From The New Brunswick Naturalist

Monarchs, Viceroys and Queens:
Who's the real pretender to the throne?

The mysteries of mimicry had a special attraction for me. Its phenomena showed an artistic perfection usually associated with man-wrought things. ..."Natural selection," in the Darwinian sense, could not explain the miraculous coincidence of imitative asp ect and imitative behavior ... carried to a point of mimetic subtlety, exuberance, and luxury far in excess of a predator's power of appreciation. -- Vladimir Nabokov

Henry W. Bates, the English naturalist and explorer spent a decade in the middle of the last century wandering the jungles of the Amazon avidly pursuing what biologist Richard Lewontin has called "the genteel upper-middle-class fascination with snails and butterflies." Nevertheless the fruits of his explorations, published in the venerable Transactions of the Linnaean Society in London in 1862 [Bates, H.W. (1862) Contributions to an insect fauna of the Amazon valley.], gave rise to a whole new sub-discipline of zoology -- mimicry.

Bates captured over a hundred species of Heliconian, Ithomid and Pierid butterflies many of which, even though they came from different lineages, showed a striking resemblance to one another. The theory, as elaborated by more recent findings, runs somewhat along these lines. Certain butterflies (models) have evolved a chemical defense system (consisting typically of cardenolides or pyrrolizidine alkaloids) against predation. They have also evolved a distinctive (aposematic) colouration to warn off possible predators. Experiments confirm that birds, after they have once attacked such a butterfly, will be much less likely to try eating it again -- a warning flag if you like.

Now, in some instances other species (mimics or 'information parasites' in the new lingo of communications) mimic this aposematic colouration. In other words, by resembling the unpalatable species they hope to avoid predation by those animals who have lea rned the warning signal. This has some inherent disadvantages for, as R.I. Van-Wright writes (no pun intended): "Bluff, with no stick to wield when challenged, is a risky sort of defense." [Vane-Wright, R.I. (1991) A case of self deception. Nature 350: 460-461.] If there are more mimics than models then potential predators get conflicting information, or even (to masticate metaphors dreadfully) take the 'warning flag' for a 'dinner bell.'

Further confirmation of this theory came from the fact that many model butterflies feed on noxious plants -- Milkweeds, Nightshades, Birthworts or Passionflowers. It was assumed that the larvae of such butterflies, having evolved immunities to the toxic chemicals, were able to somehow sequester, or stock-pile, these chemicals in their bodies and retain them through to adulthood. The larvae of mimic species, conversely, were usually found to feed on benign, non-poisonous plants. Presto -- a most convincing theory of mimicry!

Ever since the pioneering studies of Jane Van Zandt Brower in the mid 1950's [Brower, J. Vz. (1958) Experimental studies of mimicry in some North American butterflies. Evolution 35:32-47.] Danaus plexippus, the Monarch (model), and Limenitis archippus, the Viceroy (mimic), have been archtypical, textbook examples of this type of 'Batesian' mimicry. Both species are familiar New Brunswick butterflies. Anyone who has ventured along the Bay of Fundy coast in the fall will surely have seen Monarchs on their fall migration to the mountains of Michoacan in south-western Mexico. Viceroy's are commonly seen throughout the province during the summer.

Now, however, standing conventional wisdom on its head, come new findings which suggest that this whole scenario, and all that we once believed about mimicry 'ain't necessarily so.' In a definitively and provocatively titled paper -- The viceroy butterfly is not a batesian mimic -- David Ritland and Lincoln Brower [Nature 350:497-498 (1991)] studied the palatability of Monarchs, Viceroys and Queens (Danaus gilippus, a close southern relative of the Monarch and another species which, it was assumed, the Viceroy mimicked). In their work they presented Red-winged Blackbirds with abdomens of all three species (as well as of non-toxic control butterflies). They gave the birds only abdomens to prevent them from seeing or learning the aposematic patterns. Thus they could respond only to the taste of the butterfly. To their surprise they found that the Viceroy and Monarch were both equally unpalatable to the birds (only about 40% eaten, versus 98% of the controls) and both were more distasteful to birds t han Queens (approximately 70% eaten). This was borne out by several other indicies which they used to measure the birds' response (how long and the way in which the birds handled the butterfly, etc.). In one fell swoop the basis for supporting Batesian mimicry between these species disappeared.

Not all is lost, however. A few years after Bates a German zoologist, Fritz Muller also went collecting butterflies on the Amazon. In his work published in 1878 [Muller, F (1878) Ituna and Thyridia; a remarkable case of mimicry in butterflies. Proc. Entomol. Soc. London 1879: 20-29.] he reasoned as follows: Each aposematic pattern has a learning curve for predators. 'Once bitten, twice shy,' presupposes at least one bite. If all the toxic species have their own distinctive warning patterns predators will have to learn every one -- with a corresponding number of fatalities and mutilations to the prey. Now, if several noxious species select a single pattern, arriving there via convergent evolution, then all benefit! Predators have only to learn one pattern and fewer butterflies get eaten. This reciprocal kind of mimicry is called Mullerian and it seems that the relation between Monarchs and Viceroys may be an example of it.

At this stage you might well be tempted to respond; "Well isn't this just much ado about nothing? Mullerian; Batesian -- what's the big deal?" Ah well, I thought you might ask! In fact the evolutionary and ecological dynamics of these two types of mimicry are very different in terms of both predators and prey. Mullerian mimics, for example, should be converging over time on a common aposematic pattern whereas Batesian models should experience a pressure to diverge from their mimics. Moreover, other research is undermining the underpinings of mimicry.

Work done by K.S. Brown Jr.[Brown, K.S. Jr. (1985). Revista Brasileira de biologia 44: 435-460.] has shown that many noxious butterflies, such as the Ithiomids, "derive few or no defense compounds from their larval hostplants." In fact as proposed by Ackery [Ackery, P.R. (1988) Hostplants and classification: a review of Nymphalid butterflies. Biol . J. Linn. Soc. 33:95-203.], the emerging understanding of this relationship inverts it a hundred-eighty degrees. It is now thought that butterflies often evolve their own chemical defenses and only afterwards shift their feeding preferences to plants protected by similar means. Depending on the species they may or may not sequester these plant chemicals, as the Monarch appears to.

Some researchers doubt that Batesian mimicry exists, speculating that all mimicry may lie somewhere along a Mullerian spectrum. Others, as Vane-Wright suggests, argue that, "Because, in addition to sharing the same warning signal, all members of a Mullerian group are well-protected, it has been argued that no deception is involved and, therefore, they are not really mimics at all." In other words, mimicry as such, may not even exist! Well, whatever one calls it, this phenomenon in its extraordinary elaboration, casts some fascinating light on the twin concepts of parasitism and mutualism -- two pivotal ecological and evolutionary notions. Perhaps I'll leave the final words to V. Sirin, that great lepidopterist and literary thaumaturge who himself copied life as assiduously as it mimicked him:

I discovered in nature the nonutilitarian delights that I sought in art. Both were a form of magic, both were a game of intricate enchantment and deception.-- V. Sirin; Speak, Mnemosyne