Mol Phylogenet Evol 39(1):111–123.  https://doi.org/10.1016/j.ympev.2005.10.007 CrossRefPubMedGoogle Scholar
  16. Dolganov VN, Kharin VE, Zemnukhov VV (2007) Species composition and distribution of butterfishes (Stromateidae) in waters of Russia. J Ichthyol 47(8):579–584.  https://doi.org/10.1134/S0032945207080048 CrossRefGoogle Scholar
  17. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973.  https://doi.org/10.1038/srep17437 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Dulčić J, Jardas I, Pallaoro A, Lipeg L (2004) On the validity of the record of silver pomfret Pampus argenteus (Stromateidae) from the Adriatic Sea. Cybium 28(1):69–71Google Scholar
  19. Elliott NG, Haskard K, Koslow JA (1995) Morphometric analysis of orange roughy (Hoplostethus atlanticus) off the continental slope of southern Australia. J Fish Biol 46(2):202–220.  https://doi.org/10.1111/j.1095-8649.1995.tb05962.x CrossRefGoogle Scholar
  20. Euphrasen BA (1788) Beskrifning po trenne fiskar. Vetensk Akad Nya Handl Stockholm 9:49–55Google Scholar
  21. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567.  https://doi.org/10.1111/j.1755-0998.2010.02847.x CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fowler HW (1905) Some fishes from Borneo. Proc Acad Natl Sci Phila 57:455–523Google Scholar
  23. Fowler HW (1938) The fishes of the George Vanderbilt South Pacific Expedition 1937. Monographs of the Academy of Natural Sciences of Philadelphia 2:1–349Google Scholar
  24. Fowler HL (1972) A synopsis of the fishes of China, vol 1. Antiquariaat Junk, NetherlandsGoogle Scholar
  25. Haedrich RL (1967) The stromateoid fishes: systematic and a classification. Bull Mus Comp Zool 135:131–139 (in Japanese)Google Scholar
  26. Haedrich RL (1984) Stromateidae. In: Fischer W, Bianchi G (eds) FAO species identification sheets for fishery purposes. Western Indian Ocean (fishing area 51). FAO, RomeGoogle Scholar
  27. Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc B Biol Sci 270(1512):313–321.  https://doi.org/10.1098/rspb.2002.2218 CrossRefGoogle Scholar
  28. Huang W, Xu X, Xie ZZ, Li Y, Wang DD, Wang X, Chen H, Li SS, Zhang Y, Lin HR (2016) The complete mitochondrial genome of the Pampus nozawae (Perciformes: Stromateidae). Mitochondrial DNA 27(2):988–989.  https://doi.org/10.3109/19401736.2014.926518 CrossRefPubMedGoogle Scholar
  29. Ishikawa (1904) Notes on some new or little known fishes of Japan. Proc Dep Nat Hist Tokyo Imp Mus 1: 8–9Google Scholar
  30. Kocher TD (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nat Rev Genet 5(4):288.  https://doi.org/10.1038/nrg1316 CrossRefPubMedGoogle Scholar
  31. Li Y, Lin LS, Song N, Zhang Y, Gao TX (2018) Population genetics of Pampus echinogaster along the Pacific coastline of China: Insights from CR and microsatellite molecular markers. Mar Freshwater Res 69(6):971–981.  https://doi.org/10.1071/MF17218 CrossRefGoogle Scholar
  32. Li Y, Song N, Khan FS, Yanagimoto T, Gao TX (2013) New evidence of morphological characters and DNA barcoding of Pampus argenteus (Euphrasen, 1788). J Fish China 37(11):1601–1608.  https://doi.org/10.3724/SP.J.1231.2013.38824 CrossRefGoogle Scholar
  33. Li Y, Zhang ZH, Song N, Gao TX (2016) Characteristics of complete mitogenome of Pampus sp. nov. (Perciformes: Stromateidae). Mitochondrial DNA 27(3):1640–1641.  https://doi.org/10.3109/19401736.2014.958707 CrossRefPubMedGoogle Scholar
