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?Annu. Rev. Ecol. Syst. 200X . 30:201–33
Copyright c
°1999 by Annual Reviews. All rights reserved
EVOLUTION OF DIVERSITY IN WARNING COLOR
AND MIMICRY:Polymorphisms, Shifting
Balance, and Speciation
James Mallet1and Mathieu Joron2
1Galton Laboratory, 4 Stephenson Way, London NW1 2HE, England;
e-mail: j.mallet@ucl.ac.uk or http://abacus.gene.ucl.ac.uk/jim/; and 2G´
en´
etique et
Environnement, CC065 ISEM, Universit´
e de Montpellier 2, Place Bataillon, F-34095
Montpellier, cedex 5, France; e-mail: joron@isem.univ-montp2.fr
Key Words aposematism, Batesian mimicry, M¨ullerian mimicry, defensive
coloration, predator behavior
■Abstract Mimicry and warning color are highly paradoxical adaptations. Color
patterns in both M¨ullerian 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 pu-
rifying 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 polymor-
phisms 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 M¨uller
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 M¨ullerian expla-
nation, however, makes unstated assumptions about predator learning and forgetting
which have recently been challenged. Today’s “receiver psychology” models predict
that classical M¨ullerian mimicry could be much rarer than believed previously, and that
“quasi-Batesian mimicry,” a new type of mimicry intermediate between M¨ullerian 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 M¨ullerian/Batesian mimicry divide.
0066-4162/99/1120-0201$08.00 201
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202 MALLET ■JORON
INTRODUCTION
Since their discovery, antipredator mimicry and warning colors have been used
as simple and visually appealing examples of natural selection in action. This
simplicity is beguiling, and controversy has often raged behind the textbook ex-
amples. Warning color and mimicry have been discussed from three different
points of view: a traditional insect natural history angle, which makes simplistic
assumptions about both predator behavior and prey evolution (6, 103, 122, 175);
an evolutionary dynamics angle, which virtually ignores predator behavior and
individual prey/predator interactions (37, 47,54, 91,162); and a predator behavior
(or “receiver psychology”) angle (59–61, 71, 72, 84a, 115, 147a–150), which tends
to be simplistic about evolutionary dynamics. Assumptions are necessary to ana-
lyze any mathematical problem, but the sensitivity of mimicry to these different
simplifications remains untested.
We believe it will be necessary to combine these disparate views (for example,
111, 133, 181) in order to resolve controversy and explain paradoxical empirical
observations about the evolution of mimicry. Mimicry should progressively reduce
numbers of color patterns, but the actual situation is in stark contrast: There is a
diversity of “mimicry rings” (a mimicry ring is a group of species with a common
mimetic pattern) within any single locality; closely related species and even adja-
cent geographic races often differ in mimetic or warning color pattern; and there
are locally stable polymorphisms. The current controversies and problems are not
simply niggles with the theory of mimicry, designed to renew flagging interest in
a largely solved area of evolutionary enquiry. Recent challenges and critiques cast
justifiable doubt on previously unstated assumptions. A further reason for reexam-
ining the evolution of mimicry is that its frequency-dependent selective landscapes
are rugged, as in mate choice and hybrid inviability (53), so that mimicry provides
a model system for the shifting balance theory (41, 178–180); mimicry may also
act as a barrier to isolate species (96). While a number of interesting peculiarities of
mimicry arguably have little general importance (57), mimicry excels in providing
an intuitively understandable example of multiple stable equilibria and transitions
between them (41, 87, 89,97, 98, 161,167). Mimicry and warning color are highly
variable both geographically within species and also between sister species. In
this, they are similar to other visual traits involved in signaling and speciation,
such as sexually selected plumage morphology and color in birds (2). Sexual and
mimetic coloration may therefore share some explanations.
This article covers only the evolution of diversity in mimicry systems, and we
skate quickly over many issues reviewed elsewhere (19–21, 32, 40, 45, 86, 123,
125, 129, 134, 170, 176; see also a list of over 600 references in Reference 90).
Our discussion mainly concerns antipredator visual mimicry, though it may apply
to other kinds of mimicry and aposematism, for example, warning smells (62, 130)
and mimicry of behavioral pattern (18, 152–154). In addition, mostof our examples
are shamelessly taken from among the insect mimics and their models, usually
butterflies, that we know best; careful studies on the genetics or ecology of other
systems have rarely been done.
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MIMICRY AND DIVERSIFICATION 203
MIMICRY AND WARNING COLOR: THE BASICS
Bates (6) noticed two curious features among a large complex of butterflies of
the Amazon. First, color patterns of unrelated species were often closely similar
locally; second, these “mimetic” patterns changed radically every few hundred
miles, “as if by the touch of an enchanter’s wand” (8). Bates argued that very
abundant slow-flying Ithomiinae (related to monarch butterflies) were distasteful
to predators and that palatable species, particularly dismorphiine pierids (related
to cabbage whites), “mimicked” them; that is, natural selection had caused the
pattern of the “mimic” to converge on that of the “model” species. This form of
mimicry became known as Batesian (122). The term “mimicry” had already been
used somewhat vaguely by pre-Darwinian natural philosophers for a variety of
analogical resemblances (13), but Bates’s discovery was undoubtedly a triumph
of evolutionary thinking.
Bates also noticed that rare unpalatable species such as Heliconius (Heliconi-
inae) and Napeogenes (Ithomiinae) often mimicked the same common ithomiine
models (such as Melinaea, Oleria, and Ithomia) copied by dismorphiines. He
assumed that this “mimetic resemblance was intended” (6, p. 554) because, re-
gardless of its palatability, a rare species should benefit from similarity to a model.
However, where both mimic and model were common, as in the similarity of
unpalatable Lycorea (Danainae) to ithomiines, he felt this was “a curious result
of [adaptation to] local [environmental] conditions” (6, p. 517); in other words,
convergent evolution unrelated to predation. It was left to M¨uller (103) to explain
clearly the benefits of mimicry in pairs of unpalatable species. If a constant number
of unpalatable individuals per unit time must be sacrificed to teach local predators
a given color pattern, the fraction dying in each species will be reduced if they
share a color pattern, leading to an advantage to mimicry. Thus, mimicry between
unpalatable species became known as M¨ullerian.
Many mimetic species are also warning-colored, but some are not: for example,
thelarva ofa notodontid moth(6) and the pupa ofDynastor darius (Brassolidae) (1)
both mimic highly poisonous but cryptic pit vipers (Viperidae). The former mimics
even the keeled scales of its model; the latter has eyes that mimic the snake’s own
eyes, even down to the slit-shaped pupils. Many small clearwing ithomiines that
Bates studied in the tropical rainforest understory are also very inconspicuous but
are clearly mimetic. Mimicry does not require a warning-colored model, only that
potential predators develop aversions to the model’s appearance. Warning color,
or “aposematism” (122), was first developed as an evolutionary hypothesis by
Wallace in response to a query from Darwin, four years after Bates’ publication on
mimicry. Darwin’s sexual selection theory (42) explained much bright coloration
in animals but could not explain conspicuous black, yellow, and red sphingid
caterpillars found by Bates in Brazil because the adult moth could not choose
mates on the basis of larval colors. Wallace in 1866 (see 42,175) suggested that
bright colors advertised theunpalatability of the larvae, in the same way thatyellow
and black banding advertised the defensive sting of a hornet (Vespidae). Warning
color in effect must increase the efficiency with which predators learn to avoid
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204 MALLET ■JORON
unpalatable prey (see also 59,61 for excellent discussion of possible advantages
of warning color).
NUMBER-DEPENDENT SELECTION ON MIMICRY
AND WARNING COLOR
To the natural history viewpoint of early Darwinians (6,8, 103,122,175), it was
apparentlynot clear that explaining aposematism andmimicry as adaptations could
be problematic: They had not fully realized that short-term individual benefits and
long-term group benefits may conflict. In fact, the selective landscape of mimetic
evolution has multiple stability peaks that should often prevent the spread of ulti-
mately beneficial unpalatability, warning color, and some mimicry. To understand
why this is so, we must examine the evolutionary dynamics of mimicry.
M¨uller (103) was the first to formulate the benefits of mimicry explicitly, using
mathematical intuition from a natural history perspective (reprinted in 78). He
assumed that, while learning to avoid the color pattern of unpalatable species, a
predator complex killed a fixed number of individuals per unit time (nk). M¨ullerian
mimicry is favored, therefore, because the per capita mortality rate decreases when
another unpalatable species shares the same pattern. If this traditional naturalist’s
“number-dependent” (162) view of mimicry is correct, it leads to two interesting
predictions, only the first of which M¨uller himself apparently appreciated. First,
although M¨ullerian mimicry of this kind should always be mutualistic, a rare
species ultimately gains far more from mimicry than a common one, in proportion
to the square of the ratio of abundances (103). Second, a novel mimetic variant in
the rarer species resembling the commoner is always favored because the common
species generates greater numerical protection, while a mimetic variant of the
commoner species is always disfavored because it loses the strong protection of its
own kind and gains only weak protection from the rarer pattern (161). Both these
effects will tend to cause rarer unpalatable species to mimic commoner models,
rather than the other way around, in spite of the fact that M¨ullerian mimicry is a
mutualism (albeit with unequal benefits) once attained.
