Research ArticleEVOLUTIONARY BIOLOGY

Genome-wide signatures of complex introgression and adaptive evolution in the big cats

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Science Advances  19 Jul 2017:
Vol. 3, no. 7, e1700299
DOI: 10.1126/sciadv.1700299
  • Fig. 1 Evolutionary history of the great cats.

    (A) Species tree of the genus Panthera estimated from genome-wide data. All five extant species are represented as follows: lion (Panthera leo), leopard (P. pardus), jaguar (Panthera onca), snow leopard (Panthera uncia), and tiger (Panthera tigris). Numbers above branches indicate the estimated age [in million years ago (Ma)] of the adjacent node, averaged across all genomic windows (100-kb window size, 100-kb steps) that conform to the species tree (95% highest posterior density interval below the respective branch). Colored rectangles on terminal branches indicate phenotypic categories (defined below the tree; see Fig. 3B for more details) affected by species-specific episodes of positive selection. (B) PSMC plot depicting the demographic history of the five Panthera species inferred from genomic data. (C) Genealogical discordance across the genome of Panthera cats, demonstrated by a sliding window analysis (500-kb window size, 100-kb steps) of a full-genome alignment mapped to domestic cat chromosomes (gray lines at the bottom). The y axis indicates the percentage of overlapping windows within a given interval that conform to (blue) or reject (red) the species tree. Photo credits: D. Kantek (jaguar); C. Sperka (others).

  • Fig. 2 In-depth characterization of phylogenetic discordance in the Panthera.

    (A) Frequencies of the species tree (Tree 1) and alternative topologies on pooled autosomes (blue) and the X chromosome (red). Trees 12 and 23 show the leopard in a basal position relative to the other species (tables S6 and S7). (B) Chromosome-wide mean divergence times (in Ma), calculated from 100-kb windows that yielded the three most frequent topologies (shown below the graphs; nodes are color-coded). Note the marked drop in divergence time on the X chromosome for non–species tree topologies. (C) Complex patterns of historical admixture among Panthera lineages, inferred from ABBA/BABA tests. Colored arrows indicate the phylogenetic position of significant D statistics (shown in the table) for different species trios, using the domestic cat as the outgroup. Species codes in bold types indicate pairs for which significant evidence of admixture was detected. (D) Patterns of phylogenetic discordance along the X chromosome (estimated in 100-kb windows) correlate with the recombination landscape (10). Regions depicting species tree relationships (Tree 1), shown in white, correspond to higher recombination rates, whereas recombination deserts are enriched for alternative topologies with reduced divergence times (a signature of introgression). Two terminal, lower-recombination regions are enriched for topologies 12 and 23, depicting a basal position for leopard. These regions also harbor tracts of windows with old divergence times between the leopard and the other Panthera.

  • Fig. 3 Genomic evidence of natural selection in the Panthera.

    (A) Venn diagrams depicting shared genes (top) and pathways (bottom) among approaches that detect positive selection (site model and branch-site model) and interspecies introgression (Outlier window) (fig. S4 and tables S9 to S13 and S28 to S38). (B) Detailed results of the branch-site test, indicating genes bearing species-specific signatures of positive selection; phenotypic categories (color-coded as in Fig. 1A) were defined on the basis of Kegg and Pathway Commons enrichment results, along with additional literature searches. (C) Two genes with jaguar-specific signatures of positive selection affect craniofacial robustness. Silhouettes on the left depict a jaguar’s robust face relative to the inferred appearance of the Panthera ancestor. The positively selected I298Y substitution in the ESRP1 gene lies in the RRM1 domain, which is known to bind to the FGFR2IIIb gene isoform and affect craniofacial development (17). The two positively selected substitutions (R39A and R42E) in the SSTR4 gene imply substantial physicochemical amino acid changes (green, nonpolar; yellow, polar; blue, basic; red, acid). (D) Schematic representation of the Glypican pathway, showing only genes that were connected with, at most, one intermediate step (in gray) and that exhibited significant signatures of positive selection (purple, site model; orange, tiger branch-site model) or interspecies introgression (blue, outlier window test).

  • Fig. 4 Genomic evidence of positive selection following interspecific introgression.

    (A to C) Graphs depicting variation in age estimates for the trio jaguar-lion-leopard in 100-kb windows across the length of three chromosomes (top) and specific chromosomal segments containing multiple outlier windows with ages significantly younger than the genome-wide average (bottom), indicating introgression. The gray lines in the top panels (gray circles in the bottom panels) represent the basal age of the trio, whereas colored circles represent the age of the internal node in each window (blue, lion-leopard; red, lion-jaguar; green, leopard-jaguar). Below the bottom panels, the annotated exons of a candidate gene located in each focal region are indicated. (D) Intraspecific signals of positive selection in jaguars affecting the three genes highlighted in (A) to (C). The graphs depict the null distribution of the number of segregating sites per gene based on 10,000 demographic simulations (see text); the gray shading indicates significant departure (P < 0.05) from the null expectation, and the red lines represent the observed value for each gene.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/3/7/e1700299/DC1

    fig. S1. Assessment of the effect of genealogical discordance on branch-site tests of positive selection.

    fig. S2. Assessment of divergence between domestic cat and Panthera species in windows containing genes with signatures of interspecies introgression and positive selection.

    fig. S3. Maximum-likelihood phylogeny constructed with a supermatrix consisting of 2151 concatenated single-copy orthologs for 11 mammals, derived from our phylome analysis.

