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Character
Displacement
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Peter R Grant Princeton University, Princeton, New Jersey, USA
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Advanced
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doi:10.1038/npg.els.0001811
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Some
morphological differences between closely related species living in the
same environment have arisen by natural selection that has minimized
competition between them.
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Introduction and
Definition
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Naturalists and systematists have long
been aware of difficulties in drawing a distinction between some species.
Closely related species are almost always recognizably different where they
live together (in sympatry), yet some are scarcely distinguishable where
each occurs alone (in allopatry). Two implications of this contrast have
contributed powerfully to ideas about the speciation process. First,
speciation begins by divergence of geographically separated populations of
a single ancestral species. Second, interactions between the incipient
species when they met caused the divergence and this has permitted them to
coexist. Character displacement is the term first used to describe the
pattern of sympatric–allopatric contrasts (Brown and Wilson, 1956), and
subsequently the inferred process of divergence in sympatry from the
initial condition in allopatry (Grant, 1972). More generally,
the term is often used now for the process of coevolution of
competitors. See also: Speciation: introduction;
Speciation: allopatric; Speciation: sympatric and parapatric;
Isolating mechanisms; Coevolution
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Why would the species diverge in sympatry?
Brown and Wilson (1956) gave
two answers. Natural selection would favour the most dissimilar individuals
of the two populations if the most similar individuals suffered the
disadvantage of competition for a resource such as food, or chose a
heterospecific individual as a mate and reproduced poorly as a result. The
first, ecological character displacement, would result in a reduction in
the frequency or intensity of interspecific competition. The second,
reproductive character displacement, would result in reduction in the
frequency of interbreeding. This article discusses ecological character
displacement. See also: Species selection; Natural selection: introduction;
Hybrid zones
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Reduction in competition as a result of
natural selection has been invoked to explain differences in beak size
between sympatric bird species, and body size in a variety of animals
ranging from ants and fossil radiolarians to lizards and mammals. These
morphological characters are involved in the ecological use of the
environment. Character displacement has been modelled (e.g. Doebeli, 1996), and even with
restrictive assumptions the models have added theoretical plausibility to
the intuitive appeal of character displacement. Nevertheless, the pattern
of character displacement has been questioned on statistical grounds, and
the inferred process that gave rise to it has been criticized for a lack of
tests that reject alternative explanations. For example some general
feature of the environment may differ between sympatric and allopatric
regions in such a way as to cause the observed differences in morphology
independent of the presence or absence of a closely related species (Grant, 1972). In descriptive
field studies more than the usual amount of ecological detail is needed to
rule out alternative hypotheses for any given contrast.
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The Classical
Case of Character Displacement
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The classical example of character
displacement illustrates the simplicity of a pattern and the complexity of
interpretation. It involves two species of birds in Eurasia, a large species
of rock nuthatch, Sitta tephronota, and a smaller species, S.
neumayer (Figure 1). The species are
unusual in that they forage on the ground for seeds and arthropods in open
habitat, quite unlike their tree-dwelling relatives elsewhere. S.
neumayer occurs from Croatia to central Iran, and S.
tephronota from western Iran and Syria eastwards to the Tien Shan mountains of China. Placed side by
side, the westernmost S. neumayer and the easternmost S.
tephronota look identical, but where the two species naturally occur
together the difference in their appearance is profound; they differ
conspicuously in beak and body size. Beak size is an ecological trait in
the sense that the size of the beak determines the maximum size of food
that the bird can efficiently deal with. The two species in sympatry (but
not in allopatry) also differ conspicuously in the size of a black stripe
running through the eye. This appears to be a reproductive trait,
signalling identity in the context of courtship. See also: Reinforcement
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Figure 1
The classical case of character displacement is a pattern of enhanced
morphological difference in sympatry: two species of Eurasian rock
nuthatches differ more in beak size (and eye-stripe size) where they
occur together in sympatry (a and c) than where they occur alone in
allopatry (b and d). The species are Sitta neumayer (b, Greece; d, Iran) and Sitta
tephtonota (a, Iran; c, Russia). ...
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Drawing upon the work of Charles Vaurie, Brown and Wilson (1956)
suggested that beak sizes had been displaced in sympatry, and interspecific
competition for food was reduced or eliminated as a result. This may be
correct, but is not the only possibility. An alternative explanation is
that the difference evolved in allopatry, not in sympatry, and the
difference facilitated coexistence in sympatry. Consistent with this
alternative, there is no evidence that differences between the species in
sympatry are larger than what would be expected from a knowledge of size
variation in allopatry alone (Grant, 1972). Proceeding from
far allopatry towards the zone of sympatry, each species varies clinally in
body size and associated beak size. The species diverge as they approach
each other and this clinal variation continues without deviation into and
throughout the zone of sympatry in Iran. See also: Interspecific competition;
Variation, within species: introduction
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A further complication is added by
variation in the size of eye-stripes. Geographical variation in eye-stripe
size in each species parallels the variation in beak size, and both are
correlated to some extent with body size variation. If divergence had
occurred in sympatry, the primary target of selection may have been
eye-stripe size, reducing the chances of interbreeding. In this case beak
size and body size would have diverged as a correlated effect, a by-product
of selection on a morphological trait employed in courtship and mate
choice.
