Abstract
The role of structurally dynamic genomic regions in speciation is poorly understood due to challenges inherent in diploid genome assembly. Here we reconstructed the evolutionary dynamics of structural variation in five cat species by phasing the genomes of three interspecies F1 hybrids to generate near-gapless single-haplotype assemblies. We discerned that cat genomes have a paucity of segmental duplications relative to great apes, explaining their remarkable karyotypic stability. X chromosomes were hotspots of structural variation, including enrichment with inversions in a large recombination desert with characteristics of a supergene. The X-linked macrosatellite DXZ4 evolves more rapidly than 99.5% of the genome clarifying its role in felid hybrid incompatibility. Resolved sensory gene repertoires revealed functional copy number changes associated with ecomorphological adaptations, sociality and domestication. This study highlights the value of gapless genomes to reveal structural mechanisms underpinning karyotypic evolution, reproductive isolation and ecological niche adaptation.
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Data availability
Assemblies are available in NCBI under accession numbers GCA_016509475.2, GCA_016509815.2, GCA_018350155.1, GCA_018350175.1, GCA_018350195.2 and GCA_018350215.1. OR gene sequences and DXZ4 alignments are found at: https://figshare.com/s/68266360874d5078bdf5.
Code availability
Publicly available software and packages were used in this study. No custom code was used. All software and packages used in this study are described within Methods section.
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Acknowledgements
We thank the High-Performance Research Computing Center at Texas A&M University for support. DNA library preparation and long-read sequencing were performed at the University of Maryland Institute for Genome Sciences (L. Tallon and L. Sadzewicz). Illumina sequencing was performed through the Texas A&M Institute for Genome Sciences & Society research core (A. Hillhouse). We thank R. Stanyon for the flow-sorted domestic cat chromosomes for FISH experiments. This research was supported by grants from the Morris Animal Foundation (grant D19FE-04 to W.J.M. and W.C.W.), the National Science Foundation (grants DEB-1753760 and DEB-2150664 to W.J.M.) and the National Institutes of Health (NIH; grant R01 GM59290 to M.A.B.). A.J.H. was funded, in part, by a training grant from the National Institute of General Medical Sciences, NIH (T32 GM135115). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.
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W.J.M. and W.C.W. were responsible for conceptualizing the project. K.R.B., L.H., A.J.H., G.H., N.M.F., C.L., R.C., J.M.S., E.R., B.W.D., T.R., L.A.L. and S.J.O. developed the methodology. K.R.B., L.H., A.J.H., N.M.F., G.H. and T.R. were involved in data visualization. Funding for the project was acquired by W.J.M. and W.C.W. W.J.M. and W.C.W. were responsible for project administration. Supervision of the project was provided by W.J.M., W.C.W. and M.A.B. The original draft of the manuscript was prepared by W.J.M., K.R.B., L.H., A.J.H., G.H., N.M.F. and W.C.W. All authors contributed to the investigation phase of the study and participated in the review and editing of the manuscript.
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Bredemeyer, K.R., Hillier, L., Harris, A.J. et al. Single-haplotype comparative genomics provides insights into lineage-specific structural variation during cat evolution. Nat Genet 55, 1953–1963 (2023). https://doi.org/10.1038/s41588-023-01548-y
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DOI: https://doi.org/10.1038/s41588-023-01548-y
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