Ecological fitting by phenotypically flexible genotypes: Implications for species associations, community assembly and evolution

Abstract

Ecological fitting is the process whereby organisms colonize and persist in novel environments, use novel resources or form novel associations with other species as a result of the suites of traits that they carry at the time they encounter the novel condition. This paper has four major aims. First, we review the original concept of ecological fitting and relate it to the concept of exaptation and current ideas on the positive role of phenotypic plasticity in evolution. Second, we propose phenotypic plasticity, correlated trait evolution and phylogenetic conservatism as specific mechanisms behind ecological fitting. Third, we attempt to operationalize the concept of ecological fitting by providing explicit definitions for terms. From these definitions, we propose a simple conceptual model of ecological fitting. Using this model, we demonstrate the differences and similarities between ecological fitting and ecological resource tracking and illustrate the process in the context of species colonizing new areas and forming novel associations with other species. Finally, we discuss how ecological fitting can be both a precursor to evolutionary diversity or maintainer of evolutionary stasis, depending on conditions. We conclude that ecological fitting is an important concept for understanding topics ranging from the assembly of ecological communities and species associations, to biological invasions, to the evolution of biodiversity.

Full text

I D E A A N D
P E R S P E C T I V E Ecological fitting by phenotypically flexible
genotypes: implications for species associations,
community assembly and evolution
Salvatore J. Agosta* and
Jeffrey A. Klemens
Department of Biology,
University of Pennsylvania,
Philadelphia, PA 19014, USA
*Correspondence: E-mail:
agosta@sas.upenn.edu
Abstract
Ecological fitting is the process whereby organisms colonize and persist in novel
environments, use novel resources or form novel associations with other species as a
result of the suites of traits that they carry at the time they encounter the novel condition.
This paper has four major aims. First, we review the original concept of ecological fitting
and relate it to the concept of exaptation and current ideas on the positive role of
phenotypic plasticity in evolution. Second, we propose phenotypic plasticity, correlated
trait evolution and phylogenetic conservatism as specific mechanisms behind ecological
fitting. Third, we attempt to operationalize the concept of ecological fitting by providing
explicit definitions for terms. From these definitions, we propose a simple conceptual
model of ecological fitting. Using this model, we demonstrate the differences and
similarities between ecological fitting and ecological resource tracking and illustrate the
process in the context of species colonizing new areas and forming novel associations
with other species. Finally, we discuss how ecological fitting can be both a precursor to
evolutionary diversity or maintainer of evolutionary stasis, depending on conditions. We
conclude that ecological fitting is an important concept for understanding topics ranging
from the assembly of ecological communities and species associations, to biological
invasions, to the evolution of biodiversity.
Keywords
Adaptation, biogeography, biological invasion, climate change, community ecology,
exaptation, fitness space, host shift, operative environment, pre-adaptation, resource
tracking.
Ecology Letters (2008) 11: 1123–1134
I N T R O D U C T I O N
Janzen (1985) coined the term !ecological fitting"to describe
the situation in which an organism interacts with its biotic
and abiotic environment in a way that appears to indicate a
shared evolutionary history, when in fact the organismal
traits relevant to the interaction evolved elsewhere and in
response to a different set of environmental conditions.
Ecological fitting was presented as a contrasting view to,
and as an appropriate null hypothesis for, the assumption
that currently observed associations among organisms are
evidence of shared evolutionary history or, more generally,
as a response to explicitly adaptationist arguments to explain
the presence of a phenotype or species in a particular
environment.
The concept of ecological fitting developed within the
historical context of concerns about what Janzen (1980)
and others (e.g. Holmes & Price 1980; Brooks 1985)
perceived as the overuse of coevolutionary arguments to
explain associations among species (Agosta 2006 and
references therein). One of Janzen"s main concerns was
that, when cases of ecological fitting occur, it will be very
difficult to distinguish them from cases of long-term
coexistence because the essential biological result, coexis-
tence and direct or diffuse interaction, is the same. Without
an understanding of ecological fitting, biologists, naive to
the true histories of organisms present in a community,
would be encouraged to invent spurious adaptive or
coevolutionary scenarios to describe interactions for which
they are not needed.
Ecology Letters, (2008) 11: 1123–1134 doi: 10.1111/j.1461-0248.2008.01237.x
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Ecological fitting was initially recognized by Janzen
(1985), and subsequently discussed by Brooks & McLennan
(2002), as being closely related to the concept of exaptation
(Williams 1966; Gould & Vrba 1982). The process by which
an existing trait is co-opted for a different function
(exaptation) is fundamentally the same as that by which an
existing genotype obtains realized fitness in a novel selective
environment (ecological fitting). Brooks & McLennan
(2002) noted that the frequency with which ecological
fitting occurs in nature depends in part on the ability of
traits to be co-opted for novel functions. Below we will
argue that the process of ecological fitting is essentially the
process of exaptation taking place on a shorter time scale
than that over which it is normally considered. Or, in other
words, that ecological fitting is the ecological case of
exaptation.
