Skip to main content
Log in

Phylogeny and Evolution of Multiple Common Carp (Cyprinus carpio L.) Populations Clarified by Phylogenetic Analysis Based on Complete Mitochondrial Genomes

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Common carp (Cyprinus carpio L.) is one of the oldest, most widely farmed commercially important freshwater fish in the world. However, many undetermined phylogenetic relationships and origins of common carp lineages remain, which are obstacles to conservation and genetic breeding of this species. Phylogenetic analyses based on molecular tools are helpful to distinguish the origin of species, understand and clarify their evolutionary history, and provide a genetic basis for selective breeding. In this study, we demonstrated a method to extract complete mitochondrial genome sequences from whole-genome resequencing data using the Illumina platform. The complete mitochondrial genome sequences of 26 individuals representing nine strains were obtained and subjected to a phylogenetic analysis. We reconstructed the phylogenetic topologies of the nine strains and analyzed the haplotypes. Results from both analyses suggested that the genome sequences belonged to two distinct subspecies from Europe and East Asia. We also estimated the time of divergence of the nine strains, which was up to 100 KYA. The phylogenetic results clarified the breeding history of Songpu mirror carp and suggest that this species may be hybrid of paternal European mirror carp and maternal Xingguo red carp. The results also support a previous hypothesis that koi may have originated from or have close ancestry with Oujiang color carp in China.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Balon EK (1995) Origin and domestication of the wild carp. Cyprinus carpio: from Roman gourmets to the swimming flowers. Aquaculture 129:3–48

    Article  Google Scholar 

  • Bartfai R et al (2003) Genetic analysis of two common carp broodstocks by RAPD and microsatellite markers. Aquaculture 219:157–167. doi:10.1016/S0044-8486(02)00571-9

    Article  CAS  Google Scholar 

  • Botero-Castro F, Tilak MK, Justy F, Catzeflis F, Delsuc F, Douzery EJP (2013) Next-generation sequencing and phylogenetic signal of complete mitochondrial genomes for resolving the evolutionary history of leaf-nosed bats (Phyllostomidae). Mol Phylogenet Evol 69:728–739. doi:10.1016/j.ympev.2013.07.003

    Article  CAS  PubMed  Google Scholar 

  • Cheng L, Liu L, Yu X, Wang D, Tong J (2010) A linkage map of common carp (Cyprinus carpio) based on AFLP and microsatellite markers. Anim Genet 41:191–198. doi:10.1111/j.1365-2052.2009.01985.x

    Article  CAS  PubMed  Google Scholar 

  • Cox MP, Peterson DA, Biggs PJ (2010) SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinformatics 11. doi:10.1186/1471-2105-11-485

  • Cunningham CW (1997) Can three incongruence tests predict when data should be combined? Mol Biol Evol 14:733–740

    Article  CAS  PubMed  Google Scholar 

  • Davila JI et al. (2011) Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis. BMC Biol 9. doi:10.1186/1741-7007-9-64

  • 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. doi:10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  • Froufe E, Magyary I, Lehoczky I, Weiss S (2002) mtDNA sequence data supports an Asian ancestry and single introduction of the common carp into the Danube Basin. J Fish Biol 61:301–304. doi:10.1006/jfbi.2002.2046

    Article  CAS  Google Scholar 

  • Fujii S, Kazama T, Yamada M, Toriyama K (2010) Discovery of global genomic re-organization based on comparison of two newly sequenced rice mitochondrial genomes with cytoplasmic male sterility-related genes. BMC Genomics 11. doi:10.1186/1471-2164-11-209

  • Ji PF et al (2012) High throughput mining and characterization of microsatellites from common carp genome. Int J Mol Sci 13:9798–9807. doi:10.3390/Ijms13089798

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kohlmann K, Kersten P (2013) Deeper insight into the origin and spread of European common carp (Cyprinus carpio carpio) based on mitochondrial D-loop sequence polymorphisms. Aquaculture 376:97–104. doi:10.1016/j.aquaculture.2012.11.006

    Article  Google Scholar 

  • Kongchum P, Palti Y, Hallerman EM, Hulata G, David L (2010) SNP discovery and development of genetic markers for mapping innate immune response genes in common carp (Cyprinus carpio). Fish Shellfish Immun 29:356–361. doi:10.1016/j.fsi.2010.04.013

