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Evol Biol (2012) 39:219–230
DOI 10.1007/s11692-012-9182-7
SYNTHESIS PAPER
Interspecific Competition and Speciation in Endoparasitoids
Glen R. Hood • Scott P. Egan • Jeffrey L. Feder
Received: 10 December 2011 / Accepted: 5 April 2012 / Published online: 20 April 2012
Springer Science+Business Media, LLC 2012
Abstract Ecological speciation occurs when inherent
reproductive barriers to gene flow evolve between populations as a result of divergent natural selection. Frequency
dependent effects associated with intraspecific resource
competition are thought to be one important source of
divergent selection facilitating ecological speciation.
Interspecific competition may also play an important role
in promoting population divergence. Although evidence for
interspecific competition in nature is ubiquitous, there is
currently little empirical data supporting its role in the
speciation process. Here, we discuss two general models in
which interspecific competition among species can promote ecological speciation among populations within a
species. In both models, interspecific competition is the
source of divergent selection driving adaption to different
portions of the resource distribution, generating ecological
reproductive isolation from other conspecific populations.
We propose that the biology of endoparasitoids that attack
phytophagous insects make model systems for studying the
role of interspecific competition in ecological speciation.
We describe details for one such system, the community of
endoparasitic braconid wasps attacking Rhagoletis fruit
flies, as a potential model for investigating competitive
speciation. We conclude by hypothesizing that a model
in which interspecific competition forces an inferior
G. R. Hood (&) S. P. Egan J. L. Feder
Department of Biological Sciences, University of Notre Dame,
Notre Dame, IN 46556, USA
e-mail: [email protected]
S. P. Egan
Advanced Diagnostics and Therapeutics,
University of Notre Dame, Notre Dame, IN 46556, USA
competitor to alternative fly hosts may be a common theme
contributing to parasitoid diversification in the Rhagoletisparasitoid system.
Keywords Braconid wasps Rhagoletis Ecological
speciation Sequential speciation Cascading speciation Interspecific competition Divergent selection
Introduction
During the last 30 years, there has been increasing interest
in the role that ecology plays in population divergence and
speciation (Coyne and Orr 2004; Rundle and Nosil 2005;
Funk et al. 2006). Much of this interest has come from
empirical studies across various taxa (e.g., plants: Lowry
et al. 2008; bacteria: Rainey and Travisano 1998; phytophagous insects: Funk et al. 2002; fishes: Schluter 2003;
Bolnick and Preisser 2005), and from theoretical analyses
showing that speciation can potentially occur in the
absence of complete geographic isolation between populations (Dieckmann and Doebeli 1999; Kondrashov and
Kondrashov 1999). In these cases, ecological speciation
occurs when divergent adaptation to differences in local
environmental conditions generates reproductive isolating
barriers strong enough to overcome the homogenizing
effects of gene flow (Schluter 2000a, 2001; Rundle and
Nosil 2005). Specifically, ecological speciation is predicated on fitness tradeoffs in which a trait or characteristic
of an organism make it better adapted to one environment
and less well-suited for surviving and reproducing in
alternative habitats. As a result, migrants will perform less
well than resident individuals (Nosil et al. 2005) and
hybrids will suffer reduced fitness compared to parental
types in their respective natal habitats (Egan and Funk
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2009; Egan et al. 2011), generating ecologically based
reproductive isolation.
Divergent ecological adaptation can stem, for example,
from an organism’s quest to obtain food or nutrients, avoid
predators, attract pollinators, or survive varying environmental conditions in alternate habitats (Rundle and Nosil
2005). Intraspecific resource competition has also been
argued to be a common source for divergent selection
(Rundle and Nosil 2005). Individuals within a population
may often compete for limited resources. Thus, a trait that
gives an individual a performance advantage to better
garner resources should confer measurable fitness benefits
over others lacking the trait. When resources are discrete in
time, space, or physical characteristics such that different
suites of traits are necessary to effectively utilize alternative resources, intraspecific competition can result in the
evolution of ecologically specialized varieties or races
within species, potentially leading to speciation
(Rosenzweig 1978; Diehl and Bush 1989). Although less
intuitively obvious, theoretical (Dieckmann and Doebeli
1999; Kondrashov and Kondrashov 1999) and empirical
(Bolnick 2004; Bolnick and Lau 2008) studies have also
suggested that the same may be true when resources are
more continuously distributed. In this case, ecologically
differentiated subpopulations can evolve due to frequency
dependent effects resulting from intraspecific competition.
These differences generate fitness tradeoffs in which individuals specialized for the most commonly used and,
consequently, most depleted intermediate portion of the
resource distribution, are at a disadvantage compared to
individuals adapted to the extreme portions of the resource
distribution (Rosenzweig 1978; Bolnick 2004). If traits
involved in specialization become associated with assortative mating, then reproductive isolation can arise leading
to ecological speciation (Schluter 2001; Gavrilets 2004).
Although much of the focus on the role of resource
utilization in speciation has centered on intraspecific
competition, it has also been hypothesized that interspecific
competitors could play an important role in population
divergence (Rundle and Nosil 2005). If competition among
conspecifics can generate sufficiently strong disruptive
ecological selection pressures, then it stands to reason that
similar considerations should also apply for interspecific
taxa. However, while it is well established that interspecific
competition occurs commonly in nature (Goldberg and
Barton 1992; Gurevitch et al. 1992; Denno et al. 1995;
Bolnick and Preisser 2005; Maestre et al. 2005; Kaplan and
Denno 2007), the evidence for the involvement of interspecific competition in speciation is less clear. Here, we
present two verbal models in which frequency dependent
effects from interspecific competition can favor specialization for different aspects of the resource distribution,
potentially triggering ecological speciation. We then
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examine why documenting a role for interspecific competition in the speciation process is difficult and discuss how
endoparasitoids that attack phytophagous insects, and in
particular the community of parasitoid wasps attacking
Rhagoletis fruit flies, may be a test system for studying the
consequences of interspecific competition for speciation.
We conclude by proposing that a model in which interspecific competition between parasitoids forces an inferior
competitor to alternative hosts may be a common theme
contributing to parasitoid diversification in the Rhagoletisparasitoid system.
