Research ArticleZOOLOGICAL POPULATION GENETICS

Genomic analysis reveals hidden biodiversity within colugos, the sister group to primates

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Science Advances  10 Aug 2016:
Vol. 2, no. 8, e1600633
DOI: 10.1126/sciadv.1600633
  • Fig. 1 Phylogenetic placement of Dermoptera.

    (A) Phylogenies depicting alternative hypotheses for dermopteran relationships relative to primates and treeshrews. (B) Number of indels supporting each evolutionary relationship. (C) Number of transposed elements supporting each evolutionary relationship.

  • Fig. 2 Functional gene evolution and positive selection in colugos and ancestral primates.

    (A) Relative abundance of functional V1R (orange) and OR (blue) genes across sequenced mammals. The size of the circles is proportional to the number of functional genes. (B) Colugo gliding with patagium fully extended. (C). Venn diagram showing relationship between categories of enriched disease gene categories of colugo positively selected genes.

  • Fig. 3 Colugo phylogeography based on museomics.

    (A to C) Timetrees based on major lineages within phylogenies representing maternal (mtDNA; 16.6 kb), biparental (autosome + chrX; 115.6 kb), and paternal (chrY; 24.3 kb) evolutionary histories (figs. S7 to S12). Nodes with 100% maximum likelihood bootstrap support are denoted with red asterisks. Maps depict sample collection locations for each tree with corresponding colored symbol. Boxes indicate highly supported monophyletic clusters or divergent lineages representing putative species. Gray vertical bars denote times of low sea stands. VNM, Vietnam; THA, Thailand; PM, Peninsular Malaysia; S. SUM, south Sumatra; E/SE. BOR, east/southeast Borneo; NE BOR, northeast Borneo; SW BOR, southwest Borneo; NW. BOR, northwest Borneo; BUN, Bunguran; BAS, Basilan; E. MIN, eastern Mindanao; W. MIN, western Mindanao; BOL, Bohol; LTE, Leyte; SAM, Samar; DIN, Dinagat.

  • Fig. 4 Comparison of genetic distance between well-established species and proposed species groups for Galeopterus and Cynocephalus.

    (A and B) mtDNA and nuclear DNA. The x axis lists the name of each genus followed by the number of species in that genus that were compared. For colugo genera, this number represents a conservative number of proposed groups/species. Colugo genera are highlighted in red and blue boxes.

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/2/8/e1600633/DC1

    fig. S1. Maximum likelihood phylogeny of Euarchontoglires based on an alignment of 631 orthologous protein-coding sequences.

    fig. S2. Insertion-deletion evidence for colugo phylogenetic relationships based on transposons.

    fig. S3. Description of the transposon screening strategy.

    fig. S4. Phylogenetically informative protein-coding gene indels supporting Primatomorpha (P1 to P15), Sundatheria (S1 to S5), and Primates + Scandentia (PS1 to PS5).

    fig. S5. Maximum likelihood timetree showing seven nodes with external fossil calibrations.

    fig. S6. Maximum likelihood timetree showing seven nodes with external fossil calibrations, with euarchontan monophyly enforced.

    fig. S7. Maximum likelihood mtDNA tree based on a matrix of 53 colugos with ≥90% mitogenome coverage.

    fig. S8. Maximum likelihood mtDNA tree based on a matrix of 65 colugos with ≥30% mitogenome coverage.

    fig. S9. Maximum likelihood tree based on a combined nuclear (biparental + Y) matrix of 17 taxa.

    fig. S10. Maximum likelihood tree based on biparental data set (18 taxa).

    fig. S11. Maximum likelihood Y chromosome tree (depth 2) (15 taxa).

    fig. S12. Maximum likelihood Y chromosome tree (depth 3) (14 taxa).

    fig. S13. Biplot of PC1 and PC2 from PCA of colugo X chromosome variants.

    fig. S14. Biplot of PC2 and PC3 from PCA of colugo X chromosome variants.

    fig. S15. Biplot of PC3 and PC4 from PCA of colugo X chromosome variants.

    fig. S16. Biplot of PC4 and PC5 from PCA of colugo X chromosome variants.

    fig. S17. Biplot of PC5 and PC6 from PCA of colugo X chromosome variants.

    fig. S18. Biplot of morphometric PCA with males and females, and no dwarf specimens removed.

    fig. S19. Biplot of colugo morphometric PCA, with male, female, and dwarf specimens, where all measurements are normalized by body size.

    table S1. Mammals used in phylogenetic analyses.

    table S2. Presence/absence of phylogenetically informative retroposon markers and species distribution.

    table S3. Location of diagnostic retroposon markers in the human genome.

    table S4. χ2 calculation for phylogenetically informative indels.

    table S5. Colugo and select mammal V1R and OR gene annotation summaries.

    table S6. Nuclear capture efficiency.

    table S7. Adapter blocking oligos.

    table S8. Off-target mtDNA assembly statistics.

    table S9. External fossil calibrations used to calculate divergence time between the two colugo genera.

    table S10. Principal component loadings for morphometric PCA using males and females with no dwarf individuals.

    table S11. Principal component loadings for morphometric PCA using males, females, and dwarf individuals, and all measurements were normalized for body size.

    table S12. mtDNA maximum composite likelihood + Γ distance matrix calculated between seven Sunda colugo groups and five Philippine groups.

    table S13. X chromosome maximum composite likelihood + Γ distance matrix calculated between seven Sunda colugo groups and three Philippine groups.

