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The parasite paradox arises from the dual observations that parasites (broadly construed, including phytophagous insects) are resource specialists with restricted host ranges, and yet shifts onto relatively unrelated hosts are common in the phylogenetic diversification of parasite lineages and directly observable in ecological time. We synthesize the emerging solution to this paradox: phenotypic flexibility and phylogenetic conservatism in traits related to resource use, grouped under the term ecological fitting, provide substantial opportunities for rapid host switching in changing environments, in the absence of the evolution of novel host-utilization capabilities. We discuss mechanisms behind ecological fitting, its implications for defining specialists and generalists, and briefly review empirical examples of host shifts in the context of ecological fitting. We conclude that host shifts via ecological fitting provide the fuel for the expansion phase of the recently proposed oscillation hypothesis of host range and speciation, and, more generally, the generation of novel combinations of interacting species within the geographic mosaic theory of coevolution. Finally, we conclude that taxon pulses, driven by climate change and large-scale ecological perturbation are drivers of biotic mixing and resultant ecological fitting, which leads to increased rates of rapid host switching, including the agents of Emerging Infectious Disease.
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ZOOLOGIA 27 (2): 151–162, April, 2010
doi: 10.1590/S1984-46702010000200001
© 2010 Sociedade Brasileira de Zoologia | | All rights reserved.
Parasites, organisms that spend most of their life-time feed-
ing in or on a single individual of another species, may exhibit
the most common mode of life on this planet (PRICE 1980). This
includes diverse groups of organisms, from viruses and bacteria
to worms, plant-feeding insects and parasitic plants. Parasites
have managed to spread across impressively diverse taxonomic
host groups, often reaching remarkable species numbers along
the way. For example, Angiosperms comprise roughly one fourth
of all species on earth, yet most plant species host multiple spe-
cies of specialized plant-feeding insects.
Given the ubiquity of host-parasite interactions, under-
standing the factors that generate, maintain, and constrain
these associations is of primary interest with implications for a
wide range of applied ecological issues, including the dynam-
ics of emerging infectious diseases (BROOKS & FERRAO 2005, BROOKS
et al. 2006a, BROOKS & HOBERG 2007), biological control, bio-
logical introductions and invasions, and biotic responses to
climate change (BROOKS & MCLENNAN 2002). One of the most
obvious and intriguing features of parasitism is pronounced
conservatism in the range of hosts used (high host-specificity),
both on ecological (THOMPSON 1994, 2005) and evolutionary
time-scales (EHRLICH & RAVEN 1964, BROOKS & MCLENNAN 1991,
1993, 2002, THOMPSON 1994, 2005, FUTUYMA & MITTER 1996, JANZ
& NYLIN 1998, WINKLER & MITTER 2008). Not surprisingly, many
think this host specificity holds the key to understanding the
evolution of host-parasite associations – selection for increased
specialization of parasites to their hosts constrains host use
and promotes speciation. However, while this view provides a
mechanism for the evolution of existing interactions (i.e., spe-
cies become increasingly well-adapted to one another once the
interaction originates), it provides no basis for understanding
the origins of novel interactions. Coevolution can be diversi-
fying, so that local selection in different parts of a geographic
range can lead to a set of daughter populations that are locally
adapted to different resources (THOMPSON 1994, 2005, BENKMAN
1999, GODSOE et al. 2008). But how the diversified interaction
(host range) of the mother species came into existence in the
first place must still be explained. Although coevolution can
give rise to “new” species interactions in cases where the host
and parasite speciate in tandem, there is little evidence for
cospeciation as a major factor in host-parasite evolution (HOBERG
& BROOKS 2008, 2010). Indeed, ‘cospeciation’ was first proposed
How specialists can be generalists: resolving the “parasite paradox” and
implications for emerging infectious disease
Salvatore J. Agosta1, 3; Niklas Janz2 & Daniel R. Brooks1
1 Department of Ecology and Evolutionary Biology, University of Toronto. Toronto, ON M5S 3G5, Canada.
2 Department of Zoology, Stockholm University. 106 91 Stockholm, Sweden. E-mail:
3 Corresponding author. E-mail:;
ABSTRACT. The parasite paradox arises from the dual observations that parasites (broadly construed, including phy-
tophagous insects) are resource specialists with restricted host ranges, and yet shifts onto relatively unrelated hosts are
common in the phylogenetic diversification of parasite lineages and directly observable in ecological time. We synthe-
size the emerging solution to this paradox: phenotypic flexibility and phylogenetic conservatism in traits related to
resource use, grouped under the term ecological fitting, provide substantial opportunities for rapid host switching in
changing environments, in the absence of the evolution of novel host-utilization capabilities. We discuss mechanisms
behind ecological fitting, its implications for defining specialists and generalists, and briefly review empirical examples
of host shifts in the context of ecological fitting. We conclude that host shifts via ecological fitting provide the fuel for
the expansion phase of the recently proposed oscillation hypothesis of host range and speciation, and, more generally,
the generation of novel combinations of interacting species within the geographic mosaic theory of coevolution. Finally,
we conclude that taxon pulses, driven by climate change and large-scale ecological perturbation are drivers of biotic
mixing and resultant ecological fitting, which leads to increased rates of rapid host switching, including the agents of
Emerging Infectious Disease.
KEY WORDS. Climate change; coevolution; ecological fitting; host shift; plant-insect interactions; sloppy fitness.
152 S. J. Agosta et al.
ZOOLOGIA 27 (2): 151–162, April, 2010
as a descriptive term for cases in which hosts and parasites
experienced concomitant speciation events, such as being af-
fected by the same vicariance event, not as an evolutionary
mechanism (BROOKS 1979). Thus the issue of how novel inter-
actions arise remains unresolved. Our aims are to (1) synthe-
size the resolution to this problem and (2) address the implica-
tions for emerging infectious disease in humans.
Most parasites appear to be resource specialists. The over-
whelming majority of plant-feeding insects, for example, use
only a tiny fraction of the available plant species in the habitat
(THOMPSON 1994, NOVOTNY et al. 2005, DYER et al. 2007, JANZEN &
HALLWACHS 2009). Not surprisingly, this pattern has given rise to
the long-standing idea that specialization is a one-way street, an
evolutionary dead-end where parasites become increasingly well-
adapted to their hosts at the expense of the ability to perform
on alternative hosts. The idea of specialization as a dead-end
dates back to the 19th century (THOMPSON 1994) and some re-
cent studies have reported support for the ‘dead-end’ hypoth-
esis (MORAN 1988, WIEGMANN et al. 1993, KELLEY & FARRELL 1998).
Other studies, however, conclude that generalized lineages are
often derived from specialists (SCHEFFER & WIEGMANN 2000, JANZ et
al. 2001, TERMONIA et al. 2001, RADTKE et al. 2002, KERGOAT et al.
2005, YOTOKO et al. 2005). Many groups exhibit higher transi-
tion rates from generalization to specialization than vice versa,
but host specialization appears to be a dynamic trait with no
inherent necessary directionality (JANZ et al. 2001, NOSIL 2002,
NOSIL & MOOERS 2005). If this is the case, why are broad host
ranges so rare? There are obvious advantages of wider niches,
such as more abundant and reliable food supplies or oviposition
sites, so something must consistently select against them (FUTUYMA
& MORENO 1988). A great deal of attention has been devoted to
this question, and it now appears clear that selection should
favor increased host specificity over time for a variety of reasons
(FUTUYMA & MORENO 1988, BERNAYS 1989, 2001, VIA 1991, AGRAWAL
2000, JANZ 2002, JANZ et al. 2005). Paradoxically, the successful
solution to the original problem of widespread specialization
has in many ways led to the new problem of understanding
why there are exceptions at all (JOHANSSON et al. 2007, SINGER 2008).
These exceptions are important, because without them
there would be no host shifts. Every host shift must begin with
colonization (a process that leads to the establishment of a new,
persistent interaction), during which the parasite should re-
tain the capacity to use both the ancestral and novel host.
Multiple host use following such colonization may be brief or
it may be prolonged (JANZ et al. 2006, NYLIN & JANZ 2009), but
host shifts must begin with a host range expansion. Initially,
additional hosts should typically be inferior alternatives to the
original host, to which the parasite is specifically adapted, and
special circumstances should be needed to incorporate such a
host into the repertoire. Yet, host shifts and host range expan-
sions do occur, and can happen rapidly (THOMPSON 1998).
Available data on the rate of host shifts are discordant.
Phylogenetic comparative studies of hosts and parasites dem-
onstrate two macroevolutionary patterns: (1) high host spe-
cialization and conservatism in host use, as well as (2) abun-
dant evidence of switching onto relatively unrelated hosts that
in some cases seems to have been the primary driver of diversi-
fication (AGOSTA 2006, JANZ et al. 2006, JANZ & NYLIN 2008, HOBERG
& BROOKS 2008, WINKLER & MITTER 2008, NYMAN 2009). As a cor-
ollary, objective evidence for cospeciation has been rare even
among intimately associated parasites, such as helminths in-
habiting vertebrates (BROOKS & MCLENNAN 1991, 1993, 2002,
2008, 2010). For less intimate associations, such as among plants
and many plant-feeding insects, it has long been recognized
that cospeciation cannot have been a major source of diversifi-
cation (AGOSTA 2006, NYMAN 2009). Coupled with abundant
ecological evidence of rapid shifts to novel hosts, such as in-
troduced plants (TABASHNIK 1983, SINGER et al. 1993, CARROLL et
al. 1997, FOX et al. 1997, VAN KLINKEN & EDWARDS 2002, AGOSTA
2006, STRAUSS et al. 2006) and animals (CORNELL & HAWKINS 1993,
KELLY et al. 2009), these observations suggest that host shifts
are common in the interaction between hosts and parasites.
