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ORIGINAL SCIENTIFIC ARTICLE
Coevolution Between Food-Rewarding Flowers
and Their Pollinators
Steven D. Johnson & Bruce Anderson
Published online: 13 January 2010
#
Springer Science+Business Media, LLC 2010
Abstract The concept of coevolution was first developed
by Darwin, who used it to explain how pollinato rs and
food-rewarding flowers involved in specialized mutualisms
could, over time, develop long tongues and deep tubes,
respectively. He famously predicted that Angraecum ses-
quipedale, a long-spurred Malagasy orchid, must be
pollinated by a hawkmoth with an exceptionally long
tongue. Darwin’s idea of a coevolutionary “race” was
championed by contemporary naturalists, including Alfred
Wallace, and a hawkmoth fitting the expected tongue-
length profile was eventually discovered in Madagascar
during the early twentieth century. However, strong
empirical support for the mech anism behind Darwin’s
coevolutionary model has been forthcoming on ly in the
past two decades . It is now established that selection often
strongly favors plants with floral tubes that exceed the
length of their pollinator’s tongues. There is also evidence
that pollinators gain an energetic benefit from having
tongues that enable them to consume most or all of the
nectar in deep tubular flowers. Alternative explanations for
the evolution of long pollinator tongues, such as evasion of
predators that use flowers as ambush sites, are considered
much less compelling and lack quantitative support.
Another important advance in coevolution research has
been the development of approaches that explicitly predict
a geographical mosaic of coevolution. The expectation that
coevolution can lead to geographical diver sification and
trait covariation among strongly interacting organisms is
strongly supported by studies of long-probos cid fly and oil-
bee pollination systems in So uth Africa. Macro- and
microevolutionary studies of pollination systems suggest
that coevolution can operate alongside other one-sided
evolutionary processes, such as shifts, in shaping plant and
pollinator traits.
Keywords Coevolutionary arms race
.
Ecotype
.
Pollination
syndrome
.
Geographic mosaic
.
Natural selection
.
Nectar
Introduction
It is widely accepted that angiosperm flowers and their
insect pollinators have influenced each other’s evolution,
but there is still considerable uncertaint y about whether or
not coevolution has been a major process in the diversifi-
cation of these groups. Coevolution is most likely when
interacting organisms have strong effects on each other’s
fitness (Thompson 1994). This c riterion is clearly met for
pollination mutualisms in which the insects that pollinate
plants also depend on them as brood sites (Thompson
1994). Classic examples of such coevolved brood-site
pollination mutualisms are the relationships between figs
and agaoinid fig-wasps and between yuccas and Tegiticula
moths (Pellmyr et al. 1996; Sakai 2002; Weiblen 2002).
More controversial has been the role of coevolution in
shaping t he relationships between plants with food-
rewarding flowers and their pollinators (Schemske 1983;
Nilsson 1998). The mai n basis for the controversy has been
the disagreement over the level of specialization in these
plant–pollinator interactions and the role of pollinator shifts
S. D. Johnson (*)
School of Biological and Conservation Sciences,
University of KwaZulu-Natal,
P. Bag X01,
Scottsville, Pietermaritzburg 3209, South Africa
e-mail: Johnsonsd@ukzn.ac.za
B. Anderson
Department of Botany and Zoology, University of Stellenbosch,
P. Bag. X1( Matieland( Stellenbosch 7602, South Africa
Evo Edu Outreach (2010) 3:32–39
DOI 10.1007/s12052-009-0192-6
versus coevolut ion in shaping traits (Wasserthal 1997;
Whittall and Hodges 2007). W hile man y plants h ave
flowers specialized for a single functional group of
pollinators, such as moths or bees, and sometimes even a
single pollinator species, it is relatively rare for insect
pollinators to specialize on flowers of a particular plant
species. This asymmetry in specialization is now well
documented by studies of networks of interactions between
flowers and their animal visitors (Vazquez and Aizen 2004).
Although this leads to an expectation of weak or diffuse
coevolution at the level of interacting species, it has been
pointed out that generalist species often interact with a
relatively small subset of species at the local site level, and
this could l ead to a comp lex geographical mosaic of
coevolutionary interactions (Thompson 1994, 2005).
