Table 1.
Direct and indirect estimates of selection on colour pattern loci.
Combined estimates are integrating the effect of all loci involved in warning colouration. Regions/modules associated with optix: D, B; with cortex: Cr, Yb, N; with WntA: Sd, Ac; with aristaless: K.
Fig 1.
Distribution, phylogenetic relations, major colour pattern loci, and sequence capture targets of the H. melpomene, H. cydno, and H. timareta clade species.
(A) Broad distributions of the H. melpomene, H. cydno, and H. timareta colour pattern races and species (based on all known sampling localities; for details, see S2 Fig). Distribution colours match the shadings around the phylogeny and butterfly images in panel B. The dashed line indicates the Andes. Note the distinct clusters formed by individuals sampled from the H. m. vicina population. The cluster grouping with H. timareta is referred to as H. timareta ssp. nov. (Colombia) (B) FastTree cladogram inferred using capture sequence from putatively neutral loci. Colours in the tree indicate the H. melpomene (pink), H. cydno (green), and H. timareta (blue) clades and match the boxes of the distribution maps in panel A. (C) Sequence information was obtained for 4 putatively neutral regions (green) and 4 regions to which functional variation has been mapped to a yellow/white colour switch (chr 1); forewing band shape (chr 10); yellow/white fore- and hindwing bars, band margins, and ventral colour (chr 15); and red colour pattern elements (chr 18). The various phenotypes controlled by the respective colour pattern loci are depicted. Note that whereas most phenotypes have descriptive names, the red blotch at the base of the forewing was termed ‘dennis’. (D) Phylogenetic relations obtained when building a tree from all captured regions compared to the neutral regions.
Fig 2.
SFS signatures of selection for simulated classic hard sweeps (left) and introgressed sweeps (right). (A) CLR statistics (upper panel, [73,74]) and Tajima’s D (lower panel) across a simulated chromosome for different time points (0.01, 0.1, 0.2, 0.3, 0.4, 0.5, 0.6, 0.7, 0.8, and 1 in units of scaled generations, i.e., 4N generations) after a classic hard (left) or introgressed (right) sweep (effective migration rate M = 0.2). The sweep occurs in the centre of the simulated chromosome. Different colours indicate time since sweep. Full, dashed, and dotted vertical black lines in the lower panel indicate positions at different distances from the sweep centre for which time series of CLR and Tajima’s D statistics are depicted in panel B in the same style. (B) CLR (upper panel) and Tajima’s D (lower panel) statistics over time at 3 positions relative to the sweep centre as shown in panel A. Also shown are neutral background values, BG, calculated over neutral simulations, either without migration (left hand panels, for classic sweeps) or with migration at M = 0.2 (right hand panels, for introgressed sweeps). Time is given in units of scaled generations. Data are available from https://github.com/markusmoest/SelectionHeliconius.git. BG, background; CLR, composite likelihood ratio.
Fig 3.
Signature of selection across colour pattern regions in the H. melpomene clade.
The regions containing the tandem copies of aristaless, al1 and al2, WntA, cortex, and optix (left to right) are depicted. Colour pattern genes are annotated in red in the gene annotation panel. On the y-axis Sweepfinder2’s CLR statistics is shown (peaks capped at 1,000). The colour gradient indicates the estimated intensity of selection α [73] (black = high α values, weak selection; red = low α values, strong selection). Grey shadings indicate annotated colour pattern CREs [30,36,37,39] (S7–S10 Figs). Blue horizontal bars indicate regions with CLR values above threshold. Top panel shows colour pattern phenotypes and symbols indicate distinct colour pattern elements, and their presence is annotated in population panels. Note that the yellow hindwing bar controlled by the cortex region can be expressed on the dorsal and ventral side (yellow/yellow square symbol) or on the ventral side only (black/yellow square symbol) [39]. Moreover, the actual shape of the forewing band can depend on the allelic state of WntA. Full, grey lines connect colour pattern elements with annotated CREs. Phenotypes are depicted on the right. Data are available from https://github.com/markusmoest/SelectionHeliconius.git. CLR, composite likelihood ratio; CRE, cis-regulatory element.
Table 2.
Position, CLR statistics, and estimates for strength of selection (α, 2Nes, and s) for populations and sweeps discussed in detail.
Annotated colour pattern genes and CREs that overlap with peaks are given. Positions are given in Hmel2 scaffold coordinates (see S5 and S7 Tables).
Fig 4.
The 3 examples show the split forewing band (WntA region) in H. m. plessini, the yellow and white patterns (cortex region) in H. cydno weymeri f. weymeri and the red dennis patch (optix region) in H. m. meriana (left to right). The respective colour pattern elements are indicated with red and grey arrows. Colour patterns and gene annotations in the colour pattern regions are depicted in the top panel. Colour pattern genes are annotated in red. Nucleotide diversity π, Tajima’s D, and SweepFinder2’s CLR statistics (peaks capped at 1,000) show the signatures of a selective sweep (bottom panels). Loess smoother lines are depicted in yellow. The colour gradient in the CLR panel indicates the estimated intensity of selection α [73] (black = high α values, weak selection; red = low α values, strong selection). Grey shadings indicate annotated CREs, and red and grey arrows depict associations with the respective colour pattern elements in the H. melpomene clade. Data are available from https://github.com/markusmoest/SelectionHeliconius.git. CLR, composite likelihood ratio; CRE, cis-regulatory element.
Fig 5.
Signatures of selection in the co-mimic populations of H. melpomene (upper panels) and H. erato (lower panels). The regions containing WntA, cortex, and optix are shown (left to right). Co-mimics in H. melpomene and H. erato are depicted in the same order with phenotypes on the left. The y-axis indicates CLR statistics across each region (capped at 1,000). The colour gradient indicates the estimated intensity of selection α [73] (black = high α values, weak selection; red = low α values, strong selection). Grey shadings indicate annotated colour pattern CREs [30,36,37,39] (S7–S10 Figs) and blue horizontal bars indicate regions with CLR statistics above threshold. The central panel shows an alignment of the respective regions in H. melpomene and H. erato and gene annotations with colour pattern genes in red. Top and bottom panel show colour pattern phenotypes, and symbols indicate distinct colour pattern elements and their presence in each population panel. Note that the yellow hindwing bar controlled by the cortex region can be expressed on the dorsal and ventral side (yellow/yellow square symbol) or on the ventral side only (black/yellow square symbol) [39]. Full, grey lines connect colour pattern elements with annotated CREs. Note that the genetics of the yellow forewing band differs between H. erato¸ in which it involves the WntA and optix locus, and H. melpomene, in which the band is controlled by the cortex and its shape by the WntA region. Data are available from https://github.com/markusmoest/SelectionHeliconius.git. CLR, composite likelihood ratio; CRE, cis-regulatory element.
Fig 6.
Geographic mapping of colour pattern selection in H. melpomene (top) and H. erato (middle). Dark grey shadings indicate distributional ranges of the depicted colour patterns. Coloured circles indicate the colour pattern selection summarised as percentage of CLR values across the colour pattern region that are above the CLR threshold [%CLR>th] scaled by the maximum value for WntA, cortex, and optix regions (left to right) in H. melpomene (top) and H. erato (middle). The bottom panel shows correlations for percentage CLR values above threshold [%CLR>th] and maximum intensity of selection α [73] (max(1/α)) between H. melpomene and H. erato. Data are available from https://github.com/markusmoest/SelectionHeliconius.git. CLR, composite likelihood ratio.