Colonization of novel hosts must be an important driving force
behind the diversification of the interactions themselves (by
generating novel species associations) as well as the taxa in-
volved (by increasing net speciation rates). This is the ‘parasite
paradox’: how do highly specialized parasites otherwise shift
to novel hosts?
We present what we consider the broad outlines of an
emerging synthesis that resolves the parasite paradox without
proposing novel mechanisms. Various parts of this synthesis
have been proposed in the decades since EHRLICH & RAVEN (1964)
observed broad taxonomic correspondence between butterflies,
their host plants, and plant secondary chemistry. They posited
that associations between plants and plant-feeding insects re-
sult largely from a coevolutionary arms race that leads to in-
creased specialization and tends to restrict associations phylo-
genetically. Once that idea became internalized as the
overarching mechanism behind host-parasite associations,
many researchers began to scrutinize it and conclude that (1)
host-parasite associations are generally more labile than ex-
pected under models of strict one-on-one coevolution between
species, resulting in (2) historically and ecologically complex
patterns of associations (e.g., STRONG 1979, HOLMES & PRICE 1980,
JANZEN 1980, 1985, JERMY 1984, BROOKS 1985; review in BROOKS &
MCLENNAN 2002). In addition, the development of modern phy-
logenetic comparative approaches to studying host-parasite
evolution has greatly increased the capacity to understand the
history and structure of these associations empirically (BROOKS
& MCLENNAN 1991, 2002).
We first review what is needed to complete a shift to a
novel host if the shift requires newly evolved abilities to utilize
the novel resource. In this case, a full host shift will require
153How specialists can be generalists
ZOOLOGIA 27 (2): 151–162, April, 2010
more or less simultaneous correlated evolution across a num-
ber of traits to enable it to locate the new resource, identify it
as a possible host, trigger oviposition and allow appropriate
handling during oviposition. In addition, offspring finding
themselves on this novel resource will need to be triggered to
initiate feeding (and must be physically capable of doing so,
e.g. to penetrate the cuticle), and their metabolic system will
have to be able to digest the new resource and overcome its
chemical defense (or immune system). Each new host may come
with a different set of external enemies requiring new meth-
ods of defense or evasion and a different micro-habitat requir-
ing novel physiological adaptations. Such correlated changes
occurring simultaneously across all these sets of characters
ought to be so unlikely that host shifts ought to border on the
Clearly, host shifts are not impossible. We assume host
shifts comprise two different “events”: (1) colonization of the
novel host (host range expansion) followed by (2) loss of the
ancestral host (host specialization). Hence, for a host shift to
be completed, there must first be a mechanism for generaliza-
tion (increased diet breadth) and then a mechanism for spe-
cialization (decreased diet breadth). Furthermore, in order for
specialization not to be an evolutionary dead-end, these mecha-
nisms must be at least partly independent, so specialists main-
tain the potential to become generalists and generalists main-
tain the potential to become specialists. This links host shifts
to the processes that determine host specificity.
Ecological fitting
It is hard to escape the conclusion that the capacity to
utilize the novel host must have existed before a successful
shift was initiated. While this may seem counterintuitive,
mechanisms allowing organisms to colonize and persist in novel
environments do exist. For example, novel host plants can be
added through oviposition “mistakes” (LARSSON & EKBOM 1995)
if they can be metabolized as a side-effect of existing machin-
ery – a form of phenotypic plasticity (WEST-EBERHARD 2003, NYLIN
& JANZ 2009).
Phenotypic plasticity, in addition to factors discussed be-
low, provides a mechanistic basis for an ecological concept called
‘ecological fitting’ (JANZEN 1985). Ecological fitting describes the
case when an organism interacts with its environment in a way
that seems to indicate adaptation or more generally a shared
evolutionary history (e.g., between a parasite and its host), when
in fact the traits relevant to the interaction evolved elsewhere
with different species or under different conditions. Such inter-
actions can appear to be coevolved over extended evolutionary
time (JANZEN 1980), when in fact they may be the result of a
relatively recent ecological “fit”, possibly followed by rapid lo-
cal adaptation. JANZEN (1980, 1985) suggested that species often
form these ecologically fit associations and that ecological fit-
ting plays a major role in shaping communities.
When organisms encounter novel environmental con-
ditions – a new habitat, a changed climate, a change in re-
sources – they survive and persist (achieve realized fitness) where
and if they “fit” by means of characters they already possess.
In other words, successful establishment in a novel environ-
ment requires species having reaction norms that already in-
clude conditions in the novel environment. For the species to
persist, colonists facing ecological novelty must achieve real-
ized fitness within a more or less evolutionarily unfamiliar web
of species (predators, prey, competitors, symbionts, etc.) using
traits they already possess. Thus within any given ecological
community, and depending on time and contingency, at least
some traits relevant to observed species interactions will have
evolved elsewhere under different conditions, but were later
co-opted (MAYNARD SMITH & SZATHMARY 1995) or exapted (GOULD
& VRBA 1982) to form new, ecologically fit, interactions (JANZEN
1980, 1985).
Ecological and macroevolutionary evidence for ecologi-
cal fitting among hosts and parasites is abundant (AGOSTA 2006,
HOBERG & BROOKS 2008, 2010, KELLY et al. 2009). This suggests
that host shifts are often initiated because the parasite is
exapted, or “preadapted” to the novel resource. The novel host
might share important characteristics with the current host or
might have been used in the past (FUTUYMA et al. 1995, FUTUYMA
& MITTER 1996, JANZ et al. 2001, WAHLBERG 2001, BROOKS &
MCLENNAN 2002, RADTKE et al. 2002), or the parasite might for-
tuitously possess capabilities to use a novel resource (AGOSTA &
KLEMENS 2008, 2009).
AGOSTA & KLEMENS (2008) proposed a general framework
for ecological fitting as a mechanism behind the assembly of
ecological communities and the formation of novel interac-
tions between species within communities. They posited three
factors giving rise to ecological fitting and the ability of organ-
isms (genotypes) to achieve realized fitness under novel condi-
tions (e.g., a novel host). First, phenotypic plasticity can allow
organisms to mount a response to novel conditions (WEST-
EBERHARD 2003). Second, correlated trait evolution (LANDE &
ARNOLD 1983) can produce phenotypes that are “preadapted”
to some future novel condition. Third, phylogenetic conserva-
tism in traits related to resource use, including design con-
straints (e.g., the ‘spandrels’ of GOULD & LEWONTIN 1979) and
retention of traits from past selection pressures (e.g., the ‘anach-
ronisms’ of JANZEN & MARTIN 1982), provide the latent ability to
perform under apparently novel conditions, such as a parasite
encountering a new host that is actually the same or sufficiently
similar to some ancestral host (BROOKS & MCLENNAN 2002). These
capacities produce organisms possessing potential fitness out-
side the range of conditions in which the species evolved. AGOSTA
& KLEMENS (2008) termed this region of fitness space ‘sloppy
fitness space,’ a by-product of direct selection under some other
set of conditions (the ancestral ‘operative’ environment). The
operative environment comprises all components defining a
host as a resource and therefore the range of host-related vari-
154 S. J. Agosta et al.
ZOOLOGIA 27 (2): 151–162, April, 2010
ables affecting parasite evolution. In figure 1a, a parasite evolves
in response to the ancestral host operative environment de-
fined by the black circle, but as a consequence, also has poten-
tial fitness (sloppy fitness space) beyond the range of condi-
tions encountered with the ancestral host. Thus, the parasite
has some ability to perform and persist on other hosts that
represent a novel operative environment (host 2 in Fig. 1e; host
2 and 3 in Fig. 1f), in addition to the ability to add new hosts
representing the same or highly similar operative environments
(host 1 in Fig. 1 d-f).
Armed with adaptations to their ancestral hosts and the
sloppy fitness space that results, parasites can ecologically fit
with new hosts in at least two ways (AGOSTA & KLEMENS 2008).
First, due to phylogenetic conservatism or convergence of host
resources, parasites may shift to a new host species because the
new host possesses the same (or highly similar) resources as
the old host: ecological fitting via resource tracking (host 1 in
Fig. 1d-f). The possibility that parasites track plesiomorphic re-
sources both ecologically and evolutionarily was termed ‘co-
accommodation’ by BROOKS (1979) and more often than not
Figure 1. A schematic illustration showing two dimensions of the operative environment associated with fictional host resources (black
circles). Sloppy fitness space (see text) can allow realized fitness in an area outside the operative environment to which the parasite is
adapted (light grey circles). Panels a, d, and g illustrate a specialist, adapted to a single host resource, panels b, e and h illustrate a
polyspecialist that has adapted independently to three different resources, and panels c, f and i illustrate a true generalist with a more
general host recognition and tolerance system that allows it to utilize any resource that falls within the dark grey area. The open circles
in panels d-f represent three novel resources. The specialist in panel d can colonize resource 1 (which is more or less identical to the
ancestral resource) but not resource 2 and 3. The polyspecialist in panel e can colonize resource 1, but also resource 2 that falls within
its sloppy fitness space, and the generalist in panel f can colonize all three resources. In panels g-i only one host is available, and all three
parasite species will appear to be specialists, but their ecological and evolutionary potential will be very different.
155How specialists can be generalists
ZOOLOGIA 27 (2): 151–162, April, 2010
parasites seem to do so (reviewed in BROOKS & MCLENNAN 2002;
see also BROOKS et al. 2006a,b, HOBERG & BROOKS 2008, 2010).
This is perhaps most evident when host chemistry or ecology
takes priority over host phylogeny in explaining host-parasite
associations (e.g., BECCERA 1997, WAHLBERG 2001, BROOKS et al.