In this contribution, we outline the historical development
of the idea of plant–pollinator coevolution and then discuss
recent studies of coevolution between food-rewarding flowers
and their pollinators. These examples which deal with long-
tubed flowers and long-tongued (and, in one unusual case,
long-legged) pollinators can be used to teach key concepts in
evolutionary biology, including adaptation through natural
selection, coevolution, and geographical divergence.
Darwin’s Mechanistic Model
The concept of coevolution is often attributed to Ehrlich
and Raven’s classic paper on butterflies and their larval host
plants (Ehrlich and Raven 1964). However, the original
idea can be traced to Darwin (1859, 1862). General remarks
about co-adaptation between flowers and pollinators first
appeared in the Origin, but Darwin developed the concept
more explicitly in his subsequent book on orchid pollina-
tion (Darwin 1862).
In hypothesizing how the Malagasy star orchid
(Angra ecu m sesquipedale) might have evolved its extraor-
dinarily long (c. 30 centimeters) nectar spur, Darwin (1862)
proposed the first mechanistic model of the coevolutionary
process. Although he never used the term coevolution, he did
refer to “a race in gaining length between the nectary of
Angraecum and the proboscis of certain moths” (Darwin
1862). He noticed that the Angraecum, like the local British
moth-pollinated Platanthera orchids, had nectar at the very
bottom of the long spur and that moths would require a long
proboscis in order to claim this reward. The fittest moths in a
population would then be those with long tongues that could
access the nectar in even the deepest flowers, whereas the
shorter-tongued moths would access less nectar (Fig. 1).
Thus, moths would be expected to be under strong
directional selection and should evolve greater tongue
lengths (Fig. 1). By inserting rods of different diameter into
flowers, Darwin ascertained that pollen would only be
transferred between moths and Angraecum orchids if the
moths push the thickened base of their proboscis right up
against the reproductive parts of the flower when they try to
drain the last drops of nectar from the bottom of the nectar
spur. Thus, the fittest orchids would be those with spurs that
are longer than the tongues of all the visiting moths (Fig. 1).
Orchids with spurs that are shorter than the tongues of some
visiting moths would not be effectively pollinated, as the
moths would not make sufficient contact with the reproduc-
tive parts of the flower. If, in every generation, the orchids
evolved longer spurs, moths too would have to evolve longer
tongues, and so on. This is the basis of Darwin’
s “race,”
commonly known as “escalatory coevolution,” which can
lead to the evolution of extreme traits, such as those
possessed by some flowers and their pollinators. Most
pollinators and plants do not possess such extreme traits
because the coevolutionary cycle is halted early in the
process by selective pressures which oppose continued
lengthening, for example flight constraints associated with
maneuvering an elongated proboscis.
Darwin (1862) was confident enough about the pollination
mechanism of A. sequipedale to predict the existence of its
pollinator, a hawkmoth with a tongue “capable of extension
to a length of between 10 and 11 inches [25 centimeters]!”
Darwin’s Angraecum hypothesis was championed enthusias-
tically by Alfred Wallace (1867) in his essay “Creation by
Law” written as a rebuttal of an earlier anti-evolution essay in
the same journal by the Duke of Argyll, George Douglas
Campbell. In his essay, Wallace elaborated on Darwin’s
mechanism and included an illustration which showed the
hypothetical hawkmoth in the act of pollinating the Angraecum
orchid (Fig. 2). In a personal letter to Wallace, Darwin was
generally favorable about the essay but critical about the
proportions of the moth, which has wings resembling those of
Tongue length
Tube len
g
th
Selection for longer tongues
Selection for longer tubes
Frequency
Frequency
Fig. 1 Darwin’s mechanistic model for plant–pollinator coevolution
Evo Edu Outreach (2010) 3:32–39 33
a huge flying termite: “I am glad you had the courage to take up
Angraeceum after the Duke’s attack; for I believe the principle
in this case may be widely applied. I like the Figure but I
wish the artist had drawn a better sphinx” (Darwin 1867).
