Floral Mimicry.pdf

trends in plant science

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Million Tadege, Isabelle Dupuis and Cris Kuhlemeier * are at the

Institute of Plant Physiology, University of Berne, Altenbergrain 21,

CH-3013 Berne, Switzerland.

* Author for correspondence

(tel 141 31 631 4913; fax 141 31 332 2059;

e-mail cris.kuhlemeier@pfp.unibe.ch).

Floral mimicry: a fascinating

yet poorly understood

phenomenon

incompletely address the last point – the critical

question of whether the similarity is actually

adaptive. Before we suggest the tests necessary

to assess the fitness consequences of similarity,

we would first like to further describe the basic

kinds of floral mimicry, because the type of

mimicry influences the kinds of tests performed.

There are two basic types of floral mimicry,

Batesian and Müllerian, which are governed

by different selection regimes (Fig. 1). In

Batesian floral mimicry, the mimic produces no

nectar reward, whereas the model does (Fig.

2). Hence the mimic’s chances of visitation

should be increased through its similarity to a

nectar-producing model. Further, because the

Batesian mimics do not have nectar, the more

frequent they are in the population, the lower

their pollination success becomes because

pollinators can learn to avoid flowers that look

a certain way, and indeed, both mimic and

model might be avoided 9 . Thus, new Batesian

mimic phenotypes that mimic a different

model will enjoy a pollination advantage and

this type of negative-frequency-dependent

selection should select for increased diversity

of model–mimic pairs (Fig. 1).

In Müllerian floral mimicry, two or more

rewarding flower species gain a collective

advantage as a result of convergence on a

‘common advertising display’ 4,7,10–15 . The

similarity of Müllerian mimics increases the

‘perceived’ density of rewarding flowers and,

thus, might increase the probability of polli-

nation (Fig. 3). When pollinator visitation is

positively density-dependent, greater similarity

among flower species implies higher pollina-

tion success. Thus, Müllerian mimics are

undergoing positive frequency-dependent

selection (Fig. 1), and are all converging on a

similar phenotype. In spite of selective pres-

sure towards similarity, variation in Müllerian

mimics probably exists because pollinators

Bitty A. Roy and Alex Widmer

Flowers of different species that resemble each other are not necessarily mimics.

For mimicry to be occurring, the similarity must be adaptive. Unfortunately, no

case of floral mimicry has ever been fully verified and it is important that we move

beyond these perceived similarities to testing whether they are truly adaptive.

Here we explain the differences between Batesian and Müllerian floral mimicry,

illustrate what should be done to test mimicry hypotheses, and discuss how

interspecific pollen transfer influences the evolution of mimicry.

mimicry have been developed by zo-

ologists and are commonly associated

with protective mimicry in animal systems 1,2 .

However, these concepts also apply to plant

systems because the same evolutionary pro-

cesses that form them (negative and positive

frequency-dependent selection) occur whether

an animal is being warned away (protective

mimicry) or invited in (floral mimicry) (Fig. 1).

In animal Batesian mimicry, selection favors

resemblance of a palatable mimic to an un-

palatable model. Similarly, in Batesian floral

mimicry, selection favors resemblance of a

non-rewarding mimic to a rewarding model 3,4 .

In animal Müllerian mimicry, selection favors

convergence on a single, ‘aposematic’, warn-

ing pattern as a defense against predators, such

as the yellow and black striped pattern of bees,

wasps and hornets. Similarly, in floral Müllerian

mimicry, selection favors similar floral

appearance among rewarding plants for the

sake of attracting pollinators. The view that

some floral mimicry systems fall within the

concept of Batesian mimicry is now well

established 3–5 although experimental tests re-

main few. Floral Müllerian mimicry is both

less commonly accepted and less studied.

For floral mimicry to be established as

occurring between two or more similar

species, they must:

• Have strongly overlapping distributions,

and must have done so long enough for co-

evolution to have occurred.

• Require pollinators for seed set.