Second, parasites may use sloppy fitness space to shift onto
new hosts representing a novel resource: ecological fitting via
sloppy fitness space (host 2 in Fig. 1e; host 2 and 3 in Fig. 1f). In
either case, observed interactions between hosts and parasites
will appear to be newly evolved, but are products of ecological
fitting. Ecological fitting via resource tracking and via sloppy
fitness space are not mutually exclusive and may represent two
ends of a continuum (AGOSTA & KLEMENS 2008). A typical host
shift may involve both tracking plesiomorphic resources and
use of sloppy fitness space. In the case of ecological fitting via
resource tracking, the new host may be novel only in the sense
that it is a different species – from the perspective of the parasite
it may not be novel at all. This situation illustrates how para-
sites can shift to relatively unrelated hosts if the operative envi-
ronments (e.g., chemicals recognized as oviposition stimulants:
MURPHY & FEENY 2006) are plesiomorphic or convergent. It also
illustrates conceptual problems with our understanding of what
constitutes specialists and generalists.
The terms specialist and generalist are vaguely defined,
and used variously by researchers. Typically the terms refer to
the dimension of niche width that reflects diet. Hosts repre-
sent resources, and thus an operational defintion of host-
speficity should ideally reflect resource distributions and re-
source heterogeneity (NYMAN 2009). However, host-specificity
is most often simply measured as the number of hosts in a
parasite’s repertoire. As host species are themselves hierarchi-
cally related, counting host species may be misleading, and
some authors have adopted host use indices that to various
extents account for host relatedness (SYMONS & BECCALONI 1999,
JANZ et al. 2001, 2006). More important is that species with
virtually identical present-day host ranges can achieve them
in fundamentally different ways, and as a consequence have
divergent evolutionary potentials. In figure 1g-i, all three para-
sites are specialists, each using one host species. However, while
the parasite in figure 1g is restricted to one host due to a nar-
row niche width, the other two are restricted to this host be-
cause it is the only host locally available.
Two parasite species in figure 1b and c use the same three
host species, but whereas the parasite in figure 1c is a true gen-
eralist adapted to a wide niche, the host in figure 1b is best
described as a ‘polyspecialist’, as it has genetically indepen-
dent adaptive traits for all three niches (WEST-EBERHARD 2003,
NYLIN & JANZ 2009). The true generalist (Fig. 1c) presumably
has evolved a more general host recognition and tolerance sys-
tem that allows it to feed on any host that falls within the grey
circle. The polyspecialist (Fig. 1b) uses these three hosts be-
cause it has adapted independently to all three.
BROOKS & MCLENNAN (2002) suggested that, hidden among
the “true” specialists and generalists are ‘faux specialists’ and
‘faux generalists’. Faux specialists are generalists restricted to a
few or a single resource by ecological factors, such as competi-
tion, local micro-climate or non-concordant distributional ranges
(Fig. 1h-i). Faux generalists are specialists specialized on a re-
source that is phylogenetically widespread. Parasites are not spe-
cialized on particular host species; they are specialized on re-
sources that may or may not be shared among several species
(NYMAN 2009). In some cases, a plesiomorphic resource can be
shared among a set of hosts to the extent that, from the parasite’s
perspective, they are identical and interchangeable. In other cases
there will be a quantitative difference between host species in
the amount of the resource(s) they possess. For faux generalists
and faux specialists, host shifts can be initiated simply by a
change in ecological circumstances (e.g., a shift in local host
availability or local extinction of a competitor).
Observing ecological fitting
Host shifts are difficult to observe. We often must be con-
tent with scattered snapshots from different stages of the pro-
cess to draw a composite picture of the whole process. Never-
theless, researchers have occasionally observed a host shift from
the initial colonization to the final (local) loss of the ancestral
host. The butterfly Euphydryas editha Boisduval, 1852 occurs in
a fragmented population structure across the western USA and
Canada. Host use has been studied extensively in several popu-
lations over many years (SINGER 2003, SINGER et al. 2008). Singer
and colleagues have observed two instances of
anthropogenically-induced shifts in host use. In one case, the
local flora was altered by the introduction of an exotic plant,
and in the other logging removed the original host (SINGER et
al. 2008). In both cases, at least some of the local E. editha
accepted a novel host for oviposition and survived on it at first
encounter (SINGER et al. 2008). Thus, the initial stage of the colo-
nization occurred through ecological, not evolutionary change.
Transfer to a novel environment may remove the ances-
tral host and offer alternatives, but more often a parasite popu-
lation should come into contact with a novel host in sympatry
with the ancestral host. ANTONOVICS et al. (2002) showed that
the recent shift by the anther-smut disease Microbotryum
violaceum (Pers.) G. Demi & Oberw., 1982 from the ancestral
host Silene alba Poir. to S. vulgaris (Moench) Garcke was con-
tingent on local scale co-occurrence of both species. The patho-
gen was imperfectly adapted to its new host and susceptibility
to the pathogen varied considerably. Similarly, some popula-
tions of the prodoxid moth Greya politella Walsingham, 1888
in central Idaho have shifted from the ancestral host
Lithophragma parviflorum (Hook.) Nutt. Ex Torr. & A. Gray to
the related Heuchera grossulariifolia Rydb. In this case, popula-
tions feeding on novel hosts are locally adapted to them, and
preference for tetraploid variants seem to have evolved inde-
pendently in several populations (SEGRAVES et al. 1999, NUISMER
& THOMPSON 2001). Lithophragma-feeding populations exposed
156 S. J. Agosta et al.
ZOOLOGIA 27 (2): 151–162, April, 2010
to the novel host oviposited in it to a low degree, but did not
differentiate between plants of different ploidies (JANZ & TH-
OMPSON 2002). Hence, the shift likely was initiated by local con-
tingency, and local preference for tetraploid variants of the
novel host have evolved independently after the initial coloni-
zation (THOMPSON et al. 2004). These examples suggest host shifts
initiated without any evolutionary change, through ecologi-
cal fitting, followed by rapid evolution of traits associated with
host use (SINGER et al. 2008, ANTONOVICS et al. 2002, THOMPSON et
al. 2004).
Achieving the fit
As mentioned above, host use involves a number of dif-
ferent processes that must all function in concert. A potential
host may possess some but not all of the required resources.
For a phytophagous insect, the first step towards a host shift
involves a failure to fully discriminate against a plant sympat-
ric with the ancestral host, at least in part of the insect’s geo-
graphic distribution (LARSSON & EKBOM 1995). If offspring have
realized fitness on the new plant, natural selection can then
begin playing a role in modifying traits involved in host use
on this plant, through genetic accommodation and later pos-
sibly through character release, allowing utilization of the novel
plant to evolve more independently (WEST-EBERHARD 2003, NYLIN
& JANZ 2009).
Host shifts with loss of the ancestral host likely require
evolutionary modification of host utilization traits after the
initial colonization. The extent to which such modification
will happen will depend on both local circumstances and evo-
lutionary history. The butterfly Pieris napi Linnaeus, 1758 regu-
larly oviposited on the introduced Thlaspi arvense Linnaeus,
although the plant was lethal for the larvae (CHEW 1977), and
apparently this situation has not changed (CAROL BOGGS, per-
sonal communication). Presumably, the introduced plant con-
tains a similar oviposition “resource” as local hosts, but a dif-
ferent larval feeding “resource”. Mortality is 100%, leaving no
opportunity for evolutionary modification enabling a host shift.
FOX et al. (1997) reported that initial colonization of Chloroleucon
ebano (Berland.) L. Rico by the seed beetle Stator limbatus Horn,
1873 depended on pre-existing variance in the capacity to ac-
cept and utilize this novel host, and populations expanding
their host range to include this species had not locally adapted
to it. One reason for the lack of local adaptation was a signifi-
cant non-genetic effect of maternal host plant on offspring
survival on the novel host (FOX et al. 1997). Hence, successful
establishment on C. ebano depends on local co-occurrence of
one of the other hosts in the repertoire of S. limbatus.
These examples show that successful host shifts depend
on the history of the association, as well on life history, abun-
dance and distribution of the species involved. Hence, to un-
derstand and possibly predict host shifts, both ecological (eco-
logical fitting, local contingency) and evolutionary (evolution-
ary past, degree of plasticity, genetic variation) processes need
to be considered (BROOKS & MCLENNAN 2002).
Our thesis is that otherwise specialized parasites can shift
rapidly to novel (naïve) hosts via ecological fitting and that these
host shifts play an “important” role in the ecology and evolu-
tion of host-parasite associations. “Important” implies that eco-
logical fitting between hosts and parasites occurs with high
enough frequency to influence host range dynamics and the
diversity of species and interactions among species. Although
no quantitative statement of this importance can be made, it is
clear from the above discussion that shifts onto relatively unre-
lated hosts can be inferred routinely in phylogenetic analyses
and observed readily in contemporary ecological time. These
observations are fundamental for emerging infectious disease
(EID) studies: EID arise when parasite species begin infecting
and causing disease in host species with which they have no
previous history of association. If the nature of host specificity
is such that the potential for ecological fitting is small, then
host shifts are likely to be rare and attention can be focused on
managing each EID as it emerges. Little attention need be paid
to its origins, beyond a search for the taxonomic identity of the
parasite acting as the pathogen, and its immediate reservoir.
However, if the nature of host specificity is such that the poten-
tial for ecological fitting is large, then host shifts are likely to be
common, and a more predictive, pre-emptive framework for
managing EID will be needed, greatly increasing the challenge
of an already difficult problem.
As discussed earlier, empirical studies indicate that few
parasite groups conform to the phylogenetic patterns of host-
parasite associations expected if opportunities for ecological
fitting were relatively rare. Clades such as ectoparasitic
arthropods which exhibit limited host switching (HAFNER &
NADLER 1988, PATTERSON & POULIN 1999, PAGE 2003), although
interesting to evolutionary biologists and ecologists, cannot
form the general conceptual framework for dealing with EID
because they are rare. The majority of cases indicate substan-
tial host switching throughout history, and extensive diversifi-
cation through cospeciation appears to be limited (reviewed in
al. 2006).
