Research ArticleEVOLUTIONARY BIOLOGY

Repeated divergent selection on pigmentation genes in a rapid finch radiation

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Science Advances  24 May 2017:
Vol. 3, no. 5, e1602404
DOI: 10.1126/sciadv.1602404
  • Fig. 1 Genomic landscapes in southern capuchino seedeaters.

    (A) Map indicating the extent of range overlap in the nine species; note that up to six species breed sympatrically in northeastern Argentina. The range of each species is outlined by dashed lines, with colors matching species names. The schematic phylogeny was obtained from Campagna et al. (see text for name abbreviations) (14, 15). (B) PCA including 56 individuals of five species genotyped at ~11.5 million SNPs and a second PCA (60 individuals) using SNPs from divergence peaks alone. Four outlier individuals were omitted from the first PCA (see fig. S1 and Materials and Methods for details). (C) Manhattan plots for nig versus mel (top) and hypox versus pal (bottom); 12 individuals per species. Each circle indicates the mean FST value for all the SNPs within a nonoverlapping 25-kb window. Scaffolds in the reference genome were sorted by decreasing size and are indicated by alternating colors. The threshold for calling divergent windows is indicated by the dashed red line, and the percentage of total elevated windows is noted next to each comparison. The inset is a histogram showing the width distribution (in kilobases) for the 25 divergence peaks we identified.

  • Fig. 2 Repeated selection on pigmentation genes in different capuchino species.

    (A) Divergence peak on scaffold 252, which mapped to chromosome 20 in the zebra finch. The 10 possible pairwise comparisons across five capuchino species are overlaid (see color-coded legend to identify specific comparisons). Each circle is the mean FST value for all SNPs within a nonoverlapping 5-kb window. (B) PCA for 60 individuals of five species using the SNPs from under the peak in (A); see the legend to identify species. (C) FST and genomic location of individual SNPs with values of 0.85 and higher, color-coded by pairwise comparison as in (A). The positions of genes that are close to these highly divergent SNPs are indicated by arrows drawn to scale. Names in red note genes involved in the melanogenesis pathway. (D to F) As above, for the divergence peak on scaffold 412. (G to I) As above, for the divergence peak on scaffold 404. (J to L) As above, for the divergence peak on scaffold 257. (K and L) The top plot corresponds to the peak labeled “A” and the bottom one to the peak labeled “B” in (J). Annotations with question marks did not match known genes.

  • Fig. 3 Repeated selection on nonpigmentation genes in different capuchino species.

    (A) Divergence peak for scaffold 762 (left), PCA obtained from SNPs under the peak (center), and FST values for highly divergent SNPs with gene annotations (right). The GPT2 gene is involved in alanine degradation and contains the only fixed difference (FST = 1) found in a coding region in our data set (fixed in nig versus hypox and nig versus mel). DASRA-A is a gene involved in the regulation of mitosis. (B) The divergence peak on scaffold 308 did not align reliably to a zebra finch chromosome. This peak contained the genes ME2 (involved in conversion of malate to pyruvate) and ELAC1 (involved in transfer RNA maturation). (C) The gene HERC2 was found in the peak on scaffold 430. This gene contains a regulator of the pigmentation gene OCA2. Other details as in Fig. 2.

  • Fig. 4 Conserved genomic regions across multiple bird species.

    (A) PhastCons scores in regions close to ASIP. The y axis represents the probability of a nucleotide being conserved in a multigenome alignment of the budgerigar, zebra finch, chicken, and turkey genomes. For the promoter, we used a 1-kb region upstream of the gene. The area of high divergence is shown in Fig. 2C. (B) Same as in (A) for KIT ligand (KITL). In this case, the gene model did not contain intron and exon boundaries.

  • Fig. 5 LD among divergence peaks.