    Article  CAS  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li S, Wang C (2001) Genetic diversity and selective breeding of red common carps in China. Naga ICLARM Quarterly 24:56–61

    Google Scholar 

  • Li Y, Xu P, Zhao ZX, Wang J, Zhang Y, Sun XW (2011) Construction and characterization of the BAC library for common carp cyprinus carpio l. and establishment of microsynteny with zebrafish Danio Rerio. Mar Biotechnol 13:706–712. doi:10.1007/s10126-010-9332-9

    Article  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. doi:10.1093/bioinformatics/btp187

    Article  CAS  PubMed  Google Scholar 

  • Mabuchi K, Senou H, Nishida M (2008) Mitochondrial DNA analysis reveals cryptic large-scale invasion of non-native genotypes of common carp (Cyprinus carpio) in Japan. Mol Ecol 17:796–809

    Article  CAS  PubMed  Google Scholar 

  • Moens LN, van der Ven K, Van Remortel R, Del-Favero J, De Coen WM (2007) Gene expression analysis of estrogenic compounds in the liver of common carp (Cyprinus carpio) using a custom cDNA Microarray. J Biochem Mol Toxic 21:299–311. doi:10.1002/Jbt.20190

    Article  CAS  Google Scholar 

  • Rodriguez-Moreno L, Gonzalez VM, Benjak A, Marti MC, Puigdomenech P, Aranda MA, Garcia-Mas J (2011) Determination of the melon chloroplast and mitochondrial genome sequences reveals that the largest reported mitochondrial genome in plants contains a significant amount of DNA having a nuclear origin. BMC Genomics 12. doi:10.1186/1471-2164-12-424

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tong J-g, Wu Q-J (2001) Sequence conservation on segments of mitochondrial 16S rRNA and Cytochrome b in strains of common carp (Cyprinus carpio L. var.). Acta Hydrobiologica Sinica 25:60–65

    Google Scholar 

  • Wang CH, Li SF (2004a) Genetic variability and relationships in mitochondrial DNA CO II gene sequence of red common carps in China, Yi Chuan Xue Bao. Acta Genet Sinica 31:1226–1231

    CAS  Google Scholar 

  • Wang CH, Li SF (2004b) Phylogenetic relationships of ornamental (koi) carp, Oujiang color carp and long-fin carp revealed by mitochondrial DNA COII gene sequences and RAPD analysis. Aquaculture 231:83–91. doi:10.1016/j.aquaculture.2003.10.040

    Article  CAS  Google Scholar 

  • Wang BS, Ji PF, Wang J, Sun JS, Wang CH, Xu P, Sun XW (2013) The complete mitochondrial genome of the Oujiang color carp, Cyprinus carpio var. color (Cypriniformes, Cyprinidae). Mitochondrial DNA 24:19–21. doi:10.3109/19401736.2012.710230

    Article  PubMed  Google Scholar 

  • White TR, Conrad MM, Tseng R, Balayan S, Golding R, Martins AMD, Dayrat BA (2011) Ten new complete mitochondrial genomes of pulmonates (Mollusca: Gastropoda) and their impact on phylogenetic relationships. BMC Evol Biol 11. doi:10.1186/1471-2148-11-295

  • Wiens JJ (1998a) Combining data sets with different phylogenetic histories. Syst Biol 47:568–581

    Article  CAS  PubMed  Google Scholar 

  • Wiens JJ (1998b) Does adding characters with missing data increase or decrease phylogenetic accuracy? Syst Biol 47:625–640

    Article  CAS  PubMed  Google Scholar 

  • Williams DR et al (2008) Genomic resources and microarrays for the common carp Cyprinus carpio L. J Fish Biol 72:2095–2117. doi:10.1111/j.1095-8649.2008.01875.x

    Article  CAS  Google Scholar 

  • Wu XY, Luo J, Huang S, Chen ZM, Xiao H, Zhang YP (2013) Molecular phylogeography and evolutionary history of Poropuntius huangchuchieni (Cyprinidae) in Southwest China. PloS One 8. doi:10.1371/journal.pone.0079975

  • Xu J, Huang W, Zhong CR, Luo DJ, Li SF, Zhu ZY, Hu W (2011a) Defining global gene expression changes of the hypothalamic-pituitary-gonadal axis in female sGnRH-antisense transgenic common carp (Cyprinus carpio). PloS One 6. doi:10.1371/journal.pone.0021057