M¨uller’s number-dependent selection applies similarly to morphswithin a sin-
gle species (Figure 1). A warning-colored variant within a cryptic but unpalatable
prey will suffer a twofold disadvantage: First, it is more conspicuous to predators;
second,it doesnot gainfrom warningcolor becausepredators, not havinglearnedto
avoid the pattern, may attack it at higher rate than the cryptic morph. This creates a
barrier to initial spread (67), even though, once evolved, warning color is beneficial
because by definition it reduces the number of prey eaten during predator learning.
In exactly the same way, a novel warning pattern is disfavored within an already
warning-colored species, essentially because of intraspecific mimicry (27,89, 97;
also Figure 1). This selection against rarity makes it easy to understand why
warning-colored races are normally fixed and sharply separated by narrow overlap
zones from other races (27, 50, 87, 93), but in turn makes it hard to understand
how geographic races diversified in the first place (6,8, 87,89, 98,137, 167). Sim-
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MIMICRY AND DIVERSIFICATION 205
ilarly, if energy is required to synthesize or sequester distasteful compounds,
unpalatability itself may be disfavored (49,63, 67, 160) because unpalatable in-
dividuals may sacrifice their lives in teaching predators to avoid other members of
their species. Hypotheses to overcome the difficulties with this new, more sophis-
ticated evolutionary dynamic view of aposematism are detailed below.
POPULATION STRUCTURE AND THE EVOLUTION
OF WARNING COLOR AND UNPALATABILITY
The Evolution of Unpalatability
Unpalatability itself is hard to define (20, 51; see also below under M¨
ullerian
Mimicry), but here we use the term loosely to mean any trait that acts on preda-
tors as a punishment, and that causes learning leading to a reduction in attacks.
The unpalatable individual may incur costs in synthesis or processing of distasteful
chemistryand isoften likely tosuffer damage duringpredator sampling, whileother
members of the population mostly benefit from predator learning. The frequent
aposematism of gregarious larvae, often siblings from the same brood, suggests
that benefits are shared among kin, and that kin selection could have been responsi-
ble for the evolution of unpalatability (49, 63, 67,160). These authors assumed that
altruistic unpalatability was unlikely to evolve unless kin-groups already existed,
so explaining the association between gregarious larvae and unpalatability. How-
ever, unpalatability may not be very costly. First, although it may be expensive
to process distasteful secondary compounds, in some cases the same biochem-
ical machinery is required to exploit available food; for instance, Zygaena and
Heliconius, which both feed on cyanogenic host plants, can also synthesize their
own cyanogens (70,76, 104), presumably using enzyme systems similar to those
required in detoxification. Second, because most toxic compounds also taste nasty
(arguably, the sense of taste has evolved to protect eaters from toxic chemistry),
and because predators taste-test their prey before devouring them, and, finally,
because unpalatable insects are often tough and resilient, an unpalatable insect
should often gain an individual advantage by sequestering distasteful chemicals.
A good example of predator behavior showing this is possible is seen in birds
feeding on monarch (Danaus plexippus) aggregations at their overwintering sites
in Mexico: Birds repeatedly taste-reject butterflies more or less unharmed, until
they find a palatable individual, which is then killed and eaten (29).
Another problem with empirical evidence for kin selection is that gregarious-
ness, which reduces per capita detectability of the prey (14, 64, 157,160), is ex-
pected to evolve when there is any tendency toward predator satiation; and one of
thebest waysof satiating predators is to be distasteful.Thus theassociation between
gregarious larvae and unpalatability can be explained easily because gregarious-
ness will evolve more readily after unpalatability, rather than before it as required
under the kin selection hypothesis. This expected pattern of unpalatability first,
gregariousness thereafter, is now well supported in Lepidoptera by phylogenetic
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206 MALLET ■JORON
analysis (139, 141). In conclusion, the supposed necessity for kin selection in the
evolution of unpalatability is now generally disbelieved (59, 97, 139), although kin
selection could, of course, help.
Evolution of Novel Warning Colors in Cryptic
and Aposematic Defended Prey
Although the realization that aposematic insects may be altruistic came 70 years
ago (49), it was finally some 50 years later that the evolution of warning color
was explicitly disentangled from the evolution of unpalatability (66,67). Under
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MIMICRY AND DIVERSIFICATION 207
M¨uller’s number-dependent theory, intraspecific M¨ullerian mimicry acting on
a novel warning-colored variant A within a population would strongly favor
the commonest wild-type morph a; the number-dependence gives rise to fre-
quency-dependent selection, which is purifying, tending to prevent polymorphism
(Figure 1A). If unpalatable prey often survive attacks, it might be argued that the
problem will be surmounted (47, 73, 74, 177). However, fitness will be reduced
if attacks are even potentially damaging; the “effective number killed” (nk) may
take fractional or probabilistic values, but the frequency-dependent logic applies
in exactly the same way (68,97).
A critical feature of number-dependence is the great nonlinearity of frequency-
dependent selection. Many authors from the evolutionary dynamics tradition have
assumed a simpler linear frequency-dependence (dotted line in Figure 1) (47,54,
87, 91, 121). In fact, the relationship between selection and frequency becomes
more sigmoidal as nk/Ndecreases. When nk¿N, there are strong spikes of se-
lection against Aand awhen each is rare, but much of the frequency range forms
a nearly neutral polymorphic basin (e.g. N=100, Figure 1). Another interesting
feature of this model is that the mean fitness surface is flat: Assuming most preda-
tors learn the pattern and then avoid it, the mean fitness throughout the frequency
spectrum becomes approximately constant at [nk(A)+nk(a)]/N(Figure 1B).
This is an extreme example of how mean fitness cannot be guaranteed to increase
when selection is frequency-dependent (65). [Mimetic and warning color patterns
may, of course, vary continuously, rather than as discrete patterns (82); this may
also contribute to evolution of warning color and mimicry (see under Pattern En-
←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−
Figure1 Number- and frequency-dependence in mimicry and aposematism. M ¨uller’s
number-dependent theory supposes that, while they learn to avoid the pattern of an
unpalatable insect, predators kill a constant number, nk(i)of each morph iper unit
time in a given area. Assuming the local population has constant size (N) and contains
a novel pattern (A) and a wild-type pattern (a), M¨uller’s theory can give the strength
of frequency-dependent selection for or against the pattern Aat different frequencies
(qA) in the population. The fitness of Ais WA=1−(nk(A)/qAN), while that of ais
Wa=1−[nk(a)/(1−qA)N]. The measure of frequency-dependent selection acting
on Arelative to aused here is SA=(WA/Wa)−1; if SAis positive, Ais favored,
if SAis negative, Ais disfavored. The fitnesses are shown in terms of SA(graph A)
and mean fitness (graph B). The dashed and solid lines show frequency-dependent
fitnesses for a low total population size (N=10) and a high total population size
(N=100), respectively, relative to nk(A)and nk(a)(the fractions nk/Nare more
important than absolute values of nkand N). In contrast, linear frequency-dependent
selection has been more normally used to study the population genetics of warning
color and mimicry (37, 47, 54, 91, 93), for example where WA=1−sA(1−qA), and
Wa=1−saqA. This model gives frequency-dependent fitnesses shown in the dotted
curve of the figure. In both number-dependent and frequency-dependent selection,
values of sand nkhave been chosen to give an unstable equilibrium frequency of
q∗
A=0.4, which is the case if Ahas 1.5 ×X greater fitness than a.
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208 MALLET ■JORON
hancement and Peak-Shift and Mimetic Polymorphism and Genetic Architecture,
below).]
In nature, not only do warning colors exist, but also novel warning patterns
are forever being multiplied in already warning-colored species (see also Genetic
Drift and the Shifting Balance) in spite of barriers suspected to impede their initial
evolution. Various ideas have been proposed:
1. Novelty and Recognizability It has been suggested that warning colors are
favored because they induce predator neophobia and because they are easier to rec-
ognize and learn (59, 84a, 140,177). Neophobia has some experimental evidence
(45, 140), whereas increased memorability is part of the definition of warning color
(see above). These factors, coupled with a high survival rate of attacked prey, might
seem to allow warning color to increase from low frequency in spite of increased
conspicuousness (140, 177). Unfortunately, the problem with fear of novelty is that
this survival advantage evaporates after a time, and enhanced learning is useful
only if there are enough individuals available to do the teaching. This behavior
viewpointis rarely coupledwith much thought about evolutionary dynamics. Thus,
an unpalatable and brightly colored sea slug that survives 100% of attacks by fish
(158) seems likely to have some risk, or loss of fitness due to fish biting; any such
loss of fitness will be progressively diluted as the numbers increase, leading again
to frequency-dependent selection against rare the. In fact, M¨ullerian mimicry or
monomorphic warning color would be unnecessary if this selection against rarity
were not present. An increase of conspicuousness will almost always lead to an ini-
tially greater level of attack on the first few individuals with the new pattern, even if
the pattern is ultimately advantageous oncefixed within the population (59, 81, 97).