• Overlap substantially in flowering phenology.

• Share the same pollinator species and the

same individual pollinators must move

freely between the species.

• The similarity must be important for fitness 6–8 .

The majority of floral mimicry studies establish

the first four points, but either neglect or

August 1999, Vol. 4, No. 8

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T he concepts of Batesian and Müllerian

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perspectives

Negative frequency-dependent selection

There are two alternative methods for test-

ing floral Müllerian mimicry hypotheses when

there is little or no phenotypic variation in the

putative mimics. First, one could create artificial

phenotypes that lack the features associated

with the mimicry, and test whether these indi-

viduals have lower fitness than those with greater

similarity to the model. Second, one could deter-

mine whether the putative mimics have the same

or even higher fitness when they co-occur in a

patch as they do in separate, same-density

patches of the individual species. In other words,

do insects treat all the members of a Müllerian

mimic ring as if they were the same, choosing

when to forage based on the number or density

of similar shaped, colored or scented flowers,

rather than on the specific species composi-

tion of the patch? Some preference by polli-

nators might occur, but, on average, patch

density, not patch composition should determine

the fitness of flowers of similar appearance.

(a)

(b)

100

Phenotype frequency (%)

100

Time

Positive frequency-dependent selection

(c)

(d)

100

Phenotype frequency (%)

100

Interspecific pollen transfer

and evolution of mimicry

There is a limit to how similar co-flowering,

sympatric species can be to each other, because

individuals need to be able to mate with the

proper species. If two flower species look too

much alike, visitors might transfer their pollen

to the wrong species, a phenomenon called

improper pollen transfer. Improper pollen

transfer, which is a form of competition, will

tend to select for differences among species 21–23 .

A plant’s success will be enhanced if a polli-

nator transfers its pollen directly to another of

the same species. Thus, improper pollen trans-

fer could reduce selection for mimicry unless

it is ameliorated in some way.

Because there are examples of floral mim-

icry, we can look at those species to learn how

improper pollen transfer can be decreased.

Orchids, the group with the most mimetic

species (up to a third of the known orchids, or

~10 000 species according to some esti-

mates 24,25 ), package their pollen in saddlebag-

like structures called pollinia. It is suggested

that pollinia are less likely to be improperly

transferred than pollen because pollinia tend to

be like keys, fitting only into flowers with the

proper shape 26 . However, in spite of pollinia,

hybridization is thought to be common in

orchids 24 . Another trait that might be important

for co-flowering species is flower

longevity 27,28 . As long as the likelihood of

hybridization is low, and the presence of for-

eign pollen on a stigma is not in itself harmful,

mimetic flowers that can wait until the proper

pollen arrives will have an advantage. The evo-

lution of the Costus allenii–C. laevis mimicry

system (Fig. 3) might have been favored by a

combination of Costus flower longevity and

strong barriers against hybridization 7 . The

pseudoflowers produced by flower-mimic

fungi are also long-lived, producing nectar for

Time

Trends in Plant Science

Fig. 1. Frequency-dependent selection. (a) Batesian mimicry is molded by negative

frequency-dependent selection. The rarer a phenotype, the higher its fitness. As a rare pheno-

type becomes more common, its fitness will decline, leading to a decrease in frequency.

(b) Thus, in negative frequency-dependent selection, the frequency of a phenotype will vary

over time. (c) Müllerian mimicry is molded by positive frequency-dependent selection. The

more common a phenotype is, the higher its fitness. This means that over time, the more com-

mon phenotype is favored by selection and eventually becomes fixed in the population

(d). Therefore, little or no variation is expected in Müllerian mimics. (b) and (d) represent

‘idealized’ states. It is not known whether negative frequency-dependent selection by polli-

nators will lead to limit cycles of the exact form depicted, and positive frequency-dependent

selection is unlikely to be consistent enough to lead to a straight-line function.

vary across the range of a species, and might

change from one part of the season to

another 16–18 .

Several differences between the two basic

types of floral mimicry should now be clear.

