Comparative population genetics of a mimicry locus among hybridizing Heliconius butterfly species

Abstract

The comimetic Heliconius butterfly species pair, H. erato and H. melpomene, appear to use a conserved Mendelian switch locus to generate their matching red wing patterns. Here we investigate whether H. cydno and H. pachinus, species closely related to H. melpomene, use this same switch locus to generate their highly divergent red and brown color pattern elements. Using an F2 intercross between H. cydno and H. pachinus, we first map the genomic positions of two novel red/brown wing pattern elements; the G locus, which controls the presence of red vs brown at the base of the ventral wings, and the Br locus, which controls the presence vs absence of a brown oval pattern on the ventral hind wing. The results reveal that the G locus is tightly linked to markers in the genomic interval that controls red wing pattern elements of H. erato and H. melpomene. Br is on the same linkage group but approximately 26 cM away. Next, we analyze fine-scale patterns of genetic differentiation and linkage disequilibrium throughout the G locus candidate interval in H. cydno, H. pachinus and H. melpomene, and find evidence for elevated differentiation between H. cydno and H. pachinus, but no localized signature of association. Overall, these results indicate that the G locus maps to the same interval as the locus controlling red patterning in H. melpomene and H. erato. This, in turn, suggests that the genes controlling red pattern elements may be homologous across Heliconius, supporting the hypothesis that Heliconius butterflies use a limited suite of conserved genetic switch loci to generate both convergent and divergent wing patterns.

Figure 1

The genomic position of loci controlling red/brown color pattern elements is conserved across Heliconius butterflies. (a) Photos of vental wing surfaces show red and brown pattern elements. The G locus controls the presence of red vs brown (codominant) at the base of the ventral wings, Br controls the presence (dominant) vs absence (recessive) of the brown oval pattern on the ventral hind wing and B controls the presence (dominant) vs absence (recessive) of the red band on the fore wing of H. melpomene. (b) Segregation at linked loci G and Br in an F2 intercross between H. cydno and H. pachinus. (c) Mapping G and Br loci, relative to conserved markers, revealed that the G locus is tightly linked to the same candidate interval housing the B/D loci of H. melpomene and the D locus of H. erato. Unlabeled horizontal lines on linkage maps indicate positions of other linked markers. Comparative data for H. melpomene and H. erato are from Baxter et al. (2008, 2010).

Figure 2

Surveys of genetic differentiation and linkage disequilibrium (LD) through the G locus candidate interval in comparisons among H. cydno, H. pachinus and H. melpomene. For each of 116 polymorphisms (Supplementary Table S3), we calculated F_ST values in comparisons between (a) H. cydno and H. pachinus, (b) H. cydno and H. melpomene, and (c) H. pachinus and H. melpomene. Red points indicate markers with significant (P<0.05) F_ST values. Marker order: 1, DNAJ/HSP; 2, Popeye; 3, Ashwin; 4, Sin-Ex; 5, Slu7; 6, Kinesin; 7, GPCR; 8, Esterase; 9, Epoxide hydrolase; 10, Sine Oculis; 11, LRR; 12, Strabismus/Van Gogh; 13, SCY-1; 14, THAP; 15, Helicase (Supplementary Table S1). LD heat maps for (d) H. cydno, (e) H. pachinus and (f) H. cydno and H pachinus together, with similar plots for H. melpomene and pairwise comparisons with H. melpomene in Supplementary Figure S1. White rows/columns indicate comparisons involving monomorphic positions or missing data.