Essentially, nk(A)/1≤nk(a)/Nfor warning color Ato spread in a population
of size N—the learning advantage of first individual Avariant must outweigh the
population size advantage of the cryptic wild-type a.With reasonably large prey
population sizes, say N>10, for a reasonably unpalatable species, this seems
almost impossible; given that Ais more conspicuous, the possibility seems even
more remote (89, 97). In any case, high rates ofbeak-marks on the wings of brightly
colored unpalatable butterflies attest to a high frequency of potentially lethal at-
tacks (11, 30,31, 91,111). Nonetheless, various possibilities allow warning colors
to cheat against this apparent selective disadvantage. These are reviewed below.
2. Preadaptation This idea is motivated by the fact that many palatable insects,
particularly butterflies, are already brightly colored. Cryptic resting postures and
rapid, jinking flight allow these insects to expose conspicuous patterns in flight that
may be important for intraspecific signaling in mate choice and sexual selection
(42) or in territoriality and male-male interactions (138, 169), as deflection mark-
ings (45, 128, 176), or in Batesian mimicry. If these species become unpalatable,
perhaps as a result of a need to process toxic secondary compounds in food, their
conspicuous patterns, already adapted for signaling, could simply be reused in
predator education.
3. Pattern Enhancement and Peak Shift The representation of a pattern in a
predator’s memory is likely to be a caricature of the actual pattern. Thus, an exag-
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MIMICRY AND DIVERSIFICATION 209
gerated pattern may be avoided by a predator more strongly than the normal pattern
on which the predator originally trained, and exaggerated warning patterns will
evolve to exploit this predator bias. Training an artificial neural network model can
also recreate this kind of perceptual bias for supernormal stimuli (3, 48). Whether
perceptual bias is produced in computer models is strongly assumption-dependent
(79), but there is good evidence for exaggerated responses to supernormal stimuli
in vertebrate perception (156), which seem likely to have been a cause of ex-
aggerated male traits in sexual selection (110,131). Similar perceptual biases in
vertebrates may contribute to the gradual evolution of warning colors (82).
A related idea is “peak shift” whereby, if zones of negative and positive rein-
forcement are located close together along a perceptual dimension, they may each
cause the perceiver to bias their responses further apart (Figure 2). Peak shift is not
dissimilar to the old idea that warning colors function by appearing as different
as possible from the color patterns of edible prey (49, 59–61, 164). Theory shows
that peak shift can produce gradual evolution of warning colors (133,181), and
recent experiments with birds have demonstrated relevant perceptual bias (52, 84).
Figure 2 The theory of behavioral “peak shift.” If the appearances of palatable and
unpalatable species are close toeach other along somestimulus dimension, such as con-
spicuousness, predators may develop a perceptual bias that enhances discrimination,
knownby behaviorial biologistsas peakshift (notto be confused with evolutionarypeak
shift via the shifting balance). The conflicting pressures on their perceptual/learning
system may lead them to avoid patterns brighter than the norm for the unpalatable
species more strongly than they avoid the normal pattern; conspicuous unpalatable
variants would then have an advantage over the normal pattern, allowing gradual evo-
lution of greater and greater conspicuousness of the unpalatable species (arrow) (61).
It is unclear how the palatable species will evolve; it could be selected for mimicry (to
the right), or to greater inconspicuousness (to the left) to avoid detection, even though
the latter may be costly due to increased predator attack rate once detected.
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210 MALLET ■JORON
It seems likely that at least some warning colors evolved by pattern enhance-
ment. For example, the patterns of conspicuous morphine butterflies Taenaris and
Hyantis are clearly related to those of cryptic morphines and satyrines, such as
Morphopsis with deflective eyespot patterns similar to many other edible members
of the satyrid lineages to which they belong. Taenaris and Hyantis have evolved
unpalatability, perhaps as a result of feeding on toxic Cycadaceae, both as larvae on
leaves and as adults on sap and fruits. Compared with the drab Morphopsis, color
and brightness have been enhanced, eyespot size has been increased, and eyespot
number has been reduced. A variety of Batesian mimics from palatable genera
such as Elymnias agondas (Satyrinae) and females of Papilio aegeus (Papilioni-
nae) mimic Taenaris and Hyantis patterns (117, 118), showing that the latter are
unpalatable. Although likely to explain some warning color evolution, it is hard
to imagine that all novel warning patterns evolved by enhancement. The color
patterns of related species, or even races of Heliconius (24, 137, 159), for exam-
ple, seem so radically divergent as to preclude one being an enhancement of the
other. Of course, this is a dubious anthropocentric argument, but the major gene
switches in Heliconius suggest that radical shifts, rather than gradual enhancement
of existing patterns, are responsible for much of the pattern diversity within al-
ready warning-colored lineages. If this is the case for switches between warning
patterns, then the ubiquity of enhancement and predator perceptual bias, even for
the initial switch, seems in doubt.
4. M¨
ullerian Mimicry Another way that a newly unpalatable species might
become warning-colored is via M¨
ullerian mimicry. The constraints on its evolution
discussed on p. 204, apply, but the widespread existence of M¨ullerian mimicry
suggests that the idea should work both in the initial evolution of warning color
andin itsdiversification within already unpalatablelineages. Because many species
typically join in M¨ullerian mimicry rings (9, 10, 22–25, 116), it seems likely that,
in butterflies, most warning color switches are due to M¨ullerian mimicry. Only
the initial divergence of mimicry rings needs to be explained in some other way
(24, 89, 98, 167).
5. Density- and Apparency-dependent Warning Color Our formulation so far
ofnumber-dependent warning color and M¨ullerianmimicry (see Figure 1) assumes
all individuals are seen by predators, but in fact apparency as well as density
per se are important for the ultimate benefits of warning colors. If more prey
are killed while predators learn of a warning pattern than would be detected and
killed for a cryptic population of the same size, it may pay the prey to remain
cryptic. This may explain why many stationary pupae of unpalatable insects, such
as Heliconius, are brown and resemble dead leaves, while their more apparent and
mobile larvae and adults are brightly colored and classically aposematic. Density-
dependent color pattern development in Schistocerca (desert locusts and their
relatives) shows a switch from crypsis at low density to advertisement of food-
induced unpalatability at high density, and predation experiments with Anolis
lizards support this idea (155). If so, pattern enhancement (see point 3 above) of
characteristics used by predators for recognition may provide a way in which this
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MIMICRY AND DIVERSIFICATION 211
kind of context-dependent warning color evolves (133, 155,181). Nonetheless,
density-dependent facultative warning colors are unlikely in most animals, such
as adult butterflies, in which color patterns are largely genetic.
6. Kin Selection, Kin-founding, and “Green-beard” Selection Predators at-
tacking kin groups can kill or damage some individuals, but, after doing so, avoid
others, who are relatives carrying the same pattern. A superior warning pattern may
therefore increase locally under a kind of kin group selection (67). This is some-
what different to classical kin selection because benefits are transferred between
individuals of like phenotype, rather than according to degree of relationship (58):
The effect has therefore been called family selection (66), or kin-founding (97).
Warning color is a concrete and uncheatable green-beard trait (58, 59,166), a hy-
pothetical type of altruism invented by Dawkins (43), whereby altruists carrying a
badge (such as a green beard) recognize other altruists because they also carry the
badge. More recently, the general term synergistic selection (61,81, 82, 99,139)
has been applied to such traits. The synergism can be viewed as a behavioral ex-
planation of the warning color trait, once evolved, but the nature of synergism
does not explain its initial evolution because both the fixed absence of the trait and
the fixed presence of the trait are evolutionarily stable strategies (99). The popula-
tion genetic problem of frequency-dependence shown in Figure 1 still arises, and it
seems clear that kin-founding could aid the initial increase of novel warning colors
(59, 97). Whether kin-founding is important for the initial or subsequent evolution
of novel warning colors seems hard to decide (see also under Genetic Drift and
the Shifting Balance). However, kin-grouping and larval gregariousness in many
unpalatable insects does not seem such good evidence now as formerly for kin-
founding, for reasons already discussed above under The Evolution of Unpalat-
ablity: in most cases, gregariousness seems to have evolved after unpalatability
and aposematism (139, 141).