    fig. S4. Enrichment analysis for the site model test.

    table S1. DNA sequencing information for the reference jaguar individual.

    table S2. Jaguar genome assembly quality metrics.

    table S3. Annotated protein-coding genes.

    table S4. Summary of the jaguar transcriptome sequencing results.

    table S5. DNA sequencing information for the leopard genome.

    table S6. Tree topology frequencies in window- and gene-based analyses.

    table S7. Tree topology frequencies for 3732 genes and their introns.

    table S8. Detailed results of the ABBA/BABA tests.

    table S9. Branch-site results for the jaguar.

    table S10. Branch-site results for the lion.

    table S11. Branch-site results for the snow leopard.

    table S12. Branch-site results for the tiger.

    table S13. Site model results.

    table S14. Results of coalescent simulations based on jaguar exome data.

    table S15. Summary of repeat annotation for the jaguar genome.

    table S16. Tandem repeat annotation for the jaguar genome.

    table S17. Forty largest microsatellite families in the jaguar genome.

    table S18. Statistics on noncoding RNA annotation in the jaguar genome.

    table S19. Annotation of nuclear insertions of mitochondrial DNA (NUMTS) in the jaguar genome.

    table S20. Previously reported genomic resources used in our multispecies analyses.

    table S21. Consensus genome information (using the tiger assembly as a reference).

    table S22. Outlier window test results.

    table S23. Outlier Window KEGG enrichment results.

    table S24. Outlier Window Pathway Commons enrichment results.

    table S25. Outlier Window Phenotype enrichment results.

    table S26. Outlier Window Disease enrichment results.

    table S27. Detailed information on the samples used in the exome capture experiment.

    table S28. Enrichment results for the jaguar branch-site test.

    table S29. Enrichment results for the lion branch-site test.

    table S30. Tiger Pathway Commons enrichment results.

    table S31. Tiger KEGG enrichment results.

    table S32. Tiger Disease enrichment results.

    table S33. Site model Pathway Commons enrichment results.

    table S34. Site model KEGG enrichment results.

    table S35. Site model Disease enrichment results.

    table S36. Site model Biological Process enrichment results.

    table S37. Site model Molecular Function enrichment results.

  • Supplementary Materials

    This PDF file includes:

    • fig. S1. Assessment of the effect of genealogical discordance on branch-site tests of positive selection.
    • fig. S2. Assessment of divergence between domestic cat and Panthera species in windows containing genes with signatures of interspecies introgression and positive selection.
    • fig. S3. Maximum-likelihood phylogeny constructed with a supermatrix consisting of 2151 concatenated single-copy orthologs for 11 mammals, derived from our phylome analysis.
    • fig. S4. Enrichment analysis for the site model test.
    • table S1. DNA sequencing information for the reference jaguar individual.
    • table S2. Jaguar genome assembly quality metrics.
    • table S3. Annotated protein-coding genes.
    • table S4. Summary of the jaguar transcriptome sequencing results.
    • table S5. DNA sequencing information for the leopard genome.
    • table S6. Tree topology frequencies in window- and gene-based analyses.
    • table S7. Tree topology frequencies for 3732 genes and their introns.
    • table S8. Detailed results of the ABBA/BABA tests.
    • table S9. Branch-site results for the jaguar.
    • table S10. Branch-site results for the lion.
    • table S11. Branch-site results for the snow leopard.
    • table S14. Results of coalescent simulations based on jaguar exome data.
    • table S15. Summary of repeat annotation for the jaguar genome.
    • table S16. Tandem repeat annotation for the jaguar genome.
    • table S17. Forty largest microsatellite families in the jaguar genome.
    • table S18. Statistics on noncoding RNA annotation in the jaguar genome.
    • table S20. Previously reported genomic resources used in our multispecies analyses.
    • table S21. Consensus genome information (using the tiger assembly as a reference).
    • table S27. Detailed information on the samples used in the exome capture experiment.
    • table S28. Enrichment results for the jaguar branch-site test.
    • table S29. Enrichment results for the lion branch-site test.

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    Other Supplementary Material for this manuscript includes the following:

    • table S12 (Microsoft Excel format). Branch-site results for the tiger.
    • table S13 (Microsoft Excel format). Site model results.
    • table S19 (Microsoft Excel format). Annotation of nuclear insertions of mitochondrial DNA (NUMTS) in the jaguar genome.
    • table S22 (Microsoft Excel format). Outlier window test results.
    • table S23 (Microsoft Excel format). Outlier Window KEGG enrichment results.
    • table S24 (Microsoft Excel format). Outlier Window Pathway Commons enrichment results.
    • table S25 (Microsoft Excel format). Outlier Window Phenotype enrichment results.
    • table S26 (Microsoft Excel format). Outlier Window Disease enrichment results.
    • table S30 (Microsoft Excel format). Tiger Pathway Commons enrichment results.
    • table S31 (Microsoft Excel format). Tiger KEGG enrichment results.
    • table S32 (Microsoft Excel format). Tiger Disease enrichment results.
    • table S33 (Microsoft Excel format). Site model Pathway Commons enrichment results.
    • table S34 (Microsoft Excel format). Site model KEGG enrichment results.
    • table S35 (Microsoft Excel format). Site model Disease enrichment results.
    • table S36 (Microsoft Excel format). Site model Biological Process enrichment results.
    • table S37 (Microsoft Excel format). Site model Molecular Function enrichment results.

    Download Supplementary Tables

    Files in this Data Supplement:

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