14 September 2011
Daniel Layton
BIOL 6889
Space Seminar
w/ Dr. Amy Zanne
Character Displacement: Annotated Bibliography
Introduction:
Character displacement is a biological phenomenon in which two or more
species in sympatry with similar characters (i.e. morphology, behavior, ecology, etc.)
tend to evolve in opposite directions in order to reduce mutually harmful
interactions. There are two major types of character displacement: ecological and
reproductive. Ecological character displacement occurs in response to resource
competition. Characters pertaining to resource use (e.g. jaw or beak size) and
procurement will diverge when species are in sympatry so that a single resource is
not being competed for. The two species in allopatry should thus have similar
intermediate morphologies given the lack of competition. Reproductive character
displacement occurs when there is selective pressure to reduce fitness-lowering
interspecific sexual interactions, such heterospecific gamete transfer. Therefore,
reproductive characters should be affected by this type of displacement. Proponents
argue that character displacement is widespread and may be a major factor in
adaptive radiations and speciation.
Character displacement was first clearly defined in 1956, although the idea
traces back to Darwin, and especially Lack, who studied Darwin’s finches in the first
half of the 20th century. It quickly became a popular idea and many observational
studies found patterns potentially consistent with character displacement. However,
more robust statistical analyses later suggested that most of these apparent
patterns were no different from chance. During this period, character displacement
was believed to be rare and relatively unimportant. In 1992 Schluter and McPhail
published an important list of six criteria that needed to be met in order to
convincingly tie a observed pattern to character displacement. From this point
onwards, studies tended to be more thorough and interdisciplinary in order to meet
these ‘requirements’, and experimental studies also began to emerge. There are
currently over 100 published studies on character displacement, and there seems to
once again be consensus that it is an important phenomenon, although the difficulty
of tying pattern to process remains.
Annotated Bibliography:

Adams, D. (2010). Parallel evolution of character displacement driven by
competitive selection in terrestrial salamanders. BMC Evolutionary Biology,
10, 72.
Adams addresses the possibility of multiple sympatric zones experiencing the same
morphological character displacement pressures; in other words parallel evolution
of character displacement. He examines three transects, each containing three
populations of salamanders where two are separate species in allopatry and the
third is the same two in sympatry. Data are based on the morphology of the head,
with each specimen being tied to its locality and whether or not it co-exists with
another species. Various statistical analyses, including MANOVA and PCA, are used
to analyze the data. The results suggest each replicate transect had the same
morphological differences in the same directions in the sympatric populations
versus the allopatric ones. The weakness of this paper was that it did not
convincingly demonstrate that these different morphologies were due to character
displacement and not some other factor, such as the elevation, which would have
also correlated similarly with the patterns observed. Its strength and significance
lies in its attempt to connect parallel evolution with character displacement, which
seems highly plausible and worth further investigation.

Armbruster, W.S., Edwards, M.E. & Debevec, E.M. (1994). Floral Character
Displacement Generates Assemblage Structure of Western Australian
Triggerplants (Stylidium). Ecology, 75, 315-329.
This study aims to tie species assemblage structure in a group of 31 species of plants
with character displacement. The data are floral measurements in order to
characterize niche structure, number of visits to flowers at various levels of
receptivity, location of pollen placement and pollen color. The authors find that find
that the low overlap in niche type (a conglomerate measure of column length,
column reach, and nectar tube length) is lower than that expected by chance, and
that character displacement is more likely than ecological sorting based on a null
model comparison. The strength of the paper is its broad sampling and exhaustive
modeling. The paper’s obvious weaknesses are that it does not demonstrate directly
that competition exists and it does not give enough evidence to show if pollination
morphologies are heritable, although this is likely. It’s significance lies in its
suggestion that character displacement may be a very important phenomenon in
adaptive radiations, at least in some groups.