Competition, Divergent Selection and Speciation
The idea that competition can be an important factor facilitating speciation has a long history. In the Origin of Species,
Darwin (1859, pp. 112, 121) originally hypothesized that
intraspecific resource competition may lead to sympatric
speciation via disruptive selection (Kondrashov and
Kondrashov 1999). One of the first formal theoretical
models of ‘competitive speciation’ was constructed by
Rosenzweig (1978). In Rosenzweig’s model, frequency
dependent effects of intraspecific competition generate a
fitness landscape in which phenotypes using the more
extreme portions of the resource distribution have increased
fitness over intermediate phenotypes. Thus, a bimodal distribution of phenotypes representing two specialized subpopulations could evolve, that if coupled with a mechanism
generating prezygotic isolation (e.g., by positive assortative
mating based on phenotype or habitat preference), could
result in sympatric ecological speciation. Variations on
Rosenzweig’s theme of frequency dependent selection have
subsequently been incorporated into several theoretical
models of sympatric ecological speciation (Seger 1985;
Doebeli 1996; Johnson and Gullberg 1998; Dieckmann and
Doebeli 1999; Kondrashov and Kondrashov 1999; Doebeli
and Dieckmann 2000, 2003; Drossel and McKane 2000;
Kaneko 2002; Ackermann and Doebeli 2004; Brigatti et al.
2006; Burger et al. 2006; Pennings et al. 2008).
Empirical studies have tested predictions regarding the
frequency dependent effects of intraspecific competition
across a wide range of organisms (e.g., bacteria: Rainey
and Travisano 1998; insects: Bolnick 2001; fish: Schluter
2003). Specifically, it has been documented that (1)
extreme phenotypes have evolved in experimental laboratory studies, (2) the abundance of intermediate resources
have been found to be disproportionately depressed by
resource competition, and (3) intermediate phenotypes
have been shown to be most affected by resource competition. Together these findings are consistent with competitive speciation theory, however, no empirical study has
yet to directly tie shifts in resource utilization due to
Evol Biol (2012) 39:219–230
intraspecific competition to the evolution of reproductive
isolation and speciation.
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A
Interspecific Competition and Speciation
Ecological speciation could also potentially arise from
divergent selection caused by interspecific competition
between species. Similar to intraspecific competition, when
individuals from different taxa share phenotypic features
that cause them to overlap in their resource use, they will
compete (Roughgarden 1972; Slatkin 1980; Taper and
Case 1992; Doebeli 1996; Schluter 2000b). This can result
in ecological character displacement, in which species
diverge to utilize different aspects of the shared resource
distribution where the taxa co-occur. Thus, displacement in
one population can generate ecologically-based reproductive isolation with conspecifics elsewhere in the species
range.
We illustrate this scenario for speciation driven by
interspecific competition in Fig. 1. Species 1 and 2
co-occur in habitat 1 and overlap in their use of an essential
resource. Species 1 is also present in habitat 2, where
species 2 is absent (Fig. 1a). We note that differences
between habitats 1 and 2 can enhance ecological divergence, but it is not essential for competitive speciation.
Frequency dependent effects of interspecific competition in
habitat 1 result in species 1 evolving to use a different,
extreme portion of the resource distribution (Fig. 1b).
Figure 1c depicts the subsequent direct effects of ecological divergence for reproductive isolation. First, when
individuals from habitat 1 migrate to habitat 2, they will
suffer a fitness disadvantage compared to the residents in
habitat 2 because they are confined to a less lucrative
portion of the resource distribution. Second, individuals of
species 1 migrating from habitat 2 to habitat 1 would suffer
reduced fitness compared to residents due to competition
from species 2. Third, in the absence of dominance effects,
hybrids of intermediate phenotype would also be at a fitness disadvantage compared to parental types in both
habitats 1 and 2. In addition to these direct ecological
restrictions to gene flow, it is also possible for interspecific
competition to generate intrinsic reproductive isolation as a
pleiotropic by-product of ecological divergence if habitats
1 and 2 become geographically separated for a period of
time. In this case, new favorable mutations established in
species 1 in habitat 1 in allopatry can have negative epistatic effects on fitness in hybrids formed following secondary contact and migration between populations in
habitat 1 and 2. Whether due to direct extrinsic or inadvertent intrinsic causes, reduced fitness of hybrids can
favor the evolution of increased prezygotic isolation
B
C
D
Fig. 1 Model in which interspecific competition drives ecological
character displacement between species 1 and species 2 in habitat 1,
but not in habitat 2. Black and grey lines represent a distribution of
phenotypes for species 1 and 2 across a resource gradient. Thus
ecological displacement evolved by species 1 in habitat 1 can
generate ecological-based reproductive isolation with conspecifics
in habitat 2 upon secondary contact. See Section ‘‘Interspecific
Competition and Speciation’’ for full description
(reinforcement) between the populations in habitat 1 and 2
furthering the speciation process (Fig. 1d).
Interspecific competition can also foster ecological
divergence and speciation in a single habitat in a similar
manner to the original Rosenzweig (1978) model. In this
scenario, two species overlap in the use of a shared
resource in habitat 1 (Fig. 2a). Species 2 is competitively
superior to species 1, forcing it to adapt to the two extremes
of the resource distribution in habitat 1 (Fig. 2b). As a
result, two ecological races are formed in species 1 isolated
by both the direct effects of disruptive selection in the two
extreme resource tails and by hybrids with intermediate
phenotypes being outcompeted by species 2 (Fig. 2c).
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Evol Biol (2012) 39:219–230
A
B
C
However, it is not clear how often interspecific competition
leads to ecological speciation. At the time of their review
Rundle and Nosil (2005) stated, ‘‘… as far as we are aware
there are no direct tests, from nature or the laboratory,
linking the evolution of reproductive isolation to interspecific competition.’’
One exception may be populations of the Mexican
spadefoot toad (Spea multiplicata), which exist in the
presence and absence of a competing species, the plains
spadefoot toad (Spea bombifrons) (Pfennig and Rice 2007).
The Mexican spadefoot toad conforms to a key prediction
of interspecific competition: offspring derived from crosses
between individuals from populations with S. bombifrons
(i.e., within competitive environments) generally exhibited
higher fitness (were larger in body size) than those derived
from ‘‘hybrid’’ crosses between competitive environments
and this effect was accentuated in a high versus low
competition treatments. This is consistent with the model
depicted in Fig. 1. Thus, in this example, postmating ecological isolation appears to have arisen as a by-product of
interactions between species and molecular evidence suggests this may reduce gene flow between competitive
environments (Rice and Pfennig 2010).
Difficulties in Verifying a Role of Interspecific
Competition in Speciation
Fig. 2 Model in which interspecific competition fosters ecological
divergence and speciation in a single habitat in a similar manner to
the original Rosenzweig (1978) model. Black and grey lines represent
a distribution of phenotypes for species 1 and 2 across a resource
gradient. See Section ‘‘Interspecific Competition and Speciation’’ for
full description
Prezygotic reinforcement and eventually intrinsic reproductive isolation can evolve between the races furthering
the speciation process.
The Evidence for Interspecific Competition
The effects of interspecific competition on adaptive
divergence have been reviewed in detail elsewhere
(Gurevitch et al. 1992; Denno et al. 1995; Schluter 2000b;
Rundle and Nosil 2005). The general conclusion is that
interspecific competition is common in nature and can play
an important role in mediating species interactions and
structuring communities for a diverse range of organisms
(see Goldberg and Barton 1992 and Maestre et al. 2005 for
plants; Gurevitch et al. 1992 and Bolnick and Preisser 2005
for examples across various taxa; Denno et al. 1995 and
Kaplan and Denno 2007 for phytophagous insects).
