Interploidy gene flow involving the sexual-asexual cycle facilitates the diversification of gynogenetic triploid Carassius fish

  • 1.

    Muller, H. J. The relation of recombination to mutational advance. Mutat. Res. Mol. Mech. Mutagen. 1, 2–9 (1964).


    Google Scholar
     

  • 2.

    Maynard Smith, J. The Evolution of Sex (Cambridge University Press, 1978).


    Google Scholar
     

  • 3.

    Avise, J. C. Clonality (Oxford University Press, 2008).


    Google Scholar
     

  • 4.

    Hamilton, W. D., Axelrod, R. & Tanese, R. Sexual reproduction as an adaptation to resist parasites (A review). Proc. Natl. Acad. Sci. USA 87, 3566–3573 (1990).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 5.

    Lynch, M. & Gabriel, W. Mutation load and the survival of small populations. Evolution 44, 1725 (1990).

    PubMed 

    Google Scholar
     

  • 6.

    Schurko, A. M., Neiman, M. & Logsdon, J. M. Signs of sex: what we know and how we know it. Trends Ecol. Evol. 24, 208–217 (2009).

    PubMed 

    Google Scholar
     

  • 7.

    Verduijn, M. H., Van Dijk, P. J. & Van Damme, J. M. M. The role of tetraploids in the sexual-asexual cycle in dandelions (Taraxacum). Heredity 93, 390–398 (2004).

    CAS 
    PubMed 

    Google Scholar
     

  • 8.

    D’Souza, T. G., Storhas, M., Schulenburg, H., Beukeboom, L. W. & Michiels, N. K. Occasional sex in an ‘asexual’ polyploid hermaphrodite. Proc. R. Soc. B Biol. Sci. 271, 1001–1007 (2004).


    Google Scholar
     

  • 9.

    Schartl, M. et al. Incorporation of subgenomic amounts of DNA as compensation for mutational load in a gynogenetic fish. Nature 373, 68–71 (1995).

    ADS 

    Google Scholar
     

  • 10.

    Bogart, J. P., Bi, K., Fu, J., Noble, D. W. A. & Niedzwiecki, J. Unisexual salamanders (genus Ambystoma) present a new reproductive mode for eukaryotes. Genome 50, 119–136 (2007).

    CAS 
    PubMed 

    Google Scholar
     

  • 11.

    Hedtke, S. M., Glaubrecht, M. & Hillis, D. M. Rare gene capture in predominantly androgenetic species. Proc. Natl. Acad. Sci. USA 108, 9520–9524 (2011).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 12.

    Warren, W. C. et al. Clonal polymorphism and high heterozygosity in the celibate genome of the Amazon molly. Nat. Ecol. Evol. doi.org/10.1038/s41559-018-0473-y (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 13.

    Flot, J. F. et al. Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. Nature 500, 453–457 (2013).

    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • 14.

    Dawley, R. M. & Bogart, J. P. Evolution and Ecology of Unisexual Vertebrates. (Albany, University of the State of New York, State Education Department, New York State Museum, 1989).

  • 15.

    Avise, J. C. Evolutionary perspectives on clonal reproduction in vertebrate animals. Proc. Natl. Acad. Sci. USA 112, 8867–8873 (2015).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 16.

    Stöck, M. et al. Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: Along the ‘extended speciation continuum’. Philos. Trans. R. Soc. B Biol. Sci. 376, 20200103 (2021).

  • 17.

    Fujita, M. K., Singhal, S., Brunes, T. O. & Maldonado, J. A. Evolutionary Dynamics and Consequences of Parthenogenesis in Vertebrates. Annu. Rev. Ecol. Evol. Syst. 51, 191–214 (2020).


    Google Scholar
     

  • 18.

    Lehtonen, J., Schmidt, D. J., Heubel, K. & Kokko, H. Evolutionary and ecological implications of sexual parasitism. Trends Ecol. Evol. 28, 297–306 (2013).

    PubMed 

    Google Scholar
     

  • 19.

    Hosoya, K. Fishes of Japan with pictorial keys to the species, English edn. in (ed. Nakabo, T.) 308–309, 1813–1814 (Tokai University Press, 2013).

  • 20.

    Kobayashi, H., Kawashima, J. & Takeuchi, N. Comparative chromosome studies in the genus Carassius expecially with a finding of polyploidy in the ginbuna (C. auratus langsdorfi). Jpn. J. Ichthyol. 17, 153–160 (1970).


    Google Scholar
     

  • 21.

    Shimizu, Y., Oshiro, T. & Sakaizumi, M. Electrophoretic studies of diploid, triploid, and tetraploid forms of the Japanese silver crucian carp, Carassius auratus langsdorfii. Jpn. J. Ichthyol. 40, 65–75 (1993).


