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Natural selection interacts with recombination to shape the evolution of hybrid genomes

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Science  11 May 2018:
Vol. 360, Issue 6389, pp. 656-660
DOI: 10.1126/science.aar3684
  • Fig. 1 Predicted relationships between minor parent ancestry and recombination rates and properties of focal swordtail populations.

    (A) In the presence of hybrid incompatibilities, minor parent ancestry is more likely to persist in regions of high recombination. (B) One randomly chosen replicate of simulations under plausible parameters for swordtail species (21). Red points indicate the means, and whiskers indicate 2 SEM; gray points are raw data. (C) Maximum likelihood trees from RAxML for 1000 alignments of randomly selected 10-kb regions in swordtail species. Dxy refers to the average nucleotide divergence between X. birchmanni and X. malinche. (D) Locations of hybrid populations in river systems in Hidalgo, Mexico. Elevations of the hybrid populations and typical elevations for parental populations are listed in blue. (E) Inferred ancestry proportions for individuals (n) sampled from each population. (F) Effective population sizes inferred from three X. malinche genomes (sampled from two populations) and 20 X. birchmanni genomes. Fifty bootstraps are shown for one individual from each X. malinche population (21).

  • Fig. 2 Relationships between minor parent ancestry and recombination rate in swordtails and hominins.

    (A) Relationship between minor parent ancestry and recombination rate in swordtails and in humans, summarized in 50-kb windows for swordtail analyses and 250-kb windows for humans (fig. S8), so that the numbers of windows are similar. (B) Spearman’s correlations between average minor parent ancestry and recombination rate at several scales [complete results are provided in table S2, and details of the Denisovan analysis are provided in (21)]. In (A), red points and whiskers indicate the means with 2 SEM determined by bootstrapping; gray points show raw data. Quantile binning is for visualization; statistical tests were performed on the unbinned data.

  • Fig. 3 Evidence for BDMIs being the major source of selection on hybrids.

    (A and B) Correlations in ancestry between independently formed swordtail hybrid populations (in 0.1-centimorgan windows) (fig. S9). Points show the means, and whiskers indicate 2 SEM; correlations were calculated on unbinned data. (C) Predictions for different sources of selection on hybrids. rec., recombination; pops., populations; NA, not applicable. (D) The average proportion of minor parent ancestry is unusually depleted in 50-kb windows containing putative unlinked BDMIs [red points, from (23)] compared with that in 1000 null data sets (blue) (21). Lower average minor parent ancestry at putative BDMIs is not expected as a result of the way the BDMIs were originally identified (21).

  • Fig. 4 The recombination mechanism shapes the distribution of minor parent ancestry.

    (A) Neandertal ancestry is not elevated in 50-kb windows that overlap with CpG islands (CGIs) compared with windows that do not but have similar GC content. The fold difference λ is 0.95 (P = 0.91) (21). The same analysis for swordtail hybrids reveals that the proportion of minor parent ancestry is higher in windows that overlap CGIs (population 1, λ = 1.09, P < 0.005; population 2, λ = 1.09, P < 0.005; population 3, λ = 1.02, P < 0.005). Points show the means, and whiskers indicate 2 SEM obtained from 1000 joint bootstraps. (B) Simulations of incompatibility selection in swordtails predict an enrichment of minor parent ancestry near CGIs. (C) This prediction is met for all hybrid populations. In (B) and (C), gray lines show results of 500 replicate simulations bootstrapping 5-kb windows; colored lines indicate the means for all replicates in sliding 5-kb windows.

Supplementary Materials

  • Natural selection interacts with recombination to shape the evolution of hybrid genomes

    Molly Schumer, Chenling Xu, Daniel L. Powell, Arun Durvasula, Laurits Skov, Chris Holland, John C. Blazier, Sriram Sankararaman, Peter Andolfatto, Gil G. Rosenthal, Molly Przeworski

    Materials/Methods, Supplementary Text, Tables, Figures, and/or References

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    • Materials and Methods
    • Figs. S1 to S31
    • Tables S1 to S8
    • References

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