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Why is it difficult to verify a role for interspecific competition in speciation? We contend that the difficulties are
due to (1) how current theory relates to the biology and
natural history of populations and (2) empirical difficulties
in studying competitive interactions. From a natural history
perspective, there are reasons to suspect that intraspecific
competition should be stronger than interspecific competition (Armstrong and McGhee 1980). After all, conspecific
species share a common gene pool and recent common
ancestry and are thus more phenotypically similar to one
another than heterospecific species. Consequently, conspecifics will utilize resources in more similar manner
across the entirety of niche space compared to individuals
from different species. Thus, in terms of the strength of
interactions, we might expect intraspecific competition to
be a much stronger force promoting niche diversification
and speciation than interspecific competition. Indeed,
although species may a priori overlap greatly in their use of
some resource dimensions, this may not be the case for
others. As a result, species may often co-exist with little
competitive selection pressure for ecological divergence
unless the resource dimensions they share in common are
essential for population persistence. Furthermore, when the
resources are essential and interspecific competition strong,
the consequence may be for competition to impede
Evol Biol (2012) 39:219–230
ecological speciation through the local extinction of one
species (i.e., filled niches do not allow for further species
packing) (Bengtsson 1989).
Thus, there are several biological criteria that must be
met for interspecific competition to be a potential contributor to ecological speciation. First, with respect to the
scenario for competitive speciation depicted in Fig. 1, the
resource space in habitat 1 must be large enough to allow
for both species 1 and 2 to persist. Second, the resources in
habitat 1 must be sufficiently diverse such that it cannot be
occupied and dominated competitively by pre-existing
species 2 only. Third, the resource distributions of each
species cannot be too dissimilar and at least one critical
dimension must be shared extensively for the co-occurring
species to compete. If competition is weak, then divergent
ecological selection imposed on species 1 between habitats
1 and 2 divorced from the interspecific effects of species 2
will be the primary driver of population divergence.
Fourth, fitness tradeoffs must exist if migration is occurring
between habitats such that the differing ecologies experienced by species 1 in habitats 1 and 2 cannot be reconciled
by a single phenotype and reproductive isolation evolves as
a consequence of ecological adaptation. In short, the need
for interspecific competition to be strong relative to intraspecific effects and for essential resources to be shared and
of sufficient size and complexity to allow for co-existence
and specialization may limit the opportunities for interspecific interactions to significantly contribute to ecological speciation in natural populations.
The empirical difficulties and criteria for verifying a role
for interspecific competition in ecological speciation have
been discussed by Schluter (2000a, b) and we highlight
several problems here. One difficulty is that the primary
observational pattern of ecological character displacement
used to infer interspecific competition could be due to other
causal factors besides competition. Ecological character
displacement is a pattern in which divergence between
species is greater when they co-occur together (i.e.,
sympatry = interspecific competition present) compared to
when they do not (i.e., allopatry = interspecific competition absent) (Pfennig and Pfennig 2005; Rice and Pfennig
2010). This pattern could reflect the direct consequences of
interspecific competition shifting the ecologies of species
to reduce resource overlap in the area of sympatry. However, to confirm competition as an important source of
disruptive selection, it must be shown to generate differences beyond those expected by the resource distributions
alone. Thus, environmental differences between allopatric
and sympatric sites must be controlled and accounted for,
as differences in environmental conditions in sympatry,
irrespective of the presence of the additional taxon, could
also explain a pattern of ecological character displacement.
Moreover, reinforcement could be a complicating factor
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when co-occurring species are evolutionarily closely related such that heterospecific individuals court and mate.
When interspecific matings are only partly fertile and
hybrids inviable or sterile, increased prezygotic isolation
between populations can evolve to minimize fitness loss
associated with wasted energy expended in courtship,
gamete production, and hybrids formation (Rundle and
Nosil 2005). When ecology affects the potential for crossmating, differences that evolve that appear to be due to
divergent natural selection could instead be favored as a
consequence of the increased degree of conspecific assortative mating they produce (Rundle and Nosil 2005).
Resolving these causal factors can be difficult because
selection pressures for reinforcement will coincide with
those of interspecific competition, being present in sympatry where taxa co-occur and absent in allopatry where
only one taxon is present (Schluter 2001). We hypothesize
that one possible distinguishing feature may be that interspecific competition may often be intense across all life
history stages, including juvenile stages, while ecological
reinforcement may be most pronounced for sexually
mature adults.
The above considerations make it important to obtain
independent evidence that similar phenotypes compete for
resources to verify the causal basis inferred from observational patterns of ecological character displacement
(Schluter 2000a, b). Perhaps the strongest independent
evidence can come from laboratory and field experiments
in which both conspecific and heterospecific individuals
from allopatric and sympatric study sites are reared in
different combinations under varying environmental conditions to tests for measurable effects of interspecific
competition on the resource distribution and fitness of
species (see the spadefoot toad example above). A corollary of this approach for species displaying varying degrees
of character displacement or putative ecological divergence
is that the effects of interspecific competition should
diminish for species showing more and pronounced character differences for key traits as they diverge (Prichard
and Schluter 2001; Gray and Robinson 2002).
Finally, even if interspecific competition is experimentally demonstrated, it remains to be shown that the resulting ecological displacement generated in sympatry
generates reproductive isolation from other conspecific
populations if competition is contributing to speciation.
This is a difficult task that may require a combination of
crossing and reciprocal rearing studies to verify reduced
hybrid fitness, as well as genetic surveys of natural populations. The latter would be greatly aided if (1) a mosaic of
populations with and without competitors was arrayed
across the landscape and (2) the genetic basis for traits
involved in ecological character displacement are known
and quantitative trait loci (QTL) mapped in the genome.
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If this is the case, genome scans can test the prediction that
local demes separated by comparable geographic distances
and experiencing similar competitive environments (with
or without competitors) should show higher levels of gene
flow (be more genetically similar) than demes that differ.
Moreover, effective gene flow should be reduced between
demes with and without competitors around regions of the
genome containing QTL for ecologically diverged traits
(Nosil et al. 2009).
Ideal Attributes for Study Systems
Based on the above discussion, attributes of certain systems
can make them more amenable to testing if and how
interspecific competition contributes to speciation. Ideally,
it would be convenient to work on a closed system in which
the ecology can be circumscribed by a given resource
shared by a clearly demarked group of organisms. Thus, all
the interacting players rely solely on the resource for survival and influence by outside factors is minimized. In a
closed system, competition is direct and most easily measured if it results in the death of one competitor and survival of another. Furthermore, it is important that although
the system may be closed and easily defined, the key
resource can be partitioned and is not uniformly distributed
across space, time or some other aspect of the environment.