Subsequent to Janzen (1985), ecological fitting received
little attention in the ecology and evolutionary biology
literature even as the essence of the concept continued to be
implied by biologists studying species invasions and
introductions (e.g. Holway et al. 2002; Yeh & Price 2004;
Suarez et al. 2005; Strauss et al. 2006), biogeographers
debating the relative roles of dispersal and colonization vs.
vicariance (e.g. Pennington & Dick 2004), and evolutionary
biologists in discussing adaptation, !pre-adaptation"and
exaptation (see below). The term ecological fitting has
survived, however, and has been used by researchers
interested in the factors structuring species associations
(Gill 1987; White & Stiles 1992; Chenuil & McKey 1996;
Flowers & Janzen 1997; Yu & Davidson 1997; Brooks &
McLennan 2002; Janzen 2003; Agosta & Janzen 2005;
Agosta 2006; Brooks et al. 2006), whole ecosystems
(Wilkinson 2004) and even the dynamics of emerging
infectious diseases (Brooks & Ferrao 2005). Nonetheless,
there has been little attempt to operationalize the concept of
ecological fitting and incorporate it into mainstream
ecological and evolutionary theory. This is unfortunate
because ecological fitting has considerable explanatory
power (Brooks & McLennan 2002; Wilkinson 2004; Brooks
& Ferrao 2005; Agosta 2006; Brooks et al. 2006) and is a
natural null hypothesis for a range of research programmes
(e.g. any prediction of organismal form or function derived
from optimality theory; Agosta 2006).
However, we argue that ecological fitting has much
greater importance than simply acting as a null hypothesis or
null explanation in ecology and evolutionary biology. We
argue as did Janzen (1985) that ecological fitting is an
inevitable and frequent process in nature that results from
the interaction between highly flexible organisms and highly
variable biotic and abiotic environments. In what follows,
we develop a framework within which to evaluate this
assertion. We will also show how the process of ecological
fitting, whereby organisms obtain realized fitness and
establish populations under novel conditions beyond those
conditions encountered in their previous evolutionary
history, circumvents adaptive processes to produce novel
ecological interactions between organisms and the environ-
ment. These novel ecological interactions can then provide
novel selective environments (e.g. novel species associa-
tions) on which natural selection can work.
For those familiar with West-Eberhard"s (2003) recent
work, Developmental Plasticity and Evolution, the preceding
paragraph should be reminiscent of what some have termed
the !plasticity theory"of biodiversity (Janz et al. 2006;
Weingartner et al. 2006; Nylin & Wahlberg 2008). Building
on a history of ideas on the positive role of phenotypic
plasticity in evolution (e.g. the !Baldwin effect": Baldwin
1896; Robinson & Dukas 1999), West-Eberhard argues (1)
that genotypes are inherently phenotypically plastic, (2) that
this plasticity can allow genotypes (individuals) to obtain
realized fitness under novel environmental conditions and,
therefore, (3) that !…the origin and evolution of adaptive
novelty do not await mutation; on the contrary, genes are
followers, not leaders, in evolution"(p. 20). This view has
been met with some opposition. de Jong (2005) argues that
West-Eberhard"s (2003) proposed process of genetic assim-
ilation– which describes trait evolution resulting from the
initial exposure of novel phenotypic variants arising from
developmental plasticity to novel conditions – is (1) not
unique within the Darwinian synthesis if one considers
plasticity itself an evolved quantitative genetic trait and (2)
not a major avenue for trait evolution based on current
empirical or model support.
We leave the reader to delve further into these arguments.
For our purposes, we find the above issues to be largely
immaterial to West-Eberhard"s broader contribution: that
phenotypic plasticity, whether evolved or a developmental
by-product, can allow existing genotypes to obtain fitness
and therefore persist in novel environments without
awaiting novel mutations, thereby placing existing genotypes
into novel selective environments where natural selection
can potentially act. This is a fundamentally different view of
phenotypic plasticity compared to its historical role in
evolutionary thought. In this formulation, phenotypic
plasticity provides !fodder"for evolution, rather than being
merely the environmental noise that is selected against by
stabilizing selection or that drags against the efficacy of
directional selection (Stearns 1989; Thompson 1991).
The connections between recent arguments for a positive
role of phenotypic plasticity in evolution (West-Eberhard
1989, 2003; Robinson & Dukas 1999; Gorur 2004; Yeh &
Price 2004; Fordyce 2006; Janz et al. 2006; Weingartner et al.
2006; Nylin & Wahlberg 2008) and Janzen"s (1985) concept
of ecological fitting are tangible and ripe for synthesis
(Agosta 2006). This paper has four aims. First, we describe
the concept of ecological fitting and outline its basic
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premises. Second, we advance phenotypic plasticity, corre-
lated trait evolution, and phylogenetic conservatism as the
primary mechanisms that allow ecological fitting. Third, we
develop operational definitions for discussing ecological
fitting as a process by explicitly defining the terms
!environment"and !species traits"and the !environment-by-
species traits"interaction. Fourth, we derive a simple
graphical model from these definitions to illustrate the
process of ecological fitting, how it can lead to patterns
superficially indistinguishable from evolution, and how it
can, depending on circumstance, be both a promoter of
evolutionary stasis and a precursor to evolutionary diversity.
D E V E L O P M E N T O F T H E C O N C E P T O F E C O L O G I C A L
F I T T I N G
Janzen"s (1985) original formulation outlined three basic
premises of ecological fitting. First, the original, or ancestral,
range of many species is smaller than the range they
currently occupy. Second, communities have porous bor-
ders such that many of the species that comprise ecological
communities originated elsewhere and immigrated to sites
where they currently exist. Third, many species possess
!robust genotypes"that allow colonization and persistence in
this larger range without evolutionary change prior to range
expansion.