Wallace’s essay was remarkable for two reasons: First, it
conveys a sophisticated understanding of the nature of
selection among individuals belonging to a normal distribution
of trait values. “The flowers most completely fertilized by
these moths being those which had the longest nectaries, there
would in each generation be on the average an increase in the
length of the nectaries, and also an average increase in the
length of the proboscis of the moths, and this would be a
necessary result from the fact that nature ever fluctuates about
a mean, or that in every generation there would be flowers
with longer and shorter nectaries, and moths with longer and
shorter probosces than the average” (p 476). Second, Wallace
actually mentions Xanthopan (Macrosila) morganii, the
species of moth that is now considered the most likely
pollinator of A. sesquipedale. Wallace was not aware of the
long-tongued Malagasy race of this hawkmoth, but he had
measured a specimen of the African mainland form in the
British M useum and found that its tongue measured
7.5 inches [18 centimeters]. Wallace (1867)wrote“That
such a moth exists in Madagascar may be safely predicted;
and naturalists who visit that island should search for it with
as much confidence as astronomers searched for the planet
Neptune,—and they will be equally successful!”
A further indication that Darwin’s prediction would
prove correct came when the naturalist Herman Müller
(1873) reported that his brother Fritz had encountered
hawkmoths in South America that had tongues as long as
30 centimeters. Although Xanthopa n morganii praedicta,
the long-tongued Malagasy form of X. morganii, was
described in 1903, direct observations of this moth
pollinating A. sequipedale in the wild are still lacking. A
specimen has been found with remains of an A. sesquipedale
pollinarium on its tongue and captive individuals have been
photographed while visiting the orchid in large flight cages
and shown to be effective pollinators under these conditions
(Wasserthal 1997). However, interactions between other
long-spurred angraecoid orchids and very long-tongued
hawkmoths in Madagascar and the African mainland are
now well documented in the wild (Nilsson et al. 1985;
Martins and Johnson 2007).
Alternative Mechanisms: The Polli nator Shift Model
Coevolution is not the only process that can account for the
evolution of long floral tubes. The most plausible alternative is
that tube length evolves when plants undergo evolutionary
shifts between different pollinators. The pollinator shift model
was developed by Verne Grant (Grant and Grant 1965)and
Ledyard Stebbins (Stebbins 1970). In this model, pollinator
shifts (utilization of different pollinators through modifica-
tion of floral traits) are induced by changes in the local
pollinator fauna, either because of expansion of a species
range or because of a change in pollinator composition over
time (Johnson 2006). In the shift model, plants adapt to
pollinators with preexisting tongue lengths (one-sided
evolution), but the mechanism of selection on corolla tube
length is usually identical to that in the Darwin model
(Fig. 1) Studies of the African Disa draconis complex of
orchids showed that spur length evolution could be explained
by shifts between pollinators (Johnson and Steiner 1997). In
his study of A. sesquipedale, Wasserthal (1997) concluded
that the pollinator shift model, rather than coevolution, could
explain the evolution of the very long spurs of this species.
Wasserthal’s rejection of the coevolution model was
based on his belief that hawkmoth tongues evolve primarily
under directional selection from ambush predators such as
spiders in flowers (Wasserthal 1997; see below). A more
compelling reason to doubt that pairwise coevolution has
shaped the Angraecum-hawkmoth system is that the orchid
is naturally rare, and if we assume that this was also the
case in historical times, then it was unlikely to have had a
strong influence on the evolution of the tongue of X. mor ganii
or any other hawkmoth (Whittall and Hodges 2007). These
uncertainties highlight the fact that coevolutionary problems
cannot be solved by studying single species at single sites
Fig. 2 Illustration of Angraecum being pollinated by a long-tongued
hawkmoth, as predicted by Darwin. From the essay Creation by Law
by Wallace (1867)
34 Evo Edu Outreach (2010) 3:32–39
and, instead, require comparative approaches that include
studies of whole guilds of interacting species across their
geographical ranges (see below).