It is also helpful when sympatric sites possessing competitors and allopatric sites lacking competitors are arrayed
in a patchwork across the landscape. This allows one to (1)
verify that predicted patterns of ecological character displacement exists, (2) conduct transplant experiments
involving relocating individuals among sites to test whether competition occurs and is associated with the key traits
displaying character displacement, and (3) perform genetic
surveys to determine if gene flow is reduced between
populations differing in competitive environments. Finally,
systems that are amendable to manipulation in the laboratory have the added benefits of controlling the competitive environment to test for fitness effects during
interspecific interactions, as well as the ability to perform
crosses to genetically map adaptive traits and assess hybrid
performance, further demonstrating ecological reproductive isolation.
Endoparasitic Insects as Models for Competitive
Speciation
Several attributes make parasitic insects (parasitoids)
model systems for testing for competitive speciation. First,
there are a large number of parasitoid species to test for
interspecific competition distributed across five different
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orders: Coleoptera, Diptera, Lepidoptera, Hymenoptera
and Neuroptera (Godfray 1994). Collectively, parasitoids
are extremely diverse, accounting for an estimated 20 % of
all insect species. One group, parasitic wasps (Hymenoptera), is particularly species-rich, comprising 20 % of all
insect parasitoids worldwide (La Salle and Gauld 1991).
Thus, documenting competitive speciation in parasitoids,
especially wasps, would imply that the process is an
important general contributor to biodiversity, at least in
terms of raw numbers of species generated.
Second, endoparasitoids spend the immature stages of
their life cycle (larval stage) internally feeding and developing to adulthood within a single host organism, typically
killing their host in the process (Godfray 1994). Thus,
parasitoids are confined to a closed resource essential for
survival constituting a closed arena for which interspecific
competition can take place. In addition, the majority of
parasitoids are host specific at the genus or species level
(Godfray 1994) and commonly overlap within individual
hosts (Hawkins and Lawton 1987). Thus, competition
cannot be easily diffused by a parasitoid using a novel
insect host in an area where overlap with other parasitoids
sharing the same primary host exists. Moreover, when
multiparasitism occurs, it is typical for only one parasitoid
to emerge victorious (Godfray 1994). Interspecific competition is therefore direct between endoparasites and has a
clear outcome. Indeed, interspecific competition has been
documented for many systems. In a literature search on
Web of Science (Thompson Reuters) using the search
terms ‘interspecific’, ‘competition’, and ‘parasitoid’, we
documented [150 empirical studies demonstrating interspecific competition between the larval stages of two or
more species of endoparasitoids attacking over 75 different
species of plant-feeding insects. Consequently, there is
little doubt that interspecific competition is common
among endoparasitoids during larval development.
Third, although the insect host is a closed system, it can
still be potentially partitioned by life stage, space, and time
to allow for ecological differentiation and competitive
speciation in endoparasitoids. Specifically, egg, larva, pupa
and adult life stages can represent different host niches for
specialization requiring different sets of characteristics
from competing species to effectively attack (Godfray
1994). Also, these life stages can vary in abundance and
vulnerability temporally and (or) spatially across an
environment.
Fourth, many endoparsitoid systems are amenable to
manipulation in the laboratory and field. This can allow for
independent experimental evidence to be obtained to
qualitatively confirm competition and for details of the
effects of competition to be quantified. For example, by
manipulating the order, life stage, or location that a host is
exposed to parasitism, one could test for the presence of a
Evol Biol (2012) 39:219–230
competitive hierarchy among endoparasites (e.g., is the first
species to parasitize a host always victorious or is there a
consistent competitive dominance of one species over
another or is one species a superior competitor in one host
life stage and inferior in others). In addition, trait values
can also be potentially varied between competitors to test if
specific characters alleviate competition between interspecific species in sympatry and generate ecological
reproductive isolation between conspecific species.
Finally, endoparasitoid species often have patchy distributions on local and regional scales. As a result, natural
and independent replicates of competing parasitoid species
exist at the population level both allopatrically and sympatrically. Spatial variation allows for comparisons to be
made of the realized niches of different species in the
presence and absence of interspecific competitors to test for
patterns of ecological character displacement. Furthermore,
allopatric and sympatric populations of species arrayed
across the landscape provide replicates to genetically test if
gene flow is reduced between populations differing in
competitive environments.
The Braconid Parasitoids of Rhagoletis Fruit Flies
Recently, we have been studying the host specific endoparasitoid wasp community (Hymenoptera: Braconidae)
that attacks Rhagoletis fruit flies (Diptera: Tephritidae) as a
potential model for testing the role of interspecific competition in speciation. The Rhagoletis-parasitoid system has
several attributes that make it amenable to study. First, flies
in the Rhagoletis pomonella complex have adaptively
radiated onto a number of different plants in North
America including hawthorn (Crataegus spp.), snowberry
(Symphoricarpos spp.), blueberry (Vaccinium spp.), flowering dogwood (Cornus florida) and silky dogwood
(Cornus amomum), forming a series of sibling species and
ecological races in the process (Bush 1966; Berlocher et al.
1993; Feder et al. 1994). Most famously, the recent shift
*150 years ago of R. pomonella from its ancestral host the
downy hawthorn (C. mollis) to introduced, domesticated
apple (Malus domestica) in the Eastern United States is
often cited as an example of sympatric speciation in action
(Feder et al. 1988). Thus, there exists a bevy of potential
host fly resources available for parasitoids to attack and
specialize on–some of which have a well-documented
recent origin–providing a number of potential examples
to test whether and how the presence or absence of parasitoid competitors affects the potential for ecological
diversification.
The second attribute is that the life cycle of each parasitoid mirrors that of their fly host. Like Rhagoletis, each
parasitoid species typically has one generation per year.
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Wasps, like flies, mate on or near their host fruit. Female
wasps will examine the surface of a host fruit with their
antennae to detect and then directly oviposit into a fly egg
or larva in the fruit (Lathrop and Newton 1933). When fruit
fall to the ground, fly larvae leave the fruit, burrow into the
soil, and pupate. The wasp egg will then hatch and the larva
will consume its host and develop inside the fly puparium.