    table S14. Between-group mtDNA composite likelihood + Γ distance matrix for Sunda colugos from Thailand, Peninsular Malaysia, and Sumatra, and their satellite islands.

    table S15. Within-group mtDNA maximum composite likelihood + Γ distance matrix.

    table S16. Between-group mtDNA composite likelihood + Γ distance matrix for 10 Sunda colugo groups and 5 Philippine groups.

    table S17. BPP species estimation results for Sunda colugos.

    table S18. BPP species estimation results for Philippine colugos.

    table S19. Principal component loadings for X chromosome genetic variants.

    database S1. Dermopteran positively selected genes.

    database S2. Dermopteran WebGestalt results.

    database S3. Ancestral primate positively selected genes.

    database S4. Ancestral primate WebGestalt results.

    database S5. Museum specimen information.

    database S6. Primers used to amplify nuclear DNA capture probes.

    database S7. Craniodental morphometric measurements for 125 Sunda colugos.

    References (7580)

  • Supplementary Materials

    This PDF file includes:

    • fig. S1. Maximum likelihood phylogeny of Euarchontoglires based on an alignment of 631 orthologous protein-coding sequences.
    • fig. S2. Insertion-deletion evidence for colugo phylogenetic relationships based on transposons.
    • fig. S3. Description of the transposon screening strategy.
    • fig. S4. Phylogenetically informative protein-coding gene indels supporting Primatomorpha (P1 to P15), Sundatheria (S1 to S5), and Primates + Scandentia (PS1 to PS5).
    • fig. S5. Maximum likelihood timetree showing seven nodes with external fossil calibrations.
    • fig. S6. Maximum likelihood timetree showing seven nodes with external fossil calibrations, with euarchontan monophyly enforced.
    • fig. S7. Maximum likelihood mtDNA tree based on a matrix of 53 colugos with ≥90% mitogenome coverage.
    • fig. S8. Maximum likelihood mtDNA tree based on a matrix of 65 colugos with ≥30% mitogenome coverage.
    • fig. S9. Maximum likelihood tree based on a combined nuclear (biparental + Y) matrix of 17 taxa.
    • fig. S10. Maximum likelihood tree based on biparental data set (18 taxa).
    • fig. S11. Maximum likelihood Y chromosome tree (depth 2) (15 taxa).
    • fig. S12. Maximum likelihood Y chromosome tree (depth 3) (14 taxa).
    • fig. S13. Biplot of PC1 and PC2 from PCA of colugo X chromosome variants.
    • fig. S14. Biplot of PC2 and PC3 from PCA of colugo X chromosome variants.
    • fig. S15. Biplot of PC3 and PC4 from PCA of colugo X chromosome variants.
    • fig. S16. Biplot of PC4 and PC5 from PCA of colugo X chromosome variants.
    • fig. S17. Biplot of PC5 and PC6 from PCA of colugo X chromosome variants.
    • fig. S18. Biplot of morphometric PCA with males and females, and no dwarf specimens removed.
    • fig. S19. Biplot of colugo morphometric PCA, with male, female, and dwarf specimens, where all measurements are normalized by body size.
    • table S1. Mammals used in phylogenetic analyses.
    • table S2. Presence/absence of phylogenetically informative retroposon markers and species distribution.
    • table S3. Location of diagnostic retroposon markers in the human genome.
    • table S4. χ2 calculation for phylogenetically informative indels.
    • table S5. Colugo and select mammal V1R and OR gene annotation summaries.
    • table S6. Nuclear capture efficiency.
    • table S7. Adapter blocking oligos.
    • table S8. Off-target mtDNA assembly statistics.
    • table S9. External fossil calibrations used to calculate divergence time between the two colugo genera.
    • table S10. Principal component loadings for morphometric PCA using males and females with no dwarf individuals.
    • table S11. Principal component loadings for morphometric PCA using males, females, and dwarf individuals, and all measurements were normalized for body size.
    • table S12. mtDNA maximum composite likelihood + Γ distance matrix calculated between seven Sunda colugo groups and five Philippine groups.
    • table S13. X chromosome maximum composite likelihood + Γ distance matrix calculated between seven Sunda colugo groups and three Philippine groups.
    • table S14. Between-group mtDNA composite likelihood + Γ distance matrix for Sunda colugos from Thailand, Peninsular Malaysia, and Sumatra, and their satellite islands.
    • table S15. Within-group mtDNA maximum composite likelihood + Γ distance matrix.
    • table S16. Between-group mtDNA composite likelihood + Γ distance matrix for 10 Sunda colugo groups and 5 Philippine groups.
    • table S17. BPP species estimation results for Sunda colugos.
    • table S18. BPP species estimation results for Philippine colugos.
    • table S19. Principal component loadings for X chromosome genetic variants.
    • Legends for database S1 to S7
    • References (7580)

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    Other Supplementary Material for this manuscript includes the following:

    • database S1 (Microsoft Excel format). Dermopteran positively selected genes.
    • database S2 (Microsoft Excel format). Dermopteran WebGestalt results.
    • database S3 (Microsoft Excel format). Ancestral primate positively selected genes.
    • database S4 (Microsoft Excel format). Ancestral primate WebGestalt results.
    • database S5 (Microsoft Excel format). Museum specimen information.
    • database S6 (Microsoft Excel format). Primers used to amplify nuclear DNA capture probes.
    • database S7 (Microsoft Excel format). Craniodental morphometric measurements for 125 Sunda colugos.

    Download databases S1 to S7

    Files in this Data Supplement:

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