In Batesian mimicry, only the model is re-

warding, whereas in Müllerian mimicry, all

the species present pollinators with rewards.

In Batesian mimicry, the model does not gain

from the interaction, whereas in Müllerian

mimicry, all the species gain an advantage as

a result of their similarity. In Batesian mim-

icry, there is an obvious model on which the

mimic is based, whereas in Müllerian mim-

icry, there is not always an obvious model or

mimic – all the taxa involved are converging

towards one another. However, the commonest

species (or phenotype) should have the highest

fitness, and is thus the model for all of the rest.

A species that starts out as a Müllerian mimic

can itself become the model if it becomes

more abundant than the original model 19 .

To test whether resemblance is adaptive in

a Batesian system, one needs to establish that

the mimic receives more visits and has higher

fitness when the rewarding model is present

than when it is absent 6,20 . Both patch density

and composition probably influence pollinator

behavior. When the patch is dense, or when

the mimic is common, it is predicted that the

pollinators will encounter unrewarding mimetic

flowers more often, and fitness will thus

decrease 6,20 . There are only a few studies of

Batesian mimicry that have measured fitness

in the manner described here (Fig. 2).

To test whether resemblance is adaptive in

a Müllerian system, one should test whether

individuals of the rarer species (which are thus

termed the mimics) have higher fitness when

they are most similar to the more common spe-

cies (the model). However, these tests rely on

there being phenotypic variation in the mimic,

and there might not be variation if positive fre-

quency-dependent selection has run its course

and, thus, all of the mimics have the same

characteristics. For example, it is impossible to

test the Müllerian mimicry hypothesis that bees,

wasps and hornets gain a collective advantage

from their stripes warning away predators

when all of the individuals have stripes.

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Fig. 2. Possible examples of Batesian floral mimicry. (a) Evidence for the existence of Batesian floral mimicry in orchids was found for the

orchids Orchis israelitica , which mimics (b) the lily Bellevalia flexuosa 20 , and Disa ferruginea (not shown), which mimics either Tritoniopsis

triticea (Iridaceae) or Kniphofia uvaria (Asphodelaceae, not shown) 3 . In both of these systems most of the conditions for mimicry have been

established. The putative mimics overlap in distribution and flowering time with the model, they require visitation for full seed set, and they share

pollinators with the model. However, evidence for the condition that similarity must increase fitness is only circumstantial. Higher reproductive

success (i.e. pollination and pollinia removal 3 as well as capsule production 3,20 ) in the presence of the model, compared with situations where the

model is absent, suggests that the resemblance of the mimic to the model does indeed account for the increased reproductive success. However,

a similar result might also be observed in cases where non-rewarding, non-mimic flowers grow together with rewarding flowers, such as in

Orchis caspia 52 . Therefore, to prove that O. israelitica or D. ferruginea are indeed Batesian mimics, experimental evidence is needed to

demonstrate that mimics with greater similarity to the models have higher fitness than those that are less similar. Photographs (a) and (b) by

Alex Widmer. (c) Epidendrum radicans (Orchidaceae), a non-rewarding orchid, was thought to be a Batesian mimic of the rewarding neotropi-

cal weeds (d) Asclepias curassavica (Asclepiadaceae) and Lantana camara (Verbenaceae, not shown) based on their similar floral appearance

and pollinator sharing. However, contrary to expectations, a detailed study 6 revealed that flowers of Epidendrum growing interspersed with its

presumed models were not visited more often than when growing alone, suggesting that the floral similarity between the presumed mimic and its

models is not adaptive. Possible explanations might be that (1) the importance of floral mimicry changes with time and was not picked up

during the restricted time-frame of the study; (2) that co-evolution has not yet occurred because the two rewarding species are not native to

Central America; or (3) that the floral similarity is indeed not adaptive and these species are not mimics 6 . Photographs (c) and (d) by

