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Phylogenomic evidence for ancient hybridization in the genomes of living cats (Felidae)

  1. William J. Murphy1,2
  1. 1Department of Veterinary Integrative Biosciences, Texas A&M University, College Station, Texas 77843, USA;
  2. 2Interdisciplinary Program in Genetics, Texas A&M University, College Station, Texas 77843, USA;
  3. 3Faculdade de Biociências, PUCRS, Porto Alegre, RS 90619-900, Brazil
  1. Corresponding author:wmurphy{at}cvm.tamu.edu
  • 4 Present address: National Human Genome Research Institute, National Institutes of Health, Bethesda, MD 20892, USA

Abstract

Inter-species hybridization has been recently recognized as potentially common in wild animals, but the extent to which it shapes modern genomes is still poorly understood. Distinguishing historical hybridization events from other processes leading to phylogenetic discordance among different markers requires a well-resolved species tree that considers all modes of inheritance and overcomes systematic problems due to rapid lineage diversification by sampling large genomic character sets. Here, we assessed genome-wide phylogenetic variation across a diverse mammalian family, Felidae (cats). We combined genotypes from a genome-wide SNP array with additional autosomal, X- and Y-linked variants to sample ∼150 kb of nuclear sequence, in addition to complete mitochondrial genomes generated using light-coverage Illumina sequencing. We present the first robust felid time tree that accounts for unique maternal, paternal, and biparental evolutionary histories. Signatures of phylogenetic discordance were abundant in the genomes of modern cats, in many cases indicating hybridization as the most likely cause. Comparison of big cat whole-genome sequences revealed a substantial reduction of X-linked divergence times across several large recombination cold spots, which were highly enriched for signatures of selection-driven post-divergence hybridization between the ancestors of the snow leopard and lion lineages. These results highlight the mosaic origin of modern felid genomes and the influence of sex chromosomes and sex-biased dispersal in post-speciation gene flow. A complete resolution of the tree of life will require comprehensive genomic sampling of biparental and sex-limited genetic variation to identify and control for phylogenetic conflict caused by ancient admixture and sex-biased differences in genomic transmission.

Footnotes

  • ReceivedNovember 3, 2014.
  • AcceptedOctober 13, 2015.

This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (seehttp://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described athttp://creativecommons.org/licenses/by-nc/4.0/.

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  1. Published in AdvanceOctober 30, 2015, doi:10.1101/gr.186668.114 Genome Res. 26: 1-11© 2016 Li et al.; Published by Cold Spring Harbor Laboratory Press
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