Brown, W.L. & Wilson, E.O. (1956). Character Displacement. Systematic
Biology, 5, 49 -64.
Brown and Wilson present and define the concept of character displacement (and
its opposite: character convergence or release) as a common biological phenomenon
for the first time, citing numerous examples from their own work as well as the
literature. It addresses in particular many cases where hybridization was initially
suggested to explain convergence in allopatry, but given noticeable divergence in
sympatry, the authors believe character displacement to be a more plausible
explanation. Data are derived primarily from other studies, but also includes some
original work. Data center always around various character measurements (usually
ones related to feeding) as they interact with biogeography. Data are presented
from birds, ants, fish, frogs, beetles, and crabs. The authors find that a pattern
consistent with character displacement is common in many species in diverse
environments and geographical locales. The paper presents a strong case due to this
similar pattern having been observed frequently and diversely, but its weakness is
that pattern is emphasized and process is only speculated at, if at all. Furthermore,
data are nearly always morphological, not ecological, behavioral, etc. Nonetheless,
this paper defined the field by presenting a common biological pattern.

Grant, P.R. & Grant, B.R. (2006). Evolution of Character Displacement in
Darwin’s Finches. Science, 313, 224 -226.
Here character displacement in Geospiza finches on the island of Daphne Major in
the Galápagos is supported from start to finish by 33 years of data. It focuses
specifically on a severe drought in the presence of a new competitor that led to
strong morphological changes in the opposite direction that previous droughts had
produced. Various measures of bill dimensions, body size, diets, weather, population
size, each taken each year, comprised the data. Geospiza fortis, which initially lacked
close competitors on the island and had thus evolved a beak allowing it to be a
generalist seed eater, was later subject to competition from Geospiza magniostris, a
bird about twice as large and specializing on larger seeds. Competition produced no
measurable impact until a severe drought 22 years after the establishment of G.
magniostris, which led to nearly a full SD reduction in beak size for G. fortis due to
intense competition and high rates of starvation in both species. The huge amount of
data and the strongly significant results are very strong points. Perhaps the lack of
genetic data to back up their determinations, especially considering they are dealing
with morphologically overlapping species, can be considered a weakness. This
paper, in the words of the authors, is the first line of evidence for character
displacement “from the initial encounter of competitors to the evolutionary change
in one or more of them as a result of directional natural selection”, making it
exceedingly important for the field.

Le Gac, M. & Giraud, T. (2008). Existence of a pattern of reproductive
character displacement in Homobasidiomycota but not in Ascomycota. J. Evol.
Biol, 21, 761-772.
This paper examines the literature for evidence of potential reproductive barriers in
experimental crosses of fungi in pairs of species that are either allopatric or
sympatric. The authors consider evidence of reproductive isolation in sympatric
species as a potential corollary for reproductive character displacement. Data
include genetic distance based on Genbank resources, a reproductive isolation index
based on percentages of successful crosses, phylogenetic information, and ecological
data. The study finds that premating isolation is greater amongst sympatric species
pairs of homobasidiomycetes versus the allopatric pairs in their sample, but no such
pattern occurs in ascomycetes. This suggests some unknown trait of the former may
help to promote character divergence that the latter lacks. They also find that
reproductive isolation is correlated with genetic distance in allopatric
homobasidiomycetes, but not in sympatric species pairs. The major weakness of the
paper was a lack of investigation into character divergence itself. Identifying
reproductive isolation is only one of many criteria necessary to convincingly suggest
character displacement is taking place rather than some other phenomenon. The
paper’s strong point is it use of good genetic data and a relatively high sample size.
The fact that some life history component of a large higher grouping of fungi may be
responsible for promoting vs. repressing sympatric reproductive isolation makes
this paper significant. Whether or not particular biological groups are prone to
character displacement has been much discussed, but very rarely suggested with
evidence.

