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Millennium-old farm breeding of Chinese softshell turtles (Pelodiscus spp.) results in massive erosion of biodiversity

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Abstract

Chinese softshell turtles (Pelodiscus spp.) are widely distributed, ranging from the Amur and Ussuri Rivers in the Russian Far East through the Korean Peninsula, Japan, and eastern, central, and southern China to southern Vietnam. In East and Southeast Asia, Chinese softshell turtles are traditionally exploited for food and have been farm-bred in China since the Spring and Autumn Period, more than 2400 years ago. Currently, the annual production of Pelodiscus amounts to 340,000 t in China alone. Using mitochondrial DNA (2428 bp) and five nuclear loci (3704 bp), we examined broad sampling of wild and farm-bred Pelodiscus to infer genetic and taxonomic differentiation. We discovered four previously unknown mitochondrial lineages, all from China. One lineage from Jiangxi is deeply divergent and sister to the mitochondrial lineage of Pelodiscus axenaria. The nuclear loci supported species status for P. axenaria and the new lineage from Jiangxi. Pelodiscus maackii and P. parviformis, both harboring distinct mitochondrial lineages, were not differentiated from P. sinensis in the studied nuclear markers. The same is true for two new mitochondrial lineages from Zhejiang, China, represented by only one individual each, and another new lineage from Anhui, Guangdong, Jiangxi and Zhejiang, China. However, Vietnamese turtles yielding a mitochondrial lineage clustering within P. sinensis were distinct in nuclear markers, suggesting that these populations could represent another unknown species with introgressed mitochondria. Its species status is also supported by the syntopic occurrence with P. sinensis in northern Vietnam and by morphology. In addition, we confirmed sympatry of P. axenaria and P. parviformis in Guangxi, China, and found evidence for sympatry of P. sinensis and the new putative species from Jiangxi, China. We also discovered evidence for hybridization in turtle farms and for the occurrence of alien lineages in the wild (Zhejiang, China), highlighting the risk of genetic pollution of native stock. In the face of the large-scale breeding of Pelodiscus, we claim that the long-term survival of distinct genetic lineages and species can only be assured when an upscale market segment for pure-bred softshell turtles is established, making the breeding of pure lineages lucrative for turtle farms. Our findings underline that the diversity of Pelodiscus is currently underestimated and threatened by anthropogenic admixture. We recommend mass screening of genetic and morphological variation of Chinese softshell turtles as a first step to understand and preserve their diversity.

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References

  • Brandt JF (1857) Observationes quaedam ad generis Trionychum species duas novas spectantes auctore J. F. Brandt. Bull Cl Phys-Math Acad Imp Sci St-Pétersbourg 16:110–111

    Google Scholar 

  • Bu XJ, Liu L, Wang L, Nie LW (2011) Isolation and characterization of 21 novel polymorphic microsatellite loci in the Chinese soft-shelled turtle Pelodiscus sinensis. Genet Mol Res 10:1006–1010

    Article  PubMed  CAS  Google Scholar 

  • Bu X, Liu K, Nie K (2014) Genetic diversity and population differentiation of the Chinese soft-shelled turtle (Pelodiscus sinensis) in three geographical populations. Biochem Syst Ecol 54:279–284

    Article  CAS  Google Scholar 

  • Chen H-G, Liu W-B, Zhang X-J (2005) Comparative analysis of mitochondrial DNA 12S rRNA region between Pelodiscus sinensis and Pelodiscus axenaria and their molecular marker for identification. J Fisher China 29:318–322 [in Chinese, with English abstract]

    CAS  Google Scholar 

  • Chen H-G, Liu W-B, Li J-Z, Zhang X-J (2006) Comparative analysis of mitochondrial DNA cytb gene and their molecular identification markers in three species of soft-turtles. Acta Hydrobiol Sin 30:380–385 [in Chinese, with English abstract]

    CAS  Google Scholar 

  • Chkhikvadze VM (1987) O sistematicheskom polozhenii dal’nevostochnogo trioniksa. Bull Acad Sci Gruz SSR 128:609–611

    Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  PubMed  CAS  Google Scholar 

  • Dong CM, Engstrom TN, Thomson RC (2016) Origins of softshell turtles in Hawaii with implications for conservation. Conserv Genet 17:207–220

    Article  CAS  Google Scholar 

  • Ernst CH, Altenburg RGM, Barbour RW (2000) Turtles of the world. Ver. 1.2, CD-ROM. ETI BioInformatics, Amsterdam