Paulette Bierzychudek. (e) Flowers of the orchid genus Ophrys represent a special type of floral Batesian mimicry. The flowers of Ophrys mimic

female Hymenopterans and are pollinated by the deceived males when they attempt to copulate with the labellum (pseudocopulation) 53 . This type

of pollination is known as pollination by sexual deceit. The interaction is presumed to be highly specific because Ophrys flowers need to provide

the key stimuli to elicit male mating behavior. These stimuli involve optical cues, but also tactile and olfactory stimuli. Floral volatiles imitate

the species-specific female pheromones of the Hymenoptera and are thought to be crucial because they directly act on the innate behavior of

the pollinators (Ref. 5 and references therein). Pollination in Ophrys differs in one important aspect from other examples of floral Batesian

mimicry: the phenologies of the mimics and the model only partly overlap and pollination success might drop dramatically after the

emergence of female Hymenoptera. Ophrys flowers are most attractive during the short time window after the emergence of males and before

the emergence of female Hymenoptera. Photograph (e) by Alex Widmer.

up to six weeks 29 . (M. Pfunder and B.A. Roy,

unpublished), and many orchid species also

have long-lived flowers 30,31 .

The spatial distribution of species also

influences competition for visitors and the

likelihood of pollen transfer between them 14 .

Plants that grow in intermingled clumps could

attract more visitors as a result of their com-

bined density, and the fact that each of the

individual species grows in clusters might also

increase the likelihood of proper pollen trans-

fer 13,14 . However, it is also possible that

clumped distributions might increase the

ability of the pollinators to distinguish mimic

from model and choose one over the other 32 .

Experiments are needed to determine the

relative importance of clustering in influenc-

ing pollinator behavior and to determine

whether improper pollen transfer is reduced.

Competition favors character divergence

and has thus sometimes been thought to be

antithetical to the evolution of mimicry 2,8,32 .

However, competition for visitors can lead

directly to selection favoring similarity, if one

species is favored over another, and if morphs

that have greater similarity to the preferred

species receive more visits and have higher

pollination success and fitness (positive fre-

quency-dependent selection, Fig. 1). Of course,

selection can operate independently of pheno-

typic similarity for pollinator attraction and

improper pollen transfer. For example, if vis-

itation is density-dependent, and pollinators

use visual cues for deciding where to forage,

then selection will favor the convergence of

flowers towards similar coloration, shape and

size. Simultaneously, there might also be

selection to decrease the degree of improper

pollen transfer, and, thus, differences in the

shape and length of anthers would be favored

if they contacted pollinators’ bodies in differ-

ent places 33 , or if pollen is scraped off on non-

reproductive flower parts 34 . The outcome of

simultaneous selection for visual similarity

and differential pollen placement might yield

something like the red, tubular-flowered guild

that attract hummingbirds in the southwestern

USA, in which the different species place the

pollen on hummingbirds in different places.

Indeed, this guild has been suggested to be a

Müllerian mimicry ring 12 , although not all of

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Fig. 3. Possible examples of Müllerian mimicry. (a) Costus allenii and (b) Costus laevis (Zingiberaceae) co-flower in central Panama. These

species require visitation for full seed set, and share the same pollinator ( Euglossa imperialis ), which flies indiscriminately between flowers of

the two species 7 . The flowers are nearly identical in color, morphology and nectar production, but they are nonetheless different species; the

plants differ in vegetative characters and no hybrids form between them. Furthermore, recent molecular work has established that these are not

closely related species, and thus their similarity is not the result of a close relationship (D. Schemske, pers. commun.). It is hypothesized that

low flower density, which is compounded by high levels of flower predation, combined with a density-sensitive pollinator, selected for simi-

larity between these species 7 . Unfortunately, seed set in single species versus mixed species plots has not been measured, so it is not known

whether the similarity between these species facilitates reproduction. Equal visitation rates in mixtures might not always add up to the fitness

achieved by individuals in pure patches because improper pollen transfer between species can reduce seed set 21–23,54 . Photographs (a) and (b) by