Climate change and ecological perturbation as
drivers of EID
As the human population grows daily, its ecological and
technogical footprint deepens. Introducing ourselves and other
species into novel regions of the biosphere accelerates land-
scape alteration and ecological perturbation, which in global
ecosystems can initiate events that link climate change, loss of
biodiversity and EID (DASZAK et al. 2000, HARVELL et al. 2002,
WOOLHOUSE 2002, EPSTEIN et al. 2003, BROOKS & FERRAO 2005,
POUNDS et al. 2006). Such events include increased biotic mix-
ing of evolutionarily unfamiliar species, and therefore increased
opportunities for parasites and pathogens to find and infect
157How specialists can be generalists
ZOOLOGIA 27 (2): 151–162, April, 2010
novel hosts. How we adapt to these changes will depend on
how well we understand and use knowledge of the responses
of host-parasite systems during episodes of large-scale climate
and environmental change.
The taxon pulse hypothesis (ERWIN et al. 1979, ERWIN 1981)
predicts that historical biogeographic patterns result from al-
ternating episodes of biotic expansion and isolation, which lead
to complex geographic distributions. Recent empirical studies
in historical biogeography that document marked influence of
taxon pulses (HOBERG 1995, BOUCHARD et al. 2004, BROOKS & FERRAO
2005, BROOKS & FOLINSBEE 2005, HALAS et al. 2005, ZARLENGA et al.
2006, FOLINSBEE & BROOKS 2007) implicate geological phenom-
ena, such as tectonic changes and climatological phenomena,
including global or regional climate change, as taxon pulse
drivers. During biotic expansion phases, susceptible hosts come
into contact with novel (for them) parasites. Host switching
occurs rapidly, without the need for any evolutionary innova-
tion. For example, alternating cycles of biotic expansion and
isolation across Beringia at the crossroads of the northern con-
tinents are clearly associated with cyclical episodes of climate
change in the Pleistocene epoch (HOBERG 1995, ZARLENGA et al.
2006, WALTARI et al. 2007, COOK et al. 2005). Natural selection
acts only on what has happened, so there will have been no
opportunity for the evolution of resistance to, or tolerance of,
the parasite by the new hosts. This suggests that most host
switching occurs in conjunction with episodes of global cli-
mate change and associated biotic expansion and altered
trophic relationships. This has been demonstrated for tape-
worms (Taenia spp.) in humans, hookworms (Oesophagostomum
Raillet & Henry, 1913) and pinworms (Enterobius Leach, 1853)
in hominoids, and nematodes (Trichinella Railliet, 1895) in car-
nivores (HOBERG et al. 2001, BROOKS & FERRAO 2005, BROOKS &
The emerging story of human parasites is one of ancestral, eco-
logical associations with secondary host switches since the
Pliocene associated with ecological perturbation.
More recent human activities associated with the evolu-
tion of agriculture, domesticated livestock, urbanization, and
now global climate change have served to broaden the arena
and disseminate the risk for EID on a global scale. If current
climate changes have a prolonged duration and global scope,
we should expect an increase in EID. Predicted responses to
climate change by hosts and parasites include biotic expan-
sion with geographic colonization, shifting patterns of geo-
graphic range, changing phenology and habitat use, modifica-
tion of ecotones and contact zones (PARMESAN 2006, HOBERG &
BROOKS 2008), and local extinction (POUNDS et al. 2006,
MARCOGLIESE 2001). Global and regional climate change events
have had major influences on biotic structure and the distri-
bution of host-parasite assemblages throughout earth history
(HOBERG & BROOKS 2008), but recent cases might result from
anthropogenic effects beyond those caused by climate warm-
et al. 2002, LAFFERTY et al. 2004, KUTZ et al. 2004). Microevolu-
tionary responses including mosaic-like, ephemeral patterns
of local adaptation, directional changes in gene frequencies
through mutation, and selection for parasites associated with
emergence (DOBSON & FOUFOPOULUS 2001, THOMPSON 2005) have
not yet been linked directly to climate change. However, such
changes could begin with host shifts and outbreaks of disease
on local spatial and fine temporal scales, leading to ‘mosaics
of emergence’ (THOMPSON 2005, HOBERG & BROOKS 2008). New
associations might proliferate and emerge through ecological
fitting, potentially associated with disease in a changing array
of ‘reservoir’ hosts (DOBSON & FOUFOPOULUS 2001, HAYDON et al.
Complete understanding of the complex history of host-
parasite associations requires consideration of multiple, non-
mutually exclusive evolutionary and ecological mechanisms
and phenomena (BROOKS & MCLENNAN 2002, BROOKS et al. 2006b,
HOBERG & BROOKS 2008, BROOKS & HOBERG 2008), but we believe
that host shifts via ecological fitting provide a missing link in
our general understanding of the evolution and diversification
of host-parasite interactions. When ecological fitting provides
the necessary first step in the colonization process by initiat-
ing a host shift, it also provides essential raw material for co-
evolutionary interactions. Ecological fitting allows genotypes
to be exposed to novel selection regimes.
The geographic mosaic theory of coevolution (THOMPSON
1994, 2005) emphasizes the interplay between local adapta-
tion and gene flow in geographically structured populations.
Species can interact in different ways, and with different spe-
cies in different parts of its geographic range. This mosaic of
interactions can lead to the buildup and breakdown of locally
adapted coevolutionary hot spots depending on gene flow and
the local presence or absence of other interacting species (TH-
OMPSON & FERNANDEZ 2006). This perspective provides an appre-
ciation for the observation that polyphagous species are often
comprised of geographically-structured populations associated
with small sub-sets of the total species in the parasites host
range (FOX & MORROW 1981). Raw material for coevolution,
however, must be constantly regenerated through colonization
of novel resources in parts of a species geographic distribution
(JANZ & THOMPSON 2002, SINGER et al. 2008), which is made pos-
sible by ecological fitting via resource tracking and the explo-
ration of sloppy fitness space. Coevolutionary processes can
buffer a species against fragmentation, or promote diversifica-
tion depending on the nature and strength of processes acting
on local and regional scales (THOMPSON 1994, 2005, BENKMAN
1999, GODSOE et al. 2008). Host colonization by ecological fit-
ting promotes diversification only to the extent that the geo-
graphic mosaic allows local adaptation to newly formed hosts
and sufficient isolation from other populations (AGOSTA &
KLEMENS 2008).
158 S. J. Agosta et al.
ZOOLOGIA 27 (2): 151–162, April, 2010
Host shifts initiated by ecological fitting are not an end-
point, but rather one step in the process that fuels biological
expansion and generates novel combinations of interacting
species. From these novel interactions, ecological fitting can
promote evolutionary stasis (e.g., if there are many ecologi-
cally fit populations connected by sufficient gene flow) or fa-
cilitate evolutionary diversity, through subsequent divergent
local adaptation (AGOSTA & KLEMENS 2008). JANZ et al. (2006),
JANZ & NYLIN (2008), and NYLIN & JANZ (2009) recently proposed
that diversification in these systems is driven by repeated “os-
cillations” in host range. Coupled with taxon pulses, the oscil-
lation hypothesis predicts phases of host expansion during
geographic range expansion followed by phases of host spe-
cialization during geographic isolation (or, alternatively, sym-
patric speciation by host race formation). As with the geo-
graphic mosaic concept (THOMPSON 2005), the oscillation hy-
pothesis relies on constant regeneration of variation in host
use; it is the diversification of host use that drives diversifica-
tion of species whether the actual speciation process relies on
allopatric or non-allopatric modes (JANZ & NYLIN 2008).
In terms of EID, climate and disturbance driven taxon
pulses in geographic range and oscillations in host range can be
expected to influence their frequency, whereby periods of range
shifts and expansions increase biotic mixing and the opportu-
nities for ecological fitting to occur. The current EID crisis is
“new” only in the sense that this is the first such event that
scientists have witnessed directly. Previous episodes through
earth history of global climate change and ecological perturba-
tion, broadly defined, have been associated with environmental
disruptions that could have led to EID (BROOKS & HOBERG 2006,
HOBERG & BROOKS 2008). From an epidemiological standpoint,
episodes of global climate change should be expected to be as-
sociated with the origins of new host-parasite associations and
bursts of EID. The combination of taxon pulses and ecological
fitting suggests that host and parasite species with the greatest
ability to disperse should be the primary source of EID (BROOKS &
2005). Paleontological studies suggest that species with large
geographic ranges and with high ability to disperse are most
successful at surviving large scale environmental perturbation
and mass extinctions (STIGALL & LIEBERMAN 2006). Thus, the spe-
cies most successful at surviving global climate changes will be
the primary sources of EID, so host extinction will not limit the
risk of EID. From the standpoint of taxon pulses and ecological
fitting, the planet is an evolutionary and ecological minefield of
EID through which millions of people wander daily.
We thank the people who hosted and attended the 2008
“Blod Bad” conference in Tovetorp, Sweden for providing a
stimulating atmosphere for discussing these ideas and a forum
for the developement of this manuscript.
AGOSTA, S.J. 2006. On ecological fitting, plant-insect associations,
herbivore host shifts, and host plant selection. Oikos 114:
AGOSTA, S.J. & J.A. KLEMENS. 2008. Ecological fitting by
phenotypically flexible genotypes: implications for species
associations, community assembly and evolution. Ecology
Letters 11: 1123-1134.
AGOSTA, S.J. & J.A. KLEMENS. 2009. Resource specialization in a
phytophagous insect: no evidence for genetically based
performance tradeoffs across hosts in the field or laboratory.
Journal of Evolutionary Biology 22: 907-912
AGRAWAL, A.A. 2000. Host-range evolution: adaptation and trade-
offs in fitness of mites on alternative hosts. Ecology 81:
ANTONOVICS, J.; M. HOOD & J. PARTAIN. 2002 The ecology and
genetics of a host shift: Microbotryum as a model system.
American Naturalist 160: S40-S53.
BECERRA, J. X. 1997. Insects on plants: macroevolutionary
chemical trends in host use. Science 276: 253-256.
