Research ArticleEVOLUTIONARY BIOLOGY

Many functionally connected loci foster adaptive diversification along a neotropical hybrid zone

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Science Advances  25 Sep 2020:
Vol. 6, no. 39, eabb8617
DOI: 10.1126/sciadv.abb8617
  • Fig. 1 Genomic differentiation and selection in H. erato metapopulations.

    (A) Postman (western) and Radiate (eastern) metapopulations show Andean hybrid zone between morphs. (B) Genomic differentiation between Radiate and Postman metapopulations with three major color pattern loci annotated. (C) Signatures of selective sweeps in the Radiate metapopulation shows many loci under selection. Bars mark chromosomes significantly associated with red pattern variation in H. melpomene (red) and H. erato (orange).

  • Fig. 2 Optix binding sites mark loci of adaptation in the Radiate metapopulation.

    (A) Optix binding sites show significantly greater signatures of selective sweeps than expected from annotated CREs chosen randomly from the same developmental stage. The 99.5th percentile line shows the cutoff threshold for strong signals of selection, and bracket highlights the number of Optix-bound and control loci above this threshold. (B) Optix-bound loci with strong signals of selection often form three-dimensional (3D) adaptive hubs. (C) Adaptive hub transcriptional start sites (TSSs) show elevated selection compared to other regulatory elements. (D) Functional characterization of known genes at loci with strong signals of selection and adaptive hubs are often pigment associated.

  • Fig. 3 Optix-bound loci with strong signatures of selection drive genomic differentiation between Radiate and Postman metapopulations.

    The dome/wash color-patterning locus exemplifies a strong signal of selection (A) on an Optix binding site that displays elevated population differentiation (B) and population divergence (C). Loci with strong signals of selection (selected loci) and the “pigment-associated” subset show increasingly significant population differentiation (D) and divergence (E) between Radiate and Postman metapopulations relative to the genome-wide distributions.

  • Fig. 4 A model of adaptation and maintenance of the Radiate morphology.

    (A) Model showing adaptation occurs at many loci, and selection is a product of population size, the effect of a mutation, and the significance of the trait. (B) Genomic differentiation in hybrid zones is determined by both selection and the probability that a conditionally dependent allele will be functional in backcrosses. (C and D) Cartoons show phenotypes and genotypes for hybrid and pure butterflies, and potential backcross offspring broods under two scenarios of differentiation. Direct differentiation (C) of a dominant allele occurs when a hybrid individual backcrosses into the source population. Any offspring with the maladaptive allele from the hybrid parent is less fit. In conditional differentiation (D), offspring with the maladaptive dependent allele are only less fit when that individual also has the maladapted optix allele.

  • Fig. 5 Selection coefficients and conditional differentiation at Optix-bound CREs.

    (A) Plot shows the estimated selection coefficients derived from alpha produced by SweepFinder2; outlier from the dome/wash locus is not shown (s = 0.082). Red bar indicates the largest selection coefficient in the optix locus. (B) Evidence of moderately strong genomic differentiation at Optix-bound loci provides support for a model incorporating conditional differentiation. Orange arrowheads highlight Optix-bound loci with Fst greater than 0.04.

Supplementary Materials

  • Supplementary Materials

    Many functionally connected loci foster adaptive diversification along a neotropical hybrid zone

    James J. Lewis, Steven M. Van Belleghem, Riccardo Papa, Charles G. Danko, Robert D. Reed

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