Doug Schemske. (c) Senecio integerrimus and (d) Helenium hoopesii (Asteraceae) co-flower in the Rocky mountains along with numerous other

yellow-flowered Asteraceae. The same insects visit all of these species and fly freely between them, visiting individuals in mixtures at the same

rates as they visit individuals in monospecific patches 13 . A similar pattern has also been found for two species of Potentilla ( P. fruticosa and

P. gracilis ) 13 . Unfortunately, seed set was not measured in single species and mixed species plots, so it is not known whether the similar

visitation rates in mixtures led to a similar fitness as for the single species plots. Photographs (c) and (d) by Bitty A. Roy. (e) Anemone

coronaria (Ranunculaceae) and (f) Ranunculus asiaticus (Ranunculaceae) co-flower in Israel along with red-flowered Papaver rhoeas

(Papaveraceae) and Tulipa agenensis (Liliaceae). These species might form a Müllerian mimicry ring. These taxa are primarily pollinated by

scarabaeid beetles 41 . All of the flowers in the red-flowered ‘poppy guild’ are bowl-shaped, have nearly identical color reflectance and a dark spot

at the center. Interestingly, many of the species in this guild come from families and genera in which red is not a common color. Although there

are differences in flowering phenology and in species of beetle visitors, there is considerable overlap of flowering time, and beetles do fly

between plant species. It has not been experimentally determined whether the beetles forage in a density-dependent fashion, and no one has

looked at seed set in mixed versus monospecific plots. Photographs (e) by Alex Widmer, (f) by Alexander Kocyan.

the critical tests of Müllerian mimicry sug-

gested here have been performed. Another

incompletely tested hypothesis suggests that

flowers (and fungi) might sometimes attract

visitors with visual cues, which allows the

evolution of visual similarity, but simulta-

neously produce different fragrances that

might influence insect constancy at close

range 35,36 . This fragrance mechanism, if found

to function, would be similar to mimetic but-

terfly species that converge on similar warn-

ing patterns, but which use species-specific

pheromones for mate finding.

Competition is commonly cited for causing

differences in flowering phenologies 21,37,38

(but see Ref. 39 for an alternative view).

Although species that flower at different times

will partition the available pollinators among

them, species pairs that are similar to one

another might gain an advantage early in their

flowering seasons when they overlap because

there will be no ‘lag’ period as pollinators

adjust to a new morphology 40 . This mechanism

might operate in the red-flowered, beetle-

pollinated guild in Israel 41 and in co-occurring

yellow-flowered composites 40 (Fig. 3).

Areas for future research

Although Müllerian mimicry has been sug-

gested for several species of similar appear-

ance that share pollinators, no one has performed

the crucial tests to determine whether the simi-

larity is adaptive (Fig. 3). If none of the puta-

tive cases of Müllerian mimicry is a true

example, then this suggests that improper

pollen transfer is a severe constraint on the

evolution of floral mimicry. However, we

suspect that experimental evidence will soon

establish Müllerian mimicry as a fact in the

plant world.

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The two major kinds of mimicry are

governed by different types of selection –

negative or positive frequency-dependent

selection (Fig. 1). These two kinds of selec-

tion allow us to make predictions about the

degree of morphological variation that one

should expect to see in different kinds of

mimicry systems. In Batesian floral mimicry,

where no reward is offered by the mimic, a

large amount of phenotypic variation is to

be expected because the more common

a mimetic phenotype is, the more it will

be actively avoided by pollinators 9,42 . For

Müllerian floral mimicry, the opposite is true.

Little variation in the mimetic phenotype is to

be expected because the commoner the phe-

notype is, the higher its fitness is, and this

kind of positive frequency-dependent selec-

tion ultimately leads to fixation of the most

common phenotype (Fig. 1). Although these

statements about polymorphism under the

two kinds of selection are generally expected

to be true, research on mimicry in butterflies

has found the patterns of variation to be the

opposite of expectations (reviewed in Ref. 19).

