Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless - PubMed (original) (raw)

Comparative Study

. 2006 Apr 25;103(17):6575-80.

doi: 10.1073/pnas.0509685103. Epub 2006 Apr 12.

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Comparative Study

Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless

Marcus R Kronforst et al. Proc Natl Acad Sci U S A. 2006.

Abstract

Sexual isolation is a critical form of reproductive isolation in the early stages of animal speciation, yet little is known about the genetic basis of divergent mate preferences and preference cues in young species. Heliconius butterflies, well known for their diversity of wing color patterns, mate assortatively as a result of divergence in male preference for wing patterns. Here we show that the specific cue used by Heliconius cydno and Heliconius pachinus males to recognize conspecific females is the color of patches on the wings. In addition, male mate preference segregates with forewing color in hybrids, indicating a genetic association between the loci responsible for preference and preference cue. Quantitative trait locus mapping places a preference locus coincident with the locus that determines forewing color, which itself is perfectly linked to the wing patterning candidate gene, wingless. Furthermore, yellow-colored males of the polymorphic race H. cydno alithea prefer to court yellow females, indicating that wing color and color preference are controlled by loci that are located in an inversion or are pleiotropic effects of a single locus. Tight genetic associations between preference and preference cue, although rare, make divergence and speciation particularly likely because the effects of natural and sexual selection on one trait are transferred to the other, leading to the coordinated evolution of mate recognition. This effect of linkage on divergence is especially important in Heliconius because differentiation of wing color patterns in the genus has been driven and maintained by natural selection for Müllerian mimicry.

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Conflict of interest statement

Conflict of interest statement: No conflicts declared.

Figures

Fig. 1.

Fig. 1.

Probability of H. cydno and H. pachinus males approaching female wings displaying various combinations of color and pattern. (A) When given the choice of approaching females displaying four combinations of color and pattern, H. cydno males were as likely to approach the altered white H. pachinus as they were to approach their conspecific female (G1 = 0.93, P = 0.3349). They were significantly less likely to approach either the unaltered H. pachinus or altered yellow H. cydno female (G1 > 51.76, P < 0.0001, for both comparisons). In contrast, the probability of _H. pachinus_ males approaching the yellow _H. cydno_ female was equal to that of their conspecific female (G1 = 1.53, _P_ = 0.2161), whereas the probabilities for both white females were lower (G1 > 20.14, P < 0.0001, for both comparisons). (B) Males of both species responded to F1 female wings (H. pachinus female × H. cydno male) as they did to those of H. cydno. The probability of H. cydno males approaching the hybrid wings was equal to that of approaching the wings of the conspecific female (G1 = 0.00, P = 1.00), whereas H. pachinus males preferred conspecific wings over both H. cydno and hybrid wings (G1 = 34.14, P < 0.0001, for both comparisons). In each experiment, approach probabilities were estimated relative to the probability of approaching the conspecific female (gray point), which was set to 1. Support limits are shown around each estimated probability.

Fig. 2.

Fig. 2.

Segregation of male mate preference in hybrids between H. cydno and H. pachinus. The preference index (x axis) is the proportion of courtship and attempted mating events that were directed toward H. cydno females; a preference index of 1 indicates complete preference for H. cydno (white species), whereas an index of 0 indicates complete preference for H. pachinus (yellow species). (A) Parental populations, H. pachinus (gray bars) and H. cydno (black bars). (B) F1 hybrid males: H. pachinus female × H. cydno male. (C) F1 hybrid males from the reciprocal cross: H. cydno female × H. pachinus male. (D) F2 males produced by interbreeding progeny from the first F1 brood, grouped by yellow forewing (gray bars) and white forewing (black bars). (E) males produced by backcrossing a female from the first F1 brood to a pure H. cydno male.

Fig. 3.

Fig. 3.

QTL mapping of male mate preference. Logarithm of odds (LOD) profiles, estimated with both interval mapping (dashed red) and composite interval mapping (dashed blue), are shown alongside genetic linkage maps of the chromosome containing the forewing color locus and the Z chromosome. The 0.05 significance thresholds for interval mapping (solid red) and composite interval mapping (solid blue) are shown. On the chromosome maps, loci are labeled with position in cM (Left) and locus name (Right). Names of AFLP loci begin with a 1 or 2 indicating the phase in the H. cydno male parent.

Fig. 4.

Fig. 4.

Probability of white and yellow H. cydno alithea males courting white and yellow H. cydno alithea females. Although white males (homozygous or heterozygous for the white allele) courted the two female types equally (G1 = 0.00, P = 1.00), yellow males were twice as likely to court yellow females (G1 = 9.33, P = 0.0023). For each male type, probability of between-morph courtship was estimated relative to the probability of within-morph courtship (gray point), which was set to 1. Support limits are shown around each estimated probability.

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References

    1. Orr H. A., Presgraves D. C. BioEssays. 2000;22:1085–1094. - PubMed
    1. Coyne J. A., Orr H. A. Evolution. 1989;43:362–381. - PubMed
    1. Coyne J. A., Orr H. A. Evolution. 1997;51:295–303. - PubMed
    1. McMillan W. O., Jiggins C. D., Mallet J. Proc. Natl. Acad. Sci. USA. 1997;94:8628–8633. - PMC - PubMed
    1. Feder J. L., Opp S. B., Wlazlo B., Reynolds K., Go W., Spisak S. Proc. Natl. Acad. Sci. USA. 1994;91:7990–7994. - PMC - PubMed

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