7. Genetic Drift and the Shifting Balance Although kin-founding can be looked
upon as a purely deterministic model similar to kin-selection (66), it is clear that,
like Sewall Wright’s “shifting balance” model of evolution (178–180), it requires
a small local population size: The phenotypes of a small group of related indi-
viduals must dominate the learning and recognition systems of local predators,
which is only possible if the total local population is low. The evolution of warn-
ing color via kin-founding is in fact a special case of phases I and II of the shifting
balance (89, 97, 98,167). In phase I, genetic drift allows a local population to ex-
plore a new adaptive peak; in phase II, local selection causes the population to
adapt fully to the new adaptive peak. Although not usually treated in kin-founding
models (but see 66), phase III of the shifting balance, i.e. spread of the new adap-
tive peak to other populations, would clearly be an important final phase in the
kin-founding process. This would be equivalent to having local populations with
different warning colorscompeting across narrowbands of polymorphism, as isac-
tually the case in many hybrid zones between geographic races of warning-colored
species today; movement of these clines for warning color would be the equiva-
lent of Phase III (87, 98). In warning color, stable and unstable equilibria are peaks
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212 MALLET ■JORON
and troughs of relative fitness, but not necessarily of mean fitness. Under purely
number-dependent selection (Figure 1), mean fitness is a constant independent of
frequency, [nk(A)+nk(a)]/N, and even under linear frequency-dependence, the
minimum of mean fitness (at qA=0.5) is not at the unstable equilibrium (q∗
A=0.4
in Figure 1). If Ais more memorable than a, then nk(A)<n
k
(a), but this does
not increase the mean fitness when qAis high, except very close to fixation of A
when hardly any aare available to be tasted by predators.
A recent critique of the shifting balance model concluded that chromosomal
evolution, warning color evolution, and more general patterns of phenotypic adap-
tation were almost always better explained by ordinary individual selection (41).
For warning color and mimicry, the key problems are that natural selection seems
too intense so that drift is unlikely, and, in common with other examples of rugged
adaptive surfaces, phase III of the shifting balance seems an inefficient means of
spreading better warning patterns.While these problems seemserious, key features
of warning color considerably increase the chances of shifting balance occurring.
First, although selection for warning color can often be extremely strong, it would
be surprising if predator attacks were not sometimes reduced or suspended lo-
cally, due to temporary absence of key predators such as flycatchers or jacamars
(34, 35, 119, 120). If so, populations can occasionally drift to become polymorphic
because of a relaxation of selection. Provided that the prey are abundant compared
with their predator, (i.e. nk¿N), the populations will quickly enter the central
basin where selection is weak (e.g. for N=100 in Figure 1). Here drift or mild
forms of selection other than that due to warning function may cause a new pattern
to rise in frequency above the unstable equilibrium (phase I), whereupon warn-
ing selection can fix and refine the new pattern (phase II). An interface between
new and old patterns will form, resulting in a cline similar to hybrid zones be-
tween races observed today. If one pattern is superior at warning away predators,
asymmetries of selection will drive it into the range of the other behind a nar-
row moving cline, as in phase III (87,89, 98). Cline movement seems likely; with
strong selection in the clines observed in nature (93), fairly rapid movement is pre-
dicted (87, 89, 91). The shifting balance proposal is speculative because we know
little about the frequency, timing, and depth of episodes of selection relaxation re-
quired for phase I, the relative advantages of different warning colors across clinal
boundaries required for phase III, and whether population structural constraints
will prevent cline movement (4,69, 89, 98). However, empirical evidence for all
phases suggests the shifting balance is likely: (a) Polymorphism seems to exist
regularly among M¨ullerian mimics (see below under M¨
ullerian Mimicry, Polymor-
phism and the Palatability Spectrum), showing that although mimicryis sometimes
strongly selected (11, 75, 80,92), at other times, a combination of reduced selec-
tion, genetic drift, and nonmimetic selection causes polymorphism in the central
basin, and therefore that events triggering phase I seem actually to occur; (b) the
strong purifying selection that is the problem for phase I promotes phase II; and (c)
the existence of today’s narrow clines and biogeographic evidence for past cline
movementand movementin historicaltimes suggest that phase III occurs regularly.
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MIMICRY AND DIVERSIFICATION 213
The current disjunct distribution of genetically homologous “postman” patterns
of Heliconius erato and its M¨ullerian co-mimic Heliconius melpomene in periph-
eral populations strongly suggests that some such competitive cline movement
in favor of central Amazonian “dennis-ray” patterns of this nature has occurred,
even if the color patterns have been sometimes restricted to Pleistocene refuges
in the past (24, 27, 89,98, 137,164). There is some empirical evidence for move-
ment of Heliconius clines this century; although slow on a historical scale, the
movement of warning color clines could be very fast relative to an evolutionary
time scale (89). (d) The shifting balance does seem to have a strong potential in
explaining geographic divergence within species, the strong differences in warn-
ing color and mimicry between sister species, and also the extraordinary diversity
and novelty of these patterns (98). If the shifting balance is important for cur-
rent diversification, there is little reason to doubt that it could also have been
important in the murky initial stages of the origins of warning color in aposematic
lineages, though evidence has long since been erased by more recent color pattern
evolution.
DIMORPHISM AND POLYMORPHISM IN MIMICRY
Sex-Limited Mimicry
In a minority of Batesian mimetic butterflies, females are mimetic, while males,
although brightly colored, are not. Such cases can be explained if males are con-
strained to be nonmimetic by sexual selection, either via female choice (162, 163)
or by the requirements of combat or other male-male signaling (138,169). This
topic has been reviewed excellently elsewhere (164; see also 78), so we do not
treat it in detail here.
Sexual selection may explain sexually dimorphic mimicry, but there are some
peculiaritiesof female-limited mimicry for which the answers are notknown. First,
female-limitationseems restrictedto putativeBatesian mimicry.Asfar asis known,
M¨ullerian mimics lack strong sexual dimorphism. Presumably, this is explained
because M¨ullerian mimicry is under purifying density-dependent selection: As
a mimetic pattern becomes more common, its advantage increases (Figure 1). In
contrast, Batesian mimicry becomes less successfulas it becomes commoner; thus,
sexual selection is more likely to outweigh this weakening mimetic advantage in
Batesian mimics (162). Female-limited mimicry also seems virtually confined to
butterflies (46,168), whereas the sexual selection theory should apply to all ex-
amples of Batesian mimicry. Here, the explanation may be ecological. Territorial
or fighting males of many butterflies fly purposefully, fast, and can escape preda-
tors easily. Female butterflies searching for oviposition sites can be particularly
vulnerable to predator attacks (111) because they must at times fly slowly, like po-
tential models; thus ecological considerations may explain why butterfly females,
but not males, often mimic slow-flying models (111,169). Ecological constraints
on sexually dimorphic mimicry are well demonstrated by cases in which only the
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214 MALLET ■JORON
male is mimetic (168), for example, in saturniid moths with nocturnal females but
diurnal males (172).
Mimetic Polymorphism and Genetic Architecture
Batesian mimetic butterflies may be polymorphic as well as sexually dimor-
phic. This phenomenon is best known and studied genetically among female
mimetic forms of Papilionidae, particularly Papilio dardanus and P. memnon,
where each morph mimics a different unpalatable model. The maintenance of this
polymorphism is easily explained in common Batesian mimics because frequency-
dependent selection favors rare mimics. Polymorphisms in Batesian mimics are
also well-known in nonbutterfly groups: Good examples exist in hoverflies
(170, 171). However, the rarity of accurate polymorphic mimicry of the kind dis-
played in Papilio suggests that special circumstances must be involved. Mimetic
polymorphisms in these cases are usually determined at relatively few genomic
regions with large effect (“supergenes”), often with almost complete dominance
(38, 39,134, 135). The maintenance of mimetic polymorphisms probably depends
rather strongly on supergene inheritance. Without it, nonadaptive intermediates
would be produced.
While it is easy to understand the maintenance of polymorphisms at mimetic
supergenes, it is far from clear how these supergenes initially evolved. Early
Mendelians used these genetic switches as evidence that mutations of major effect
were prime movers of adaptation (123). Fisher argued forcefully that most adaptive
evolution could be explained via multiple genetic changes of individually small
effect being sorted by natural selection (49). Essentially, Fisher proposed that se-
lection rather than mutation was the creative process in adaptation. Goldschmidt
(56) then revived mutationist theory in more sophisticated form and proposed that
mimics could exploit major (“systemic”) mutations that reused the same develop-
mental machinery originally exploited by the model. He felt it unlikely that the
same genes were reused by mimics and models, proposing instead that different
genes had access to the same developmental pathways. Gradualists were quick to
point out cases in which development of mimicry was clearly analogous rather
than homologous, such as colored spots on the head and body of models being
mimicked by basal wing patches on mimetic Papilio memnon (135). Single gene
switches in P. memnon were demonstrated to consist of tightly linked multiple ge-
netic elements that could be broken apart by recombination or mutation, and it was
suggested by gradualists that these “supergenes” had been gradually constructed
by a process of linkage tightening to reduce the breakup of adaptive combinations
by recombination (38, 39).
