Evolution of diversity in warning color and mimicry: Polymorphisms, shifting balance, and speciation

Mimicry and warning color are highly paradoxical adaptations. Color patterns in both Mullerian and Batesian mimicry are often determined by relatively few pattern-regulating loci with major effects. Many of these loci are "supergenes," consisting of multiple, tightly linked epistatic elements. On the one hand, strong purifying selection on these genes must explain accurate resemblance (a reduction of morphological diversity between species), as well as monomorphic color patterns within species. On the other hand, mimicry has diversified at every taxonomic level; warning color has evolved from cryptic patterns, and there are mimetic polymorphisms within species, multiple color patterns in different geographic races of the same species, mimetic differences between sister species, and multiple mimicry rings within local communities. These contrasting patterns can be explained, in part, by the shape of a "number-dependent" selection function first modeled by Fritz Muller in 1879: Purifying selection against any warning-colored morph is very strong when that morph is rare, but becomes weak in a broad basin of intermediate frequencies, allowing opportunities for polymorphisms and genetic drift. This Mullerian explanation, however, makes unstated assumptions about predator learning and forgetting which have recently been challenged. Today's "receiver psychology" models predict that classical Mullerian mimicry could be much rarer than believed previously, and that "quasi-Batesian mimicry," a new type of mimicry intermediate between Mullerian and Batesian, could be common. However, the new receiver psychology theory is untested, and indeed it seems to us unlikely; alternative assumptions could easily lead to a more traditional Mullerian/Batesian mimicry divide.