  34. Li Y, Zhang Y, Gao TX, Han ZQ, Lin LS, Zhang XM (2017) Morphological characteristics and DNA barcoding of Pampus echinogaster (Basilewsky, 1855). Acta Oceanol Sin 36:18–23.  https://doi.org/10.1007/s13131-017-1124-x CrossRefGoogle Scholar
  35. Linnaeus C (1758) Systema Naturae, Ed. X. (Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata) Holmiae 1(1):1–824Google Scholar
  36. Liu J, Li CS (1998a) Redescription of a stromateoid fish Pampus punctatissimus and comparison with Pampus argenteus from Chinese coastal waters. Chin J Oceanol Limnol 16(2):161–166.  https://doi.org/10.1007/BF02845182 CrossRefGoogle Scholar
  37. Liu J, Li CS (1998b) A new pomfret species, Pampus minor sp. nov (Stromateidae) from Chinese waters. Chin J Oceanol Limnol 16(3):280–285CrossRefGoogle Scholar
  38. Liu J, Li CS (2013) A new species of the genus Pampus (Perciformes, Stromateidae) from China. Acta Zootaxon Sin 38(4):885–890Google Scholar
  39. Liu J, Li CS, Li XS (2002a) Phylogeny and biogeography of Chinese pomfret fishes (Pisces: Stromateidae). Stud Mar Sinica 44:235–239 in ChineseGoogle Scholar
  40. Liu J, Li CS, Li XS (2002b) Studies on Chinese pomfret fishes of the genus Pampus (Pisces: Stromateidae). Stud Mar Sinica 44:240–252 in ChineseGoogle Scholar
  41. Liu JX, Gao TX, Wu SF, Zhang YP (2007) Pleistocene isolation in the Northwestern Pacific marginal seas and limited dispersal in a marine fish, Chelon haematocheilus (Temminck & Schlegel, 1845). Mol Ecol 16:275–288.  https://doi.org/10.1111/j.1365-294X.2006.03140.x CrossRefPubMedPubMedCentralGoogle Scholar
  42. Liu J, Li CS, Ning P (2013a) A redescription of grey pomfret Pampus cinereus (Bloch, 1795) with the designation of a neotype (Teleostei: Stromateidae). Chin J Oceanol Limnol 31(1):140–145.  https://doi.org/10.1007/s00343-013-2039-9 CrossRefGoogle Scholar
  43. Liu J, Li CS, Ning P (2013b) Identity of silver pomfret Pampus argenteus (Euphrasen, 1788) based on specimens from its type locality, with a neotype designation (Teleostei, Stromateidae). Acta Zootaxon Sin 38(1):171–177Google Scholar
  44. Marques DA, Jones FC, Di Palma F, Kingsley DM, Reimchen TE (2018) Experimental evidence for rapid genomic adaptation to a new niche in an adaptive radiation. Nat Ecol Evol 2(7):1128–1138.  https://doi.org/10.1038/s41559-018-0581-8 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Marques DA, Meier JI, Seehausen O (2019) A combinatorial view on speciation and adaptive radiation. Trends Ecol Evol 34:6.  https://doi.org/10.1016/j.tree.2019.02.008 CrossRefGoogle Scholar
  46. Nakabo T (2013) Fishes of Japan with Pictorial Keys to the Species. Tokai University Press, Kanagawa (in Japanese)Google Scholar
  47. Oh CW, Na JH, Kim JK (2009) Population biology of Korean pomfret Pampus echinogaster (Basilewsky, 1855) (Perciformes: Stromateidae) on the western coast of Korea, Yellow Sea. Anim Cells Syst 13(1):83–89.  https://doi.org/10.1080/19768354.2009.9647197 CrossRefGoogle Scholar
  48. Parin NV, Piotrovsky AS (2004) Stromateoid fishes (suborder Stromateoidei) of the Indian Ocean (species composition, distribution, biology, and fisheries). J Ichthyol 44(1):33–62Google Scholar
  49. Piper R (2010) Re-occurrence of silver pomfret Pampus argenteus in the North Sea. Mar Biodiver Rec 3(e102):1–3.  https://doi.org/10.1017/S175526721000093X CrossRefGoogle Scholar
  50. Regan CT (1902) A revision of fishes of the family Stromateidae. Ann Mag Nat Hist 10: 115–207Google Scholar
  51. Richardson SJ (1846) Report on the Ichthyology of the seas of China and Japan. Rept Brit Assoc Ad Sci 15: 187–320Google Scholar