    Google Scholar 

  • Fong JJ, Chen TH (2010) DNA evidence for the hybridization of wild turtles in Taiwan: possible genetic pollution from trade animals. Conserv Genet 11:2061–2066

    Article  Google Scholar 

  • Fritz U, Guicking D, Auer M, Sommer RS, Wink M, Hundsdörfer AK (2008) Diversity of the Southeast Asian leaf turtle genus Cyclemys: how many leaves on its tree of life? Zool Scr 37:367–390

    Article  Google Scholar 

  • Fritz U, Gong S, Auer M, Kuchling G, Schneeweiss N, Hundsdörfer AK (2010) The world’s economically most important chelonians represent a diverse species complex (Testudines: Trionychidae: Pelodiscus). Org Divers Evol 10:227–242

    Article  Google Scholar 

  • Fritz U, Stuckas H, Vargas-Ramírez M, Hundsdörfer AK, Maran J, Päckert M (2012) Molecular phylogeny of Central and South American slider turtles: implications for biogeography and systematics (Testudines: Emydidae: Trachemys). J Zool Syst Evol Res 50:125–136

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • He Y, Liu K, Wang C, Zhu S, Liu J, Jin W, Jiang Y, Chen H, Dong Z (2018) Twenty microsatellite loci from Chinese soft-shelled turtles Trionyx sinensis, a vulnerable species on the IUCN Red List. Conserv Genet Resour 10:13–15

    Article  Google Scholar 

  • Ihlow F, Vamberger M, Flecks M, Hartmann T, Cota M, Makchai S, Meewattana P, Dawson JE, Kheng L, Rödder D, Fritz U (2016) Integrative taxonomy of Southeast Asian snail-eating turtles (Geoemydidae: Malayemys) reveals a new species and mitochondrial introgression. PLoS One 11:e0153108

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  PubMed  CAS  Google Scholar 

  • Jung S-O, Lee Y-M, Kartavtsev Y, Park I-S, Kim DS, Lee J-S (2006) The complete mitochondrial genome of the Korean soft-shelled turtle Pelodiscus sinensis. DNA Seq 17:471–483

    Article  CAS  Google Scholar 

  • Kang CX, Yan ZM (2000) Cultivation and processing technology of medicinal plants and animals: turtles. Chinese Medicine Press, Beijing [in Chinese]

    Google Scholar 

  • Kindler C, Chèvre M, Ursenbacher S, Böhme W, Hille A, Jablonski D, Vamberger M, Fritz U (2017) Hybridization patterns in two contact zones of grass snakes reveal a new Central European snake species. Sci Rep 7:7378

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

  • Kuzmin SL (2002) The turtles of Russia and other ex-Soviet Republics. Edition Chimaira, Frankfurt am Main

    Google Scholar 

  • Laikre K, Schwartz MK, Waples RS, Ryman N, The GeM Working Group (2010) Compromising genetic diversity in the wild: unmonitored large-scale release of plants and animals. Trends Ecol Evol 25:520–529

    Article  PubMed  Google Scholar 

  • Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701

    Article  PubMed  CAS  Google Scholar 

  • Li ZQ, Li JL, Feng XY, Xie N, Feng JB, Yue GH (2010) Sixteen polymorphic microsatellites for breeding of Chinese soft-shelled turtles (Pelodiscus sinensis). Anim Genet 41:445–448

    Google Scholar 

  • Li T, Zhao J, Li W, Shi Y, Shi XY, Zhu XP (2016) Development of microsatellite markers and genetic diversity analysis for Pelodiscus sinensis. Genet Mol Res 15:gmr.15038346

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ma X, Xiong G, Wang L (2014) Development and characterization of 17 microsatellite markers for Chinese soft-shelled turtle, Pelodiscus sinensis. Conserv Genet Res 6:955–956

    Article  Google Scholar 

  • Parham JF, Simison WB, Kozak KH, Feldman CR, Shi H (2001) New Chinese turtles: endangered or invalid? A reassessment of two species using mitochondrial DNA, allozyme electrophoresis and known locality specimens. Anim Conserv 4:357–367

    Article  Google Scholar 

  • Praschag P, Stuckas H, Päckert M, Maran J, Fritz U (2011) Mitochondrial DNA sequences suggest a revised taxonomy of Asian flapshell turtles (Lissemys Smith, 1931) and the validity of previously unrecognized taxa (Testudines: Trionychidae). Vertebr Zool 61:147–160