  • Xu P et al (2011b) Genomic insight into the common carp (Cyprinus carpio) genome by sequencing analysis of BAC-end sequences. BMC Genomics 12. doi:10.1186/1471-2164-12-188

  • Xu P et al. (2011c) Generation of the first BAC-based physical map of the common carp genome BMC Genomics 12. doi:10.1186/1471-2164-12-537

  • Xu P et al (2014) Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Nat Genet 46:1212–1219. doi:10.1038/Ng.3098

    Article  CAS  PubMed  Google Scholar 

  • Yan XC, Ding L, Li YC, Zhang XF, Liang Y, Sun XW, Teng CB (2012) Identification and profiling of microRNAs from skeletal muscle of the common carp. PloS One 7. doi:10.1371/journal.pone.0030925

  • Zhang XF (2013) A consensus linkage map provides insights on genome character and evolution in common carp (Cyprinus carpio L.). Mar Biotechnol 15:275–312. doi:10.1007/s10126-012-9485-9

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Liang LQ, Jiang P, Li DY, Lu CY, Sun XW (2008) Genome evolution trend of common carp (Cyprinus carpio L.) as revealed by the analysis of microsatellite loci in a gynogentic family. J Genet Genomics 35:97–103. doi:10.1016/S1673-8527(08)60015-6

    Article  CAS  PubMed  Google Scholar 

  • Zheng YC, Peng R, Kuro-O M, Zeng XM (2011) Exploring patterns and extent of bias in estimating divergence time from mitochondrial DNA Sequence Data in a Particular Lineage: a case study of salamanders (order Caudata). Mol Biol Evol 28:2521–2535. doi:10.1093/molbev/msr072

    Article  CAS  PubMed  Google Scholar 

  • Zhou JF, Wang ZW, Ye YZ, Wu QJ (2003a) PCR-RFLP analysis of mitochondrial DNA ND5/6 region among 3 subspecies of common carp (Cyprinus carpio L.) and its application to genetic discrimination of subspecies Chinese. Sci Bull 48:465–468. doi:10.1360/03tb9098

    Article  CAS  Google Scholar 

  • Zhou JF, Wu QJ, Ye YZ, Tong JG (2003b) Genetic divergence between Cyprinus carpio carpio and Cyprinus carpio haematopterus as assessed by mitochondrial DNA analysis, with emphasis on origin of European domestic carp. Genetica 119:93–97. doi:10.1023/A:1024421001015

    Article  CAS  PubMed  Google Scholar 

  • Zhou J, Wu Q, Wang Z, Ye Y (2004a) Genetic variation analysis within and among six varieties of common carp (Cyprinus carpio L.) in china using microsatellite markers Russ. J Genet 40:1144–1148. doi:10.1023/B:Ruge.0000044758.51875.25

    CAS  Google Scholar 

  • Zhou J, Wu Q, Wang Z, Ye Y (2004b) Molecular phylogeny of three subspecies of common carp Cyprinus carpio, based on sequence analysis of cytochrome b and control region of mtDNA. J Zool Syst Evol Res 42:266–269. doi:10.1111/j.1439-0469.2004.00266.x

    Article  Google Scholar 

Download references

Acknowledgments

We acknowledge grant support from the National High-Technology Research and Development Program of China (863 Program; 2011AA100401), the National Natural Science Foundation of China (No. 31422057), and the Special Scientific Research Funds for Central Non-profit Institutes of Chinese Academy of Fishery Sciences (2013C011).

Conflict of Interest

The authors declare no competing interests.

Author’s Contributions

PX conceived the study. CD and PX wrote the manuscript. CD, JX, and BW performed the bioinformatics analysis to obtain the complete mitochondrial genome sequences. CD conducted the phylogenetic analysis. JF and ZJ collected samples. XS supervised the genome study. All authors have read and approved the final version of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Xiaowen Sun or Peng Xu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(JPEG 434 kb)

High resolution image (TIFF 1430 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dong, C., Xu, J., Wang, B. et al. Phylogeny and Evolution of Multiple Common Carp (Cyprinus carpio L.) Populations Clarified by Phylogenetic Analysis Based on Complete Mitochondrial Genomes. Mar Biotechnol 17, 565–575 (2015). https://doi.org/10.1007/s10126-015-9639-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-015-9639-7

Keywords

Navigation