Genetics and the Evolution of Muellerian Mimicry in Heliconius Butterflies

• Published in: Philosophical transactions of the Royal Society of London. Series B, Biological sciences Biological sciences, 1985-02, Vol.308 (1137), p.433-610
• Main Authors: Sheppard, Philip Macdonald, Turner, John Richard George, Brown, K. S., Benson, W. W., Singer, M. C.
• Format: Article
• Language: English
• Subjects: Alleles; Animals; Biological and medical sciences; Butterflies; Classical genetics, quantitative genetics, hybrids; Colors; Female animals; Fundamental and applied biological sciences. Psychology; Genetic loci; Genetics of eukaryotes. Biological and molecular evolution; Genotypes; Heterozygotes; Insecta; Invertebrata; Invertebrates; Mimicry; Morphology. Histology. Cytology; Phenotypes; Rectangles
• ISSN: 0962-8436; 0080-4622; 1471-2970; 2054-0280
• DOI: 10.1098/rstb.1985.0066

A protected and warningly coloured butterfly can become a muellerian mimic of another species in two steps: (i) a major mutation converts the pattern of the less protected species to an approximate resemblance of the better protected (one-way convergence); (ii) after the spread of this mutant, the species, which now resemble each other sufficiently to be mistaken one for the other by predators, undergo mutual convergence, using whatever major or minor genetic variation is available to them. Although sometimes one or other step might occur alone, in general early theorists were mistaken in attributing muellerian mimicry to only one of these processes. By hybridizing races of Heliconius melpomene and races of H. erato (a pair of parallel mimetic species from the neotropics, held in mutual muellerian mimicry across wide inter-racial variations in colour pattern) we have shown that, as expected from the two-step theory, the races differ at a number (two to nine) of genetic loci, usually unlinked or loosely linked, including at least one mutant of major effect in each case. We describe the genetic constitution of eight races of H. melpomene (for 11 loci affecting colour pattern) and of eight races of H. erato (for up to 15 loci), and have started to identify the linkage groups. Map distances for those loci that are linked range from around 0.3 to zero in males, with no recombination in females. Muellerian mimicry is expected to produce total uniformity of pattern: universal exceptions to this are the existence of distinct mimicry rings flying within the same habitat, geographical variation within nearly all the more widespread species (divergence in the face of normalizing selection), and, in a few species, polymorphism or sexual dimorphism. Sympatric mimicry rings will, according to the two-step model of evolution, persist indefinitely if their patterns are so distinct that under no circumstances do predators mistake one for the other. Gradual mutual convergence is then impossible, although members of a weakly protected mimicry ring that can produce a mutation giving sufficient initial resemblance to a better protected ring can still be captured by it. Batesian mimics promote this by lowering the protection of the ring that they belong to, but their models can escape only in this way as normalizing selection prevents their gradual evolution away from the batesian mimic. If the rings are too distinct in pattern even this capture of species becomes impossible as