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Phylogenomic analyses of all species of swordtail fishes (genus Xiphophorus) show that hybridization preceded speciation

Author

Listed:
  • Kang Du

    (Texas State University, San Marcos)

  • Juliana Morena Bonita Ricci

    (Texas State University, San Marcos)

  • Yuan Lu

    (Texas State University, San Marcos)

  • Mateo Garcia-Olazabal

    (Texas State University, San Marcos)

  • Ronald B. Walter

    (Texas State University, San Marcos)

  • Wesley C. Warren

    (University of Missouri, Bond Life Sciences Center)

  • Tristram O. Dodge

    (Stanford University)

  • Molly Schumer

    (Stanford University)

  • Hyun Park

    (Korea University)

  • Axel Meyer

    (University of Konstanz)

  • Manfred Schartl

    (Texas State University, San Marcos
    University of Wuerzburg, Am Hubland
    University of Innsbruck)

Abstract

Hybridization has been recognized to play important roles in evolution, however studies of the genetic consequence are still lagging behind in vertebrates due to the lack of appropriate experimental systems. Fish of the genus Xiphophorus are proposed to have evolved with multiple ancient and ongoing hybridization events. They have served as an informative research model in evolutionary biology and in biomedical research on human disease for more than a century. Here, we provide the complete genomic resource including annotations for all described 26 Xiphophorus species and three undescribed taxa and resolve all uncertain phylogenetic relationships. We investigate the molecular evolution of genes related to cancers such as melanoma and for the genetic control of puberty timing, focusing on genes that are predicted to be involved in pre-and postzygotic isolation and thus affect hybridization. We discovered dramatic size-variation of some gene families. These persisted despite reticulate evolution, rapid speciation and short divergence time. Finally, we clarify the hybridization history in the entire genus settling disputed hybridization history of two Southern swordtails. Our comparative genomic analyses revealed hybridization ancestries that are manifested in the mosaic fused genomes and show that hybridization often preceded speciation.

Suggested Citation

  • Kang Du & Juliana Morena Bonita Ricci & Yuan Lu & Mateo Garcia-Olazabal & Ronald B. Walter & Wesley C. Warren & Tristram O. Dodge & Molly Schumer & Hyun Park & Axel Meyer & Manfred Schartl, 2024. "Phylogenomic analyses of all species of swordtail fishes (genus Xiphophorus) show that hybridization preceded speciation," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50852-6
    DOI: 10.1038/s41467-024-50852-6
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    References listed on IDEAS

    as
    1. Mohamed A. F. Noor, 2003. "Genes to make new species," Nature, Nature, vol. 423(6941), pages 699-700, June.
    2. Bob B.M. Wong & Heidi S. Fisher & Gil G. Rosenthal, 2005. "Species recognition by male swordtails via chemical cues," Behavioral Ecology, International Society for Behavioral Ecology, vol. 16(4), pages 818-822, July.
    3. Melisa Olave & Alexander Nater & Andreas F. Kautt & Axel Meyer, 2022. "Early stages of sympatric homoploid hybrid speciation in crater lake cichlid fishes," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    4. Yun Sung Cho & Li Hu & Haolong Hou & Hang Lee & Jiaohui Xu & Soowhan Kwon & Sukhun Oh & Hak-Min Kim & Sungwoong Jho & Sangsoo Kim & Young-Ah Shin & Byung Chul Kim & Hyunmin Kim & Chang-uk Kim & Shu-Ji, 2013. "The tiger genome and comparative analysis with lion and snow leopard genomes," Nature Communications, Nature, vol. 4(1), pages 1-7, December.
    5. Paolo Franchini & Julia C. Jones & Peiwen Xiong & Susanne Kneitz & Zachariah Gompert & Wesley C. Warren & Ronald B. Walter & Axel Meyer & Manfred Schartl, 2018. "Long-term experimental hybridisation results in the evolution of a new sex chromosome in swordtail fish," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
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