Genetics and the evolution of muellerian mimicry in heliconius butterflies

Abstract

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 8 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. The capture of a species by another ring can produce geopraghic variation both in the species capture and in the capturing ring, whose pattern is somewhat altered by mutual convergence with the capture species in the second step of the evolution of muellerian resemblance. We suggest that the striking differences between the races within H. melpomene, H. erato and other Heliconius species resulted from these effects of inter-ring capture. Distributional evidence suggests that this chiefly occurred in refuges formed by the contraction of the neotropical rain forests during the cool dry periods in the Quaternary; these, by differential extinction of elements of the flora and fauna of different refuges, could have produced long-term changes in the relative abundances of the mimicry rings, and hence (as the protection given to a ring is proportional to its abundance) somewhat different capture events in each refuge. Seveal existing species confirm that this mode of evolution occurs, by retaining a distinctive pattern in the absence of any other remotely similar species, but becoming mimetic in areas where they encounter a pattern somewhat like their own. The isolated populations of Heliconius hermathena show this particularly clearly; the effect can be discerned also in H. melpomene and H. erato. Although polymorphism in muellerian mimics is largely unexplained in 2 species of Heliconius it may result from the existence of 2 or more similar but slightly differing ''sub-rings'' among their comimics in the family Ithomiidae, which show both spatial and temporal heterogeneity in their local distribution, which apparently is able to maintain a polymorphic equilibrium in the more uniformly distributed Heliconius. We have tentatively reconstructed the ancestral patterns of H. melpomene and H. erato by 2 independent methods: first, as dominant genes are much more likely to be incorporated than recessive ones during changes of pattern, the phenotype produced by the recessive alleles at all the known loci will be close to the ancestral pattern; secondly species that are becoming mimics evolve more than those that are not, so that non-mimetic relative os H. melpomene and H. erato will have a pattern close to ancestral. Both methods suggest, for both species, that the ancestor was a black butterfly with yellow (or possibly white) bars, and it may be that H. melpomene and H. erato have been comimics for a very long time. Previous climatic cycles in the Quaternary have apparently caused full speciation within 2 mutually mimetic evolving lineages, producing pairs of parallel mimetic species within the genus, of which H. melpomene and H. erato constitute 1 pair.