    Google Scholar 

  • Praschag P, Ihlow F, Flecks M, Vamberger M, Fritz U (2017) Diversity of North American map and sawback turtles (Testudines: Emydidae: Graptemys). Zool Scr 46:675–682

    Article  Google Scholar 

  • Que Y, Zhu B, Rosenthal H, Chang J (2007) Isolation and characterization of microsatellites in Chinese soft-shelled turtle, Pelodiscus sinensis. Mol Ecol Notes 7:1265–1267

    Article  Google Scholar 

  • Raemy M, Fritz U, Cheylan M, Ursenbacher S (2017) Hybridisation between turtle subspecies: a case study with the European pond turtle (Emys orbicularis). Conserv Genet 18:287–296

    Article  Google Scholar 

  • Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. http://beast.bio.ed.ac.uk/tracer 2014. Accessed 30 June 2015

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed  PubMed Central  Google Scholar 

  • Sato H, Yoshino T, Ota H (1997) Origin and distribution of the Chinese soft-shelled turtle, Pelodiscus sinensis (Reptilia: Testudines), in islands of Okinawa Prefecture, Japan. Biol Mag Okinawa 35:19–26

    Google Scholar 

  • Spinks PQ, Thomson RC, Pauly GB, Newman CE, Mount G, Shaffer HB (2013) Misleading phylogenetic inferences based on single-exemplar sampling in the turtle genus Pseudemys. Mol Phylogenet Evol 68:269–281

    Article  PubMed  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: Maximum Likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

  • Stuart BL, Parham JF (2007) Recent hybrid origin of three rare Chinese turtles. Conserv Genet 8:169–175

    Article  Google Scholar 

  • Stuckas H, Fritz U (2011) Identity of Pelodiscus sinensis revealed by DNA sequences of an approximately 180-year-old type specimen and a taxonomic reappraisal of Pelodiscus species (Testudines: Trionychidae). J Zool Syst Evol Res 49:335–339

    Article  Google Scholar 

  • Suzuki D, Hikida T (2014) Taxonomic status of the soft-shell turtle populations in Japan: a molecular approach. Curr Herpetol 33:171–179

    Article  Google Scholar 

  • Suzuki D, Yabe T, Hikida T (2014) Hybridization between Mauremys japonica and Mauremys reevesii inferred by nuclear and mitochondrial DNA analyses. J Herpetol 48:445–454

    Article  Google Scholar 

  • Tang Y (1997) Research on a new species of Pelodiscus, Trionychidae in China. Zool Res (Kunming Inst Zool) 18:13–17 [in Chinese, with English abstract]

    CAS  Google Scholar 

  • Tian Y, Gao Y, Han L (2016) Testudinate China. The 8th World Congress of Herpetology, Hangzhou

    Google Scholar 

  • TTWG [Turtle Taxonomy Working Group] (2017) Turtles of the world. Annotated checklist and atlas of taxonomy, synonymy, distribution, and conservation status, 8th edn. Chelonian Research Foundation and Turtle Conservancy (Chelonian Research Monographs 7), Lunenburg, Massachusetts

  • Vamberger M, Stuckas H, Sacco F, D’Angelo S, Arculeo M, Cheylan M, Corti C, Lo Valvo M, Marrone F, Wink M, Fritz U (2015) Differences in gene flow in a twofold secondary contact zone of pond turtles in southern Italy (Testudines: Emydidae: Emys orbicularis galloitalica, E. o. hellenica, E. trinacris). Zool Scr 44:233–249

    Article  Google Scholar 

  • Vamberger M, Durkin L, Kim C, Handschuh M, Seng R, Fritz U (2017) The leaf turtle population of Phnom Kulen National Park (northwestern Cambodia) has genetic and morphological signatures of hybridization. J Zool Syst Evol Res 55:167–174

    Article  Google Scholar 

  • Yang P, Tang Y, Ding L, Guo X, Wang Y (2011) Validity of Pelodiscus parviformis (Testudines: Trionychidae) inferred from molecular and morphological analyses. Asian Herpetol Res 2:21–29

    Article  CAS  Google Scholar 

  • Zhang C, Xu X-J, Zhang H-Q, Mu C-K, He Z-Y, Wang C-L (2015a) PCR-RFLP identification of four Chinese soft-shelled turtle Pelodiscus sinensis strains using mitochondrial genes. Mitochondrial DNA 26:538–543