Losos, J.B. (1990). A phylogenetic analysis of character displacement in
Caribbean Anolis lizards. Evolution, 558–569.
Losos tests for character displacement (here often called ‘size adjustment’) versus
presumed competitive exclusion (or ‘size assortment’) in a genus of lizards which
have diversified on 27 islands. Specifically, he tries to explain why islands with two
species always have one large species and on small species, while islands with one
species always have an intermediately sized species. The paper marks an important
early use of phylogenetic data (based on immunology, electrophoresis, karyology,
and morphology) to answer an ecological question. These data were then analyzed
with various algorithms and statistical tests. His models support character
displacement in the northern islands but not in the south, and a separate analysis
indicates competitive exclusion played a role on all islands. Unfortunately, his
phylogeny has multiple polytomies, is based on outdated techniques, and is
compiled from multiple sources, suggesting the true phylogeny would look
substantially different if repeated with modern methods, thus changing the results
of the analyses in kind. In the discussion he acknowledges this, but argues some
evidence is better than no evidence. The paper’s strong point, as well as its
significance in the field, is its acknowledgement that current ecological conditions
alone cannot be expected to explain a fundamentally historical process; phylogeny
must be integrated.

Losos, J.B. (2000). Ecological character displacement and the study of
adaptation. Proceedings of the National Academy of Sciences, 97, 5693 -5695.
This paper summarizes the state of character displacement research, and also looks
at a case study with two species of eastern North American salamanders. The data
from the case study include morphological measurements of the jaw in allopatric
and sympatric populations and surveys of insect prey availability to demonstrate
similar resource availability in both situations. The results of this case study suggest
that competition led one species to become smaller and focus on smaller prey and
the other to become larger and focus on larger prey. The paper also argues that
character displacement studies have only recently overcome something of a
technology barrier due to the multi-disciplinary approach required to convincingly
show that character displacement has occurred. It also reviews these criteria in the
context of the case study. This paper (and moreover the corresponding study,
Adams and Rohlf 2000) is strong in that it is able to demonstrate that competition
for a limiting resource is the driver of a morphological change clearly tied to that
competition. Its weakness is it failure to incorporate genetics or show that the
morphological characters of interest are heritable. The study’s significance lies in its
correlation of what seems at first glace to be an unimportant morphological trait
with resource competition on closer inspection.

Marshall, D.C. & Cooley, J.R. (2000). Reproductive Character Displacement
And Speciation In Periodical Cicadas, With Description Of A New Species,
13‐Year Magicicada Neotredecim. Evolution, 54, 1313-1325.
Marshall and Cooley examine potential reproductive character displacement in two
species of cicada in which the decibel level of mating calls diverge when the species
are sympatric but are similar in allopatry. Data include field surveys of range
overlap, call recordings, measures of female preference, and morphological
measurements. The study finds a strong relationship between morphology and call
pitch, as well as female preference for one or the other of these calls, confirming the
presence of two species. They also find that in allopatry, the pitch of one species’ call
drops from 1.7-1.9 to 1.4-1.5 kHz, but the other species call remains constant in both
allopatry and sympatry at 1.1 kHz. Female preference co-varies male pitch changes.
The strength of this paper was simultaneous recognition of a new species coupled
with data suggesting character displacement. Sampling was also quite strong
considering the once-in-13-years opportunity to examine the species of interest.
One weakness was that the authors only had time to characterize allopatric vs.
sympatric characters in one of the two species. The paper is significant because it is
one of the few examples of character displacement in insects.

Muchhala, N. & Potts, M.D. (2007). Character displacement among batpollinated flowers of the genus Burmeistera: analysis of mechanism, process
and pattern. Proc. Biol. Sci, 274, 2731-2737.
Muchhla and Potts explore the notion that the reduction in fitness caused by
interspecific pollen transfer may be a driver of character displacement in flowering
plants. They examine bat-pollinated plants in the neotropical genus Burmeistera,
looking at the distribution of anther exertion as the character potentially being
displaced. The important data is of two types: (1) distance from the end of the
anther to the point of petal fusion for 19 species of Burmeistera encountered in 50
populations in 18 cloud forests; and (2) interspecific pollen transfer rates for a
variety of species pairs obtained using caged bats and manipulated flowers. The
cage experiments were later correlated with wild measurements. The results
support the idea that greater anther exertion differences between species reduce
interspecific pollen transfer. Comparisons with null models also indicate the mean
exertion differences are overdispersed compared with random expectations. This
paper’s strength is its combination of experimental and observational data to
demonstrate the existence of competition and character displacement. However, the
experiments are also its weakness: they do not demonstrate that significant loss of
fitness is caused by the presence heterospecific pollen transfer, however plausible
this might be. The paper is significant because it suggests that reproductive
competition may be a major driver of speciation via character divergence in
flowering plants.