The following summer wasps will eclose as adults. Parallels in life history translate to similarities in the ecology
between flies and parasitoids. In particular, differences in
diapause timing and host fruit odor discrimination are
important ecological adaptations involved in host plant
shifting and speciation for Rhagoletis. Diapause timing is
important because flies are univoltine and have a short life
span, thus adults must phenologically synchronize eclosion
to the availability of ripe host fruit to maximize fitness
(Feder et al. 1993, 1994). In addition, Rhagoletis use the
volatile compounds emitted from the surface of ripening
fruit as olfactory cues to locate and discriminate host plants
(Linn et al. 2003; Forbes et al. 2005). This is particularly
important as adult flies use host fruit as rendezvous sites for
mating. The parasitoids of Rhagoletis likely experience
similar divergent selection pressures on diapause life history timing and host fruit odor discrimination (for one
species, Diachasma alloeum, this has been documented;
see below). Parasitoid eclosion phenology must be synchronized with the phenology of fly development in fruits
to ensure maximum resource availability. Also, because
each species of wasp has a free living, sexual adult stage,
and mate on or near their host fruit, host odors are also
likely used to locate and discriminate host plants. Consequently, these shared characteristics highlight ecological
that are critical for host-related specialization contributing
to reproductive isolation and speciation and are candidates
for ecological character displacement.
When Rhagoletis flies shift and adapt to a new host plant
they create a new niche and opportunity for their host
specific parasitoids to follow suit and speciate in kind. If
the life cycles and ecologies of organisms are linked, and
similar characteristics are under divergent selection, speciation by one organism can drive similar diversification
of associated organisms in adjacent trophic levels in a
term coined sequential speciation. Forbes et al. (2009)
documented sequential speciation among populations of
D. alloeum, an endoparasitoid attacking flies in the
R. pomonella complex, which is diverging in parallel with
its fly host, forming genetically and ecologically diverging
incipient host races. Paralleling their fly hosts, sympatric
populations of D. alloeum attacking apple, hawthorn, and
blueberry flies differ in microsatellite allele frequencies,
diapause timing and host odor discrimination. Evidence for
sequential speciation in D. alloeum shows parasitoids can
diversify through ecological means, with the critical
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divergent selection pressures cascading up trophic levels in
the ecosystem from plant to fly to parasitoid. It remains to
be seen if similar processes are affecting the remaining
members of the parasitoid community and if ecological
divergence is being accentuated by interspecific competition. However, the possibility exists, as a clear connection
can be made between ecological adaptation and reproductive isolation for D. alloeum and competitive interactions have been documented between all three species (see
below).
The third attribute is that interspecific competition exists
for a limited resource in the larval stage of the parasitoid
life cycle. At least three genera of host specific parasitoids
attack flies in the R. pomonella complex, Utetes, Diachasmimorpha, and Diachasma (Forbes et al. 2010). Furthermore, each species attacks a different life stage of its fly
host (Table 1). Utetes oviposit into fly eggs while Diachasma and Dichasmimorpha attack 2nd and 3rd instar
larvae. Dissection and genetic analysis have indicated that
Rhagoletis flies are often parasitized by more than one
species of wasp (Lathrop and Newton 1933; G. Hood et al.
unpublished). For example, in a genetic survey of 104
hawthorn-origin flies from Fennville, MI, analyzed shortly
after puparium formation using species–specific mtDNA
markers, we found an overall parasitism rate of 65 %, with
7.5 % of hosts being multi-parasitized by at least two, and
in one case three different parasitoid species. Moreover,
only one species at most has ever been observed to eclose
from a fly puparium and upon emergence the fly pupa and
any other parasitoid rivals are completely consumed
(Lathrop and Newton 1933). Thus, there is clear evidence
for direct interactions among endoparasitoids of Rhagoletis
flies for a critical and limited resource.
How does competition manifest itself between species?
One common mechanisms of competitive interaction
between parasitoids is physical attack. Lathrop and Newton
(1933) observed that 1st instar larvae of D. alloeum (= O.
malleus) have mandibular mouthparts used for fighting.
Parasitoids with ‘fighting mandibles’ have been shown to
have a competitive advantage over species with succulent
mouthparts during direct combat (Harvey and Partridge
1987; Harvey et al. 2000; van Nouhuys and Punju 2009).
Consequently, the presence of mandibles in D. alloeum
implies that Rhagoletis parasitoids engage in direct combat
as larvae, although it remains to be determined whether
Utetes and (or) Diachasmimorpha possess mandibular
mouthparts as well.
The fourth attribute concerns the geographic distributions and host associations of Rhagoletis-attacking parasitoids. On a local scale in the Eastern U.S., surveys
Table 1 Host associations and geographic locations for each member of the Rhagoletis pomonella sibling species complex and its associated
community of braconid parasitoid wasps in the Northeastern (NE), Midwestern (MW) and Southern (S) USA
Rhagoletis species
Host plant
Common name
Attacking parasitoid spp.
Relative abundance
Location
R. pomonella
Crataegus spp.
Hawthorn
D. alloeum
High
NE, MW
D. mellea
Low
NE, MW
U. canaliculatus
Low
NE, S
U. lectoides
Low
MW
D. alloeum
High
NE, MW
D. mellea
Low
NE, MW
U. canaliculatus
Low
NE
U. lectoides
Low
MW
D. alloeum
Rare
NE
D. mellea
Medium
MW
U. canaliculatus
High
NE
D. alloeum
High
NE
D. mellea
Low
NE, Sa
R. pomonella
R. nr. pomonella
R. mendax
R. zephyria
R. cornivora
Malus pumila
Cornus florida
Vaccinium spp.
Symphoricarpos spp.
Cornus amomum
Apple
Flowering dogwood
Blueberry
Snowberry
Silky dogwood
Detailed distributions of each species are given in Forbes et al. (2010)
a
Species is rare in that specific geographic location
123
U. richmondii
Low
NE, S
D. alloeum
D. mellea
Rare
Medium
NE
NE
U. canaliculatus
High
NE
U. lectoides
Low
MW
U. canaliculatus
High
NE
Evol Biol (2012) 39:219–230
indicate a patchwork pattern of parasitism across the
landscape. At the majority of sites, D. alloeum is the most
abundant parasitoid attacking hawthorn, apple and blueberry flies, followed by Utetes canaliculatus and then
Diachasmimorpha mellea (Table 1) (Forbes et al. 2010).
This pattern suggests that D. alloeum attacking hawthorn,
apple, and blueberry flies may be competitively superior.
For related species attacking flowering dogwood, silky
dogwood, and snowberry flies, U. canaliculatus is the
numerically dominant while D. alloeum is less abundant or
absent (Table 1). On a regional level in the Southern
United States D. alloeum is uncommon (Table 1). Spatial
variation in host associations of parasitoids therefore allow
for comparisons to be made of the realized niches for
different species in the presence and absence of interspecific competitors to test for ecological character displacement.
We predict that competition should have more dramatic
effects between larval-attacking parasitoid (D. alloeum and
D. mellea) compared to egg-attacking parasitoids (Utetes).
Consistent with this prediction, on a common apple, hawthorn and blueberry host, D. alloeum predominates, while
on flowering dogwood, silky dogwood, and snowberry
flies, D. mellea is more common. In comparison, Utetes is
more uniform in its density across hosts (Table 1). Consequently, coexistence may be permitted because the host
is vulnerable at different life stages that require mutually
exclusive adaptations to parasitize. For example, adult
parasitoids attacking fly eggs must eclose earlier while
parasitoids attacking 2nd and 3rd instar larvae must eclose
later. Thus, if egg-attacking parasitoids are superior in
direct competition with larval-attacking parasitoids
because they are first to attack hosts, for example, they may
not be able to numerically supplant the larval-attacking
parasitoids due to the narrow temporal window that eggs
are vulnerable to parasitism (*48 h) (Feder 1995).