More recently, opinion has swung back (but only part way) toward mutation-
ism. It has been realized that it would be hard to construct supergenes by means of
natural selection alone. Separate elements of a supergene must have been tightly
linked initially in order that a sufficiently high correlation between favorable traits
was available for selection for tighter linkage. Thus polymorphic mimicry must to
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MIMICRY AND DIVERSIFICATION 215
some extent have depended on the pre-existence of gene clusters (36, 37). If so, this
could explain why M¨ullerian mimics and models such as Heliconius often them-
selves show major gene inheritance. M¨ullerian mimics are not expected to have
polymorphisms, and usually they do not (but see below under M¨
ullerian Mimicry);
thus they are not expected to require supergene inheritance of their color patterns
under the gradualist hypothesis. Heliconius patterns are inherited at multiple loci;
this was interpreted as confirming a gradualist expectation for polygenic inheri-
tance of mimicry (113, 137,164). However, a closer look at Heliconius shows that
many of the pattern switches are indeed major, have major fitness effects, and can
also in some cases be broken down into tightly linked component parts by recom-
bination or mutation (87a, 93, 137), again suggesting mimetic “supergenes.” For
example, in both M¨ullerian mimics H. erato and H. melpomene, a large forewing
orange patch known as “dennis,” and orange hindwing “ray” patterns are very
tightly linked but are separable via recombination or mutation that shows up only
in rare individuals from hybrid zones (87a). Probably, mutations with major effect
are required even in M¨ullerian mimicry because, during adaptation, a M¨ullerian
mimic loses its current warning pattern while approaching that of a model. There
is thus a phenotypic fitness trough between the old pattern and the new pattern.
Only if a mutation produces instant protection by the new pattern can the gene
be favored, unless the two patterns are already extremely close. After approxi-
mate mimicry has been achieved by mutation, multilocus “modifiers” can im-
prove the resemblance in the normal way (37,105, 161, 164). This hybrid view
of M¨ullerian mimicry, known as the Nicholson “two-step” theory, combines what
is arguably a mutationist argument with a gradualist hypothesis to explain the
perfection of resemblances.
This explanation fits majorgene adaptations in M¨ullerian mimicry, especially as
itis now realizedthat Fisher’sargument for adaptation via small mutations has seri-
ous flaws (112), even without the frequency-dependent stability peaks of mimicry
(Figure 1). However, two-step theory cannot explain why genes for forewing and
hindwing patterns should be tightly linked in both model and mimic in Heliconius.
Why should H. erato and H. melpomene (the former is almost certainly the model
driving the divergence—see 55, 89) both diverge geographically using probable
supergenes of major genetic effect? One possibility is that genetic architecture
for color pattern change in Heliconius simply has limited flexibility (87a). We
now know that there is widespread reuse of homeotic gene families throughout
the animal kingdom, including some involvement in color pattern development
in butterflies (16,33). It would not be surprising if mimicry gene families were
not also reused similarly (106–108, 164) in the lineages leading to H. erato and
H. melpomene. This argument is similar to Goldschmidt’s (56), but in one sense
more extreme, since Goldschmidt thought it likely only that the same patterning
control would be reused, ratherthan the verysame genes. Others argue from similar
data that the evidence is in favor of analogous rather than homologous develop-
mental pathways and gene action (88), but a true test will be possible only when
mimicry genes are characterized at the molecular level in both lineages (51,95).
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216 MALLET ■JORON
In conclusion, current opinion based on nearly a century of genetic studies and
mathematical population genetic theory suggests how mimetic as well as other
adaptations may often require mutations of major effect, at least initially, both
because of the ruggedness of the selective landscape, and probably also because
of constraints imposed by pattern genetics. Perfection of these adaptations then
involves effects generated at multiple genes of increasingly small effect. The ge-
netic architectures required, especially for polymorphic mimicry, may be rare.
This would explain why some lineages involved in mimicry, such as the Papilion-
idae, are able to colonize multiple mimicry rings and become polymorphic (164),
while others are rarely mimetic. Disruptive mimetic selection is perhaps as likely
to be an agent causing an alternative, speciation, as it is to be a common cause of
polymorphism (see Mimicry and Speciation, below).
M¨
ullerian Mimicry, Polymorphism, and
the Palatability Spectrum
M¨ullerianmimicry andwarningcolor arestandard textbookexamplesof frequency-
dependent selection within species (e.g. 99, 126). Polymorphisms should be rare
due to high ratesof attack onrare variants(Figure 1;) (27, 47, 67, 87, 89). In general,
workers in the field of mimicry assert that this is so (89,97, 98, 161,164, 167), but
thereare some veryembarrassing exceptions to the rule among even the best known
M¨ullerian mimics. The most famous case is Danaus chrysippus and its M¨ullerian
mimics Acraea encedon,A. encedana, together with their Batesian mimic Hy-
polimnas misippus. While distinct color patterns are virtually fixed in the periph-
eries of their respective ranges, these species arehighly polymorphic over an area of
Central and Eastern Africa larger than Europe (57,146). Similarly embarrassing
widespread polymorphisms are found in two-spot ladybirds (15,85) and in La-
parus doris (Heliconiinae) (151, 159). Arguably, mimicry in many of these cases
is weak: Non- or poorly mimetic morphs are common (85, 114, 143, 144, 159).
However, there are equally problematic examples in which mimicry is very accu-
rate. For instance, Heliconius cydno is mostly monomorphic in Central America
(94, 142), but becomes polymorphic throughout much of the Andes of Colombia
and Western Ecuador (80, 83); each morph can be clearly identified as an accurate
mimic of other Heliconius, particularly H. sapho and H. eleuchia. The pinnacle
of M¨ullerian mimetic polymorphism is found in Heliconius numata. This species
is polymorphic throughout virtually its whole range, and some populations of the
Amazon basin near the slopes of the Eastern Andes may have up to seven different
morphs, each an accurate mimic of a separate species of Melinaea or Mechaniti
(Ithomiinae) (23, 26). Three explanations have been proposed, and we here add a
further hypothesis that may contribute to the persistence of polymorphisms once
they have been established.
1. Batesian Overload and Coevolutionary Chase If an unpalatable species has
many Batesian mimics, it may suffer from Batesian overload. According to this
hypothesis, the deleterious effects of mimics may force the model to diverge from
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MIMICRY AND DIVERSIFICATION 217
its normal pattern to escape mimicry, leading to a coevolutionary chase of model
by mimic. This idea has generated some controversy (54,71, 72, 109, 165) but
has been well reviewed recently (164,165), and we merely summarize: It does
Z not seem likely that coevolutionary chase or Batesian overload can explain
polymorphisms in unpalatable models. Frequency-dependent purifying selection
on the models must almost always be stronger than the diversifying selection due
to mimetic load (57, 78, 109, 165).
2. The Palatability Spectrum Unpalatability cannot be absolute; there must be
variation in unpalatability, which could lead to some interesting evolutionary ef-
fects. M¨ullerian and Batesian mimicry are differentiated by means of palatabilities.
Models and M¨ullerian mimics are negatively reinforcing, while Batesian mimics
positively reinforce predatorattacks. Hence, the straightforward view that Batesian
mimics are parasitic and hurt their models, while M¨ullerian mimics are mutual-
istic and benefit their models (103). However, a second equally straightforward
idea apparently conflicts with this view: If two M¨ullerian mimics are not equally
unpalatable, the presence of the more palatable could increase the rate of attack on
the less palatable, so that weakly unpalatable mimics may harm stronger models
or co-mimics, leading to a parasitic form of M¨ullerian mimicry. A series of behav-
ioral modelers since the 1960s have suggested that parasitic M¨ullerian mimicry
may explain some of the embarrassing examples of polymorphism in aposematic
species.Because benefitsand costs become decoupled fromthe M¨ullerian/Batesian
palatability divide in this latter prediction, a new terminology must be developed.
An appropriate name for the new parasitic form of M¨ullerian mimicry is “quasi-
Batesian” (148). [There is also a category of palatability-defined Batesian mimicry
that is beneficial to the model as well as the mimic—“quasi-M¨ullerian” mimicry
(84a, 147a, 151,165). This is possible if seeing a palatable mimic “jogs” the mem-
ory, reminding predators of unpleasant experiences with the model, thus leading
to greater avoidance of the model than if there were no mimic. Quasi-M¨ullerian
mimicry seems unlikely (151); anyway, it should not lead to polymorphism and
is not discussed further.] In quasi-Batesian mimicry, the more palatable mimic
may suffer increasing attacks as its numbers increase relative to the model’s, even
though its effect while alone would be to reduce its predation progressively as
density increases (Figure 3B,C) (71, 72,115, 148–151). It has been suggested that
this leads to the evolution of polymorphism in M¨ullerian mimicry systems (71, 72,
147a–151).