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The Classical
Case of Character Release
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The obverse of character displacement is
character release. Released from the constraints of a potential competitor,
a species on its own may undergo change by natural selection towards
occupying the niche of the missing species. This could happen, for example,
on an island that is colonized by only one of two sympatric closely related
species. Providing that the food supply of both species is present on the
island, natural selection might favour intermediate phenotypes of the one
species present to exploit the normal foods of both species. Such was the
explanation given by Lack (1947) to morphological
patterns among several Darwin’s finch species on
the Galápagos Islands. Brown and Wilson (1956) used
two of them to illustrate the principle of displacement. See also: Darwin′s finches
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The medium ground finch, Geospiza
fortis, is smaller on the island of Daphne Major in the absence of the
small ground finch, G. fuliginosa, than in its presence on the
nearby large island of Santa Cruz (Figure 2). Conversely, G. fuliginosa is larger on
the islands of Los Hermanos (Crossmans) in the absence of G. fortis
than in its presence on the nearby large island of Isabela. Modern studies
have provided some support for the character release explanation in showing
that beak sizes of the two species on the small islands are predictable
from the food supply in the absence of a competitor species (Schluter et al., 1985).
In contrast, on the large islands where both species are present, knowledge
of the food supply alone is not sufficient to make the prediction; a
knowledge of which other species are present is needed as well.
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Figure 2
The classical case of character release is a pattern of morphological
intermediacy where a species is alone. The medium ground finch (a,
Geospiza fortis) is larger than a competitor, the small ground finch (b,
G. fuliginosa) on the Galápagos island of Santa Cruz, but in the absence
of G. fuliginosa on Daphne Major island G. fortis has become intermediate
in size (c). ...
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Nevertheless, despite the simplicity of
this example there are some illuminating complexities. First, on Daphne
Major, the missing competitor G. fuliginosa is not missing after
all! It is a regular breeding species on the island, although its numbers
are extremely low. Second, there are other competitors present in the form
of cactus finches G. scandens. Their diet includes small seeds which
are the dominant component of the G. fortis diet in the dry season.
Third, G. fortis hybridizes with both of these species, although
rarely, and its small size is partly influenced by the genes it receives
from these species, especially G. fuliginosa. Finally, a third
species and potential competitor to G. fortis, should not be
ignored. The large ground finch, G. magnirostris, immigrates to the
island and feeds on the largest and hardest seeds in the dry season when
food supply is most likely to be limiting (Grant, 1999). In 1983, at the
beginning of an El Niño year of exceptional rainfall, G. magnirostris
began breeding on the island.
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During a drought from the middle of 1984
onwards G. fortis with small beaks survived better than those with
large beaks as the seed supply declined. Beak size variation being
heritable, the effects of selection were transmitted to the next generation
and evolution occurred. All of this happened because the seed supply
changed from being dominated by large seeds to being dominated by small
seeds as a result of greater production by the small-seed producing plants.
These changes are sufficient to account for natural selection, but there is
an alternative hypothesis: character displacement (Grant, 1994). G.
magnirostris consumed some of the large and hard seeds. They must have
contributed to the decline in abundance of G. fortis to some extent,
and to the selective disadvantage of the larger members of the G. fortis
population that occasionally feed on large seeds. Thus the classical
example of character release involving Darwin’s finches also
provides suggestive evidence of character displacement observed and
documented in action. See also: Adaptation and natural selection:
overview
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These and many other examples of patterns
in nature can be interpreted plausibly in terms of character displacement,
but they are inevitably accompanied by difficulties of interpretation. Some
of the difficulties can only be circumvented by experiments. The best
experiments, demonstrating a competitive and selective effect of one
species on another, have been carried out with two fish species, sticklebacks
in the genus Gasterosteus (Schluter, 1994).
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Experimental
Studies
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Two species of threespine sticklebacks
in the G. aculeatus complex occur together in several lakes in the
northwestern part of North America. They have not yet
been named. Where they occur together they are morphologically and
ecologically distinctive. One lives in open waters at depth in the benthic
zone and the other lives closer to the shore in the limnetic zone. The
benthic species is large and deep-bodied, and has a few, short gill rakers
and a wide mouth. A wide mouth is well suited to its diet of invertebrates.
The limnetic species is small and slender and has numerous long gill rakers
and a narrow mouth. The feeding apparatus is used to filter and feed on
zooplankton. Where one species lives alone in a lake, it is morphologically
and ecologically intermediate. Thus the pattern is one of character
displacement, and the theory of character displacement has an explanation
for it: competition for resources, occurring when two previously separated
species came together, gave rise to selective pressures that caused
evolutionary divergence in food-gathering traits of one or both of the
interactants. See also: Geographical variation
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Schluter (1994) tested this
hypothesis by placing a solitary species in two separated halves of an
experimental pond and adding a limnetic species to just one of the halves.