Pfennig, K.S. & Pfennig, D.W. (2005). Character displacement as the “best of a
bad situation”: fitness trade-offs resulting from selection to minimize
resource and mate competition. Evolution, 59, 2200-2208.
This paper addresses the balance between potential benefits of character
displacement (i.e. reduced competition) with potential downsides (i.e. reduced
fitness) in two sympatric species of spadefoot toads. The authors aim to determine if
the two species differ in size due to character displacement, if so why, and finally
whether this has impacted the fitness of one or both species. Data include clutch size
for fitness measures, adult length for morphological character displacement
analysis, mtDNA allozymes for species identification, and survivorship numbers in
identical aquarium conditions. The study shows a significant difference in size
between the two species in sympatry as well as lower survivorship and reduced
clutch size for the smaller species. The paper’s strength lies in its combination of
observation and experimentation to attempt to answer a novel question about the
potential negative “side-effects” of character displacement. A potentially large flaw
in the study was the use of mtDNA allozymes for tadpole identification. Because
mtDNA is maternally inherited and because hybridization is known to occur
between these species, this is likely a rather poor method of identification.
Furthermore, they equate reduced clutch size with lower fitness, which is not
demonstrated. The paper is important in the field because it examines character
displacement more holistically by looking at potential negative pleiotropy. It also
introduces a limited (albeit imperfect) use of genetics to confirm tricky species
identifications.

Reifová, R., Reif, J., Antczak, M. & Nachman, M.W. (2011). Ecological character
displacement in the face of gene flow: evidence from two species of
nightingales. BMC Evol. Biol, 11, 138.
This study addresses ecological character divergence in sympatric species where
hybridization and gene flow are still occurring. The paper seeks to determine to
what degree, if any, species must be reproductively isolated before ecological
character displacement can take place. The authors use two Z-linked (i.e. sex linked
for birds) nuclear genes in order to detect hybrid males in a genetic sample, as well
as morphological measures for body and bill size. The results show that body size
converges but bill size diverges in sympatry despite evidence of at least 3%
hybridization. Controlling for latitudinal shifts in morphology, the body size
convergence is shown to be an environmental effect, while bill size divergence
remains better explained by displacement. They also find evidence of displacement
as opposed to character sorting by comparing the range of allopatric and sympatric
variation. The use of z-linked genes for haplotyping and environmental controls in
the statistical analyses were a strong point of the research. The rather crude
quantification of hybridization was a weak point; better work in this area would
have made the results much more interesting. Overall, the paper is significant
because it provides a robust observational example of character displacement
despite the fact that hybridization is known to occur.

Rice, A.M. & Pfennig, D.W. (2007). Character displacement: in situ evolution
of novel phenotypes or sorting of pre-existing variation? J. Evol. Biol, 20, 448459.
This paper asks if an invading species vs. an invaded species is more or less likely to
‘win’ during asymmetric character displacement. That is to say, when displacement
leads to mutually exclusive use of two unequal resources by two species, is one
more likely to get the better resource than the other? The authors examine two
species of spadefoot toads to attempt to answer this question. The data are 663 bp
of cytochrome b mtDNA for haplotyping, assessing genetic diversity, and
reconstructing ancestral distributions. Spea bombifrons has low haplotype and
nucleotide diversity, shows no isolation by distance in an IBD analysis, and a
coalescent-based analysis shows high population growth. S. multiplicata shows
opposite trends. This is a strong paper because of its use of population genetics, a
powerful tool underutilized in the field. The weaknesses lie in the deceptive
question it claimed to address (a study of two species cannot tell us if invaders are
more commonly ‘winners’), and its use of only 663 bp of genetic material from the
mitochondrion, which, as it were, only tells a small part of half the genetic story. The
significance of this approach is that it has the potential to bridge invasive species
biology (a study largely of the present) and speciation studies (a study largely of the
past and future), potentially leading to the ability to make predications about how
speciation might proceed given contemporary widespread introduction of invasives.