The behavioral assumptions that lead to quasi-Batesian mimicry pose a se-
vere threat to traditional natural history and evolutionary dynamical views of
mimicry, possibly “the end of traditional M¨ullerian mimicry” (148). This prob-
lem never arose until behavioral biologists attempted to model memory realis-
tically. It is apparent that M¨uller and subsequent naturalists and evolutionists
made an unstated assumption: that the sum of learning and forgetting over all
predators would cause an approximately constant number (nk) of unpalatable in-
dividuals of each phenotype to be killed (or damaged) per unit time (Figure 1).
Purifyingfrequency-dependentselection resultsfrom M¨uller’sassumptionbecause
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218 MALLET ■JORON
Figure 3 Mimicry and the palatability spectrum. The effect of assumptions about learning
and forgetting on fitnesses of model and mimic are shown in this figure. Equilibrated attack
rates at varying mimic densities are shown for model alone, mimic alone, and model-mimic
pair. Comparisons of attack rate clearly demonstrate whether mimic, model, or both benefit
from the association (115) (the mimic is here considered by convention to be the more
palatable species). In all panels, the model density is a constant set at 1.6 (115). These
assumptions (71, 115,148, 149,151, 166) can reproduce classical parasitic Batesian mimicry
(A;λMo =0.2,λ
Mi =1,α
Mo =0.3,α
Mi =0.0) and mutualistic M¨ullerian mimicry (D;
λMo =0.2,λ
Mi =0.2,α
Mo =0.3,α
Mi =0.3), but they also produce intermediate types
of mimicry, including parasitic quasi-Batesian mimicry between pairs of unpalatable species
(B;λMo =0.2,λ
Mi =0.6,α
Mo =0.3,α
Mi =0.5), and a cusped quasi-Batesian/M¨ullerian
combination (C;λMo =0.2,λ
Mi =0.3,α
Mo =0.3,α
Mi =0.5). The curves were generated
from a general equation for attack rate equilibrium at particular density (115, 149). Note that
Owen & Owen’s own figures are sketches only, and contain some incorrect features (149).
the average attack fraction nk/Ndecreases as the total number of individuals, N,
increases. The existence of quasi-Batesian mimicry, in contrast, requires that the
attack fraction on a M¨ullerian mimic increases as Nincreases, implying that nkcan
be a rising function of Nrather than a constant. We here follow the development
of these ideas and discuss why we feel the assumptions that lead to quasi-Batesian
mimicry may not be met in most real situations.
The original idea for what is now called quasi-Batesian mimicry was proposed
by Huheey (71 and earlier). After a single trial experience with an unpalatable
individual, the predator was imagined to learn to avoid it totally; thereafter, the
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MIMICRY AND DIVERSIFICATION 219
predator would forget after seeing, but not attacking, a fixed number of individuals
with the same pattern. In this formulation, unpalatability affected only the rate of
memory loss, rather than its acquisition; very unpalatable species caused slower
forgetting than mildly unpalatable species. Increasing the density of less nasty
mimics caused a rise in the average forgetting rate and led to an increasing frac-
tion of models attacked. Thus, if two unpalatable species differed in palatability,
only one benefited, while the other suffered, though the more palatable species on
its own was still unpalatable in the sense that predators are negatively reinforced.
Mimicry, even when at the point of equal palatability, was neutral; increases in
density of either co-mimic caused a faster rate of both learning and forgetting,
rather than a reduction in fraction attacked. The predicted absence of mutualistic
mimicry in Huheey’s theory was strongly attacked (12, 115, 136,151). The prob-
lem appeared to be theevent-triggered forgetting model, in which avoidancelapsed
after a certain number of prey were avoided. This meant that the total number of
prey in the population had no effect on the evolution; selection was assumed to
depend only on relative frequency of mimics and models.
To avoid this pathology of Huheey’s formulation, it was proposed that forget-
ting should be time-dependent (12, 115, 136, 166), rather than depending on the
number of avoidances; forgetting should cause the attack fractions to decline or
rise exponentially with rates αMi and αMo (for mimic and model, respectively)
toward the “naive attack rate” asymptote, i.e. a naive attack fraction (115, 149).
At the same time, a more flexible system of learning was proposed, in which un-
palatability was represented as an asymptotic fraction of prey attacked, λMi and
λMo; these asymptotes were again approached exponentially, with learning rates
forming another set of parameters (84a, 115, 147a,148, 151). These theories could
reproduce the full spectrum of mimicry from Batesian mimicry (Figure 3A)to
M¨ullerian mimicry (Figure 3D), including quasi-Batesian mimicry (Figure 3B),
and also a curious form of biphasic mimicry, which is quasi-Batesian at low mimic
density, but traditionally M¨ullerian at higher mimic densities (Figure 3C).
The behavior of these models is easy to explain. Learning and forgetting each
result in an exponential approach to a different asymptote of attack fraction, so
the combination of the two processes will itself lead to a stationary resultant at-
tack fraction independent of density for either model or mimic on their own. The
joint attack fraction on model and mimic together (assuming models and mimics
are visually indistinguishable) is simply an average between the curves for model
and mimic asymptotic attack fractions. When mimic density is very low, the joint
response is very like that of the model; when mimic density is high, the effect
of the mimic dominates, and the joint response increasingly obeys the mimic’s
asymptote. Because the averaging process is of the form of a harmonic mean (115)
rather than an arithmetic mean, curious peaks in the density response can occur, the
“Owen & Owen effect” (149) (Figure 3C), implying a quasi-Batesian/M¨ullerian
transition across a density threshold. Speed & Turner (151,167a) recently exam-
ined the behavior of a number of different formulations and combinations of these
basic memory assumptions. They concluded that (a) many of the assumptions
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220 MALLET ■JORON
produce quasi-Batesian responses like that of Figure 3B-C and (b) behavioral
experiments on mimicry and warning color are not usually set up to test for den-
sity responses and therefore cannot easily be used to test whether mimicry falls
into quasi-Batesian categories. Well-known polymorphic M¨ullerian mimics often
have intermediate levels of acceptance in tests both with caged and wild birds
(20, 34, 35, 77, 119, 120, 132), showing that many supposedly unpalatable species
may often be attacked. Therefore, the known biology of predation on unpalatable
species as well as theory mesh with the possibility of a palatability spectrum that
could lead to quasi-Batesian mimicry.
However, if theories like those in Figure 3 are correct, the whole basis for
traditional number-dependent and frequency-dependent mimicry of Figure 1 is
suspect. Our own belief is that new and incorrect assumptions lurking in the be-
havioral models are to blame for the conflict. Our objections, which are more
fundamental than those raised in an earlier critique (84a), are as follows:
(a) We think it unlikely that attack rates on unpalatable species will reach an
asymptotic fraction independent of density, unless that fraction is zero. To under-
stand this, imagine that forgetting is switched off, so that all learning is perfect
(see also 84a). Under this assumption, the new theories (115, 148) predict that
learning should asymptote at constant frequency; number-dependence enters into
memory dynamics only through time-based forgetting. With no forgetting, there is
then no number-dependent selection, and mutualistic M¨ullerian mimicry becomes
impossible (149–151). Intuitively, it seems odd that perfect memory does not lead
to extremely successful M¨ullerian mimicry, and we here attempt to show why this
intuition is correct. With no forgetting, the absence of M¨ullerian mimicry is due
to a density-independent asymptotic attack fraction. In other words, as the density
of an unpalatable mimic in Figure 3 rises, the predator is supposed to stuff itself
with more and more unpalatable prey in order to maintain a constant asymptotic
fraction of prey attacked. Learning to avoid prey is more likely to depend on dose
received by the predator per unit time, rather than dose per individual prey. This
will lead to a fraction attacked that declines with density rather than a constant
asymptotic fraction. Note that this argument does not depend on “hunger lev-
els,” because unpalatable prey are unlikely to form a large component of the diet
(166). The new theories in effect have the same problem in their learning module
(i.e. not being time-based) as did Huheey’s much- criticized forgetting module
(12, 115, 136). It seems much more likely to us that for “unpalatable” prey, an
asymptotic number of prey attacked per unit time would be required for learning,
leading to strongly number-dependent and frequency-dependent selection like that
of Figure 1, and a resultant attack fraction that declines to zero as prey densities
increase.
(b) It is hard to justify the term “unpalatability” unless the effect is density-
independent; predators should reject and increasingly avoid unpalatable prey
whenever they encounter them at whatever density. However, the new theories
see a species as unpalatable if it has a learning asymptote lower than the “naive
attack fraction,” and as palatable if it has a learning asymptote higher than the
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MIMICRY AND DIVERSIFICATION 221
naive attack fraction (149,151). But only when the asymptotic attack fraction
is zero do we produce avoidance, whatever the attack fraction prior to experi-
ence; this was the case, for example, in an original simulation model designed to
disprove Huheey’s assertions, and which recovered only Batesian and M¨ullerian
mimicry, with a sharp transition between them (166). If our argument is correct,
the whole of the palatability spectrum above an asymptotic attack fraction of zero
is then “palatable,” and quasi-Batesian mimicry simply becomes Batesian, para-
sitic mimicry. The “palatability spectrum” represented by 0 <asymptotic attack
fraction ≤1 is just that, a spectrum of palatability rather than of unpalatability.