We currently have too little information on

the degree of phenotypic variation in flower

mimics to make any general statements about

patterns, although it appears that orchids

might support the predicted pattern for

Batesian mimics. Considerable morphologi-

cal variation has been reported in orchid

species that have been suggested to be

Batesian mimics (reviewed in Ref. 9). Again,

this variation is expected to be adaptive,

because variation in the mimic will reduce the

ability of pollinators to learn to avoid non-

rewarding flowers 43,44 .

Botanists lag far behind their zoological

counterparts in terms of understanding the

genetics of mimicry. We have no solid under-

standing of any traits involved in floral mim-

icry systems, and thus cannot test models

suggesting that the evolution of mimicry is a

two-step process 45 . Furthermore, there are no

tests of basic phylogenetic hypotheses con-

cerning mimicry. For example, does deceptive

pollination always evolve from reward polli-

nation systems 25,43 ? Another obvious phylo-

genetic question, as yet untested in floral

mimicry, is do species in Müllerian rings show

evidence of co-evolution?

Finally, the importance of the ‘signal per-

ceiver’ or ‘operator’ should not be forgotten in

the evolution of mimicry because the habits and

perceptual biases of the pollinators are crucial.

It is intriguing to note that many of the

pollinators implicated in potential Müllerian

mimicry systems are trapline-pollinating

euglossine bees or hummingbirds 7,12,46 . Trap-

liners (pollinators that visit the same plants

daily) frequently include many species in

a foraging bout 25 , and are sensitive to floral

density 7,46 . On the other hand, most flower

visitors of deceptive Batesian mimics in the

Mediterranean region are solitary bees 5,20,47,48 .

The more we understand about what polli-

nators perceive, the better we will be able to

identify the causes and consequences of mim-

icry. A critical issue is the degree of pattern

recognition and resolution by pollinators.

Flowers appear differently to insects than they

do to us 49,50 and different pollinators might

react to different stimuli 50,51 . We have con-

centrated on visual mimicry here, and because

we are a visually oriented species we are more

likely to observe visual mimicry. However,

we should remain aware of the possibility for

other characters, such as fragrances, to show

mimicry.

Floral mimicry is a dynamic evolutionary

process involving the perception of pollinators

and the signaling capabilities of plants and

some fungi. There is no reason to expect that

selection for mimicry will be the same from

one season to the next, or from one geographic

area to another. Experimental approaches

replicated throughout the flowering season

and across geographic ranges are required to

study floral mimicry, yet they have almost

never been applied. Thus our understanding of

floral mimicry remains in its infancy.

9 Ferdy, J.B. et al. (1998) Pollinator behavior and

deceptive pollination: learning process and floral

evolution, Am. Nat. 152, 696–705

10 Macior, L.W. (1971) Co-evolution of plants and

animals – systematic insights from plant–insect

interactions, Taxon 20, 17–28

11 Proctor, M. and Yeo, P. (1972) The Pollination of

Flowers , Taplinger, New York, USA

12 Brown, J.H. and Kodric-Brown, A. (1979)

Convergence, competition and mimicry in a

temperate community of hummingbird-pollinated

flowers, Ecology 60, 1022–1035

13 Thomson, J.D. (1981) Spatial and temporal

components of resource assessment by

flower-feeding insects, J. Anim. Ecol. 50,

49–59

14 Thomson, J.D. (1983) Component analysis of

community-level interactions in pollination

systems, in Handbook of Experimental

Pollination Biology (Jones, C.E. and Little, R.J.,

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Boiss. (Liliaceae), Oecologia 49, 229–232

21 Waser, N.M. (1978) Interspecific pollen transfer

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22 Rathcke, B. (1983) Competition and facilitation

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Acknowledgements

We appreciate the constructive comments

made by J. Shykoff, A. Dafni and the anony-

mous reviewers. This paper was supported by

a Swiss Federal Institute of Technology

(ETH) internal grant to A.W., B.A.R. and A.

Erhardt.

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