Schluter, D. (1994). Experimental Evidence That Competition Promotes
Divergence in Adaptive Radiation. Science, 266, 798 -801.
British Columbian Stickleback fishes were examined experimentally in artificial
ponds in order to provide direct experimental evidence of character displacement. A
generalist species occurring alone in nature was subjected to the presence of a
limnetic specialist, the latter naturally occurring with a benthic specialist, from
which it was believed to have separated via character displacement. The author
expected generalists with more limnetic characters to be most severely impacted by
competition with limnetic specialists. The data are experimentally derived and
consist primarily of a number of morphological measurements to assess growth rate
taken at the beginning and end of the 90-day trial. The experiment found limneticleaning generalists were most strongly affected by competition with limnetic
specialists as reflected by a much reduced growth rate in the former. The use of an
experimental approach was the paper’s strong point. Two weaknesses were the
short duration of the experiment and the fact that growth rates and not mortality
rates were shown to have been caused by competition. Nonetheless, the fact that an
experimental approach was brought to the field through this study makes it a
landmark paper.

Schluter, D. (2000). Ecological Character Displacement in Adaptive Radiation.
The American Naturalist, 156, S4-S16.
This work assesses existing research on character displacement by performing a
meta-analysis on 61 published studies. The paper also assesses progress in the field,
searches for commonalities between studies, and reviews the author’s experimental
work on stickleback fishes. The data include character ratios and displacement
symmetry ratios obtained from the literature, as well as statistics on the number of
published studies meeting six criteria laid out to assess how well character
displacement has been demonstrated. He finds that divergence is greater where
divergence is also symmetrical (i.e. affecting both competitors), that carnivores are
overrepresented in the existing studies, and that a demonstration of competition is
the most likely factor to be missing from a character displacement study. The paper
makes a thorough critique of existing work and points out the more
experimentation and demonstration of competition is needed. The focus on the
author’s own work at the expense of others could be seen as a weakness, as could
his omission of examples that counter rather than support character displacement.
The paper’s most significant contribution to the field is likely its recognition that
observation alone cannot be relied upon to convincingly demonstrate character
displacement in most cases.

Smith, R.A. & Rausher, M.D. (2008). Experimental evidence that selection
favors character displacement in the ivyleaf morning glory. Am. Nat, 171, 1-9.
Smith and Rausher examine character displacement due to reproductive
competition in plants. Because one species of morning glory (Ipomoea purpurea) can
reduce fitness in another species (I. hederacea) by producing sterile hybrid seeds
where they co-occur, the authors test with a selection analysis whether character
displacement occurs to reduce hybridization in sympatry vs. allopatry. Data include
flower number per plant, several floral measurements, and fitness values based on
seed set for two different treatments (exposed to interspecific pollen or not). The
selection analysis found directional selection in I. hederacea when it was exposed to
I. purpurea pollen, but no directional selection in its absence. Stigma position and
anther position were both selected in such a way as to potentially increase selfing
and increase anther coverage of the stigma. The well-planned experimental design
that accounted for confounding environmental factors was a strength, while the lack
of second or third generation plants in the study was a weakness. The experimental
demonstration of directional selection in plants in sympatry, but not in allopatry is
significant because previously almost all character displacement studies were
animal centered.
Conclusion:
As mentioned in the introduction, studies of character displacement have
seen a major resurgence in the last two decades. Nonetheless, much remains to be
done, and further integration of diverse methods will be the key to further
solidifying the theory. For example, population genetic approaches have only very
recently been adopted, but their explanatory power for evaluating competitive
interactions, how sympatry might have arisen, and genetic structure in sympatric
species groups is potentially huge. Phylogenetics has also been largely neglected in
observational studies of community assemblages, perhaps due to cost and time
constraints, although this should change in the future. Phylogenetics, like population
genetics, helps to get at the historical context for character displacement, which is
unknowable from direct observation alone. Finally, experimentation has only
recently been shown to be a powerful tool in the field, and surely further
experiments will serve to provide more direct evidence of character displacement
while complimenting the wealth of observational data.