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Multi-allelic major effect genes interact with minor effect QTLs to control adaptive color pattern variation in Heliconius erato - PubMed

Multi-allelic major effect genes interact with minor effect QTLs to control adaptive color pattern variation in Heliconius erato

Riccardo Papa et al. PLoS One. 2013.

Abstract

Recent studies indicate that relatively few genomic regions are repeatedly involved in the evolution of Heliconius butterfly wing patterns. Although this work demonstrates a number of cases where homologous loci underlie both convergent and divergent wing pattern change among different Heliconius species, it is still unclear exactly how many loci underlie pattern variation across the genus. To address this question for Heliconius erato, we created fifteen independent crosses utilizing the four most distinct color pattern races and analyzed color pattern segregation across a total of 1271 F2 and backcross offspring. Additionally, we used the most variable brood, an F2 cross between H. himera and the east Ecuadorian H. erato notabilis, to perform a quantitative genetic analysis of color pattern variation and produce a detailed map of the loci likely involved in the H. erato color pattern radiation. Using AFLP and gene based markers, we show that fewer major genes than previously envisioned control the color pattern variation in H. erato. We describe for the first time the genetic architecture of H. erato wing color pattern by assessing quantitative variation in addition to traditional linkage mapping. In particular, our data suggest three genomic intervals modulate the bulk of the observed variation in color. Furthermore, we also identify several modifier loci of moderate effect size that contribute to the quantitative wing pattern variation. Our results are consistent with the two-step model for the evolution of mimetic wing patterns in Heliconius and support a growing body of empirical data demonstrating the importance of major effect loci in adaptive change.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Crossing strategy and color pattern variation.

Mendelian segregation of the major color pattern genes in H. erato as seen in our collection of crosses. Four distinct geographic races (from left H. e. etylus (A), H. e. erato (B), H. e. cyrbia (C), and H. e. notabilis (D)) were crossed to H. himera (top) to generate backcross (BC) and F2 mapping families. The nine major phenotypes produced by the segregation of alternative alleles at major loci are arranged in each box with D (top) and Sd, Ly, Sd, and Cr (left) with contributions from H. himera (top and left) and H. erato (bottom and right). Heterozygotes for these major color pattern loci are found in the middle column and row with double heterozygotes in the center. Inferred genotypes are indicated across the top and on the side of each box (see text for details).

Figure 2
Figure 2. Major effect alleles at major color pattern loci segregating in the H. himera×H. erato mapping families.

(A) Distinct geographic races of H. erato and the sister species H. himera used in the mapping crosses. (B) Homozygous phenotypes of the loci that control the distribution of black pigment (“melanin shutter genes”). (C) Homozygous phenotypes produced by the D locus. Allelic variation at this locus controls the distribution of red and yellow color patterns. See text for brief description of major color pattern loci.

Figure 3
Figure 3. Variation of color and forewing band shape in a H. himera×H. erato notabalis F2 cross.

In Panel A, the variation of white/red scale proportions in the forewing is presented across particular color pattern genotypes. All the offspring homozygous with the H. himera D allele showed only yellow pigments, whereas individuals homozygous for the H. e. notabilis alleles possessed were white. Heterozygous individuals were typically white, although there was some variation (Panel B). Panel C and D shows variation in forewing band shape among F2 individuals as a function of Sd genotype.

Figure 4
Figure 4. F2-Not9 linkage map and overall QTL analysis.