Under this view, levels of unpalatability may differ, but they cause changes only
in rates of learning and forgetting, rather than in level of the learning asymptote
itself, which must be zero.
(c) Another problem is that, strictly speaking, “attack fraction” is not “palata-
bility” at all, but a transformation of palatability onto a behavioral response axis.
What we mean by “unpalatability” is easiest to interpret as a simple linear, or
perhaps logarithmic, function of noxious compound dosage, which can vary from
zero to infinity. The behavioral effect of these compounds may be to produce an
asymptotic attack fraction of 0%, 100%, or somewhere in between (Figure 3).
However, the behavioral response will certainly be a sigmoidal function of dose;
the majority of dosages will yield approximately 100% (palatable) or 0% (unpalat-
able) asymptotic attack, with only a relatively narrow intervening band of dosages
giving rise to intermediate levels of attack. Thus, the behavioral “palatability spec-
trum” as modeled by attack fraction is a highly distorted view of the underlying
palatability, or dosage, of noxious chemistry; in fact, most of the dosage spectrum
is not considered by these attack rate spectrum models (115, 147a–151). In reality,
intermediate asymptotic attack fractions, even if they do exist, are likely to form a
small part of the palatability (dosage) spectrum.
Empirical data from caged and wild birds showing intermediate levels of at-
tack on models are of great interest, but they do not necessarily conflict with the
points made above. Attack fractions in the laboratory or in nature tell us neither
how they vary with prey density (167a) nor how they asymptote. The behavioral,
“receiver psychology” view, which leads to possibly novel forms of mimicry, sug-
gests that attack fraction will reach a nonzero asymptote as density is increased;
the number-dependent (natural history) view predicts that attack fractions on un-
palatable insects will always decline with increasing density. Unfortunately, ex-
periments have not clearly distinguished between these alternatives because they
were designed with other ends in mind (167a). It does not seem impossible to
design more appropriate experiments, however.
In conclusion, theories of palatability from a receiver psychology angle have
led to a potentially major upset in traditional views of mimicry. To decide which
view is correct, we need to understand memory dynamics of actual predators, and,
given that many of the controversial theories are supposedly based on a standard
Pavlovian learning theory (124,148), understanding the evolutionary results of
memory on mimicry could lead to advances in memory theory in general. Even if
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222 MALLET ■JORON
quasi-Batesian mimicry turns out, as we believe, to be unlikely, the threat posed
by these new theories demonstrates the naivet´e of the original natural history
assumption that memory is a black box producing number-dependence.
3. Spatial and Temporal Variation in Mimetic Selection Geographic variation
in mimetic color patterns within a mimic can obviously be maintained by geo-
graphic divergence of models. If mimicry is M¨ullerian, then divergence becomes
self-reinforcing. Patches of habitat with different M¨ullerian mimetic patterns will
be separated by zones of polymorphism; the width of the polymorphic region will
be proportional to average dispersal distance and inversely proportional to the
square root of the strength of selection (92), as for clines in general (5). Thus, if
selection is weak and dispersal extensive, bands of polymorphism may be wide
compared to areas of monomorphism. This situation undoubtedly pertains in many
species; for example, it is often not realized how common this is within Helico-
nius. The hybrid zones between races of Heliconius erato or H. melpomene are
renowned for their narrowness (e.g. 87,93); however, zones of polymorphism be-
tween weakly differentiated races, for instance in the Amazon basin, are much
broader, so that polymorphism is almost the norm (see maps in 24,27; many other
maps of Heliconius races oversimplify the actual distributions).
Asimilar situation may existfor wide bandsof polymorphism in theunpalatable
Acraea encedon, A. encedana, Danaus chrysippus, and their Batesian mimic Hy-
polimnas misippus in Central and Eastern Africa: Peripheral populations of these
species are nearly monomorphic (146). Similarly, spatially varying mimetic and
other selection pressures, rather than quasi-Batesian mimicry (151), may explain
the polymorphisms of ladybirds such as Adalia bipunctata (15, 85) and butterflies
such as Laparus doris (159).
There may also be temporal as well as spatial variation in mimetic selection.
The diverse polymorphism of Heliconius numata may be selected because the
models (ithomiines in the genus Melinaea) vary greatly in abundance over time
and space (26). However, it would be hard to explain how polymorphism is
maintained via temporal variation unless the color pattern loci have, on aver-
age, a net heterozygote advantage. Given that the supergenes affecting mimicry in
H. numata are visually dominant (26), any heterozygous advantage must usually
be nonvisual. Another example of polymorphism in a M¨ullerian mimic with mul-
tiple models is Heliconius cydno. There are strong differences across W. Ecuador
in the frequency of models Heliconius sapho and H. eleuchia, causing divergent
patterns of natural selection (80). In conclusion, the observed polymorphisms of
many M¨ullerian mimics can be explained without quasi-Batesian mimicry, via
spatial and possibly temporal variation in model abundance.
4. The Shape of Frequency-Dependence The maintenance of polymorphism
in unpalatable species will be considerably aided by the shape of frequency-
dependence, given number-dependent selection (Figure 1). When population sizes
of prey (N) are large relative to the numbers sacrificed during predator learning,
the fraction nk/Nwill be small, say 1/100 or less, and there will be little selection
in the central polymorphic basin.
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MIMICRY AND DIVERSIFICATION 223
Although we do not know the values of nk/Ntypical in the wild, a variety of ex-
periments (11, 75, 80,92) indicate that selection can be strong, i.e. nk/N≥1/10.
On the other hand, it seems likely that many predators will require few learning
trialsto avoidan aposematic insect. Models andcommon M¨ullerian mimics will of-
ten outnumber their predators considerably, and, furthermore, predators live much
longer and will often be able to generalize between prey generations. Experiments
by Kapan on H. cydno in W. Ecuador showed that selection against polymorphism
was much weaker where H. cydno was abundant than where it was rare (80). Thus,
it seems not unlikely that nk/N≤1/100, at least some of the time.
Drift can explain the origin but not the maintenance of polymorphism in the
central basin. However, polymorphisms, once attained, should be removed only
slowly via mimetic selection. Second-order selective forces such as nonvisual se-
lection (for instance, thermal selection in ladybirds), arbitrary mate choice, or
other factors (15, 85,144–147) may become important and contribute to nonadapt-
edness of mimetic polymorphisms. Strong selection at some times and places
(nk/N=1/10 or greater) is clearly required to produce near-perfect resemblance
and narrow hybridzones between races.But if aM¨ullerian mimic or model, perhaps
by an ecological fluke, becomesabundant relative to its predators (nk/N≤1/100),
it could then be relatively free to experiment with nonadaptive and polymorphic
color patterns. In short, the shape of frequency-dependence, together with vary-
ing selection for mimicry and mild selection of other types can explain M¨ullerian
polymorphism without the need for quasi-Batesian mimicry.
MIMICRY AND SPECIATION
Bates, Wallace, and Darwin were all of the opinion that strong natural selection,
which must occur sometimes to explain mimicry, could lead to speciation. The
continuum between forms, races, and species of diversely patterned tropical but-
terflies led to this idea in the first place (6, 7, 173,174). This view has since faded
into the background, probably because of a postwar concentration on reproductive
characteristics (“reproductive isolating mechanisms”) thought important in spe-
ciation under the “biological species concept” (100). However, mimicry causes
strong selection against nonmimetic hybrids or intermediates and should therefore
contribute strongly to speciation and species maintenance, by acting as a form
of ecologically mediated postmating isolation. Together with the evolution of as-
sortative mating, mimetic shifts may have led to speciation in butterflies such as
H. himera and H. erato (96, 101).
If mimicry contributes to speciation, mimetic shifts should often be associated
with speciation within phylogenies. Mimicry-related speciation would explain the
curious pattern of “adaptive radiation” in Heliconius:M¨ullerian co-mimics are
usually unrelated, while closely related species almost always belong to different
mimicry rings (164). Mimetic pattern has been switched between eight of nine
pairs of terminal sister taxa in a mtDNA phylogeny of Heliconius (17, 95). Many
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224 MALLET ■JORON
sister taxa that have switched mimicry are known from other groups as well. For
example, among butterflies, the viceroy (Limenitis archippus) mimics queen and
monarch butterflies (Danaus spp.), while its close relative, the red-spotted purple
(Limenitis arthemis astyanax) mimics an unpalatable papilionid, Battus philenor.
The two Limenitis are very closely related and hybridize occasionally in the wild
(127). Similar examples exist in the Papilionidae. Mimetic lineages do not seem to
speciate more rapidly than nonmimetic lineages in the genus Papilio (F Sperling,
in litt.); however closely related, species do often differ in their mimicry ring.