Selection on Flower Tube Length
In a landmark test of Darwin’s mechanism of selection on
flower tube length, the Swedish pollination biologist Anders
Nilsson experimentally shortened spurs of the hawkmoth-
pollinated European orchid Platanthera bifolia. His findings
were, in accordance with Darwin’s idea, that flowers with
experimentally shortened spurs experienced lower levels of
pollen deposition and removal (Nilsson 1988). Alexandersson
and Johnson (2002) later demonstrated a positive relation-
ship between fitness (measured by the number of seeds
produced) and naturally varying corolla tube length in the
hawkmoth-pollinated Iris Gladiolus longicollis.Plantswith
shorter tubes were not effectively pollinated because of their
misma tch with the tongue lengths of the majority of
individuals of the hawkmoth pollinator Agrius convolvuli
(range in tongue length: 85–135 millimeters). Similar results
have been obtained in studies of selection on tube length in
flowers pollinated by long-proboscid flies (Johnson and
Steiner 1997; Anderson and Johnson 2008, 2009;Pauwetal.
2009). For example, mismatches in the length of the proboscis
of the fly Moegistorhynchus longirostris and the tube length
of its nectar host plant Lapeirousia anceps (Fig. 3)leadto
lowered pollination success (Pauw et al. 2009).
The general principle that selection favors flower tubes
that are longer than the tongues of animal visitors was
recently extended to interactions between long-tubed (80–
90 millimeters) flowers of the plant Centropogon nigricans
and its specialist pollinator, the long-tongued bat Anoura
fistulata (Muchhala and Thomson 2009). The tongue, which
is stored in a modified thoracic cavity, has similar dimensions
to the plant tube lengths and can be extended 1.5 times the
body length of the bat. In flight cage experiments in which
flowers were offered to Anoura bats, flowers with long tubes
received more pollen and also exported more pollen to other
flowers than did short-tubed flowers.
Selection on Pollinator Tongue Length
Long tongues have evolved in many groups of flower-
visiting animals, including hummingbirds (bill s u p to
10 centimeters), hawkmoths (tongues up to 25 centimeters),
and nemestrinid flies (tongues up to 8 centimeters), and it
seems fairly obvious that the elongation of these tongues
represents adaptation for feeding on nectar. In one of the
few demonstrations of the utility of long tongues, Pauw et
al. (2009) presented flowers singly to foragi ng nemestrinid
flies (M. longirostris) and found that individuals with
longer tongue lengths were able to drink more nectar in a
single visit to the deep-tubed flowers of the iris L. anceps.
Although this study did not include a measure of the
efficiency of feeding (nectar consumed per unit time), it did
confirm that directional selection on tongue length could
potentially occur through an energetic benefit.
As an alternativ e to the nectar access hypothesis ,
Wasserthal (1997) has argued that the evolution o f long
Fig. 3 Nemestrinid flies
M. longirostris with a tongue
length of approximately
50 millimeters probe flowers of
two morphs of L. anceps that
differ in tube length. a Long-
tubed flowers (53 millimeters)
that match the length of a fly
which has not yet fully inserted
its proboscis. b Short-tubed
flowers (28 millimeters) that are
mismatched to the proboscis of
a fly and thus receive less pollen
on stigmas (Pauw et al. 2009).
Photos: Steve Johnson
Evo Edu Outreach (2010) 3:32–39 35
tongues in flower-visiting animals has been driven by
directional selection from ambush predators in flowers. The
basis of his claim is that long-tongued hawkmoths are
generalist foragers that frequently feed on short-tubed
flowers and sometimes do so while violently swinging
their bodies from side to side, behavior which can be
triggered by the presence of spiders in flowers. He
interprets the long tongues and the behavior as traits
selected by predators. However, as was pointed out by
Nilsson (1998), naturalists who have worked on hawkmoth-
pollinated flowers seldom find any spiders large enough to
prey on hawkmoths, and so the predation avoidance
hypothesis remains unsupported by any hard evidence.
Another potential explanation for long tongues in flower-
feeding animals is that they simply reflect an allometric
relation with body size; however, several studies have
shown that the evolution of tongue lengths (and even leg
lengths) in flower-feeding anim als is not closely coupled to
body size (Steiner and Whitehead 1990; Anderson and
Johnson 2008; Pauw et al. 2009).
Geographical Patterns of Coevolution
in a Community Context
Selective pressures on pollinator tongues and tubes are not
uniform across geographic landscapes because interacting
organisms seldom have precisely overlapping distribution
ranges (Grant and Grant 1965). As a result, plants may have
different floral visitors in different populations, and floral
visitors may forage from different plant communities in
different parts of their range. For example, Gom ez et al.
