Polymorphic butterfly reveals the missing link in ecological speciation

Abstract

Ecological speciation occurs when ecologically based, divergent selection causes the evolution of reproductive isolation. There are many empirical examples of this process; however, there exists a poorly characterized stage during which the traits that distinguish species ecologically and reproductively segregate in a single population. By using a combination of genetic mapping, mate-choice experiments, field observations, and population genetics, we studied a butterfly population with a mimetic wing color polymorphism and found that the butterflies exhibited partial, color-based, assortative mate preference. These traits represent the divergent, ecologically based signal and preference components of sexual isolation that usually distinguish incipient and sibling species. The association between behavior and recognition trait in a single population may enhance the probability of speciation and provides an example of the missing link between an interbreeding population and isolated species.

Fig. 1

Parallel divergence and Müllerian mimicry in Heliconius butterflies. (A) In Costa Rica, co-mimetic species pairs are restricted to opposite drainages. In western Ecuador H. eleuchia, H. sapho, and polymorphic H. cydno alithea (red arrows point to alternate Ac phenotypes) co-occur. (B) Spectral reflectance measurements of light (white or yellow) and dark (black or irridescent blue) wing patches show concordance between co-mimics and parallel divergence in Costa Rica and Ecuador (averaged across 10 nm intervals, error bars are standard deviation).

Fig. 2

Distribution of H. cydno alithea mate preference indices for yellow (yellow bars, maximum likelihood estimate = 0.36 [0.423 − 0.299]) and white (white bars, maximum likelihood estimate = 0.54 [0.604 − 0.475]) males. The preference index (x-axis) is the proportion of courtship and attempted mating events that were directed toward white females; a preference index of 1 indicates complete preference for white whereas 0 indicates complete preference for yellow. All males with two or more courtship events are shown.

Fig. 3

Population genetics of H. cydno alithea, H. cydno galanthus, and H. pachinus. (A) Bootstrap neighbor-joining tree of polymorphic AFLP markers (bootstrap values > 50% are shown). (B) STRUCTURE clustering (no-admixture and admixture) on AFLP data correctly identified the three populations at K=3 but clustering at K=4 resulted in a reduced likelihood and did not subdivide alithea by color. (C) Bootstrap neighbor-joining tree of mtDNA sequences (bootstrap values > 50% are shown). In each panel, individuals are designated by colored symbols (triangles for the Costa Rican taxa H. cydno galanthus and H. pachinus, circles for H. cydno alithea; white/yellow indicates wing color).