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Comparative Study
. 2008 Mar 7;275(1634):493-500.
doi: 10.1098/rspb.2007.1378.

The population genetics of mimetic diversity in Heliconius butterflies

Affiliations
Comparative Study

The population genetics of mimetic diversity in Heliconius butterflies

Marcus R Kronforst et al. Proc Biol Sci. .

Abstract

Theory predicts strong stabilizing selection on warning patterns within species and convergent evolution among species in Müllerian mimicry systems yet Heliconius butterflies exhibit extreme wing pattern diversity. One potential explanation for the evolution of this diversity is that genetic drift occasionally allows novel warning patterns to reach the frequency threshold at which they gain protection. This idea is controversial, however, because Heliconius butterflies are unlikely to experience pronounced population subdivision and local genetic drift. To examine the fine-scale population genetic structure of Heliconius butterflies we genotyped 316 individuals from eight Costa Rican Heliconius species with 1428 AFLP markers. Six species exhibited evidence of population subdivision and/or isolation by distance indicating genetic differentiation among populations. Across species, variation in the extent of local genetic drift correlated with the roles different species have played in generating pattern diversity: species that originally generated the diversity of warning patterns exhibited striking population subdivision while species that later radiated onto these patterns had intermediate levels of genetic diversity and less genetic differentiation among populations. These data reveal that Heliconius butterflies possess the coarse population genetic structure necessary for local populations to experience pronounced genetic drift which, in turn, could explain the origin of mimetic diversity.

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Figures

Figure 1
Figure 1
Variation in gene diversity and number of polymorphic AFLP loci among eight Heliconius butterfly species from Costa Rica. To account for sample size differences on our estimates of genetic diversity, we resampled species datasets 1000 times in groups of eight individuals from which we estimated means and 95% CIs (error bars).
Figure 2
Figure 2
Examining the genetic structure of Heliconius populations. For each species ((a) H. erato: FST=0.125, p=0.000, pairwise FST=0.029–0.216; (b) H. sapho; (c) H. hewitsoni: FST=0.038, p=0.000, pairwise FST=0.023–0.047; (d) H. sara; (e) H. melpomene: FST=0.095, p=0.000, pairwise FST=0.037–0.136; (f) H. cydno: FST=0.009, p=0.012, pairwise FST=0.002–0.018; (g) H. pachinus: FST=0.007, p=0.129, pairwise FST=−0.004–0.016; (h) H. hecale: FST=0.008, p=0.134, pairwise FST=−0.006–0.026) we performed MDS based on pairwise genetic distances. Individuals were then plotted using the two dimensions that encompassed the most inter-individual variation. Fixation indexes (FST) were estimated for each species as a whole and pairwise between all populations using an AMOVA framework. The p-values for FST estimates were estimated by shuffling genotypes among populations 1000 times. Only eight individuals were analysed for (b) H. sapho and (d) H. sara so it was not possible to test for genetic differentiation among populations of these two species. Of the remaining six species, four exhibited significant genetic differentiation among populations; (a) H. erato, (c) H. hewitsoni, (e) H. melpomene, and (f) H. cydno (Location legend. Pacific drainage (triangles): dark blue, Sirena station; light blue, Dominical; red, PN Manuel Antonio; yellow, PN Carara; pink, Santiago; green, Colon. Caribbean drainage (squares): black, PN Tapanti; white, Orosi; dark orange, Cachi; light green, Cariblanco; yellow, OTS La Selva; light blue, Horquetas; maroon, Guapiles; dark blue, Guacimo; grey, Barbilla; pink, Bananito; light orange, PN Hitoy Cerrere; dark green, Vesta; violet, Cahuita).
Figure 3
Figure 3
Examining IBD in Heliconius butterflies. For each species ((a) H. erato: Mantel r=0.274, p=0.000; (b) H. sapho: Mantel r=0.301, p=0.042; (c) H. hewitsoni: Mantel r=0.056, p=0.054; (d) H. sara: Mantel r=0.553, p=0.004; (e) H. melpomene: Mantel r=0.406, p=0.000; (f) H. cydno: Mantel r=0.011, p=0.369; (g) H. pachinus: Mantel r=−0.019, p=0.315; (h) H. hecale: Mantel r=0.008, p=0.407) we plotted pairwise geographical and pairwise genetic distance among all individuals and tested the association between these two variables using a Mantel test. Four species exhibited significant IBD; (a) H. erato, (b) H. sapho, (d) H. sara and (e) H. melpomene.

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