(2009) found that the mustard Erysimum mediohispanicum
has very different pollinator communities in different
populations and that this accounted for differences among
the populations in selection on traits such as corolla width
and shape. Although not an example of coevolution, the
results of this study predict that coevolutionary relationships
should also have geographically variable outcomes when
community structure differs. This is an important idea which
has been developed over the last few decades by John
Thompson and his colleagues (Thompson 1994, 2005).
Community composition has been shown to influence
whether a relationship between an interacting species pair is
mutualistic, commensalistic, or antagonistic (e.g., Thompson
and Cunningham 2002). Similarly, in other pollination
relationships, it can be imagined that the strength and even
direction of selection exerted by one partner on the other
would also be dependent on community context. For
example, a community of long-tubed plants may select
strongly for pollinators with long tongues. However, a
community of mixed long- and short-tubed species may
not select very strongly for long-tongued pollinators but may
in fact select for pollinators with shorter tongues. As the
pollinators evolve shorter tongues, they may then also select
for shorter tubes in the long-tubed plant species. One
outcome of this may be a landscape where tube and tongue
lengths match each other closely in each population but
where the magnitude of morphological traits differs between
populations. This was first observed in oil-collecting bees
and the flowers that they visit (Steiner and Whitehead 1990,
1991). Oil-collecting bees such as Rediviva neliana have
long forelimbs which are used to mop up oil rewards from
the twin spurs of the genus Diascia (Scrophulariaceae) and
some orchids. When Steiner and Whitehead (1990) examined
multiple populations of the bee and various Diascia species,
they found a strong pattern of covariation between the
average foreleg length of the bees and the spur length in
Diascia populations.
Since then, even more spectacular examples of morpho-
logical covariation have been found in the tube and tongue
lengths of long-tongued flies and the flowers that they visit
(Anderson and Johnson 2008, 2009; Pauw et al. 2009). The
tongues of these flies can be many times the length of their
own bodies, and in the case of Moegistorynchus longirostris
(Fig. 3) the tongues can reach a length exceeding 85 milli-
meters. In both of these systems, the tube and tongue lengths
of interacting species show two- or three-fold variation
across the landscape but were nevertheless closely correlated
(Anderson and Johnson 2008, 2009
;Pauwetal.2009)
(Figs. 4 and 5). These results have been interpreted as
evidence to suggest that coevolution can generate geographic
diversification in the morphology of interacting species pairs
which may ultimately play an important role in the
speciation process. Coevolution may also conceivably result
in geographically divergent outcomes if abiotic factors, such
as climate, determine how far the coevolutionary process is
able to proceed.
The three pollination systems mentioned above were
good candidate systems to study coevolution because the
plants in all three speci es were dependent on a single
pollinator species in each population, and the pollinators
were all heavily dependent on these abundant plants as a
source of food. Thus it can be imagined that the process of
reciprocal selection operates. Although geographic covaria-
tion is consistent with the model of how tube–tongue length
coevolution proceeds, demonstrating geographic covariation
alone does not demonstrate that coevolution has occurred.
This is because many other processes can also give rise to the
geographic covariation of traits. If environmental factors have
exactly the same effects on tube length and tongue length
morphology, or even on other correlated body or floral traits,
then tubes and tongues could correlate with each other without
any reciprocal adaptation being involved in the process.
Environmental variables and potentially correlated morpho-
logical traits (also see Steiner and Whitehead 1990, 1991)
36 Evo Edu Outreach (2010) 3:32–39
were incorporated into the models used to explain the
geographic variation in the tongue lengths of the long-
tongued fly Prosoeca ganglbaueri and its host plant
Zaluzianskya microsiphon (Anderson and Johnson 2008).
Despite the inclusion of these additional variables, tube
length was best explained by the tongue lengths of the insect
pollinators and vice versa, which supports the coevolution
hypothesis. Furthermore, in one of these systems, the
hypothesis of local co-adaptation was supported by reciprocal
translocation experiments in which short-tubed plants trans-
located to sites with longer-tongued flies performed poorly
relative to local forms with long tubes (Anderson and Johnson
2008, 2009).