    Google Scholar
     

  • 22.

    Eschmeyer, W. N., Fricke, R. & van der Laan, R. Catalog of Fishes: Genera, Species, References. (2017). researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp.

  • 23.

    Mishina, T. et al. Molecular identification of species and ploidy of Carassius fishes in Lake Biwa, using mtDNA and microsatellite multiplex PCRs. Ichthyol. Res. 61, 169–175 (2014).


    Google Scholar
     

  • 24.

    Iguchi, K., Yamamoto, G., Matsubara, N. & Nishida, M. Morphological and genetic analysis of fish of a Carassius complex (Cyprinidae) in Lake Kasumigaura with reference to the taxonomic status of two all-female triploid morphs. Biol. J. Linn. Soc. 79, 351–357 (2003).


    Google Scholar
     

  • 25.

    Ohara, K., Ariyoshi, T., Sumida, E. & Taniguchi, N. Clonal diversity in the Japanese silver crucian carp, Carassius langsdorfii inferred from genetic markers. Zoolog. Sci. 20, 797–804 (2003).

    PubMed 

    Google Scholar
     

  • 26.

    Takada, M. et al. Biogeography and evolution of the Carassius auratus-complex in East Asia. BMC Evol. Biol. 10, 7 (2010).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 27.

    Luo, J. et al. Tempo and mode of recurrent polyploidization in the Carassius auratus species complex (Cypriniformes, Cyprinidae). Heredity 112, 415–427 (2014).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 28.

    Murakami, M., Matsuba, C. & Fujitani, H. Characterization of DNA markers isolated from the gynogenetic triploid ginbuna (Carassius auratus langsdorfi) by representational difference analysis. Aquaculture 208, 59–68 (2002).

    CAS 

    Google Scholar
     

  • 29.

    Cao, L. et al. Evolutionary dynamics of 18S and 5S rDNA in autotriploid Carassius auratus. Gene 737, 144433 (2020).

    CAS 
    PubMed 

    Google Scholar
     

  • 30.

    Yahara, T. Evolution of agamospermous races in Boehmeria and Eupatorium. Plant Species Biol. 5, 183–196 (1990).


    Google Scholar
     

  • 31.

    Li, C., Ortí, G., Zhang, G. & Lu, G. A practical approach to phylogenomics: the phylogeny of ray-finned fish (Actinopterygii) as a case study. BMC Evol. Biol. 7, 44 (2007).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 32.

    Yue, G. H. & Orban, L. Polymorphic microsatellites from silver crucian carp (Carassius auratus gibelio Bloch) and cross-amplification in common carp (Cyprinus carpio L.). Mol. Ecol. Notes 2, 534–536 (2002).

    CAS 

    Google Scholar
     

  • 33.

    Takeshima, H. et al. Rapid and effective isolation of candidate sequences for development of microsatellite markers in 30 fish species by using kit-based target capture and multiplexed parallel sequencing. Conserv. Genet. Resour. 9, 479–490 (2017).


    Google Scholar
     

  • 34.

    Gao, Y. et al. Quaternary palaeoenvironmental oscillations drove the evolution of the Eurasian Carassius auratus complex (Cypriniformes, Cyprinidae). J. Biogeogr. 39, 2264–2278 (2012).


    Google Scholar
     

  • 35.

    Konishi, S. & Yoshikawa, S. Immigration times of the two proboscidean species, Stegodon orientalis and Palaeoloxodon naumanni, into the Japanese Islands and the formation of land bridge. Earth Sci. (Chikyu Kagaku) 53, 125–134 (1999).


    Google Scholar
     

  • 36.

    Kitamura, A., Takano, O., Takata, H. & Omote, H. Late pliocene-early pleistocene paleoceanographic evolution of the Sea of Japan. Palaeogeogr. Palaeoclimatol. Palaeoecol. 172, 81–98 (2001).


    Google Scholar
     

  • 37.

    Dong, J., Murakami, M., Fujimoto, T., Yamaha, E. & Arai, K. Genetic characterization of the progeny of a pair of the tetraploid silver crucian carp Carassius auratus langsdorfii. Fish. Sci. 79, 935–941 (2013).

    CAS 

    Google Scholar
     

  • 38.

    Murakami, M. & Fujitani, H. Polyploid-specific repetitive DNA sequences from triploid ginbuna (Japanese silver crucian carp, Carassius auratus langsdorfi). Genes Genet. Syst. 72, 107–113 (1997).

    CAS 
    PubMed 

    Google Scholar
     

  • 39.

    Mada, Y., Miyagawa, M., Hayashi, T., Umino, T. & Arai, K. Production of tetraploids by introduction of sperm nucleus into the eggs of gynogenetic triploid ginbuna Carasius langsdorfii. Aquac. Sci. 49, 103–112 (2001).