Speciation results from a sufficient amount of reproduc-
tive isolation of one or more gene pools (Mayr 1963;
Futuyma & Mayer 1980), and thus condition (1) is probably
true for many if not most species (e.g. Leigh et al. 2004). It
will obtain whenever the initial population is a relatively
small geographical or ecological isolate that evolves in
response to the cast of biotic and abiotic characters in its
ancestral environment.
Condition (2) is likewise uncontroversial in and of itself,
and is equivalent to saying that dispersal and colonization
play important roles in biogeography and community
assembly (MacArthur & Wilson 1967; Schluter & Ricklefs
1993; Hurtt & Pacala 1995; Hubbell 2001; Brooks &
McLennan 2002; Pennington & Dick 2004; Urban et al.
2008). Together, conditions (1) and (2) imply that the range
of environmental variables and the number and identity of
interacting species in the ancestral environment will be a
subset of or different from the environments experienced
and species encountered following range expansion. This, in
turn, leads to the conclusion that ecological communities are
comprised of some proportion of relatively recent arrivals
with little !deep"in situ evolutionary history. These species
carry with them a historical legacy of traits that evolved
elsewhere, and will interact with many other species with
similarly varied histories (Brooks 1985; Janzen 1985, 1986,
2003; Brooks & McLennan 2002; Agosta & Janzen 2005;
Brooks & Ferrao 2005; Agosta 2006; Brooks et al. 2006).
The third premise is that some species possess !robust
genotypes"that allow persistence across varied environ-
ments without adaptation to local conditions or to the new
species with which it interacts in the expanded range. Janzen
posited that many widespread species are in an !evolutionary
quiescent"stage of a cyclical pattern that consists of a small
population occupying an initially small area, mass selection
on this small population and abrupt expansion of the
species range when some particularly !robust genotype"is
stumbled upon in the ancestral environment. In this stage,
the species is widespread, evolutionarily static and insensi-
tive to local selective regimes because it is comprised of
many populations under myriad selective pressures that
!…are fine-scale, heterogeneous and contradictory…"(Janzen
1985:308).
Condition (3) is not as obvious as conditions (1) and (2),
and requires consideration of two questions. The first is
whether it is plausible, based on what we know about the
biology and biogeography of species, that species expand
rapidly into new ranges in the absence of local adaptation.
The second, and the subject of the next section of this
paper, is to ask whether there exist mechanisms that can
account for the development of Janzen"s!robust genotype".
One test of the plausibility of condition (3) has already
been performed. Human-mediated dispersal of species can
be considered an extreme relaxation of dispersal limitation,
and the success of invasive species is evidence that many
taxa easily persist in novel environmental conditions and
with an evolutionarily unfamiliar flora and fauna. The
!escape hypothesis", whereby invasive species are released
from the constraints imposed by coevolved parasites and
pathogens (Mitchell & Power 2003; Torchin et al. 2003),
provides a particularly instructive example. Although the
escape hypothesis is often presented so as to emphasize the
absence of species that have negative effects on the invasive
species, this is not a sufficient explanation for biological
invasions. Implicit in the escape hypothesis is that, following
release, invaders interact with entirely novel assemblages of
competitors, pollinators, dispersers, predators and prey, yet
do not seem to be hindered by a lack of past evolutionary
history with these organisms. Release from parasites and
pathogens alone cannot ensure success in a new habitat. The
robust genotype must maintain a broad ability to function
when the identities of all other species in the community
have changed.
Perhaps even more germane is Mack"s (2003) discussion
of absent life forms and community invasibility. Mack notes
that due to phylogenetic and biogeographic constraints,
natural communities do not contain the full range of life
forms observed globally. He goes on to describe a number
of cases, particularly invasions of grasslands by woody
species, where a life form previously excluded from a habitat
by dispersal limitation, in the broad biogeographic sense,
Idea and Perspective Ecological fitting 1125
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becomes invasive or even dominant in a new environment,
indicating that there was never an intrinsic biological barrier
to the species"presence in the system. For example, he asks
if South American grasslands are inherently inhospitable to
woody species, or if the absence of pines (Pinus spp.) and
other woody species adapted to xerophytic conditions
within the South American biogeographic realm has resulted
in grasslands persisting in habitats that would be quickly
colonized by woody species in conifer-rich North America.
In fact, these grasslands are currently undergoing rapid
invasion by introduced pine species (Mack 2003; see also
Stohlgren et al. 2008); a forceful demonstration of ecological
fitting in practice.
One consequence of release from dispersal limitation and
invasion of new habitats is that it adds novel members to
ecological communities, which introduces novel genetic
variation, fosters novel ecological interactions and can lead
to effects that reverberate throughout the community
(Urban et al. 2008; Whitham et al. 2008). Cases of the
incorporation of novel host plants into the diets of
phytophagous insects provide particularly instructive exam-
ples of how easily these novel ecological interactions can
form in the first place (Agosta 2006). For instance, Thomas
et al. (1987) documented the incorporation of a recently
acquired host plant into the diet of several populations of
the butterfly Euphydryas editha in California, USA. Females
normally oviposit on the native plant Collinsia parviflora
(Scrophulariaceae), but some populations also use Plantago
lanceolata (Plantaginaceae), which was introduced from
Europe in the last !100 years. Populations of E. editha
previously unexposed to P. lanceolata showed evidence that
at least some females were !pre-adaptated"to oviposit on
this novel host. Furthermore, larvae from these populations
were able to survive and develop on the novel host. The
inference was that, assuming gene flow in the study was
negligible, E. editha populations currently using P. lanceolata
initially required no evolutionary change to incorporate the
novel host into their diet. In our terms, E. editha could be
said to have possessed a relatively robust genotype that
allowed use of a novel resource for survival and reproduc-
tion at the moment of contact.