Patterns of geographic trait covariation can also arise if
one species adapts to another but not vice versa (i.e.,
unilateral evolution instead of coevolution). Perhaps the
best documented case is the guild of long-proboscid fly-
pollinated plants studied by Ande rson et al. (2005 ) and
Anderson and Johnson (2009 ). Anderson et al. (2005)
demonstrated that the long-tongued fly P. ganglbaueri was
the main poll inator of Z. microsiphon as well as the orchid
Disa nivea. One difference between these two plants is that
Z. microsiphon offers nectar rewards to its pollinators, but
D. nivea offers no rewards. In a case of floral Batesian
mimicry, D. nivea superficially resembles the rewarding
plant Z. microsiphon and in so doing deceives pollinators
into visiting it through mistaken identity. As a result, fly
pollinators gain no benefit in matching the tube lengths of
these rewardless orchids, but the orchid spurs nevertheless
match the tongues of the flies as this maximizes the
efficiency of pollen transfer (Fig. 5). Thus, although the
orchids are not directly involved in a coevolutionary race
with the flies, coevolution still affects them indirectly
because they have to keep pace with the coevolutionary
Mean fly proboscis len
g
th (mm)
10 20 30 40 50
Mean flower depth (mm)
10
20
30
40
50
60
Zaluzianskya microsiphon
Disa nivea
Fig. 5 Covariation in the length of the proboscis of the nemestrinid fly
P. ganglbaueri and two plant species that it pollinates, Z. microsiphon,
the main nectar source for the flies, and D. nivea, a nonrewarding orchid
which tracks the evolution of the fly proboscis length. Values represent
means for various populations in the Drakensberg Mountains of South
Africa (see Fig. 3). Redrawn from Anderson and Johnson (2008, 2009)
N
South
Africa
50 km
Free State
Lesotho
KwaZulu-Natal
P. ganglbaueri
Z. microsiphon
25 mm
Fig. 4 Geographical variation
in trait values for Z. microsiphon
and P. ganglbaueri.
Redrawn from Anderson
and Johnson (2008)
Evo Edu Outreach (2010) 3:32–39 37
race between the flies and other rewarding plants, leading
to identical patterns of geographic trait matching (Fig. 5).
Rewardless plants may not be the only plants tracking
the evolutionary races of others. Entire guilds of less
common plants may track coevolutionary races instead of
driving them because they are too rare to exert much
selective pressure on the pollinators. Anderson and Johnson
(2009) and Pauw et al. (2009) found local convergence of
floral morphology among unrelated plant species in the
same community. Character traits such as tube length were
more similar among different species in the same communities
than they were between different populations of the same
species. The important message from this is that trait evolution
in coevolving species can have implications for other guild
members that either track the evolution of these traits or
become incorporated into these guilds. One of us recently
argued that these pollination guilds can be interpreted as
evolving niches which drive diversification (Johnson 2010).
Macroevolution
The idea that coevolution between angiosperms and insects
led to diversification of both groups has long been popular. It
was first proposed by the nineteenth century French paleon-
tologist Gaston de Saporta who argued that “insects and plants
have therefore been simultaneously cause and effect through
their connection with each other” (cited in Friedman 2009).
De Saporta’s hypothesis was enthusiastically endorsed by
Darwin in letters that he wrote to de Saporta and Hooker
towards the end of his life (Friedman 2009).
Studies suggest that plant diversification has indeed been
stimulated by interactions with animal pollinators (Dodd et al.
1999). The radiation of angiosperms does not appear to have
accelerated the origins of higher taxa of flower-feeding
insects (Labandeira and Sepkoski 1993), but it would be
hard not to accept that the species-level diversification of
some insects groups such as bees was stimulated by the
expanding availability of angiosperm floral niches, as shown
in the elegant studies of oil-bees by Steiner and Whitehead
(1990, 1991).
Studies which have traced the evolution of floral traits
using phylogenies of particular plant groups suggest that
shifts between different pollinators, rather than coevolution
with them, has been the main driver of diversification. In
Aquilegia, the direction of floral spur length evolution has
been from short to long and was associated with shifts from
bee to hummingbird to hawkmoth pollination throu gh time
(Whittall and Hodges 2007). Furthermore, the divergence
has been very recent, suggesting that Aquilegia species
adapted to pollinators with preexisting trait values.