    Article  PubMed  CAS  Google Scholar 

  • Zhang HQ, Zhang C, Xu XJ, Zhu JJ, He ZY, Shao JZ (2015b) Differentiation of four strains of Chinese soft-shelled turtle (Pelodiscus sinensis) based on high-resolution melting analysis of single nucleotide polymorphism sites in mitochondrial DNA. Genet Mol Res 14:13144–13150

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Xu X, He Z, Zheng T, Shao J (2017a) De novo transcriptome analysis reveals insights into different mechanisms of growth and immunity in a Chinese soft-shelled turtle hybrid and the parental varieties. Gene 605:54–62

    Article  PubMed  CAS  Google Scholar 

  • Zhang HQ, Xu XJ, He ZY, Shao JZ, Zhang XH, Meng QH, Huang FY (2017b) A comparative study on genetic characteristics of two new varieties of Pelodiscus sinensis and their hybrid. Genet Mol Res 16:gmr16039148

    Google Scholar 

  • Zhang J, Zhou Q, Yang X, Yu P, Zhou W, Gui Y, Ouyang X, Wan Q (2018) Characterization of the complete mitochondrial genome and phylogenetic analysis of Pelodiscus sinensis, a mutant Chinese soft-shell turtle. Conserv Genet Res. https://doi.org/10.1007/s12686-018-1007-2

  • Zhou G, Zhang X, Fang Z (1991) Bulletin of a new species Trionyx. Acta Scient Nat Univ Norm Hunan 14:379–382 [in Chinese, with English abstract]

    Google Scholar 

  • Zhou F, Ding X-Y, Feng H, Xu Y-B, Xue H-L, Zhang J-R, Ng W-K (2013) The dietary protein requirement of a new Japanese strain of juvenile Chinese soft shell turtle, Pelodiscus sinensis. Aquaculture 412:74–80

    Article  CAS  Google Scholar 

  • Zhou F, Wang Y-Q, Ding X-Y, Ng W-K, He F, Xue H-L (2016) Partial replacement of fish meal by soy protein concentrates in diets for a new Japanese strain of juvenile soft-shelled turtle, Pelodiscus sinensis. Aquac Res 47:875–886

    Article  CAS  Google Scholar 

  • Zhu L, Li Z, Li J, Feng X, Nie N (2012) Genetic diversity of farmed Chinese soft-shelled turtle (Pelodiscus sinensis) evaluated from microsatellite analysis. J Anim Vet Adv 11:1217–1222

    Article  Google Scholar 

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Acknowledgments

We would like to thank Yan Ge and Qingsong Xie for their help in sample collection. Genetic investigations were conducted in the Senckenberg Dresden laboratory (SGN-SNSD-Mol-Lab). Many thanks for processing samples go to Anke Müller and for help with old literature to Balázs Farkas. Three anonymous reviewers and Oliver Hawlitschek provided helpful comments on an earlier draft of this study.

Funding

Our study was financially supported by the National Natural Science Foundation of China (grant no. 31471966) and the GDAS Special Project of Science and Technology Development (2017GDASCX-0107).

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Author notes

  1. Shiping Gong and Melita Vamberger contributed equally to this work.

Authors and Affiliations

  1. Guangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Guangdong Institute of Applied Biological Resources, Guangzhou, 510260, China

    Shiping Gong

  2. Museum of Zoology, Senckenberg Dresden, A. B. Meyer Building, 01109, Dresden, Germany

    Melita Vamberger, Markus Auer & Uwe Fritz

  3. Turtle Island, Am Katzelbach 98, 8054, Graz, Austria

    Peter Praschag

Authors
  1. Shiping Gong
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  2. Melita Vamberger
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  3. Markus Auer
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  4. Peter Praschag
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  5. Uwe Fritz
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Contributions

SG and UF conceived and designed research. SG, MA, and PP collected samples. MV analyzed data. UF, MV, and SG wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Uwe Fritz.

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The authors declare that they have no conflict of interest.

Ethical approval

This study is not based on any experiments with humans or animals. Samples for genetic investigation were taken minimally invasive according to all applicable international and national guidelines, regulations, and best ethical and experimental practice of the Senckenberg Nature Research Society.

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Communicated by: Sven Thatje

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Gong, S., Vamberger, M., Auer, M. et al. Millennium-old farm breeding of Chinese softshell turtles (Pelodiscus spp.) results in massive erosion of biodiversity. Sci Nat 105, 34 (2018). https://doi.org/10.1007/s00114-018-1558-9

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