M E C H A N I S M S
Having established that something akin to Janzen"s!robust
genotypes"occur in nature, what mechanisms might give rise
to this phenomenon? Phenotypic plasticity, a seemingly
universal property of organisms (Bradshaw 1965; West-
Eberhard 1989, 2003; Schlichting & Pigliucci 1998), probably
plays a primary role (Fig. 1). The precise mechanisms that
give rise to, and in a sense render inevitable, the wide range
of plastic behaviours, morphologies and physiologies exhib-
ited by organisms are discussed in detail by West-Eberhard
(2003) and are beyond the scope of this paper. We will simply
note that they include the phenomena of hypervariability
followed by somatic selection, homeostatic physiologies,
hormonal regulation, learning and the tendency of the
modular nature of organisms to produce independence in
form and function of otherwise integrated parts.
Regardless of their particular causes, the fact that
organisms do possess plastic phenotypes provides an
appropriate level of mechanism for understanding ecological
fitting as a process. A central insight from plasticity studies,
discussed in great detail by West-Eberhard (2003; see also
Robinson & Dukas 1999), is that phenotypic plasticity
allows organisms greater flexibility in the use of novel
resources than if mutations and changes in gene frequencies
were a pre-requisite for their exploitation. Phenotypic
plasticity allows organisms to mount a response (i.e. achieve
realized fitness) to novel environmental conditions (e.g. Yeh
& Price 2004), and it seems likely that all organisms possess
some degree of potential fitness outside the range of
conditions under which the species evolved (Fig. 1). We call
this region of ecological space !sloppy fitness space"
(Fig. 2a), a key element of the model of ecological fitting
presented in later sections. Interestingly, the existence of
!sloppy fitness space"appears to be a prediction of classic
quantitative genetic models of optimizing selection on
reaction norms (de Jong 2005).
Although phenotypic plasticity alone would presumably
lead to the development of robust genotypes, the correlated
evolution of traits (Lande & Arnold 1983) can also be
expected to produce organisms that possess the ability to
perform in novel environments. For example, Herrera et al.
(2002) showed evidence in the plant Helleborus foetidus for the
correlated evolution of pollinator- and herbivore-related
traits, such that selection by mutualistic pollinators can
indirectly affect the plant"s response to antagonistic herbi-
vores. Quite simply, if direct selection on trait A causes a
correlated change in trait B, then this could lead to a
phenotype that is somehow !pre-adaptated"for some future,
novel environmental condition.
A third mechanism behind the existence of sloppy fitness
space and robust genotypes is simply latent genetic variation
resulting from the conservation of genetic information
within a phylogeny. Phylogenetic conservatism, inertia or
constraint of traits related to resource use can, for example,
allow parasites to track host resources across taxa and shift
to novel hosts that possess similar resources (Brooks &
McLennan 2002; Murphy & Feeny 2006). The reason, for
example, an individual parasite may recognize a seemingly
!novel"host is because some ancestral species may have long
ago encountered that host or a sufficiently similar host.
From that point on, sufficient conditions may be met for
retaining the genetic changes resulting from that past
interaction, such that the contemporary genome possesses a
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useful response to that host when it or something similar is
encountered in the future.
Together, phenotypic plasticity, correlated trait evolution,
and phylogenetic conservatism broadly defined provide the
raw material (sloppy fitness space) for ecological fitting to
occur (Fig. 1). They can all be viewed as contributing to the
overall flexibility of individual organisms in dealing with
novel environmental conditions. Furthermore, they can all
be seen as proximate mechanisms of exaptation.
Exaptation – the co-option of traits for novel functions
over evolutionary time scales – is a widely accepted and
historically important concept in evolutionary biology
(Gould & Vrba 1982). A trait that has been exapted for a
novel function (e.g. Armbruster 1996, 1997) is merely the
endpoint of a process that must have begun with an initial
case of ecological fitting, as an evolved genotype came into
contact with a novel environmental condition (Brooks &
McLennan 2002). Compared to some of the most well-
known cases of exaptation (e.g. feathered terrestrial dino-
saurs), cases of ecological fitting as we have described it are
much less likely to leave discrete historical signals in, for
example, the fossil record. However, this difference between
ecological and evolutionary time scales should not distract
from the essential unity of these processes (Brooks &
McLennan 2002). Whether viewed through an ecological or
an evolutionary lens, for ecological fitting or exaptation to
occur, individual organisms must at some point exploit
novel environmental conditions with the traits that they
carry at the moment of contact.
The remainder of this paper focuses on the process of
ecological fitting, its implications for how we view ecological
communities and species associations, and its potential
evolutionary consequences. We elaborate on the process
shown in Fig. 1, which depicts individuals using sloppy
fitness space to obtain realized fitness in a novel condition.
This leads to the persistence of species in novel environ-
ments and results in novel species associations. In this way
ecological fitting, as a result of Janzen"s robust genotypes,
circumvents adaptive evolution to produce ecological
novelty, which can then, potentially, lead to adaptive
evolution.