This arrangement was replicated in a second experimental pond, and was
designed to allow a comparison of the performance and fate of the solitary
species in the presence and in the absence of a presumed competitor
species. It thus recreates some of the conditions that are likely to have
occurred when the two species originally met, about 10 000–12 000
years ago. (Molecular data have the potential of confirming or refuting the
hypothesized sequence of events, but so far have lacked sufficient
resolution.)
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Growth and survival of the solitary
species were compared under experimental (limnetic species present) and
control (limnetic species absent) conditions to test for competition (Figure 3). If competition occurred and was
size-selective in its effects, then those individuals of the solitary
species most similar to the limnetic species should have suffered to a
disproportionate extent. Since there are not many solitary individuals that
are very similar to the limnetic species, Schluter increased their
frequency by adding some hybrids. This is not so artificial as it might
appear because hybridization does occur naturally, albeit infrequently, and
hybrids in nature have remarkably high fitness in terms of growth and
survival. See also: Genetics and variation in survival and
reproduction; Hybrid speciation
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Figure 3
The classical experiment of character displacement. The growth of sticklebacks
is reduced in the presence (broken line) of a competitor species compared
with their growth in the absence of competitors (solid line). The effect
of competitors is strongest on the fish that are most similar to the
competitors in morphology (large index values). ...
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Despite the low power of the statistical
tests, a clear difference between experimental and control treatments was
observed. The experiment demonstrated a density-dependent effect of
competition upon growth: the solitary phenotypes grew on average at lower
rates in the presence of the other species than in its absence. Moreover,
within the single generation of the experiment natural selection occurred.
The solitary phenotypes closest in morphology to the other species had the
most depressed growth rates. Their survival was apparently depressed as
well, although the effect was not so marked.
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The experiment was designed to isolate and
expose a possible effect of the limnetic species on the solitary species,
and succeeded in doing this. It was not designed to expose a reciprocal
effect of the solitary species upon the limnetic species. This would have
been difficult, given the large scale of the experimental ponds and the
need for two more ponds for a fully balanced experimental design.
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In demonstrating a causal link between
natural selection and the presence of an ecological competitor, the stickleback
experiment was a landmark in the study of character displacement. There is
a need to go one step further and demonstrate an evolutionary change in the
next generation in response to natural selection in the experimentally
manipulated generation. If this can be achieved, then it can be claimed
that character displacement, an evolutionary phenomenon, has been
established. Beyond that, the experiment should be repeated with a variety
of organisms to see if character displacement occurs widely among
organisms, environments and character systems, or if it is restricted by ecological
limitations or by genetic constraints on responses to selection pressures.
The full scope of character displacement in nature has yet to be
determined.
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Relation to
Adaptive Radiations
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The importance of character displacement
lies in the fact that it helps to explain how complex communities of
potential competitors develop from simple ones.
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Communities of organisms are multispecies
assemblages structured by complex patterns of energy transfer that result
from consumption and exploitation. Periodically in the history of the Earth
there have been large scale extinction events followed by the origination
and geographical spread of new taxa. Complex communities have been built up
from simple ones, partly by the evolutionary process of species
multiplication and partly by the ecological process of species
interactions. Character displacement is at the centre of these processes.
If allopatric speciation is the main mode of speciation, and coexisting
related species were once allopatric, then the crucial events leading to
coexistence in increasingly complex, species-rich communities occurred at
the time the previously separated populations made contact with each other.
Character displacement may have been a necessary ingredient for the
attainment of broad-scale sympatry. Its signature should be seen most
clearly in relatively recent adaptive radiations; assemblages of
ecologically differentiated species derived from one or a few ancestral
species living in a circumscribed region such as archipelagos or lakes (Givnish and Sytsma, 1998; Schluter, 2000). See also: Adaptive radiation
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Ecologists wonder why tropical forests are
so rich in species. Part of the answer may be that over long periods of
time unilateral or mutual evolutionary adjustments have been made by
competitors that exploit an overlapping set of resources. The adjustments
may have been small and subtle, and the competitors need not have been
closely related. Evidence of the original processes could have been
obscured by subsequent changes and lost in history. That is why the
greatest success in investigating character displacement has been achieved
not in complex arenas such as tropical rainforests but in simple systems,
such as pairs of sticklebacks in lakes, and birds and lizards on
islands. Yet character displacement is not likely to be seen everywhere in
simple systems either. At high latitudes particularly, there may not have
been sufficient time since the last glaciation disturbances for competitive
adjustments to be made. Membership of such communities may be more
determined by which species have arrived in a given area from elsewhere,
and on their ecological differences already acquired before they met, than
on any adjustments in sympatry.
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