Research ArticleEVOLUTIONARY BIOLOGY

Hyena paleogenomes reveal a complex evolutionary history of cross-continental gene flow between spotted and cave hyena

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Science Advances  13 Mar 2020:
Vol. 6, no. 11, eaay0456
DOI: 10.1126/sciadv.aay0456
  • Fig. 1 Sampling distribution and mitogenomic timetree of the hyaenidae family.

    (A) Map showing the geographic origins of our spotted and cave hyena samples. The color of the dot represents the age of the sample. (B) Dated Bayesian phylogenetic tree constructed using complete mitochondrial genomes and a strict molecular clock. Haplogroups are those previously defined in Rohland et al. (9). Red-colored labels show Pleistocene cave hyena and blue-colored labels show modern spotted hyena. The yellow star represents a putative mitochondrial introgression event of unknown direction. The Hyaena/Parahyaena node was fixed for fossil calibration (as indicated by the bone image), and Proteles was set as the outgroup. All major nodes had posterior probability values of 1 (fig. S1). Dark blue node bars show the 95% credibility interval of the divergence dating.

  • Fig. 2 Population structure analyses comparing nuclear genomic information from Pleistocene cave hyena and modern spotted hyena.

    (A) PCA based on genome-wide SNPs. Red shaded area encompasses cave hyenas and blue shaded area encompasses spotted hyenas. (B) Densitree constructed using 2 Mbp sliding windows and a maximum likelihood approach. Light gray lines represent single phylogenetic trees produced from each window. Dark black lines represent the root canal as defined by Densitree. Sample name colors represent the previously defined mitochondrial haplogroups.

  • Fig. 3 PSMC demographic analyses of three modern spotted hyena nuclear genomes.

    The y axis represents effective population size (×10,000), and the x axis represents millions of years before present. Faded lines show bootstrap values.

  • Fig. 4 D statistics results and a schematic overview of the divergence of and post-divergence gene flow between spotted and cave hyenas.

    (A) D statistics results using two cave hyenas, one spotted hyena, and the striped hyena as outgroup. (B) D statistics results using two spotted hyenas, one cave hyena, and the striped hyena as outgroup. Filled circles show significant D scores while nonfilled circles show nonsignificant D scores. (C) Phylogenetic tree presenting the admixture events found between African spotted and Eurasian cave hyena. Blue color represents African inhabitancy and red color represents Eurasian inhabitancy. Arrows show the direction of gene flow events. (Illustration credit: Binia De Cahsan, https://sites.google.com/view/decahsanillustrations.)

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/6/11/eaay0456/DC1

    Table S1. Results from the five-taxon topology test for admixture when considering only Ccsp040 and Ccsp041 as C1 and C2 and all combinations of spotted hyena.

    Table S2. Results from the five-taxon topology test for admixture when considering only Ccsp040 and Ccsp042 as C1 and C2 and all combinations of spotted hyena.

    Table S3. Results from the five-taxon topology test for admixture when considering only Ccsp041 and Ccsp042 as C1 and C2 and all combinations of spotted hyena.

    Table S4. D statistics results with spotted hyena as H1 and H2 and cave hyena as H3.

    Table S5. D statistics results with cave hyena as H1 and H2 and spotted hyena as H3.

    Table S6. Parameter estimates from fastsimcoal.

    Table S7. List of orthologous domestic cat genes found in windows showing signs of admixture from cave hyena into spotted hyena.

    Table S8. List of protein classes of the orthologous domestic cat genes found in windows showing signs of admixture from cave hyena into spotted hyena.

    Table S9. List of biological processes of the orthologous domestic cat genes found in windows showing signs of admixture from cave hyena into spotted hyena.

    Table S10. List of orthologous domestic cat genes found in windows showing signs of admixture from spotted hyena into cave hyena.

    Table S11. List of protein classes of the orthologous domestic cat genes found in windows showing signs of admixture from spotted hyena into cave hyena.

    Table S12. List of biological processes of the orthologous domestic cat genes found in windows showing signs of admixture from spotted hyena into cave hyena.