Both the coevolution and pollinator shift models are
often misunderstood to imply that selection will always
occur in the direction of more extreme traits, but reversals
are a well-known aspect of floral macroevolution (Stebbins
1970). Evolutionary transitions from long to short er floral
tubes are evident in many plant groups, including Angraecum
and its allies where it is associated with shifts from
hawkmoth to bird pollination (Micheneau et al. 2008,
2009). This macroevolutionary pattern is supported by
microevolutionary evidence that selection can favor shorter
flowers tubes when the current pollinators have short tongues
(Bloch and Erhardt 2008)
Conclusions
Studies carried out over the past two decades have
confirmed both Darwin’s mechanism for pollinator-
mediated selec tion on tube length in flowers and the
concept of a geographic mosaic of coevolution between
pollinators and plants wi th food-r ewarding flowers. These
studies, alongside others dealing with brood-site pollination
mutualisms (Pellmyr et al. 1996; Weiblen 2002)and
antagonistic (interactions in which one partner is harmed)
seed-predation systems (Toju and Sota 2006), confirm that
coevolution can be an important d river of phenotypic
divergence among populations of strongly interacting species.
Coevolution (two-sided evolut ion) and pollinator shifts
(one-sided evolution) have been viewed as alternative
explanations for the evolution of floral trai ts (Wasserthal
1997; Nilsson 1998; Whittall and Hodges 2007). However,
traits of species that show strong reciprocal interactions
over long periods of time may be shaped largely by
coevolution, while evolution is probably largely one-sided
in the case of nonrewarding guild members or rewarding
species that are either naturally rare or which have made
recent shifts into established guilds (Johnson and Steiner
1997; Anderson and Johnson 2009; Pauw et al. 2009). Thus
it seems that coevolution can operate alongside other one-
sided evolutionary processes to shape the traits of interact-
ing species.
References
Alexandersson R, Johnson SD. Pollinator mediated selection on flower-
tube length in a hawkmoth-pollinated Gladiolus (Iridaceae). Proc R
Soc B. 2002;269:631–6.
Anderson B, Johnson SD. The geographical mosaic of coevolution in
a plant–pollinator mutualism. Evolution. 2008;62:220–5.
Anderson B, Johnson SD. Geograp hical covariation and local
convergence of flower depth in a guild of fly-pollinated plants.
New Phytol. 2009;182:533–40.
Anderson B, Johnson SD, Carbutt C. Exploitation of a specialized
mutualism by a deceptive orchid. Am J Bot. 2005;92:1342–9.
Bloch D, Erhardt A. Selection toward shorter flowers by butterflies whose
probosces are shorter than floral tubes. Ecology. 2008;89:2453–60.
38 Evo Edu Outreach (2010) 3:32–39
Darwin C. On the origin of species by means of natural selection or the
preservation of favoured races in the struggle for life. London: John
Murray; 1859.
Darwin CR. On the various contrivances by which British and foreign
orchids are fertilized by insects, facsimile edn. London: John
Murray; 1862.
Darwin C (1867) Letter 5648—Darwin, C. R. to Wallace, A. R., 12–13 Oct.
http://www.darwinproject.ac.uk/entry-5648. Accessed 4 Jan 2010.
Dodd ME, Silvertown J, Chase MW. Phylogenetic analysis of trait
evolution and species diversity variation among angiosperm
families. Evolution. 1999;53:732–44.
Ehrlich PR, Raven PH. Butterflies and plants: a study in coevolution.
Evolution. 1964;18:586–608.
Friedman WE. The meaning of Darwin’s “abominable mystery”.AmJ
Bot. 2009;96:5–21.
Gomez JM, Perfectti F, Bosch J, Camacho JPM. A geographic
selection mosa ic in a generalized plant–pollinator-herbivore
system. Ecol Monogr. 2009;79:245–63.
Grant V, Grant KA. Flower pollination in the Phlox family. New York:
Columbia University Press; 1965.
Johnson SD. Pollinator-driven speciation in plants. In: Harder LD,
Barrett SCH, editors. The ecology and evolution of flowers.
Oxford: Oxford University Press; 2006. p. 295–310.