Therefore, if we are seeking to detect interspecific effects
on population divergence on a common resource as
depicted in Figs. 1 and 2, then it would seem that Diachasma and Diachasmimorpha are the best targets for study.
The structure of the egg-parasitoid community implies
that competition may preclude multiple egg-attacking
wasps from using the same host in a common area.
Three egg-attacking parasitoid species, U. canaliculatus,
U. richmondi, and U. lectoides, attack species within the
genus Rhagoletis. These include U. canaliculatus and
U. richmondi, which are sympatric across most of their
respective ranges, however, they do not overlap in
host species attacked (Forbes et al. 2010). Moreover,
U. lectoides is isolated by distance from U. canaliculatus
and U. richmondi. Thus, egg–attacking parasitoids do not
co-occur on the same host in a given geographic area,
implying that the egg resource may be too limited to
227
support multiple species. As a consequence, the absence of
other egg-attacking parasitoids may be a prerequisite for
successful host shifting and race formation in Utetes.
Despite the apparent constricting effects that competition among U. lectoides, U. canaliculatus, and U. richmondi place on diversification, it is still conceivable that
interspecific interactions among parasitoids have creative
consequences for speciation. Specifically, instead of being
limited to one fly species, the host resource may be a
bi-modal distribution of two Rhagoletis species (fly 1 and
fly 2), with fly 1 being a more optimal resource. Again,
competition excludes the inferior egg–attacking parasitoid
species 1 from the more optimal host 1 where the eggattacking parasitoid 1 and 2 overlap. However, in other
geographically areas lacking fly 2 and parasitoid species 2,
parasitoid 1 is free of competition and utilizes fly host 1
exclusively. It is therefore possible that competition played
a role in fostering divergence if the population of parasitoid
species 1 in the non-overlapping region was ancestral and
colonized the area where parasitoid species 2 is present.
Competition then forced parasitoid 1 to shift to fly host 2,
resulting in subsequent adaptive changes that potentially
reproductively isolate it from the ancestral population
attacking fly host 1. Similar considerations may also apply
to larval-attacking parasitoids. If it can be shown that (1)
Diachasmimorpha attack flies in the South where Diachasma is rare, (2) Diachasmimorpha is largely excluded by
Diachasma in the North, (3) flies attacked by Diachasmimorpha in the Northeast are either not present or not
attacked in the South, (4) adaptation to the new fly
host(s) in the Northeast generated reproductive isolation,
and (5) southern populations of Diachasmimorpha are
ancestral, competition likely played a role in host shifting
events. The latter point is important because it is also
possible that Diachasmimorpha form the North migrated
southward and took advantage of the open fly resource
niche in that area. In this case, rather than competition
fostering speciation, it was the release from interspecific
competition that allowed for divergence.
Blueprint for Future Studies
Details of the Rhagoletis-parasitoid system provide good
evidence that interspecific competition is occurring for a
limited resource. Support also exists for sequential host
race formation and speciation in Diachasma alloeum
(Forbes et al. 2009). Thus, differential ecological adaptation to Rhagoletis hosts can drive diversification at the
higher trophic level. It remains to be seen if similar cascading ecological considerations apply to Utetes and
Diachasmimorpha. This will require genetic surveys and
tests for diapause and host odor discrimination behaviors to
123
228
Evol Biol (2012) 39:219–230
confirm the existence of ecologically specialized parasitoid
taxa attacking different Rhagoletis hosts. If sequential
divergence is found throughout the parasitoid community,
then the next issue is to assess if interspecific competition
played a role in facilitating the observed patterns of
adaptive radiation. To accomplish this, we need to expand
mtDNA analysis to accurately quantify levels of interspecific competition (e.g., what proportion of flies are multiply
parasitized by different species) and whether a competitive
hierarchy exists among taxa. Presently, the major attribute
lacking for the Rhagoletis-parasitoid system is that we
cannot rear large numbers of the parasitoids in the laboratory to perform manipulative experiments. While we are
working on improving this aspect of parasitoid husbandry,
related Diachasmimorpha and Utetes species can be reared
in mass on the Mexican fruit fly, Anastrepha ludens
(Ovruski et al. 2000). Thus, it is possible to conduct
manipulative rearing experiments on related species to
assess several assumptions outlined above. Surveys will
then be required to determine whether ecological character
displacement is occurring through comparisons of sites
where competitors are both allopatric and sympatric. In this
regard, aspects of the natural history and distributions of
Diachasma, Diachasmimorpha, and Utetes suggest that
subdivision of a shared host resource may not be the only
or primary means by which interspecific competition is
fostering divergence. In addition, it is possible that competition between species attacking the same life stage of a
shared host exerts selection pressures on the inferior species to shift and adapt to a secondary Rhagoletis host that is
not utilized. Thus, interspecific competition may constrain
diversity within fly hosts, but still acts creatively by forcing
radiation of parasitoids onto alternative fly hosts locally.
Testing this hypothesis will entail confirming that populations attacking alternate hosts represent evolutionarily
derived populations that are genetically differentiated and
owe their reproductive isolation to ecological adaptations
resulting from host shifts imposed upon them by competitors present on the ancestral host. Finally, intraspecific
crosses can also be performed with the related species
described above to allow for genetic analysis and marker
mapping. While not ideal, the ability to experimentally
and genetically manipulate species related to Rhagoletisattacking parasitoids will produce results relevant to
discerning the role interspecific competition plays in
ecological speciation.
Denno et al. 1995; Bolnick and Preisser 2005; Maestre et al.
2005; Kaplan and Denno 2007). These ideas have influenced
the longstanding view that, given the proper set of ecological
conditions, intraspecific competition can facilitate speciation (Rundle and Nosil 2005). However, it is not definitively
established whether interspecific competition plays a significant role in creating new biodiversity by fostering ecological divergence and speciation. While empirical studies
have supported patterns of ecological character displacement driven by interspecific interactions (Pfennig and
Pfennig 2009), to confirm that competition is an important
source of divergent selection driving ecological differentiation, it must be shown to generate differences beyond those
expected by the resource distributions alone. Moreover, this
accentuation of ecological differentiation must be linked to
the evolution of reproductive isolation to confirm competitive speciation. It is the latter connection that has not been
convincingly made.
Herein, we contend that the host specific endoparasitoid
communities of phytophagous insect have several attributes that make them models for investigating the role that
interspecific competition plays in the speciation process.