    Table S13. Modern spotted hyena sample information.

    Table S14. Pleistocene cave hyena sample information.

    Table S15. Spotted hyena mapping values.

    Table S16. Cave hyena mapping values.

    Table S17. Genomic features and substitution model within each partition determined using Partionfinder2 on the Hyaenidae mitochondrial genomes.

    Table S18. Distance matrix used to calculate divergence time between spotted and cave hyena.

    Fig. S1. Bayesian dated phylogenetic tree of the Hyaenidae family constructed using complete mitochondrial genomes.

    Fig. S2. Spotted and cave hyena cladogram consensus tree constructed using 467 maximum likelihood phylogenetic trees from 2 Mbp nonoverlapping windows along the nuclear genome.

    Fig. S3. PCA constructed using only Pleistocene cave hyena individuals.

    Fig. S4. PCA constructed using only modern spotted hyena individuals.

    Fig. S5. Cumulative size distributions of regions returning putative admixture topologies, determined by counting the number of consecutive 100-kb blocks showing a putative admixture topology.

    Fig. S6. MapDamage results for cave hyena genome data.

  • Supplementary Materials

    The PDF file includes:

    • Legends for tables S1 to S3
    • Table S4. D statistics results with spotted hyena as H1 and H2 and cave hyena as H3.
    • Table S5. D statistics results with cave hyena as H1 and H2 and spotted hyena as H3.
    • Table S6. Parameter estimates from fastsimcoal.
    • Table S7. List of orthologous domestic cat genes found in windows showing signs of admixture from cave hyena into spotted hyena.
    • Table S8. List of protein classes of the orthologous domestic cat genes found in windows showing signs of admixture from cave hyena into spotted hyena.
    • Table S9. List of biological processes of the orthologous domestic cat genes found in windows showing signs of admixture from cave hyena into spotted hyena.
    • Table S10. List of orthologous domestic cat genes found in windows showing signs of admixture from spotted hyena into cave hyena.
    • Table S11. List of protein classes of the orthologous domestic cat genes found in windows showing signs of admixture from spotted hyena into cave hyena.
    • Table S12. List of biological processes of the orthologous domestic cat genes found in windows showing signs of admixture from spotted hyena into cave hyena.
    • Table S13. Modern spotted hyena sample information.
    • Table S14. Pleistocene cave hyena sample information.
    • Table S15. Spotted hyena mapping values.
    • Table S16. Cave hyena mapping values.
    • Table S17. Genomic features and substitution model within each partition determined using Partionfinder2 on the Hyaenidae mitochondrial genomes.
    • Table S18. Distance matrix used to calculate divergence time between spotted and cave hyena.
    • Fig. S1. Bayesian dated phylogenetic tree of the Hyaenidae family constructed using complete mitochondrial genomes.
    • Fig. S2. Spotted and cave hyena cladogram consensus tree constructed using 467 maximum likelihood phylogenetic trees from 2 Mbp nonoverlapping windows along the nuclear genome.
    • Fig. S3. PCA constructed using only Pleistocene cave hyena individuals.
    • Fig. S4. PCA constructed using only modern spotted hyena individuals.
    • Fig. S5. Cumulative size distributions of regions returning putative admixture topologies, determined by counting the number of consecutive 100-kb blocks showing a putative admixture topology.
    • Fig. S6. MapDamage results for cave hyena genome data.

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    Other Supplementary Material for this manuscript includes the following:

    • Table S1 (Microsoft Excel format). Results from the five-taxon topology test for admixture when considering only Ccsp040 and Ccsp041 as C1 and C2 and all combinations of spotted hyena.
    • Table S2 (Microsoft Excel format). Results from the five-taxon topology test for admixture when considering only Ccsp040 and Ccsp042 as C1 and C2 and all combinations of spotted hyena.
    • Table S3 (Microsoft Excel format). Results from the five-taxon topology test for admixture when considering only Ccsp041 and Ccsp042 as C1 and C2 and all combinations of spotted hyena.

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