A C O N C E P T U A L M O D E L
To develop a conceptual model of ecological fitting, we first
explicitly define the term !environment"as it is relevant to
Phenotypic plasticity
Potential fitness in novel conditions
( sloppy fitness space’)
Genotype encounters
novel conditions
Realized fitness in
novel conditions
Population establishes
in novel conditions
Existence of species in
novel environments
Novel selective
environments for evolution
to potentially act on
Raw
material
of
ecological
fitting
Process of
ecological fitting
Products of
ecological fitting
Correlated evolution
of traits
Existence of novel species
associations
Mechanistic basis
of ecological
fitting
Phylogenetic conservatism,
inertia, and constraint
’
Figure 1 Flow-diagram outlining the major
components of ecological fitting from its
mechanistic basis in factors that give rise to
the overall flexibility of phenotypes in
dealing with variable environments, to its
ecological and potentially evolutionary end-
products. See text for details.
Idea and Perspective Ecological fitting 1127
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ecological fitting and explicitly define what we mean by
!species traits"in terms of the environment. We posit that a
complete description of any organism that bridges evolu-
tionary and ecological perspectives can be represented as a
fitness space mapped onto a set of environmental variables.
We then illustrate ecological fitting in relation to our
definitions of environment, species traits and fitness space.
An explicit definition of environment
!Environment"is a term that has been variously defined by
biologists working at different levels of organization (Peters
1991). For our purposes, we define environment as
consisting of only those variables that an organism perceives
in an evolutionarily relevant way, which is to say those
variables that through their effect on the individual affect
the vital rates of the population: birth, death and migration.
Collectively, these environmental variables comprise the
!operative environment"(Spomer 1973; Dunham et al. 1989;
Dunham 1993; Dunham & Overall 1994). With its focus on
vital rates of the population, the concept of operative
environment (OE) derives from the concept of the
Hutchinsonian niche (Hutchinson 1957; Pulliam 2000).
Translating the OE to the biogeographic context, we will say
that it is the set of biotic and abiotic variables that will
determine whether a species is present or absent, rare or
common in any particular area.
An explicit definition of species traits
In the context of the OE, the most appropriate definition of
species trait is any intrinsic property of an organism that
interacts with the OE to determine growth, reproduction
and survival of the individual (Violle et al. 2007), thereby
determining the vital rates of the population. By this
definition, phenomena such as geographic range, abundance,
xy
a
b
xy
a
b
OV2
OV1
OV1
OV1
OV1
OV2
OV2
OV2
(a)
(b)
xyw z
c
d
b
a
Geographic area 1 or time 1
(host species 1)
Geographic area 2 or time 2
(host species 2)
Geographic area 1
(host species 1)
Geographic area 2
(host species 2)
Sloppy fitness space
Figure 2 The left panel in (a) is a simple graphical representation of the interaction between a phenotype and its environment in terms of its
potential to achieve realized fitness. In this case, the environment is defined by two operational variables (OVs) and the box defines the
combined subset of these variables that comprises the species"ancestral operative environment (OE). Letters on the axes indicate the range of
values over which the OVs occur, which define the OE. The shaded ellipse represents the fitness isocline, i.e. those combinations of OVs
where realized fitness can be achieved. That portion of the fitness isocline which lies outside the ancestral OE represents the potential to
achieve realized fitness under some combination of OVs never before encountered in the evolutionary history of the species. We refer to this
portion of the fitness isocline as !sloppy fitness space". The entire figure is a graphical representation of (a) ecological resource tracking and
(b) ecological fitting. In both cases, the graphs preceding the arrow represent initial conditions. The arrow represents either dispersal to a new
area (a and b), rapidly altered environmental conditions without dispersal (b), or the encountering of a novel host species by a parasite
(a and b). The graph following the arrow represents the set of conditions following dispersal to a new area (a and b), rapidly altered
environmental conditions (b), or the encountering of a novel host species (a and b), respectively. See text for further details.
1128 S. J. Agosta and J. A. Klemens Idea and Perspective
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diet breadth, number of interactions with other species, etc.,
are not species traits per se but higher level descriptors that
arise from species trait-by-OE interactions. This definition
serves to integrate evolutionary and ecological perspectives,
as only properties that affect the vital rates of the population
are available to be acted upon by natural selection. For
example, the geographic range of a species cannot evolve,
but the traits that interact with the OE to determine
geographic range can.
Fitness space and fitness isocline
Natural selection acts on phenotypes, which for our
purposes is simply the set of all species traits weighted by
their relative abundances within a population. Likewise, OE
variables (OVs) are spatially inter- and autocorrelated and
occur with a particular frequency distribution across the
physical landscape of the earth. Therefore, we may consider
an OE to be the subset (relative to the global maxima and
minima) of values for all OVs occurring over any arbitrarily
selected area of physical landscape, weighted by the relative
abundance of those OVs within that area. Mapping the
phenotype onto the OE gives three-dimensional !fitness
space",the distribution of fitnesses for a particular pheno-
type or set of phenotypes across the OE. Or, working
backwards, all components of the equation whose output is
fitness are either the OVs that comprise the OE or the
species traits that comprise the phenotype.
From this point onwards, we concern ourselves only with
the potential for a species to be present or absent in some
portion of global OE space and not with questions of
relative abundance. Thus we consider only the veil line of
fitness space, or the !fitness isocline"where the population
growth rate, k, is 1 (a concept roughly equivalent to the
zero-net-growth isoclines of resource-ratio models: Tilman
1982; Chase & Leibold 2003). Whether a species is
potentially present or absent in any particular area boils
down to one question: how does its fitness isocline map
onto the available OE space (e.g. Fig. 2)?