BENKMAN, C.W. 1999. The selection mosaic and diversifying
coevolution between crossbills and lodgepole pine.
American Naturalist 53: S75-S91.
BERNAYS, E.A. 1989. Host range in phytophagous insects: the
potential role of generalist predators. Evolutionary Ecology
3: 299-311.
BERNAYS, E.A. 2001. Neural limitations in phytophagous insects:
implications for diet breadth and evolution of host
affiliation. Annual Review of Entomology 46: 703-727.
BOUCHARD, P.; D.R. BROOKS & D.K. YEATES. 2004. Mosaic
macroevolution in Australian wet tropics arthropods:
community assemblage by taxon pulses, p. 425-469. In: E.
BERMINGHAM, C.W. DICK & C. MORITZ (Eds). Tropical rainforest:
past, present, future. Chicago, University of Chicago Press.
BROOKS, D.R. 1979. Testing the context and extent of host-
parasite coevolution. Systematic Zoology 28: 299-307.
BROOKS, D.R. 1985. Historical ecology: a new approach to
studying the evolution of ecological associations. Annals
of the Missouri Botanical Garden 72: 660-680.
BROOKS, D.R. & A.L. FERRAO. 2005. The historical biogeography
of coevolution: emerging infectious diseases are evolutionary
accidents waiting to happen. Journal of Biogeography 32:
BROOKS, D.R. & K.E. FOLINSBEE. 2005. Paleobiogeography:
documenting the ebb and flow of evolutionary diversification.
Paleontological Society Papers 11: 15-43.
BROOKS, D.R. & E.P. HOBERG. 2006. Systematics and emerging
infectious diseases: from management to solution. Journal
of Parasitology 92: 426-429.
BROOKS, D.R. & E.P. HOBERG. 2007. How will global climate change
affect parasite-host assemblages? Trends in Parasitology 23:
159How specialists can be generalists
ZOOLOGIA 27 (2): 151–162, April, 2010
BROOKS, D.R. & E.P. HOBERG. 2008. Darwin’s necessary misfit and
the sloshing bucket: the evolutionary biology of emerging
infectious diseases. Evolution Education Outreach 1: 2-9.
BROOKS, D.R. & D.A. MCLENNAN. 1991. Phylogeny, ecology, and
behavior. Chicago, University of Chicago Press.
BROOKS, D.R. & D.A. MCLENNAN. 1993. Parascript: parasites and
the language of evolution. Washington DC, Smithsonian
Institution Press.
BROOKS, D.R. & D.A. MCLENNAN. 2002. The nature of diversity:
an evolutionary voyage of discovery. Chicago, University
of Chicago Press.
BROOKS, D.R. & M.G.P. VAN VELLER. 2008. Assumption 0 analysis:
comparative evolutionary biology in the age of complexity.
Annals of the Missouri Botanical Garden 95: 201-223.
2006a. Phylogeny, ecological fitting and lung flukes: helping
solve the problem of emerging infectious diseases. Revista
Mexicana de Biodiversidad 77: 225-233.
2006b. Ecological fitting as a determinant of parasite
community structure. Ecology 87: S76-S85.
CARROLL, S.P.; H. DINGLE & S.P. KLASSEN. 1997. Genetic
differentiation of fitness-associated traits among rapidly
evolving populations of the soapberry bug. Evolution 51:
CHEW, F.S. 1977. Coevolution of pierid butterflies and their
cruciferous food plants. II. The distribution of eggs on
potential food plants. Evolution 31: 568-579.
CLEAVELAND, S.; M.K. LAURENSON & L.H. TAYLOR. 2001. Diseases of
humans and their domestic mammals: pathogen
characteristics, host range and the risk of emergence.
Philosophical Transactions of the Royal Society of
London, Series B, 356: 991-999.
& V. HAUKISALMI. 2005. Beringia: intercontinental exchange
and diversification of high latitude mammals and their
parasites during the Pliocene and Quaternary. Mammal
Study 30: S33-S44.
CORNELL, H.V. & B.A. HAWKINS. 1993. Accumulation of native
parasitoid species on introduced herbivores: a comparison
of hosts as natives and hosts as invaders. American
Naturalist 141: 847-865.
DASZAK, P.; A.A. CUNNINGHAM & A.D. HYATT . 2000. Emerging
infectious diseases of wildlife – threats to biodiversity and
human health. Science 287: 443-449.
DOBSON, A. & J. FOUFOPOULUS. 2001. Emerging infectious
pathogens of wildlife. Philosophical Transactions of the
Royal Society of London, Series B, 356: 1001-1012.
RAIS; I.R. DINIZ; T.A. KURSAR & P.D. COLEY. 2007. Host specificity
of Lepidoptera in tropical and temperate forests. Nature 448:
EHRLICH, P.R. & P.H. RAVEN. 1964. Butterflies and plants: a study
in coevolution. Evolution 18: 586-608.
EPSTEIN, P.R.; E. CHIVIAN & K. FRITH. 2003. Emerging diseases
threaten conservation. Environmental Health Perspectives
111: A506-A507.
ERWIN, T.L. 1979. Thoughts on the evolutionary history of
ground beetles: hypotheses generated from comparative
faunal analyses of lowland forest sites in temperate and tro-
pical regions, p. 539-592. In: T.L. ERWIN; G.E. BALL & D.R.
WHITEHEAD (Eds). Carabid beetles – their evolution, natu-
ral history, and classification. The Hauge W. Junk.
ERWIN, T.L. 1981. Taxon pulses, vicariance, and dispersal: an
evolutionary synthesis illustrated by carabid beetles, p. 159-
196. In: G. NELSON & D.E. ROSEN (Eds). Vicariance
biogeography – a critique. New York, Columbia University
ERWIN, T.L.; G.E. BALL & D.R. WHITEHEAD. 1979. Carabid beetles
– their evolution, natural history, and classification. The
Hauge W. Junk.
FENTON, A. & A.B. PEDERSEN. 2005. Community epidemiology
framework for classifying disease threats. Emerging
Infectious Diseases 11: 1815-1821.
FOLINSBEE, K. & D.R. BROOKS. 2007. Early hominoid biogeography:
pulses of dispersal and differentiation. Journal of
Biogeography 34: 383-397.
FOX, C.W.; J.A. NILSSON & T.A. MOUSSEAU. 1997. The ecology of
diet expansion in a seed-feeding beetle: pre-existing variation,
rapid adaptation and maternal effects? Evolutionary Ecology
11: 183-194.
FOX, L.R. & P.A. MORROW. 1981. Specialization: species property
or local phenomenon? Science 211: 887-893.
FUTUYMA, D.J. & G. MORENO. 1988. The evolution of ecological
specialization. Annual Review of Ecology and Systematics
19: 207-233.
FUTUYMA, D.J. & C. MITTER. 1996. Insect-plant interactions: the
evolution of component communities. Philosophical
Transactions of the Royal Society of London, Series B,
351: 1361-1366.
FUTUYMA, D.J.; M.C. KEESE & D.J. FUNK. 1995. Genetic constraints
on macroevolution: the evolution of host affiliation in the
leaf beetle genus Ophraella. Evolution 49: 797-809.
Coevolution and divergence in the Joshua tree/yucca moth
mutualism. American Naturalist 171: 816-823.
GOULD, S.J. & R.C. LEWONTIN. 1979. The spandrels of San Marco
and the Panglossian paradigm: a critique of the adaptationist
programme. Proceedings of the Royal Society of London,
Series B, 205: 581-598.
GOULD, S.J. & E.S. VRBA. 1982. Exaptation – a missing term in
the science of form. Paleobiology 8: 4-15.
HAFNER, M.S. & S.A. NADLER. 1988. Phylogenetic trees support
the coevolution of parasites and their hosts. Nature 332:
160 S. J. Agosta et al.
ZOOLOGIA 27 (2): 151–162, April, 2010
HALAS, D.; D. ZAMPARO & D.R. BROOKS. 2005. A protocol for
studying biotic diversification by taxon pulses. Journal of
Biogeography 32: 249-260.
R.S. OSTFELD & M.D. SAMUEL. 2002. Ecology, climate warming
and disease risks for terrestrial and marine biota. Science
296: 2158-2162.
Identifying reservoirs of infection: a conceptual and practical
challenge. Emerging Infectious Diseases 8: 1468-1473.
HOBERG, E.P. 1995. Historical biogeography and modes of
speciation across high latitude seas of the Holarctic: concepts
for host-parasite coevolution among the Phocini (Phocidae)
and Tetrabothriidea (Eucestoda). Canadian Journal of
Zoology 73: 45-57.
HOBERG, E.P. & D.R. BROOKS. 2008. A macroevolutionary mosaic:
episodic host-switching, geographical colonization and
diversification in complex host-parasite systems. Journal
of Biogeography 35: 1533-1550.
HOBERG, E.P. & D. R. BROOKS. 2010. Beyond vicariance: integrating
taxon pulses, ecological fitting and oscillation in evolution
and historical biogeography, in press. In: S. MORAND & B.
KRASNOV (Eds). The biogeography of host-parasite
interactions. Oxford, Oxford University Press.
HOBERG, E.P. & G.J. KLASSEN. 2002. Revealing the faunal tapestry:
co-evolution and historical biogeography of hosts and
parasites in marine systems. Parasitology 124: S3-S22.
Africa: origins of the Taenia tapeworms in humans.
Proceedings of the Royal Society of London, Series B,
268: 781-787.
HOMLES, J.C. & P.W. PRICE. 1980. Parasite communities: the roles
of phylogeny and ecology. Systematic Zoology 29: 203-213.
JANZ, N. 2002. Evolutionary ecology of oviposition strategies,
p. 349-376. In: M. HILKER & T. MEINERS (Eds). Chemoecology
of insect eggs and egg deposition. Berlin, Blackwell.
JANZ, N. & S. NYLIN. 1998. Butterflies and plants: a phylogenetic
study. Evolution 52: 486-502.