Johnson SD. The pollination niche and its role in the diversification
and maintenance of the southern African flora. Phil Trans R Soc
B. 2010;365:499–516.
Johnson SD, Steiner KE. Long-tongued fly pollination and evolution
of floral spur length in the Disa draconis complex (Orchidaceae).
Evolution. 1997;51:45–53.
Labandeira CC, Sepkoski JJ. Insect diversity in the fossil record.
Science. 1993;261:310–5.
Martins DJ, Johnson SD. Hawkmoth pollination of aerangoid orchids
in kenya, with special reference to nectar sugar concentration
gradients in the floral spurs. Am J Bot. 2007;94:650–9.
Micheneau C, Carlsward BS, Fay MF, Bytebier B, Pailler T, Chase
MW. Phylogenetics and biogeography of Mascarene angraecoid
orchids (Vandeae, Orchidaceae). Mol Phylogenet Evol.
2008;46:908–22.
Micheneau C, Johnson SD, Fay MF. Orchid pollination: From Darwin
to the present day. Bot J Linn Soc. 2009;161:1–19.
Muchhala N, Thomson JD. Going to great lengths: selection for long
corolla tubes in an extremely specialized bat-flower mutualism.
Proc R Soc B-Biol Sci. 2009;276:2147–52.
Müller H. Proboscis capable of sucking the nectar of Angraecum
sesquipedale. Nature. 1873;8:223.
Nilsson LA. The evolution of flowers with deep corolla tubes. Nature.
1988;334:147–9.
Nilsson LA. Deep flowers for long tongues. Trends Ecol Evol.
1998;13:259–60.
Nilsson LA, Jonsson L, Rason L, Randrianjohany E. Monophily and
pollination in Anaraocum arachnites Schlrt. (Orchidaceae) in a
guild of long-tongued hawk-moths (Sphingidae) in Madagascar.
Biol J Linn Soc. 1985;26:1–19.
Pauw A, Stofberg J, Waterman RJ. Flies and flowers in Darwin
’s race.
Evolution. 2009;63:268–79.
Pellmyr O, Thompson JN, Brown JM, Harrison RG. Evolution of
pollination and mutualism in the yucca moth lineage. Am Nat.
1996;148:827–47.
Sakai S. A review of brood-site pollination mutualism: plants
providing breeding sites for their pollinators. J Plant Res.
2002;115:161–8.
Schemske DW. Limits to specialization and coevolution in p lant-
animal mutualisms. In: Nitecki MH, editor. Coevolution. Chicago:
University of Chicago Press; 1983. p. 67–109.
Stebbins GL. Adaptive radiation of reproductive characteristics in
angiosperms. I. Pollination mechanisms. Annu Rev Ecol Syst.
1970;1:307–26.
Steiner KE, Whitehead VB. Pollinator adaptation to oil-secreting
flowers - Redivivia and Diascia. Evolution. 1990;44:1701–7.
Steiner KE, Whitehead VB. Oil flowers and oil bees: further evidence
for pollinator adaptation. Evolution. 1991;45:1493–501.
Thompson JN. The coevolutionary process. Chicago: Chicago
University Press; 1994.
Thompson JN. The geographic mosaic of coevolution. Chicago:
University of Chicago Press; 2005.
Thompson JN, Cunningham BM. Geographic structure and dynamics
of coevolutionary selection. Nature. 2002;417:735–8.
Toju H, Sota T. Imbalance of predator and prey armament: Geographic
clines in phenotypic interface and natural selection. Am Nat.
2006;167:105–17.
Vazquez DP, Aizen MA. Asymmetric specialization: A pervasive
feature of plant–pollinator interactions. Ecology. 2004;85:1251–7.
Wallace AR. Creation by law. Q J Sci. 1867;4:470–88.
Wasserthal LT. The pollinators of the Malagasy star orchids Angraecum
sesquipedale, A. sororium and A. compactum and the evolution of
extremely long spurs by p ollinator shift. Botanica Acta.
1997;110:343–59.
Weiblen GD. How to be a fig wasp. Annu Rev Entomol. 2002;47:299–330.
Whittall JB, Hodges SA. Pollinator shifts drive increasingly long nectar
spurs in columbine flowers. Nature. 2007;447:706–U712.
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