We consider a species ancestral OE to be defined by the
ranges and frequency distributions of OVs that exist within
its ancestral range. We expect that the fitness isocline of a
species will reflect the OE under which it evolved, but do
not expect it to be perfectly optimized to this OE due to
historical and genetic constraints. Ecological fitting is
therefore a process that takes place when an organism,
after some dispersal event or some rapidly altered environ-
mental condition, comes to rest in some part of physical
space that is outside of its species"ancestral OE. At this
point, it is clear that one of two things will happen: the
organism will either !fit"into this novel environment, that is,
it will have realized fitness, or it will not. Because we are
largely concerned with the role of ecological fitting
in assembling communities and the associations among
species, we will use this model to explore two non-mutually
exclusive cases of ecological fitting: (1) colonization of new
areas and (2) formation of new species associations.
A G R A P H I C A L M O D E L
The left panel of Fig. 2a is a simple way to visualize the
interaction between a phenotype or set of phenotypes and
the environment in our conceptual framework. The axes
represent two OVs and define a vector space of possible
environmental conditions, the solid box represents the
available OE space in the current environment, and the
shaded ellipse represents the phenotype"s fitness isocline
(k‡1). The shape and breadth of the fitness isocline are
arbitrary. We choose an ellipse for simplicity. More
importantly, if we consider the OE space defined by the
box to represent the ancestral OE, then the fitness isocline
is, at least in part, a direct product of evolution in this OE.
The fitness isocline in the left panel of Fig. 2a extends
beyond the bounds of the OE space in the ancestral
environment. This overlap indicates that this genotype
possesses sloppy fitness space in that it has fitness over a
wider range of environmental variation than it encounters in
the ancestral environment.
Figure 2 as a whole is a graphical model of ecological
fitting. Using this graphical model, we can visualize what
ecological fitting might look like in our conceptual
framework. We recognize two distinct scenarios that might
give rise to ecological fitting and consider a colonization and
species association case for each. The first scenario is the
simplest case of ecological fitting and is equivalent to
ecological resource tracking.
Scenario 1. Ecological resource tracking
The first scenario we consider is the situation where some
new area or resource (e.g. host species) presents identical
OE space to the ancestral OE (Fig. 2a). We therefore
consider this the simplest case of ecological fitting, which is
equivalent to resource tracking in ecological time stricto sensu.
Some plant community ecologists might also term this
scenario !ecological sorting", which is a concept used to
describe how species within plant communities align
themselves along edaphic gradients (Ackerly 2003). We
include this scenario in our graphical model for complete-
ness and because, particularly from the perspective of
species associations, it illustrates how resource tracking can
lead to patterns similar to those produced by adaptation and
coevolution.
Colonization by ecological resource tracking. This is the case of
colonization of new areas by using more of the same OE
space. The species evolves in geographic area 1 under the
Idea and Perspective Ecological fitting 1129
!2008 Blackwell Publishing Ltd/CNRS

OE space defined by the box in Fig. 2a, and then expands
into geographic area 2, which contains identical OE space.
If, for example, daily variance in temperature and soil
moisture were the two OVs, areas 1 and 2 would have
effectively the same thermal and soil moisture regimes.
Formation of new species associations by ecological resource
tracking. Alternatively, we can interpret Fig. 2a in terms of
the formation of species associations. For example, if the
fitness isocline represents that of some parasite, and we
substitute !host species"for !geographic area", then host
species 1 represents the ancestral host and host species 2
represents a novel host. From the perspective of a parasite,
a host is a package of resources guarded by a certain suite
of defences. In this case, the parasite evolves in response
to a set of host conditions defined by the OE space
provided by host species 1. Upon encountering the novel
host species 2, this parasite simply utilizes more of the
same OE space packaged in the form of a different
species. This case, although fundamentally identical to
colonizing new areas with more of the same OE space, is
not trivial because it leads to patterns that are superficially
indistinguishable from those produced by evolution. As
parasites track resources but biologists tend to track
species (Brooks & McLennan 2002), what looks like a case
of increased diet breadth (i.e. the addition of host
species 2) is actually a case of the parasite using more of
the same OE space. Although existing fitness space has
been co-opted to form a novel species association, from
the perspective of the parasite, it is simply doing what it
has always done.
Scenario 2. Ecological fitting
The second scenario which we consider is the situation
where some new area or host species presents OE space
that is outside the OE space encountered in the ancestral
area or host (Fig. 2b). This scenario is what we define as
ecological fitting proper.
Colonization by ecological fitting. In this case, organisms can
either physically move from areas 1 to 2 or can remain in the
same area but respond to rapidly altered environmental
conditions (times 1 to 2). In either case, the organisms
encounter some set of novel environmental conditions. That
is, the available OE space in the new environment is
different than the OE space in the species ancestral
environment. Now organisms will persist only if some
portion of the fitness isocline overlaps with some portion of
the novel OE space, i.e. only if realized fitness is obtained in
the novel environment. The fitness isocline in Fig. 2b
permits persistence because some portion of it overlaps with
some portion of OE space in the novel environment. This
portion of the fitness isocline is a by-product of history and
selection in the ancestral OE and it has been co-opted for
novel use. Again, the species may appear to be adapted to
this environment when in fact it is ecologically fit.
Formation of new species associations by ecological fitting.
Referring again to the parasite above, it now forms a novel
association with host species 2. However, rather than simply
tracking more of the same OE space, it is able to form an
association with a novel host that provides novel OE space
because of the pre-requisite traits (sloppy fitness space) it
carries at the time. Once again, the process depicted in
Fig. 2b can lead to observed species associations that appear
adapted but are nonetheless a product of ecological fitting.