JANZ, N. & S. NYLIN. 2008. The oscillation hypothesis of host plant-
range and speciation, p. 203-215. In: K.J. TILMON (ED).
Specialization, speciation, and radiation: the evolutionary
biology of herbivorous insects. Berkley, University of
California Press.
JANZ, N. & J.N. THOMPSON. 2002. Plant polyploidy and host
expansion in an insect herbivore. Oecologia 130: 570-575.
JANZ, N.; A. BERGSTRÖM & A. SJÖGREN. 2005. The role of nectar
sources for oviposition decisions of the common blue
butterfly Polyommatus icarus. Oikos 109: 535-538.
JANZ, N.; S. NYLIN & K. NYBLOM. 2001. Evolutionary dynamics of
host plant specialization: a case study of the tribe
Nymphalini. Evolution 55: 783-796.
JANZ, N.; S. NYLIN & N. WAHLBERG. 2006. Diversity begets diversity:
host expansions and the diversification of plant-feeding
insects. BMC Evolutionary Biology 6: 4.
JANZEN, D.H. 1980. When is it coevolution? Evolution 34: 611-
JANZEN, D.H. 1985. On ecological fitting. Oikos 45: 308-310.
JANZEN, D.H. & P.S. MARTIN. 1982. Neotropical anachronisms:
the fruits the Gomphotheres ate. Science 215: 19-27.
JANZEN, D.H. & W. HALLWACHS. 2009. Event-based database of
caterpillars, their host plants, and their parasitoids in
the Area de Conservación Guanacaste, northwestern
Costa Rica. Available online at:
[Accessed: 05/IV/2010]
JERMY, T. 1984. Evolution of insect-host plant relationships.
American Naturalist 124: 609-630.
JOHANSSON, J.; A. BERGSTROM & N. JANZ. 2007. Search efficiency
and host range expansion in a polyphagous butterfly: the
benefit of additional oviposition targets. Journal of Insect
Science 7: 3.
KELLEY, S.T. & D.B. FARREL. 1998. Is specialization a dead end?
The phylogeny of host use in Dendroctonus bark beetles
(Scolytidae). Evolution 52: 1731-1743.
TOMPKINS. 2009. Parasite spillback: a neglected concept in
invasion ecology? Ecology 90: 2047-2056.
Both host-plant phylogeny and chemistry have shaped the
African seed-beetle radiation. Molecular Phylogenetics and
Evolution 35: 602-611.
Emerging parasitic infections in arctic ungulates. Integrative
and Comparative Biology 44: 109-118.
LAFFERTY, K.D.; J.W. PORTER & S.E. FORD. 2004. Are diseases increasing
in the ocean? Annual Review of Ecology, Evolution and
Systematics 35: 31-54.
LANDE, R. & S.J. ARNOLD. 1983. The measurement of selection on
correlated characters. Evolution 37: 1210-1226.
LARSSON, S. & B. EKBOM. 1995. Oviposition mistakes in
herbivorous insects: confusion or a step towards a new host
plant? Oikos 72: 155-160.
LOVEJOY, T.E. & L. HANNAH. 2005. Climate change and
biodiversity. New Haven, Yale University.
MARCOGLIESE, D.J. 2001. Implications of climate change for
parasitism of animals in the aquatic environment. Canadian
Journal of Zoology 79: 1331-1352.
MAYNARD SMITH, J. & E. SZATHMARY. 1995. The major transitions
in evolution. Oxford, W.H. Freeman.
MORAN, N.A. 1988. The evolution of host-plant alternation in
aphids: evidence for specialization as a dead end. American
Naturalist 132: 681-706.
MURPHY, S.M. & P. FEENY. 2006. Chemical facilitation of a naturally
occurring host shift by Papilio machaon butterflies (Papilioni-
dae). Ecological Monographs 76: 399-414.
NOSIL, P. 2002. Transition rates between specialization and genera-
lization in phytophagous insects. Evolution 56: 1701-1706.
161How specialists can be generalists
ZOOLOGIA 27 (2): 151–162, April, 2010
NOSIL, P. & A.Ø. MOOERS. 2005. Testing hypotheses about
ecological specialization using phylogenetic trees. Evolution
59: 2256-2263.
NOVOTNY, V. & Y. BASSET. 2005. Host specificity of insect
herbivores in tropical forests. Proceedings of the Royal
Society of London, Series B, 272: 1083-1090.
NUISMER, S. L. & J.N. THOMPSON. 2001. Plant polyploidy and non-
uniform effects on insect herbivores. Proceedings of the
Royal Society of London, Series B, 268: 1937-1940.
NYLIN, S. & N. JANZ. 2009. Butterfly host plant range: an example
of plasticity as a promoter of speciation? Evolutionary
Ecology 23: 137-146.
NYMAN, T. 2009. To speciate, or not to speciate? Resource
heterogeneity, the subjectivity of similarity, and the macro-
evolutionary consequences of niche-width shifts in plant-
feeding insects. Biological Reviews: doi: 10.1111/j.1469-
PAGE, R.D.M. 2003. Tangled trees. Chicago, University of Chi-
cago Press.
PARMESAN, C. 2006. Ecological and evolutionary responses to
recent climate change. Annual Review of Ecology,
Evolution and Systematics 37: 637-669.
PATERSON, A.M. & R. POULIN. 1999. Have chondracanthid
copepods co-speciated with their teleost hosts? Systematic
Parasitology 44: 79-85.
STILL & B.E. YOUNG. 2006. Widespread amphibian extinctions
from epidemic disease driven by global warming. Nature
439: 161-167.
PRICE, P.W. 1980. Evolutionary biology of parasites. Princeton,
Princeton University Press.
RADTKE, A.; D.A. MCLENNAN & D.R. BROOKS. 2002. Resource
tracking in North American Telorchis sp (Digenea:
Plagiochiformes: Telorchidae). Journal of Parasitology 88:
SCHEFFER, S.J. & B.M. WIEGMANN. 2000. Molecular phylogenetics
of the holly leaf miners (Diptera: Agromyzidae: Phytomyza):
species limits, speciation, and dietary specialization.
Molecular Phylogenetics and Evolution 1: 244-255.
Multiple origins of polyploidy and the geographic structure
of Heuchera grossulariifolia. Molecular Ecology 8: 253-262.
SINGER, M.C. 2003. Spatial and temporal patterns of checkerspot
butterfly-hostplant association: the diverse roles of
oviposition preference, p. 207-228. In: C.L. BOGGS; W.B. WATT
& P.R. EHRLICH (Eds). Ecology and evolution taking flight:
butterflies as model study systems. Chicago, University
of Chicago Press.
SINGER, M.C.; C.D. THOMAS & C. PARMESAN. 1993. Rapid human-
induced evolution of insect-host associations. Nature 366:
SINGER, M.C.; B. WEE & S. HAWKINS. 2008. Rapid anthropogenic
and natural diet evolution: three examples from checkerspot
butterflies, p. 311-324. In: K.J. TILMON (Ed). Specialization,
speciation, and radiation: the evolutionary biology of
herbivorous insects. Berkeley, University of California Press.
SINGER, M.S. 2008. Evolutionary ecology of polyphagy, p. 29-
42. In: K.J. TILMON (Ed). Specialization, speciation, and
radiation: the evolutionary biology of herbivorous
insects. Berkeley, University of California Press.
STIGALL, A.L. & B.S. LIEBERMAN. 2006. Quantitative palaeo-
biogeography: GIS, phylogenetic biogeographical analysis,
and conservation insights. Journal of Biogeography 33:
STRAUSS, S.Y.; LAU J.A. & S.P. CARROLL. 2006. Evolutionary responses
of natives to introduced species: what do introductions tell
us about natural communities? Ecology Letters 9: 357-374.
STRONG, D.R. 1979. Biogeographic dynamics of insect-host plant
communities. Annual Review of Entomology 24: 89-119.
SYMONS, F.B. & G.W. BECCALONI. 1999. Phylogenetic indices for
measuring the diet breadths of phytophagous insects.
Oecologia 119: 427-434.
TABASHNIK, B.E. 1983. Host range evolution: the shift from native
legume hosts to alfalfa by the butterfly, Colias philodice
eriphyle. Evolution 37: 150-162.
Feeding specialization and host-derived chemical defense
in Chrysomeline leaf beetles did not lead to an evolutionary
dead end. Proceedings of the National Academy of
Science, USA 98: 3909-3914.
THOMPSON, J.N. 1994. The coevolutionary process. Chicago,
University of Chicago Press.
THOMPSON, J.N. 1998. Rapid evolution as an ecological process.
Trends in Ecology and Evolution 13: 329-332.
THOMPSON, J.N. 2005. The geographic mosaic of coevolution.
Chicago, University of Chicago Press.
THOMPSON, J.N. & C.C. FERNANDEZ. 2006. Temporal dynamics of
antagonism and mutualism in a geographically variable
plant-insect interaction. Ecology 87: 103-112.
THOMPSON, J.N.; S.L. NUISMER & K. MERG. 2004. Plant polyploidy
and the evolutionary ecology of plant/animal interactions.
Biological Journal of the Linnaean Society 82: 511-519.
VAN KLINKEN, R.D. & O.R. EDWARDS. 2002. Is host-specificity of
weed biological control agents likely to evolve rapidly
following establishment? Ecology Letters 5: 590-596.
VIA, S. 1991. The population structure of fitness in a spatial
network: demography of pea aphid clones from two crops
in a reciprocal transplant. Evolution 45: 827-852.
WAHLBERG, N. 2001. The phylogenetics and biochemistry of host
plant specialization in melitaeine butterflies (Lepidoptera:
Nymphalidae). Evolution 55: 522-537.