  52. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S et al (2012) Mrbayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542.  https://doi.org/10.1093/sysbio/sys029 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Sami M, Rym E, Othman J, Hechmi M (2014) First record of Pampus argenteus (Euphrasen, 1788) (Osteichthyes: Stromateidae) in the Tunisian coast (Mediterranean Sea). J Mar Biol Oceanogr 3:1.  https://doi.org/10.4172/2324-8661.1000123 CrossRefGoogle Scholar
  54. Seehausen O (2006) African cichlid fish: a model system in adaptive radiation research. Proc R Soc B Biol Sci 273(1597):1987–1998.  https://doi.org/10.1098/rspb.2006.3539 CrossRefGoogle Scholar
  55. Sun P (2015) Comparison of genetic difference in cultured Pampus populations between China and Kuwait based on COI partial sequences. Mar Sci 39(1):53–58.  https://doi.org/10.11759/hykx20131205003 in ChineseCrossRefGoogle Scholar
  56. Sun P, Yin F, Shi ZH, Peng SM (2013) Genetic structure of silver pomfret (Pampus argenteus) in the Arabian Sea, Bay of Bengal, and South China Sea as indicated by mitochondrial COI gene sequences. J Appl Ichthyol 29(4):733–737.  https://doi.org/10.1111/jai.12130 CrossRefGoogle Scholar
  57. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739.  https://doi.org/10.1093/molbev/msr121 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Temminck CJ, Schlegel H (1845) Fauna Japonica, Pisces, p 121Google Scholar
  59. Terekhanova NV, Logacheva MD, Penin AA, Neretina TV, Barmintseva AE, Bazykin GA et al (2014) Fast evolution from precast bricks: genomics of young freshwater populations of threespine stickleback Gasterosteus aculeatus. PLoS Genet 10(10):e1004696.  https://doi.org/10.1371/journal.pgen.1004696 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Wang YK (1958) Fish taxonomy. Shanghai Science and Technology Press, Shanghai (in Chinese)Google Scholar
  61. Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc B 360(1462):1847–1857.  https://doi.org/10.1098/rstb.2005.1716 CrossRefGoogle Scholar
  62. Yamada U, Tokimura M, Horikawa H, Nakabo T (2007) Fishes and fisheries of the East China and Yellow Seas. Tokai University Press, Kanagawa (in Japanese)Google Scholar
  63. Yamada U, Tokimura M, Hoshino K, Deng S, Zheng Y, Li S, Kim Y, Kim J (2009) Name and illustrations of fish from the East China Sea and the Yellow Sea—Japanese·Chinese·Korean. Overseas fishery Cooperation Foundation of Japan, Tokyo in JapaneseGoogle Scholar
  64. Yang WH, Cheng QT (1987) Retrieval China fish system. Ocean Press, Beijing in ChineseGoogle Scholar
  65. Zhang CL, Cheng QT, Zheng BS (1994) Fishes of Yellow Sea and Bohai Sea. Aquatic Press, Keelung. (in Chinese)Google Scholar
  66. Zhu YD, Cheng QT, Zhang CL (1962) Fishes of South China Sea. Science Press, Beijing (in Chinese)Google Scholar
  67. Zhu YD, Zhang CL, Cheng QT (1963) Fishes of East China Sea. Ocean Press, Beijing (in Chinese)Google Scholar
  68. Zhu YD, Wu HL, Jin XB, Meng QW, Zhang QY, Qiu SY (1985) Fish of Fujian (II). Fujian Science and Technology Press, Fujian (in Chinese)Google Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung 2019

Authors and Affiliations

  1. 1.Third Institute of OceanographyMinistry of Natural ResourcesXiamenChina
  2. 2.National Engineering Research Center for Marine AquacultureZhejiang Ocean UniversityZhoushanChina
  3. 3.Fishery CollegeZhejiang Ocean UniversityZhoushanChina

Personalised recommendations