    CAS 

    Google Scholar
     

  • 40.

    Alves, M. J., Coelho, M. M. & Collares-Pereira, M. J. Evolution in action through hybridisation and polyploidy in an Iberian freshwater fish: A genetic review. Genetica 111, 375–385 (2001).

    CAS 
    PubMed 

    Google Scholar
     

  • 41.

    Collares-Pereira, M. J., Matos, I., Morgado-Santos, M. & Coelho, M. M. Natural pathways towards polyploidy in animals: The Squalius alburnoides fish complex as a model system to study genome size and genome reorganization in polyploids. Cytogenet. Genome Res. 140, 97–116 (2013).

    CAS 
    PubMed 

    Google Scholar
     

  • 42.

    Lafond, J., Hénault, P., Leung, C. & Angers, B. Unexpected oogenic pathways for the triploid fish chrosomus eos-neogaeus. J. Hered. 110, 370–377 (2019).

    CAS 
    PubMed 

    Google Scholar
     

  • 43.

    Gauze, G. F. The Struggle for Existence (The Williams & Wilkins Company, 1934).


    Google Scholar
     

  • 44.

    Vrijenhoek, R. C. Ecological differentiation among clones: the frozen niche variation model. in Population Biology and Evolution (eds. Wöhrmann, K. & Loeschcke, V.) 217–231 (Springer Berlin Heidelberg, 1984).

  • 45.

    Weeks, A. R. & Hoffmann, A. A. Frequency-dependent selection maintains clonal diversity in an asexual organism. Proc. Natl. Acad. Sci. USA 105, 17872–17877 (2008).

  • 46.

    Vrijenhoek, R. C. Coexistence of clones in a heterogeneous environment. Science 199, 549–552 (1978).

    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • 47.

    Dagan, Y., Liljeroos, K., Jokela, J. & Ben-Ami, F. Clonal diversity driven by parasitism in a freshwater snail. J. Evol. Biol. 26, 2509–2519 (2013).

    CAS 
    PubMed 

    Google Scholar
     

  • 48.

    Otto, S. P. & Lenormand, T. Evolution of sex resolving the paradox of sex and recombination. Nat. Rev. Genet. 3, 252–261 (2002).

    CAS 
    PubMed 

    Google Scholar
     

  • 49.

    Yamashita, M., Jiang, J., Onozato, H., Nakanishi, T. & Nagahama, Y. A tripolar spindle formed at meiosis I assures the retention of the original ploidy in the gynogenetic triploid. Dev. Growth Differ. 35, 631–636 (1993).


    Google Scholar
     

  • 50.

    Kobayasi, H. A cytological study on the maturation division in the oogenic process of the Triploid Ginbuna (Carassius auratus langsdorfii). Jpn. J. Ichthyol. 22, 234–240 (1976).


    Google Scholar
     

  • 51.

    Yamashita, M., Onozato, H., Nakanishi, T. & Nagahama, Y. Breakdown of the sperm nuclear envelope is a prerequisite for male pronucleus formation: Direct evidence from the gynogenetic crucian carp Carassius auratus langsdorfii. Dev. Biol. 137, 155–160 (1990).

    CAS 
    PubMed 

    Google Scholar
     

  • 52.

    Kobayasi, H. A cytological study on gynogenesis of the triploid ginbuna (Carassius auratus langsdorfii). Zool. Mag. 80, 316–322 (1971).


    Google Scholar
     

  • 53.

    Lampert, K. P. & Schartl, M. A little bit is better than nothing: the incomplete parthenogenesis of salamanders, frogs and fish. BMC Biol. 8, 78 (2010).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 54.

    Lu, Y. et al. Fixation of allelic gene expression landscapes and expression bias pattern shape the transcriptome of the clonal Amazon molly. Genome Res. 31, 372–379 (2021).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 55.

    Science Council of Japan. Guidelines for Proper Conduct of Animal Experiments. (2006).

  • 56.

    du Sert, N. P. et al. The arrive guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biol. 18, 1–12 (2020).


    Google Scholar
     

  • 57.

    code by Richard A. Becker, O. S. & version by Ray Brownrigg., A. R. W. R. mapdata: Extra Map Databases. (2018).

  • 58.

    Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. (2013).

  • 59.

    Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 60.

    Chen, S., Zhou, Y., Chen, Y. & Gu, J. Fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 61.

    McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 62.

    Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 63.

    Stacklies, W., Redestig, H., Scholz, M., Walther, D. & Selbig, J. pcaMethods – A bioconductor package providing PCA methods for incomplete data. Bioinformatics 23, 1164–1167 (2007).