WALTARI, E.; E.P. HOBERG; E.P. LESSA & J. COOK. 2007. Eastward
Ho: phylogeographical perspectives on colonization of hosts
and parasites across the Beringian nexus. Journal of
162 S. J. Agosta et al.
ZOOLOGIA 27 (2): 151–162, April, 2010
Biogeography 34: 561-574.
WEST-EBERHARD, M.J. 2003. Developmental plasticity and
evolution. New York, Oxford University Press.
WIEGMANN, B.M.; C. MITTER & B. FARRELL. 1993. Diversification of
carnivorous parasitic insects – extraordinary radiation or
specialized dead-end? American Naturalist 142: 737-754.
WINKLER, I.S. & C. MITTER. 2008. The phylogenetic dimension of
insect-plant interactions: a review of recent evidence, p. 240-
263. In: K.J. TILMAN (Ed). The evolutionary biology of
herbivorous insects: specialization, speciation, and
radiation. Berkeley, University of California Press.
WOOLHOUSE, M.E.J. 2002. Population biology of emerging and
Submitted: 02.II.2010; Accepted: 05.IV.2010.
Editorial responsibility: Walter P. Boeger
reemerging pathogens. Trends in Microbiology 10 (Suppl.):
Testing the trend towards specialization in herbivore-host
plant associations using a molecular phylogeny of Tomoplagia
(Diptera: Tephritidae). Molecular Phylogenetics and
Evolution 35: 701-711.
2006. Post-Miocene expansion, colonization, and host
switching drove speciation among extant nematodes of the
archaic genus Trichinella. Proceedings of the National
Academy of Sciences, USA 103: 7354-7359.
... Pathogens are usually thought to be specialists to their host species and, hence, trapped in a single lineage of hosts (Haldane, 1951;Gioti et al., 2013;Rychener et al., 2017;Scheiner and Mindell, 2019). However, pathogens are resource specialists (Agosta et al., 2010), and specific sets of resources may be widespread among distinct host species. Often what has been assumed to be coadaptation or coevolution reflects a process of ecological fitting (EF) (Janzen, 1985;Brooks and McLennan, 2002;Agosta, 2006;Agosta and Klemens, 2008) (see Box 1). ...
... By exploring the available capacity represented by the SFS (Agosta and Klemens, 2008;Agosta et al., 2010), a pathogen can colonize new hosts, exploiting new elements of a community (i.e., the resources offered by hosts). During the simulation presented in Araujo et al. (2015), part of the pathogen population tries to colonize a new host but only a fraction succeeds. ...
... While the involvement of other mammal species in the dynamics of SARS-COV-2 has been reported since the beginning of the COVID-19 pandemic, most researchers ignored it, assuming a more traditional perspective on the evolution of pathogens-that pathogens are highly specialized and incapable of crossing host barriers easily, except when releasing mutations occur (CDC, 2022). The SP predicted (Agosta et al., 2010;Brooks et al., 2014Hoberg and Brooks, 2015) and it is recently becoming empirically evident (Fenollar et al., 2021;Kuchipudi et al., 2022;Mallapaty, 2022) that nonhuman mammals (at least) likely play a significant role, not only as reservoirs for the virus in urban, peri-urban, and wildlife systems but also on the origin of new variants Hoberg et al., 2022). The above-proposed dynamics of pathogenic species was replicated in many regions of the planet, involving most likely a much larger number of species than we presently know . ...
Emerging infectious diseases (EIDs) are, besides a question of food safety and public health, an ecological and evolutionary issue. The recognition of this condition combined with the accumulation of evidence that pathogens are not specialists in their original hosts evidences the need for understanding how the dynamics of interaction between pathogens and hosts occurs. The Stockholm Paradigm (SP) provides the theoretical fundaments to understand the dynamics of diseases and design proactive measures to avoid the emergence and reemergence of infectious diseases. In this review, we revisit the models that evaluate several aspects of the proposed dynamics of the SP, including the complexity nature of the elements that have been associated with this new framework for the evolution of associations. We integrate the results from these studies into a putative dynamic of infectious diseases, discuss subordinate elements of this dynamic, and provide suggestions on how to integrate these findings into the DAMA (Document, Assess, Monitor, Act) protocol.
... Species in the Tremella caloplacae complex seem to be specialists restricted to grow on a single genus or species in the Teloschistaceae. The fact that parasites are often specialists with restricted host ranges and that at the same time they commonly switch onto different hosts along their evolutionary history has been referred to as the 'parasite paradox' (Agosta et al., 2010). The so-called 'Stockholm Paradigm' (e.g., McLennan and Brooks, 2002;Agosta et al., 2010;Janz, 2011;Hoberg and Brooks, 2015) solved this paradox suggesting that host switching and host range expansion are more often the consequence of taking advantage of opportunities offered by a changing host landscape than of the previous evolution of novel host-use capabilities of the parasite. ...
... The fact that parasites are often specialists with restricted host ranges and that at the same time they commonly switch onto different hosts along their evolutionary history has been referred to as the 'parasite paradox' (Agosta et al., 2010). The so-called 'Stockholm Paradigm' (e.g., McLennan and Brooks, 2002;Agosta et al., 2010;Janz, 2011;Hoberg and Brooks, 2015) solved this paradox suggesting that host switching and host range expansion are more often the consequence of taking advantage of opportunities offered by a changing host landscape than of the previous evolution of novel host-use capabilities of the parasite. The Stockholm paradigm lays, among others, on the concept of Ecological Fitting (Janzen, 1985). ...
Lichenicolous fungi are a heterogeneous group of organisms that grow exclusively on lichens, forming obligate associations with them. It has often been assumed that cospeciation has occurred between lichens and lichenicolous fungi, but this has been seldom analysed from a macroevolutionary perspective. Many lichenicolous species are rare or are rarely observed, which results in frequent and large gaps in the knowledge of the diversity of many groups. This, in turn, hampers evolutionary studies that necessarily are based on a reasonable knowledge of this diversity. Tremella caloplacae is a heterobasidiomycete growing on various hosts from the lichen-forming family Teloschistaceae, and evidence suggests that it may represent a species complex. We combine an exhaustive sampling with molecular and ecological data to study species delimitation, cophylogenetic events and temporal concordance of this association. Tremella caloplacae is here shown to include at least six distinct host-specific lineages (=putative species). Host switch is the dominant and most plausible event influencing diversification and explaining the coupled evolutionary history in this system, although cospeciation cannot be discarded. Speciation in T. caloplacae would therefore have occurred coinciding with the rapid diversification – by an adaptive radiation starting in the late Cretaceous – of their hosts. New species in T. caloplacae would have developed as a result of specialization on diversifying lichen hosts that suddenly offered abundant new ecological niches to explore or adapt to.
... Identification across many groups of pathogens (e.g., among macroparasites) has remained linked to host association under the idea that knowing the host provides fundamental insight into knowing parasite identity and to expectations emerging from assumptions about cospeciation and specificity (Nylin et at., 2018;Brooks et al., 2019). Identity linked to host taxonomy rather than parasite attributes, whether morphological or molecular, continues to codify a centuries-old, host-centric expectation of the distribution of parasite diversity that has been powerfully refuted (e.g., Agosta et al., 2010;Brooks et al., 2015Brooks et al., , 2019Nylin et al., 2018). Host-based identification of parasites, however, continues as a common theme in wildlife biology and veterinary medicine, and such identifications can and will remain unchallenged in the absence of archived specimens that can be examined and studied at a later time. ...
... Proactive approaches to emergent pathogens and diseases are derived from an understanding of diversity (phylogenetic triage and spatial/temporal distribution) and capacity on the part of micro-and macro-parasites to use historically (evolutionarily) conserved host-based resources (Agosta et al., 2010;Brooks et al., 2019). These fundamental cornerstones provide the ability to anticipate colonization and emergence across changing environmental interfaces and are critically linked to actions (behaviors) that serve to break the links or pathways for opportunity. ...
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This article sets out the essential nature of knowing the biosphere and maintaining that information in archives and natural history collections for implementing the DAMA protocol for coping proactively with the emerging infectious disease crisis
... Some regions of the Earth have become exposed to droughts and wildfires, while others to floods [9]. In turn, this results in altered lifestyles of communities most affected by climate change [14][15][16][17]. Overcrowding of some areas, depopulation of others and the parallel augmented level of people migration, especially in low-income countries, worsen the level of hygiene, impair immunity and often cause epidemics. ...
... An host range increase provides allowance for future possible imperfections, discrepancies and disparities in host-parasite co-phylogeny during the periods of host range contraction. Moreover, it should be stressed that the fitness space is inherently sloppy, with the idea first being advanced by Salvatore Agosta [14,45,46]. ...
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This review paper discusses the Stockholm Paradigm (SP) as a theoretical framework and practical computational instrument for studying and assessing the risk of emerging infectious diseases (EIDs) as a result of climate change. The SP resolves the long-standing parasite paradox and explains how carbon emissions in the atmosphere increase parasites’ generalization and intensify host switches from animals to humans. The SP argues that the growing rate of novel EID occurrence caused by mutated zoonotic pathogens is related to the following factors brought together as a unified issue of humanity: (a) carbon emissions and consequent climate change; (b) resettlement/migration of people with hyper-urbanization; (c) overpopulation; and (d) human-induced distortion of the biosphere. The SP demonstrates that, in an evolutionary way, humans now play a role migratory birds once played in spreading parasite pathogens between the three Earth megabiotopes (northern coniferous forest belt; tropical/equatorial rainforest areas; and hot/cold deserts), i.e., the role of “super-spreaders” of parasitic viruses, bacteria, fungi and protozoa. This makes humans extremely vulnerable to the EID threat. The SP sees the +1.0–+1.2 °C limit as the optimal target for the slow, yet feasible curbing of the EID hazard to public health (150–200 years). Reaching merely the +2.0 °C level will obviously be an EID catastrophe, as it may cause two or three pandemics each year. We think it useful and advisable to include the SP-based research in the scientific repository of the Intergovernmental Panel on Climate Change, since EID appearance and spread are indirect but extremely dangerous consequences of climate change.