Patterns of species overlap between members of the
endoparasitoid community that attack Rhagoletis fruit flies
imply that rather than biodiversity being generated exclusively by subdividing a shared host resource, interspecific
competition may exert its effects on speciation by forcing
taxa to shift and adapt to alternate, underused hosts in areas
of species overlap. Subsequent adaptation to the new,
derived host is the source for ecological reproductive isolation in this scenario. This hypothesis can be tested, but
will require the application of a combination of field, laboratory, and genetic approaches to do so. Perhaps most
significantly, advances in next generation DNA sequencing
and massively parallel genotyping will allow comprehensive surveys of the genome to estimate levels of gene flow,
identify genomic regions under divergent selection and
map traits associated with ecological adaptation linking the
evolutionary responses to interspecific competition to
reproductive isolation and speciation.
Conclusions
References
Competition is common in nature and competitive interactions help shape the structure and composition of communities (Goldberg and Barton 1992; Gurevitch et al. 1992;
Ackermann, M., & Doebeli, M. (2004). Evolution of niche width and
adaptive diversification. Evolution, 58, 2599–2612.
Armstrong, R. A., & McGhee, R. (1980). Competitive exclusion.
American Naturalist, 115, 151–170.
123
Acknowledgments GRH would like to thank P. Morton for continuous support and SPE would like to thank J. L. Greene for permanent support. JLF and GRH would like to thank Mazatlan in
Pendleton, OR. Funding was provided by NSF and USDA grants
awarded to JLF and The Entomological Society of America, Sigma Xi
and The Indiana Academy of Science grants awarded to GRH.
Evol Biol (2012) 39:219–230
Bengtsson, J. (1989). Interspecific competition increases local
extinction rate in a metapopulation system. Nature, 340,
713–715.
Berlocher, S. H., McPheron, B. A., Feder, J. L., & Bush, G. L. (1993).
Genetic differentiation at allozyme loci in the Rhagoletis
pomonella (Diptera, Tephritidae) species complex. Annals of
the Entomological Society of America, 86, 716–727.
Bolnick, D. I. (2001). Intraspecific competition favours niche width
expansion in Drosophila melanogaster. Nature, 410, 463–466.
Bolnick, D. I. (2004). Can intraspecific competition drive disruptive
selection? An experimental test in natural populations of
sticklebacks. Evolution, 58, 608–618.
Bolnick, D. I., & Lau, O. L. (2008). Predictable patterns of disruptive
selection in stickleback in postglacial lakes. American Naturalist, 172, 1–11.
Bolnick, D. I., & Preisser, E. L. (2005). Resource competition
modifies the strength of trait-mediated predator-prey interactions. Ecology, 86, 2771–2779.
Brigatti, E., Sa Martins, J. S., & Roditi, I. (2006). Evolution of
biodiversity and sympatric speciation through competition in a
unimodal distribution of resources. Physica A, 376, 378–386.
Burger, R., Schneider, K. A., & Willensdorfer, M. (2006). The
conditions for speciation through intraspecific competition.
Evolution, 60, 2185–2206.
Bush, G. L. (1966). The taxonomy, cytology, and evolution of the
genus Rhagoletis in North America (Diptera, Tephritidae).
Bulletin of the Museum of Comparative Zoology, 134, 431–562.
Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland, MA:
Sinauer Associates.
Darwin, C. (1859). The origin of species by means of natural selection
(1st ed.). London: Murray.
Denno, R. F., McClure, M. S., & Ott, J. R. (1995). Interspecific
interactions in phytophagous insects: competition reexamined
and resurrected. Annual Review of Entomology, 40, 297–331.
Dieckmann, U., & Doebeli, M. (1999). On the origin of species by
sympatric speciation. Nature, 400, 354–357.
Diehl, S. R., & Bush, G. L. (1989). The role of habitat preference in
adaptation and speciation. In D. Otte & J. Endler (Eds.),
Speciation and its consequences (pp. 345–365). Sunderland,
MA: Sinauer Associates.
Doebeli, M. (1996). A quantitative genetic competition model for
sympatric speciation. Journal of Evolutionary Biology, 9,
893–909.
Doebeli, M., & Dieckmann, U. (2000). Evolutionary branching and
sympatric speciation caused by different types of ecological
interactions. American Naturalist, 156, S77–S101.
Doebeli, M., & Dieckmann, U. (2003). Speciation along environmental gradients. Nature, 421, 259–264.
Drossel, B., & McKane, A. (2000). Competitive speciation in
quantitative genetic models. Journal of Theoretical Biology,
204, 467–478.
Egan, S. P., & Funk, D. J. (2009). Ecologically dependent postmating
isolation between sympatric ‘host forms’ of Neochlamisus
bebbianae leaf beetles. Proceedings of the National academy
of Sciences of the United States of America, 106, 19426–19431.
Egan, S. P., Janson, E. M., Brown, C. G., & Funk, D. J. (2011).
Postmating isolation and genetically variable host use in
ecologically divergent host forms of Neochlamisus bebbianae
leaf beetles. Journal of Evolutionary Biology, 24, 2217–2229.
Feder, J. L. (1995). The effects of parasitoids on sympatric host races
of Rhagoletis pomonella (Diptera: Tephritidae). Ecology, 76,
801–813.
Feder, J. L., Chilcote, C. A., & Bush, G. L. (1988). Genetic
differentiation between sympatric host races of the apple maggot
fly Rhagoletis pomonella. Nature, 336, 61–64.
229
Feder, J. L., Hunt, T. A., & Bush, L. (1993). The effects of climate,
host-plant phenology and host fidelity on the genetics of apple
and hawthorn infesting races of Rhagoletis pomonella. Entomologia Experimentalis et Applicata, 69, 117–135.
Feder, J. L., Opp, S. B., Wlazlo, B., Reynolds, K., Go, W., & Spisak,
S. (1994). Host fidelity is an effective premating barrier between
sympatric races of the apple maggot fly. Proceedings of the
National academy of Sciences of the United States of America,
91, 7990–7994.
Forbes, A. A., Fisher, J., & Feder, J. L. (2005). Habitat avoidance:
Overlooking an important aspect of host-specific mating and
sympatric speciation? Evolution, 59, 1552–1559.
Forbes, A. A., Powell, T. H. Q., Stelinski, L. L., Smith, J. J., & Feder,
J. L. (2009). Sequential sympatric speciation across trophic
levels. Science, 323, 776–779.
Forbes, A. A., Hood, G. R., & Feder, J. L. (2010). Geographic and
ecological overlap of parasitoid wasps associated with the
Rhagoletis pomonella (Diptera: Tephritidae) species complex.
Annals of the Entomological Society of America, 103, 908–915.
Funk, D. J., Filchak, K. E., & Feder, J. L. (2002). Herbivorous insects:
Model systems for the comparative study of speciation ecology.