In summary, the processes of ecological resource tracking
and ecological fitting, and their differences, can be easily
visualized using this graphical framework, which is bivariate
and therefore greatly oversimplified. It is important to
realize that (1) real OEs are multivariate and (2) ecological
resource tracking and ecological fitting can be non-mutually
exclusive processes. Agosta (2006) offered that many
instances of host shifts by herbivorous insects can be
interpreted as examples of ecological fitting, but acknow-
ledged that these host shifts tend to occur onto taxonom-
ically related plants likely because they tend to possess
similar oviposition stimulants, nutrients or defences to be
overcome (i.e. host shifts tend to involve resource tracking).
In fact, these arguments are not contradictory. For example,
even if a novel host species provides identical nutrients for
larval growth and development, it likely differs from the
original host in many other ways (e.g. plant architecture,
microclimate, phenology, abundance, spatial distribution,
suite of heterospecific herbivores, suite of natural enemies,
etc.). Thus, it seems likely that a host shift, especially one
involving dispersal to a new area, often involves ecological
resource tracking (Fig. 2a) and ecological fitting (Fig. 2b).
Returning to our example of the butterfly E. editha
incorporating a novel host into its diet via ecological fitting
(Thomas et al. 1987), the old question of how successful
host shifts occur can be recast in terms of similarities (strict
ecological resource tracking) and differences (ecological
fitting proper) between host-specific OEs. When apparently
novel OE space has been invaded via ecological fitting, the
next questions are by what mechanisms has realized fitness
been achieved and what, if any, evolutionary responses have
ensued (e.g. adaptation to the novel host). In principal, the
same questions apply when organisms colonize new areas.
F U R T H E R E C O L O G I C A L A P P L I C A T I O N S
We offer that our conception of Dan Janzen"s original
ecological fitting provides one particular framework for
what should be a pluralist approach to studying species
distributions and community ecology. At this point, we
realize this framework is largely conceptual. It will be very
difficult, for example, to wholly measure and compare real
1130 S. J. Agosta and J. A. Klemens Idea and Perspective
!2008 Blackwell Publishing Ltd/CNRS

OEs, just as it has been to measure a Hutchinsonian or
Grinellian niche (Chase & Leibold 2003). Nonetheless, we
feel that the framework developed here offers some useful
insights into some of ecology"s most pertinent topics,
including species"responses to climate change, biological
invasions and introductions, and the resulting assembly and
dynamics of novel ecological interactions and communities.
For instance, we discussed earlier the !escape hypothesis"to
explain successful biological invasions, which posits that
release from coevolved parasites and pathogens is respon-
sible for success in the invaded habitat (Mitchell & Power
2003; Torchin et al. 2003). In light of the OE perspective
developed here, this line of inquiry can produce only an
incomplete understanding of invasions because it imposes
an a priori, top–down approach to defining an organisms
selective environment. In addition, it ignores a role for
ecological fitting and the mechanisms by which it occurs.
Alternatively, the overarching question defined in this
paper in the case of biological invasions is: to what degree
does the former OE differ from the invaded OE, and if they
do differ, by what mechanisms is realized fitness achieved in
the invaded OE? In the aggregate, we want to know the
degree to which the invasion of new habitats or formation
of new species associations involves cases of simple
resource tracking, cases of ecological fitting proper (i.e.
the process outlined in Fig. 1) or some likely combination of
both. To accomplish this task, a more integrative, bottom–
up approach to defining species"selective environments
(OEs) is required. This approach would enable more robust
predictions of future species"responses to environmental
change, which to date rely in large part on correlational
habitat modelling (Kearney 2006). Predicting future distri-
butions and abundance in response to environmental
change based solely on the overlap between current
distributions and a few environmental variables (1) suffers
from the same a priori, top–down approach to defining
selective environments as imposing the !escape hypothesis"
in the study of invasions, and similarly (2) ignores the
potential for ecological fitting by phenotypically flexible
organisms (in addition to explicitly evolutionary processes
such as adaptation).
Finally, we note the growing fields of community and
ecosystem genetics, which seek to understand how standing
genetic variation and novel genetic variation introduced via
dispersal and colonization influence community dynamics
and ecosystem functioning (Urban et al. 2008; Whitham
et al. 2008). Ecological fitting not only acts as a mechanism
for the introduction of novel genetic variation within
communities, but also has implications for how other
organisms already in the community may respond to this
novelty and the community and ecosystem dynamics that
may ensue.
E V O L U T I O N A R Y I M P L I C A T I O N S
Ecological fitting is not, of course, an endpoint. For
example, although many instances of host shifts by native
insect herbivores onto introduced plants can be interpreted
as instances of ecological fitting (Agosta 2006), these host
shifts can lead to population divergence and adaptation to
the novel hosts (Strauss et al. 2006). Returning to the
butterfly example given earlier, Thomas et al. (1987)
showed that after the initial incorporation of the novel
host plant into their diets, some populations actually
evolved a preference for this novel host in the last
!100 years. Therefore, although evolution is not a pre-
requisite for the formation of novel species associations or
colonizations by introduced species, one outcome of
ecological fitting is that it can be a precursor to
evolutionary diversity. As a process whereby organisms
invade novel environments, use novel resources or form
novel associations with other species, ecological fitting can
place existing genotypes into novel selective environments.
