The genetics of warning colour in Peruvian hybrid zones of Heliconius erato and H. melpomene

Abstract Heliconius warning colour is a good example of a genetic system shaped by strong selection. The genetics of colour patterns in interracial hybrid zones within both H. erato and H. melpomene was investigated. Within each species, the loci controlling these pattern differences are mostly homologous to those known from other races, but have somewhat different phenotypic effects. The precise genetic control varies geographically, even for nearly identical colour patterns. Independent evolution of the same pattern is unlikely; instead evolution of the genetic system is hypothesized to have occurred while stabilizing selection preserved the pattern itself. Single genes often control more than one pattern element. This apparent pleiotropy is in part due to tightly linked loci within 'supergenes': rare recombinants (possibly mutants) in genes controlling 'dennis' and 'ray' patterns were found in both species. However, supergenes, which are likely in polymorphic Batesian mimicry, are not expected to accumulate in Müllerian mimics because polymorphisms, which would favour their evolution, are too transient. The existence of supergenes in Heliconius suggests that major switch genes are gradually built up within a locus rather than evolving wholly by macromutation or by selection for tighter linkage of mimetic genes. This gradual evolution at a single locus might be necessitated by a lack of other sites that can control warning patterns. These genes are strongly epistatic, and heterozygotes and hybrid homozygotes have 'fuzzier' (less sharply defined) and more variable patterns than the pure races. The genetic system controlling colour pattern in Heliconius is clearly canalized and coadapted to produce efficient warning signals.