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

• Published in: Nature communications 2024-08, Vol.15 (1), p.6609-15, Article 6609
• Main Authors: Du, Kang, Ricci, Juliana Morena Bonita, Lu, Yuan, Garcia-Olazabal, Mateo, Walter, Ronald B., Warren, Wesley C., Dodge, Tristram O., Schumer, Molly, Park, Hyun, Meyer, Axel, Schartl, Manfred
• Format: Article
• Language: English
• Subjects: 45/22; 45/23; 45/77; 631/181/2474; 631/181/757; 631/181/759; 631/208/212/2306; Animals; Annotations; Biological evolution; Biology; Cyprinodontiformes - classification; Cyprinodontiformes - genetics; Developmental biology; Evolution, Molecular; Evolutionary biology; Evolutionary genetics; Gene families; Genes; Genetic analysis; Genetic control; Genetic Speciation; Genome - genetics; Genomes; Genomic analysis; Genomics - methods; Humanities and Social Sciences; Hybridization; Hybridization, Genetic; Medical research; Melanoma; Molecular evolution; multidisciplinary; Phylogenetics; Phylogeny; Predictive control; Puberty; Science; Science (multidisciplinary); Speciation; Vertebrates; Xiphophorus
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-50852-6

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. The phylogenetic and hybridization history of Xiphophorus fish remains contentious, despite their long-standing role as models in evolutionary biology and human disease research. This study presents a complete genome resource that resolves the previously conflicting phylogeny and evolutionary history of the group, revealing that hybridizations preceded speciation.