What initiates speciation in passion-vine butterflies?

Abstract

Studies of the continuum between geographic races and species provide the clearest insights into the causes of speciation. Here we report on mate choice and hybrid viability experiments in a pair of warningly colored butterflies, Heliconius erato and Heliconius himera, that maintain their genetic integrity in the face of hybridization. Hybrid sterility and inviability have been unimportant in the early stages of speciation of these two Heliconius. We find no evidence of reduced fecundity, egg hatch, or larval survival nor increases in developmental time in three generations of hybrid crosses. Instead, speciation in this pair appears to have been catalyzed by the association of strong mating preferences with divergence in warning coloration and ecology. In mate choice experiments, matings between the two species are a tenth as likely as matings within species. F1 hybrids of both sexes mate frequently with both pure forms. However, male F1 progeny from crosses between H. himera mothers and H. erato fathers have somewhat reduced mating success. The strong barrier to gene flow provided by divergence in mate preference is probably enhanced by frequency-dependent predation against hybrids similar to the type known to occur across interracial hybrid zones of H. erato. In addition, the transition between this pair falls at the boundary between wet and dry forest, and rare hybrids may also be selected against because they are poorly adapted to either biotope. These results add to a growing body of evidence that challenge the importance of genomic incompatibilities in the earliest stages of speciation.

Figure 1

Proportion of egg-hatch (A) and larval survival (B) for hybrid and pure matings. Cross type is given within each bar. Hybrid individuals are designated by a combination of letters, where the female parent of each cross is listed first. The number of eggs laid per female is listed above the proportion hatching bar in A. Individuals raised together are designated by roman numerals.

Figure 2

Excess larval developmental time (in days) as a function of the proportion of erato genes. Each point represents the mean egg-to-adult developmental time of five females and five males from a single cross. Differences in mean developmental time were calculated relative to the developmental time of H × H crosses reared at the same time. The regression line was calculated forcing the y-intercept through the origin.