    CAS 
    PubMed 

    Google Scholar
     

  • 64.

    Buerkle, C. A. Maximum-likelihood estimation of a hybrid index based on molecular markers. Mol. Ecol. Notes 5, 684–687 (2005).

    CAS 

    Google Scholar
     

  • 65.

    Gompert, Z. & Alex Buerkle, C. Introgress: A software package for mapping components of isolation in hybrids. Mol. Ecol. Resour. 10, 378–384 (2010).

    CAS 
    PubMed 

    Google Scholar
     

  • 66.

    Liu, S. et al. Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross. Proc. Natl. Acad. Sci. USA 113, 1327–1332 (2016).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 67.

    Li, C. Y. et al. The transcriptomes of the crucian carp complex (Carassius auratus) provide insights into the distinction between unisexual triploids and sexual diploids. Int. J. Mol. Sci. 15, 9386–9406 (2014).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 68.

    Chen, Z. et al. De novo assembly of the goldfish (Carassius auratus) genome and the evolution of genes after whole-genome duplication. Sci. Adv. 5, 1–13 (2019).


    Google Scholar
     

  • 69.

    Dobin, A. et al. STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).

    CAS 
    PubMed 

    Google Scholar
     

  • 70.

    der Auwera, G. A. Genomics in the Cloud: Using Docker, GATK, and WDL in Terra. Genomics in the cloud: Using Docker, GATK, and WDL in Terra (O’Reilly Media, 2020).


    Google Scholar
     

  • 71.

    Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 72.

    Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer-Verlag, 2016).

    MATH 

    Google Scholar
     

  • 73.

    Drummond, A. J. & Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 1–8 (2007).


    Google Scholar
     

  • 74.

    Liu, H.-T. & Su, T.-T. Pliocene fishes from Yüshe Basin, Shansi. Vertebr. Palasiat. 6, 1–47 (1962).


    Google Scholar
     

  • 75.

    Rüber, L., Kottelat, M., Tan, H. H., Ng, P. K. L. & Britz, R. Evolution of miniaturization and the phylogenetic position of Paedocypris, comprising the world’s smallest vertebrate. BMC Evol. Biol. 7, 1–10 (2007).


    Google Scholar
     

  • 76.

    Tominaga, K., Nagata, N., Kitamura, J., Watanabe, K. & Sota, T. Phylogeography of the bitterling Tanakia lanceolata (Teleostei: Cyprinidae) in Japan inferred from mitochondrial cytochrome b gene sequences. Ichthyol. Res. 67, 105–116 (2020).


    Google Scholar
     

  • 77.

    Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772–772 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 78.

    Ritchie, A. M., Lo, N. & Ho, S. Y. W. The impact of the tree prior on molecular dating of data sets containing a mixture of inter- and intraspecies sampling. Syst. Biol. 66, 413–425 (2017).

    PubMed 

    Google Scholar
     

  • 79.

    Clement, M., Posada, D. & Crandall, K. A. TCS: A computer program to estimate gene genealogies. Mol. Ecol. 9, 1657–1659 (2000).

    CAS 
    PubMed 

    Google Scholar
     

  • 80.

    Excoffier, L. & Lischer, H. E. L. 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 (2010).

    PubMed 

    Google Scholar
     

  • 81.

    Oksanen, J. et al. vegan: Community Ecology Package. (2017).

  • 82.

    Legendre, P. & Legendre, L. F. J. Numerical Ecology (Elsevier Science, 1998).

    MATH 

    Google Scholar
     

  • 83.

    Muggeo, V. M. R. segmented: An R package to fit regression models with broken-line relationships. R NEWS 8(1), 20–25 (2008).


    Google Scholar
     

  • 84.

    Bruvo, R., Michiels, N. K., D’Souza, T. G. & Schulenburg, H. A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Mol. Ecol. 13, 2101–2106 (2004).

    CAS 
    PubMed 

    Google Scholar
     

  • 85.

    Clark, L. V. & Jasieniuk, M. polysat: An R package for polyploid microsatellite analysis. Mol. Ecol. Resour. 11, 562–566 (2011).

    PubMed 

    Google Scholar
     

  • 86.

    Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 87.

    Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol. Ecol. 14, 2611–2620 (2005).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 88.

    Earl, D. A. & von Holdt, B. M. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4, 359–361 (2012).


    Google Scholar
     

  • 89.

    Rolf, F. J. tpsDig, Digitize Landmarks and Outlines, Version 2.05. (Department of Ecology and Evolution, State University of New York at Stony Brook, 2006).

  • 90.

    Klingenberg, C. P. MorphoJ: An integrated software package for geometric morphometrics. Mol. Ecol. Resour. 11, 353–357 (2011).

    PubMed 

    Google Scholar
     

  • Read more here: Source link