For example, in Fig. 3, a species invades novel OE space
and persists by ecological fitting. However, as opposed to
Fig. 4, the population is relatively isolated (i.e. negligible
gene flow) and responds to directional selection in the new
OE.
xy
b
a
Ancestral operative environment Novel operative environment
time = 0
Novel operative environment
time > 0
OV2
OV1OV1OV1
OV2
OV2
zw
d
c
z
w
d
c
Figure 3 Graphical representation of ecological fitting as a precursor to evolutionary diversity. From left to right, a species evolves a fitness
isocline under a set of conditions in the ancestral OE, then uses sloppy fitness space (see Fig. 2a) to establish a population in some novel OE,
and then, because it is sufficiently isolated from other populations, evolves in response to the novel OE (i.e. its fitness isocline changes in
response to selection in the novel OE). See text for further details.
Idea and Perspective Ecological fitting 1131
!2008 Blackwell Publishing Ltd/CNRS

Alternatively, ecological fitting can promote and maintain
evolutionary stasis if it leads to many populations occupying
different OEs connected by sufficient amounts of gene
flow. In Fig. 4, what was once an initially isolated
population experiencing a relatively homogeneous OE
now, via ecological fitting, is many populations experiencing
heterogeneous OEs. In this case, as long as sufficient gene
flow is maintained, ecological fitting is a process that
promotes evolutionary stasis by opposing drift and local
adaptation. This scenario is one meaning of Janzen"s (1985)
!evolutionary quiescence"and partly what he related to
Gould & Eldredge"s (1977) ideas on stasis in the fossil
record.
C O N C L U S I O N S
We have argued that ecological fitting plays a fundamental
role in structuring ecological communities to the extent that
it is a mechanism for the formation of species associations,
species introductions and invasions, and community assem-
bly in general (Janzen 1985; Brooks & McLennan 2002;
Wilkinson 2004; Brooks & Ferrao 2005; Agosta 2006;
Brooks et al. 2006). Using a graphical framework, we have
illustrated (1) the process of ecological fitting, (2) how the
process differs from strict ecological resource tracking, (3)
how the process can produce patterns superficially indistin-
guishable from adaptation and (4) how the process can be
both a promoter of evolutionary stasis and a precursor to
evolutionary diversity.
We have also posited that phenotypic plasticity is a primary
mechanism behind ecological fitting. Modern ideas regarding
the role of phenotypic plasticity in producing ecological and
evolutionary novelty advanced by West-Eberhard (1989,
2003) and others (Robinson & Dukas 1999; Gorur 2004; Yeh
& Price 2004; Fordyce 2006; Janz et al. 2006; Weingartner
et al. 2006; Nylin & Wahlberg 2008) are integral to the
concept of ecological fitting. Phenotypic plasticity will be a
major determinant of the shape and breadth of the fitness
isocline, and moreover, along with correlated trait evolution
and phylogenetic constraints, will determine the amount and
direction of sloppy fitness space organisms possess.
Ecological fitting is facilitated by flexible genotypes – it is
the outcome of organisms possessing greater flexibility in
the environments, resources and other species that they can
utilize for survival and reproduction than if mutation and
changes in genes frequency were a pre-requisite for escaping
the limited context under which species evolve. Because it
can place existing genotypes into novel selective environ-
ments, ecological fitting by phenotypically flexible organ-
isms can play an important role in the origin and evolution
of biological diversity.
A C K N O W L E D G E M E N T S
We especially thank Dan Janzen who first started our
thinking about ecological fitting. We also thank Dan Brooks
and Art Dunham for fostering many of the ideas presented
in this paper. We also thank Kellie Kuhn and Niklas Janz,
OV1
OV2
OV1
OV1
OV1
OV1
OV2
OV2
OV2
OV2
x y
b
a
z w
c
d
t
s
e
f
r q
c
d
z w
e
f
Ancestral operative environment
Figure 4 Graphical representation of ecological fitting as a promoter of evolutionary stasis. The central graph represents a population
experiencing the ancestral OE. The peripheral graphs represent populations experiencing novel OEs. Arrows indicate significant levels of
gene flow. Because each population is experiencing a different selective environment but is connected to other populations via gene flow, the
species experiences heterogeneous and possibly contradictory selection pressures that promote evolutionary stasis (i.e. there is little to no
change in the fitness isoclines). See text for further details.
1132 S. J. Agosta and J. A. Klemens Idea and Perspective
!2008 Blackwell Publishing Ltd/CNRS

who independently recommended consultation of
M.J. West-Eberhard"s recent book on phenotypic plasticity
and evolution. We acknowledge that none of them may
agree with everything we have said. Any faults and omissions
are our own. While writing this paper, SJA was supported by
a GIAR grant from Sigma Xi, the Binns-Williams Fund
from the University of Pennsylvania and NSF Doctoral
Dissertation Improvement Grant DEB 0508573. JAK was
supported by an NSF Post-doctoral Fellowship in Microbial
Biology Grant No. 0400833. Significant portions of this
paper were conceived and written while both authors were
living and working in the A
´rea de Conservacio´n Guanacaste
(ACG), Costa Rica. We acknowledge the entire staff of the
ACG for their continued logistic support. Finally, we thank
David Wilkinson and two anonymous referees for com-
ments and suggestions that significantly improved the final
version of the manuscript.
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Editor, Tadashi Fukami
Manuscript received 14 March 2008
First decision made 17 April 2008
Second decision made 30 June 2008
Manuscript accepted 3 July 2008
1134 S. J. Agosta and J. A. Klemens Idea and Perspective
!2008 Blackwell Publishing Ltd/CNRS