Genetica, 116, 251–267.
Funk, D. J., Nosil, P., & Etges, W. J. (2006). Ecological divergence
exhibits consistently positive associations with reproductive
isolation across disparate taxa. Proceedings of the National
academy of Sciences of the United States of America, 103,
3209–3213.
Gavrilets, S. (2004). Fitness landscapes and the origin of species. In
Monographs in population biology (Vol. 41). Princeton, NJ:
Princeton University Press.
Godfray, H. C. J. (1994). Parasitoids: Behavioral and evolutionary
ecology. Princeton, NJ: Princeton University Press.
Goldberg, D. E., & Barton, A. M. (1992). Patterns and consequences
of interspecific competition in natural communities: A review of
field experiments with plants. American Naturalist, 139,
771–801.
Gray, S. M., & Robinson, B. W. (2002). Experimental evidence that
competition between stickleback species favours adaptive character divergence. Ecology Letters, 5, 264–272.
Gurevitch, J., Morrow, L. L., Wallace, A., & Walsh, J. S. (1992). A
meta-analysis of competition in field experiments. American
Naturalist, 14, 539–572.
Harvey, J. A., Corley, L. S., & Strand, M. R. (2000). Competition
induces adaptive shifts in caste rations of a polyembryonic wasp.
Nature, 406, 183–186.
Harvey, J. A., & Partridge, L. (1987). Murderous mandibles and black
holes in hymenopteran wasps. Nature, 326, 128–129.
Hawkins, B. A., & Lawton, J. H. (1987). Species richness for
parasitoids of British phytophagous insects. Nature, 326,
788–790.
Johnson, P. A., & Gullberg, U. (1998). Theory and models of
sympatric speciation. In D. J. Howard & S. H. Berlocher (Eds.),
Endless forms: Species and speciation (pp. 79–89). New York,
NY: Oxford University Press.
Kaneko, K. (2002). Symbiotic sympatric speciation: Consequences of
interaction-driven phenotype differentiation through developmental plasticity. Population Ecology, 44, 71–85.
Kaplan, I., & Denno, R. F. (2007). Interspecific interactions in
phytophagous insects revisited: A quantitative assessment of
competition theory. Ecology Letters, 11, 841–851.
Kondrashov, A. S., & Kondrashov, F. A. (1999). Interactions among
quantitative traits in the course of sympatric speciation. Nature,
400, 351–354.
La Salle, J., & Gauld, I. D. (1991). Parasitic Hymenoptera and the
biodiversity crisis. Redia, 74, 315–334.
123
230
Lathrop, F. H., & Newton, R. C. (1933). The biology of Opius melleus
Gahan, a parasite of the blueberry maggot. Journal of Agricultural Research, 48, 143–160.
Linn, C., Feder, J. L., Nojima, S., Dambroski, H. R., Berlocher, S. H.,
& Roelofs, W. (2003). Fruit odor discrimination and sympatric
host race formation in Rhagoletis. Proceedings of the National
academy of Sciences of the United States of America, 100,
11490–11493.
Lowry, D. B., Modliszewski, J. L., Wright, K. M., Wu, C. A., &
Willis, J. H. (2008). The strength and genetic basis of
reproductive isolating barriers in flowering plants. Philosophical
Transactions of the Royal Society B, 363, 3009–3021.
Maestre, F. T., Valladares, F., & Reynolds, J. F. (2005). Is the change
of plant–plant interactions with abiotic stress predictable? A
meta-analysis of field results in arid environments. Journal of
Ecology, 93, 748–757.
Nosil, P., Funk, D. J., & Ortı́z-Barrientos, D. (2009). Divergent
selection and heterogeneous genomic divergence. Molecular
Ecology, 18, 375–402.
Nosil, P., Vines, T. H., & Funk, D. J. (2005). Perspective:
reproductive isolation caused by natural selection against
immigrants from divergent habitats. Evolution, 59, 705–719.
Ovruski, S., Aluja, M., Sivinski, J., & Wharton, R. (2000). Hymenopteran parasitoids on fruit-infesting Tephritidae (Diptera) in
Latin American and the Southern United States: Diversity,
distribution, taxanomic status and their use in fruit fly biological
control. Integrated Pest Management Reviews, 5, 81–107.
Pennings, P. S., Kopp, M., Meszena, G., Dieckmann, U., &
Hermisson, J. (2008). An analytically tractable model for
competitive speciation. American Naturalist, 171, E44–E71.
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.
Pfennig, D. W., & Rice, A. M. (2007). An experimental test of
character displacement’s role in promoting postmating isolation
between conspecific populations in contrasting competitive
environments. Evolution, 61, 2433–2443.
123
Evol Biol (2012) 39:219–230
Pfennig, K. S., & Pfennig, D. W. (2009). Character displacement:
Ecological and reproductive responses to a common evolutionary problem. The Quarterly Review of Biology, 84, 253–276.
Prichard, J. R., & Schluter, D. (2001). Declining interspecific
competition during character displacement: Summoning the ghost
of competition past. Evolutionary Ecology Research, 3, 209–220.
Rainey, P. B., & Travisano, M. (1998). Adaptive radiation in a
heterogeneous environment. Nature, 394, 69–72.
Rice, A. M., & Pfennig, D. W. (2010). Does character displacement
initiate speciation? Evidence of reduced gene flow between
populations experiencing divergent selection. Journal of Evolutionary Biology, 23, 854–865.
Rosenzweig, M. L. (1978). Competitive speciation. Biological
Journal of the Linnean Society, 10, 275–289.
Roughgarden, J. (1972). Evolution of niche width. American Naturalist, 106, 683–718.
Rundle, H. D., & Nosil, P. (2005). Ecological speciation. Ecology
Letters, 8, 336–352.
Schluter, D. (2000a). The Ecology of Adaptive Radiation. Oxford:
Oxford University Press.
Schluter, D. (2000b). Ecological character displacement in adaptive
radiation. American Naturalist, 156, S4–S16.
Schluter, D. (2001). Ecology and the origin of species. Trends in
Ecology & Evolution, 16, 372–380.
Schluter, D. (2003). Frequency dependent natural selection during
character displacement in sticklebacks. Evolution, 57,
1142–1150.
Seger, J. (1985). Intraspecific resource competition as a cause of
sympatric speciation. In P. J. Greenwood, P. H. Harvey, &
M. Slatkin (Eds.), Evolution: Essays in honour of John Maynard
Smith. Cambridge: Cambridge University Press.
Slatkin, M. (1980). Ecological character displacement. Ecology, 61,
163–177.
Taper, M., & Case, T. J. (1992). Coevolution among competitors.
Evolutionary Biology, 8, 63–109.
van Nouhuys, S., & Punju, E. (2009). Coexistence of competiting
parasitoids: Which is the fugitive and where does it hide? Oikos,
119, 61–70.