    The r2 statistic was calculated among all possible combinations of positions that were fixed (FST = 1) in at least one pairwise comparison between species. Fixed SNPs were found in a total of five divergence peaks (the peaks on scaffolds 252, 308, 567, 404, and 762). Lower triangular matrices display the r2 value averaged across all the positions in that comparison. The upper triangular matrices display the highest r2 value that was observed. The calculation was carried out within species (nig and hypox shown) and when all species were pooled together. The size of the circle and the shade of blue (see scale) indicate the magnitude of the r2 value.

  • Table 1 Areas of the genome that are highly differentiated in capuchino seedeaters.
    ScaffoldChromosomePeak size
    (kb)
    Highest FST
    for 5-kb window
    SNPs with
    FST > 0.85 (=1)*
    Melanogenesis
    gene
    Function of
    melanogenesis gene
    Total no. of genes
    (known function)
    Figure
    25220900.83383 (57)ASIPInduces melanocytes to
    synthesize pheomelanin
    (yellow) instead of
    eumelanin (black/brown)
    6 (4)Fig. 2
    76211350.63178 (22)9 (9)Fig. 3
    4121A2050.70113KITLStimulates melanocyte
    proliferation
    1 (1)Fig. 2
    308Unknown1400.65112 (14)4 (4)Fig. 3
    4301850.481054 (1)Fig. 3
    404Z7650.6092 (5)SLC45A2Transports substances
    needed for
    melanin synthesis
    21 (20)Fig. 2
    257 (A)Z5000.5370TYRP1Enzyme important for
    melanin biosynthesis
    7 (6)Fig. 2
    17174300.7870CAMK2DCell communication9 (7)fig. S3
    362213850.483744 (17)
    257 (B)Z8400.5429MLANAPlays a role in
    melanosome biogenesis
    28 (20)Fig. 2
    56722600.6523 (1)8 (4)
    57916700.331316 (13)
    19545750.57113 (2)
    5915850.3586 (2)
    1182250.6173 (2)
    257Z2650.39611 (6)
    404Z1950.5553 (3)
    257Z3700.53423 (10)
    7664650.5346 (6)
    637Z400.4540
    16356300.4631 (1)
    257Z450.31216 (15)
    263Z5350.342MYO5AActin-based motor
    protein involved in
    melanosome transport
    24 (11)fig. S3
    7911500.401TYR or DCT§TYR: Enzyme involved in
    converting
    tyrosine to melanin
    DCT: Regulates
    eumelanin and
    pheomelanin levels
    4 (3)fig. S3
    637Z3000.3010

    *Scaffolds are ranked from top to bottom by the number of highly divergent SNPs (FST > 0.85).

    †Information from DAVID (Database for Annotation, Visualization and Integrated Discovery) (https://david.ncifcrf.gov/) and GeneCards (www.genecards.org).

    ‡Total of 257 annotations, of which 246 were unique and 11 were predicted more than once. Approximately 63% (156) of the unique annotations matched a record in the UniProt database with a known name and function.

    §Annotation predicted on the basis of protein similarity of both TYR and DCT, which are on chromosome 1 in the zebra finch.

    Supplementary Materials

    • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/3/5/e1602404/DC1

      fig. S1. Clustering of individuals by species.

      fig. S2. Genomic landscapes of differentiation in 10 pairwise comparisons of five species.

      fig. S3. Repeated selection on pigmentation genes in different capuchino species II.

      fig. S4. Absolute sequence divergence inside and outside of peak areas.

      fig. S5. MC1R is not differentiated in capuchinos.

      fig. S6. Structural variants found comparing two capuchino species (hypox and pil).

      table S1. Details on the samples used in this study.

    • Supplementary Materials

      This PDF file includes:

      • fig. S1. Clustering of individuals by species.
      • fig. S2. Genomic landscapes of differentiation in 10 pairwise comparisons of five species.
      • fig. S3. Repeated selection on pigmentation genes in different capuchino species II.
      • fig. S4. Absolute sequence divergence inside and outside of peak areas.
      • fig. S5. MC1R is not differentiated in capuchinos.
      • fig. S6. Structural variants found comparing two capuchino species (hypox and pil).
      • table S1. Details on the samples used in this study.

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