While we believe mimicry contributes to speciation, this section must remain
somewhat speculative. We cannot point to any convincing case in which mimicry
hasbeen themajor oronly causeof speciation.But thenperhaps speciationis almost
always caused by multiple, rather than single, episodes of disruptive selection.
EVOLUTION AND MAINTENANCE OF MULTIPLE
MIMICRY RINGS
A naive view of M¨ullerian mimicry would suggest that all similarly sized species
should converge locally onto a single color pattern. In fact, there are often ten or
more mimicry rings among ithomiine and heliconiine butterflies of the Amazon
basin (6, 9, 102, 137). The reason for the lack of a single uniform mimicry ring
among similarly sized butterflies is currently disputed and parallels, at an inter-
specific level, the debate on M¨ullerian polymorphisms.
Papageorgis (116) provided data from Peru showing that different heliconiine
and ithomiine mimicry rings fly at different heights in the forest canopy. She sug-
gestedthat dual selectionfor camouflage andmimicry might explainthese patterns.
In other words, particular mimicry rings are better camouflaged in the lighting con-
ditions pertaining at theirfavored flightheights. However, heliconiine flightheights
are now well-documented to overlap far more extensively than appeared from Pa-
pageorgis’ data, although weak mimicry associations do exist for habitat and noc-
turnal roosting height (25, 28, 94). It is unclear how dual selection would work, and
it is anyway hard to imagine that the garish reds, yellows, blacks, and iridescent
blues of heliconiines are ever very cryptic against subdued forest backdrops.
Nonetheless, recent studies of ithomiines do demonstrate some patterning of
mimicry rings in flight height as well as in horizontal (habitat-related) distribution
(10, 25, 44,102). A possible explanation for these community patterns is that dif-
ferent guilds of predators are found preferentially in the different habitats or micro-
habitats, so that, within each habitat, mimicry is tuned to local predator knowledge
(10, 94). There must be some selection pressure of this sort to explain the micro-
habitat associations; however, it would be hard to imagine birds ignoringbutterflies
a meter or two higher or lower than their normal flight height in the forest under-
story, and it seems highly unlikely that the proposed subcommunities of predators
and particular mimicry rings are very discrete. The overlap between mimicry rings
is rather more noticeable to the naturalist than the somewhat statistical differences
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MIMICRY AND DIVERSIFICATION 225
in average heights or microhabitats (10,25, 44,94, 102). Instead, statistical differ-
ences may exist because newly invading unpalatable species are most likely to
join mimicry rings already most prevalent in their habitats. Major mimicry rings
that overlap substantially may be unlikely to join together as species accumulate
in each ring for the same reason that intraspecific polymorphisms have a nearly
neutral central basin (Figure 1); the selection for convergence of two abundant
mimicry rings will simply not be that strong.
CONCLUSIONS: MIMETIC DIVERSITY AND THE FORM
OF FREQUENCY DEPENDENCE
We have shown that the shape of number-dependent selection on the color patterns
of unpalatable species can help explain many mutually conflicting data of mimicry
and mimetic diversity. When the attack fraction is high because of a high preda-
tor/prey ratio, selection on mimicry can clearly be extremely strong and has been
measured to be so in a handful of field studies. But when predator/prey ratios are
low (nk/N≤1/100), there is a wide central basin of near-neutrality where only
weak purifying selection acts on polymorphisms. Therefore, once an unpalatable
butterfly becomes abundant relative to predators, nk/Ndecreases hyperbolically,
and its morphology becomes less constrained by selection. A temporary relax-
ation of selection may then result in polymorphisms, which become relatively
impervious to further bouts of selection. The weakness of purifying selection in
polymorphic populations can help explain why puzzling polymorphisms persist in
some M¨ullerian mimics. Such polymorphisms enable populations to explore the
selective landscape, which can increase the chances of shifting balance, one of
the few ways to explain the empirical observation that utterly novel color patterns
evolve continually in warning-colored and mimetic butterflies. Similarly, weak
selection against multiple rings may be partially responsible for the diversity of
mimicry in any one area.
But these arguments will fail if predator memory and perception do not produce
number-dependent selection. If predators behave according to some current theo-
ries of “receiver psychology,” these conclusions based on extensions of traditional,
number-dependent M¨ullerian theory are in jeopardy. We do not think that this is
the case; however, appropriate experimental studies are urgently required to test
between these conflicting models of memory and forgetting.
ACKNOWLEDGMENTS
We are very grateful to George Beccaloni, Chris Jiggins, Gerardo Lamas, Russ
Naisbit, Mike Speed, Felix Sperling, Maria Servedio, Greg Sword, John Turner,
Dick Vane-Wright, Dave Williams for critiques, conversations, and comments, and
to NERC, BBSRC, the British Council, and the Ministries of Higher Education
and Research and of Foreign Affairs, France, for financial support.
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226 MALLET ■JORON
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Annual Review of Ecology and Systematics
Volume 30, 1999
CONTENTS
THE ORIGIN AND EARLY EVOLUTION OF TURTLES, Olivier
Rieppel, Robert R. Reisz 1
USES OF EVOLUTIONARY THEORY IN THE HUMAN GENOME
PROJECT, Alan R. Templeton 23
STREAMS IN MEDITERRANEAN CLIMATE REGIONS: Abiotic
Influences and Biotic Responses to Predictable Seasonal Events, Avital
Gasith, Vincent H. Resh 51
CHOOSING THE APPROPRIATE SCALE OF RESERVES FOR
CONSERVATION, Mark W. Schwartz 83
CONSPECIFIC SPERM AND POLLEN PRECEDENCE AND
SPECIATION, Daniel J. Howard 109
GLOBAL AMPHIBIAN DECLINES: A Problem in Applied Ecology,
Ross A. Alford, Stephen J. Richards 133
USING PHYLOGENETIC APPROACHES FOR THE ANALYSIS OF
PLANT BREEDING SYSTEM EVOLUTION, Stephen G. Weller, Ann
K. Sakai 167
EVOLUTION OF DIVERSITY IN WARNING COLOR AND
MIMICRY: Polymorphisms, Shifting Balance, and Speciation, James
Mallet, Mathieu Joron 201
CONSEQUENCES OF EVOLVING WITH BACTERIAL
SYMBIONTS: Insights from the Squid-Vibrio Associations, Margaret J
M
cFall-N
g
ai 235
THE RELATIONSHIP BETWEEN PRODUCTIVITY AND SPECIES
RICHNESS, R. B. Waide, M. R. Willig, C. F. Steiner, G. Mittelbach, L.
Gough, S. I. Dodson, G. P. Juday, R. Parmenter 257
ANALYSIS OF SELECTION ON ENZYME POLYMORPHISMS,
Walter F. Eanes 301
POLYMORPHISM IN SYSTEMATICS AND COMPARATIVE
BIOLOGY, John J. Wiens 327
PHYSICAL-BIOLOGICAL COUPLING IN STREAMS: The Pervasive
Effects of Flow on Benthic Organisms, David D. Hart, Christopher M.
Finelli 363
ASTROBIOLOGY: Exploring the Origins, Evolution, and Distribution of
Life in the Universe, D. J. Des Marais, M. R. Walter 397
EVOLUTION OF EASTERN ASIAN AND EASTERN NORTH
AMERICAN DISJUNCT DISTRIBUTIONS IN FLOWERING
PLANTS, Jun Wen 421
FULL OF SOUND AND FURY: History of Ancient DNA, Robert K.
Wayne, Jennifer A. Leonard, Alan Cooper 457
Annu. Rev. Ecol. Syst. 1999.30:201-233. Downloaded from arjournals.annualreviews.org
by University of Arizona Library on 03/13/05. For personal use only.
DO PLANT POPULATIONS PURGE THEIR GENETIC LOAD?
EFFECTS OF POPULATION SIZE AND MATING HISTORY ON
INBREEDING DEPRESSION, D. L. Byers, D. M. Waller 479
HISTORICAL EXTINCTIONS IN THE SEA, James T. Carlton,
Jonathan B. Geller, Marjorie L. Reaka-Kudla, Elliott A. Norse 515
GENE FLOW AND INTROGRESSION FROM DOMESTICATED
PLANTS INTO THEIR WILD RELATIVES, Norman C. Ellstrand,
Honor C. Prentice, James F. Hancock 539
RESISTANCE OF HYBRID PLANTS AND ANIMALS TO
HERBIVORES, PATHOGENS, AND PARASITES, Robert S. Fritz,
Catherine Moulia, George Newcombe 565
EVOLUTIONARY COMPUTATION: An Overview, Melanie Mitchell,
Charles E. Taylor 593
Annu. Rev. Ecol. Syst. 1999.30:201-233. Downloaded from arjournals.annualreviews.org
by University of Arizona Library on 03/13/05. For personal use only.