(A) F2-Not9 linkage map and overall QTL analysis of the H. himera×H. erato notabilis cross showing the 20 autosomal and two sex linkage groups generated with AFLP and co-dominant anchor loci (Tables S5, Table S6, Table S7, and Table S8). Numbers of the left side represent distance in cM rounded to the closest integer value, while letters on the right side represent marker names. Approximate positions of major color pattern genes (Sd-LG 10, D-LG 18, Cr-LG 15) are indicated with a black square within each linkage group. Vertical bars next to the chromosomes represent QTL regions with colors corresponding to phenotypes measured: red bars = redness; white bars = whiteness; grey bars = Big-Spot (BS); and black bars = Not-Spot (NS). (B) Pie charts show the relative contributions of individual markers to the total variance explained when all significant QTLs were analyzed under the best model (additive or epistatic). Note that F2-Not9 LG 1, LG 10, LG 18 and LG 15 correspond to LG 4, LG 3, LG 6 and LG 2 in Kapan et al. (2006) and to LG 1, LG 10, LG 18 and LG 15 in Jiggins et al. (2005) respectively. Linkage analysis and autosomal LG numbers for the F2-NotF29 reference map are arranged with the same numbers as H. melpomene when homology could have ben established.

Figure 5
Figure 5. The homologous position of the D color pattern gene in four different races of H. erato and its pleiotropic effect on forewing color pattern.

(A) The fine resolution map (over 600 Kb) of several co-dominant markers linked to the D color pattern gene across all our collection of crosses. The relative position and number of recombinant individuals for the eight co-dominant markers linked to the D color pattern gene (see Table S1) confirmed the homologous position of D across all H. erato races used in our crosses. The numbers within brackets in panel A represent the total number of recombinant individuals generated by combining the information from all crosses (Table S1). (B) The linkage analysis of LG 18 in the F2-Not9 cross and the relative position of the D locus on the chromosome, including the position and name of AFLP loci, two of the eight co-dominant markers (D23/24 and optix) and the D locus along the chromosome. (C) QTL analysis for the forewing band color (red and/or white) on LG 18. The very high LOD score coupled with the significance of the D locus make the entire LG 18 a significant QTL (P<0.01) (black stars) (see Table S5).

Figure 6
Figure 6. A single locus controls variation in the forewing black patterns of the H. erato radiation.

(A) Linkage analysis of forewing black pattern variation segregating in three types of H. himera×H. erato F2 crosses. The dotted lines connect anchor AFLP loci indicating that the loci responsible for much of the variation in forewing band shape maps to homologous genomic intervals. The linkage analysis for the best placement of Sdety was published in Kapan et al. (2006) while the genetic map of the other three loci Ly, Sdnot and St is novel to this study. For each linkage analysis the black bars represent the probability of placement of each gene in a particular interval (see Kapan et al. 2006), while on the right side of the figure the overall probability for the best placement assuming a single locus affects these melanic patterns in all three crosses. (B) The effect of LG 10 on quantitative variation size of the lower (BS = grey line) and upper (NS = black line) forewing band is shown. For the lower band, there is evidence for a single QTL centered at Sd (WntA) that explains near 1/3 of the variation in the size of the band (QTL region 1). For the upper band, epistatic interaction between possibly two linked QTLs (QTL region 1 and QTL region 2) on LG 10 explain over 82% of the observed variation (see Table 1 and Table S8).

Figure 7
Figure 7. A developmental model for the observed phenotypic effects of the alleles at the Sd locus on the black pattern of the forewing.

(A) The arrangement of organizing centers for Heliconius wing patterns. Lower case letters indicate serially homologous organizing centers (Nijhout and Wray 1988). The organizing centers control development of the black parts of the color pattern. The dotted line, delimit a hypothetical region (shaded) that represent s the influence of the two QTLs (Sd = WntA and possibly Ro color pattern genes) that control the upper forewing H. e. notabilis patch (see Figure 6). The Sd black melanization pattern is centered on the d and f NGP elements while the Ro melanization pattern coincide with the h NGP elements. (B) Expansion of the black pattern controlled by each of the Sd alleles. Each allele controls a different aspect of pattern expansion from organizing centers d and f. The Sdera allele also controls melanization along the wing veins, which breaks up the colored background pattern into discrete patches. The hypothetical region of action for the Sd and Ro color pattern genes is shown as well for the individual H. erato races.

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Funding for this study was provided by National Science Foundation grants (IOS 1052541, DEB-0844244, DEB-9806792) to WOM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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