... To our knowledge, there are no R packages that simulate the events of host switch using the theoretical approach briefly presented above and widely discussed in previous papers (Araujo et al., 2015;Agosta et al., 2010;Brooks et al., 2019). However, is worth to mention that there are one putatively similar packages that may be used to simulate host switches. ...
In biology a general definition for host switch is when an organism (consumer) uses a new host (which represents a resource). The host switch process by a consumer may happen through its pre-existing capability to use a sub-optimal resource. The HostSwitch R package provides functions to simulate the dynamics of host switching (extent and frequency) in the population of a consumer that interacts with current and potential hosts over the generations. The HostSwitch package is based on a Individual-Based mock-up model published in FORTRAN by Araujo et al. (2015). The package largely improve the previous mock-up model, by implementing numerous new functionalities such as comparison and evaluation of simulations with several customizable parameters to accommodate several types of biological consumer-host associations, an interactive visualization of the model, an in-depth description of the parameters in a biological context. Finally, we provided three real world scenarios taken from the literature selected from ecology, agriculture and parasitology. This package is intended to reach researchers in the broad field of biology interested in simulating the process of host switch of different types of symbiotic biological associations.
... Indeed, the species with the highest level of parasitism by T. sinensis in the NCOT was A. curvator, which was also the only non-target species parasitized in the field experiments, suggesting it could be one of the most vulnerable to T. sinensis. Also, the connection between T. sinensis and its potential parasitism of native Cynipini galls with a morphology shared by or similar to that of D. kuriphilus, which may be related to a parasitism niche, fits with the 'ecological fitting' hypothesis (Agosta et al., 2010) and the 'Stockholm paradigm' (Brooks et al., 2019). ...
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Highlights •Torymus sinensis can attack native species under laboratory and field conditions. •Molecular and mating data show that there is no hybridization with the native species. •We detected the presence of the alien species Torymus beneficus in Spain. •Decisions on biological control of D. kuriphilus by T. sinensis are discussed. BACKGROUND A common strategy to limit the negative impact of biological invasions is biological control through the release of specialized alien natural enemies. However, biological control plans are not without risks, which include parasitism of native hosts and hybridization with related native species, particularly those that are potential natural enemies of the invasive species. Here, we evaluate these potential risks resulting from the introduction of the parasitoid wasp Torymus sinensis (Hymenoptera: Torymidae) in Europe to control the invasive Asian chestnut gall wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae). RESULTS We found that, under laboratory conditions, the physiological host range of T. sinensis includes several native non-target species of Cynipidae, with oviposition observed on the galls of 8 of the 11 species tested. However, physiological host range of T. sinensis appears to be limited under field conditions, as we observed only one parasitized gall of Andricus curvator in the field. Regarding hybridization, inter-species mating between T. sinensis and its phylogenetically closest native Torymus species was not observed in the laboratory. Moreover, discordance between nuclear (ITS2) and mitochondrial (coxI) data does not support the presence of genetic introgression, suggesting that hybridization between T. sinensis and native Torymus species does not occur. In addition, we cite and discuss the unexpected presence of one individual of the related alien species Torymus beneficus in Spain. CONCLUSION Our results suggest that T. sinensis may negatively impact several non-target species, highlighting the need for careful monitoring of the extent of such undesired behaviour and its effects on the native fauna.
... These studies highlighted just how quickly agroecosystems can assemble themselves when introduced species (crops) interact with the surrounding biodiversity in which they are embedded. In addition to Strong's work, there is a growing understanding of how rapidly new interactions can form in ecological time Agosta & Klemens 2008;Agosta et al. 2010;Nylin et al. 2018). We suggest that the dramatic differences in the dynamics of agroecosystems around the world may have more to do with the ecological context in which they are imbedded than is traditionally appreciated. ...
Heterogeneity is a ubiquitous feature of ecosystems and perhaps an important contributing factor to the oft noted difficulties associated with making generalizations in community ecology. Our answers to questions regarding the origins and consequences of various types of heterogeneity in ecological systems have long been met with contingencies and context dependency, highlighting the need to continually revisit our organizing metaphors. The work presented in this dissertation is concerned with these metaphors and especially those associated with the ecological processes that generate spatial heterogeneity in ecosystems. In eleven case studies, we attempt to understand the generation and subsequent implications of spatial heterogeneity for the assembly and functioning of ecological communities in agroecosystems. We first address how ecological interactions create spatial pattern in Chapter 1 by presenting a novel demographic framework for understanding consumer-resource generated spatial patterns. We then explore how spatial heterogeneity influences ecological interactions in Chapter 2 and Chapter 3. Whereas in the former we ask how basic ecological interactions are influenced by dynamic patterns of heterogeneity in ecosystems, in the later we ask how changes in spatial structure influences pathogen epidemics. Chapter 4 then empirically explores how dispersal differentially alters community structure in leaf-litter metacommunities and Chapter 5 explores the use of coupled oscillators as a metaphor for ecological communities. These first five chapters represent an attempt to understand the feedbacks between ecological interactions that create spatial heterogeneity and how spatial heterogeneity structures ecological communities. The dissertation then shifts focus to a fungal pathogen of coffee, the coffee leaf rust, and uses its community of consumers as a model system to understand how spatial heterogeneity influences community structure and how community structure influences biological control of the pathogen. Chapter 6 gives a brief overview of the history and ecology of the pathogen and its community, and Chapters 7-9 explore the assembly and organization of these communities, highlighting their interactions with the pathogen as well as among themselves. Finally, Chapters 10 and 11 are concerned with the structure of interaction networks associated with the coffee leaf rust and the provisioning of top-down control of the coffee leaf rust pathogen in both Mexico and Puerto Rico. Taken together, this dissertation contributes to our understanding of how ecological communities create and are impacted by the heterogeneous environments they occupy. Furthermore, this work attempts to highlight the importance of such concepts in an agroecological context where questions of community structure and population regulation have the potential for practical significance.
... Ancestral hosts sometimes evidently will remain as potential hosts for the future even when they are temporarily not used (Braga et al., 2018b;Nylin & Wahlberg, 2008;Nylin et al., 2014), and the realized host range can thus fluctuate between including them or not. Very similar evolutionary patterns of specialization, phylogenetic conservatism, colonizations, re-colonizations, and oscillations in host range are observed in other parasite-host and even mutualistic species associations, broadening the perspective even further and implying consequences for invasive species and emerging infectious diseases (Agosta et al., 2010;Brooks et al., 2019;Nylin et al., 2018;Torres-Martinez et al., 2021). ...
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In this study, we investigated whether patterns of gene expression in larvae feeding on different plants can explain important aspects of the evolution of insect-plant associations, such as phylogenetic conservatism of host use and re-colonization of ancestral hosts that have been lost from the host repertoire. To this end, we performed a phylogenetically informed study comparing the transcriptomes of 4 nymphalid butterfly species in Polygonia and the closely related genus Nymphalis. Larvae were reared on Urtica dioica, Salix spp., and Ribes spp. Plant-specific gene expression was found to be similar across butterfly species, even in the case of host plants that are no longer used by two of the butterfly species. These results suggest that plant-specific transcriptomes can be robust over evolutionary time. We propose that adaptations to particular larval food plants can profitably be understood as an evolved set of modules of co-expressed genes, promoting conservatism in host use and facilitating re-colonization. Moreover, we speculate that the degree of overlap between plant-specific transcriptomes may correlate with the strength of trade-offs between plants as resources and hence to the probability of colonizing hosts and complete host shifts.
... This contradiction between the prevailing paradigm and empirical observations is referred to as the "parasite paradox" (Agosta et al., 2010), and it has significant consequences in how public health addresses EIDs. Public health deems emergence rare, and therefore of low global health concern, and at the same time unpredictable, thus judging prevention efforts to be impossible. ...
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The emerging infectious disease (EID) crisis has been challenging global health security for decades, dealing substantial damage to all socioeconomic landscapes. Control measures have failed to prevent or even mitigate damages from an accelerating wave of EIDs, leading to the emergence and devastation caused by the COVID-19 pandemic. In the wake of the pandemic, we must critically review our public health policies and approaches. Current health security measures are based on the evolutionary theorem of host-parasite coevolution, which falsely deems EIDs as rare and unpredictable. The DAMA protocol (Document, Assess, Monitor, Act) is nested in a novel evolutionary framework that describes how emergence can be prevented before the onset of an outbreak. In this paper, we discuss the importance of establishing efficient communication channels between various stakeholders affected by EIDs. We describe implementation strategies for preventive interventions on global, regional, and local scales and provide guidelines for using such strategies in the relevant policy environments of human, livestock, and crop diseases.
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A database on host plant records from 437 ingroup taxa has been used to test a number of hypotheses on the interaction between butterflies and their host plants using phylogenetic methods (simple character optimization, concentrated changes test, and independent contrasts test). The butterfly phylogeny was assembled from various sources and host plant clades were identified according to Chase et al.'s rbcL-based phylogeny. The ancestral host plant appears to be associated within a highly derived rosid clade, including the family Fabaceae. As fossil data suggest that this clade is older than the butterflies, they must have colonized already diversified plants. Previous studies also suggest that the patterns of association in most insect-plant interactions are more shaped by host shifts, through colonization and specialization, than by cospeciation. Consequently, we have focused explicitly on the mechanisms behind host shifts. Our results confirm, in the light of new phylogenetic evidence, the pattern reported by Ehrlich and Raven that related butterflies feed on related plants. We show that host shifts have generally been more common between closely related plants than between more distantly related plants. This finding, together with the possibility of a higher tendency of recolonizing ancestral hosts, helps to explain the apparent large-scale conservation in the patterns of association between insects and their host plants, patterns which at the same time are more flexible on a more detailed level. Plant growth form was an even more conservative aspect of the interaction between butterflies and their host plants than plant phylogeny. However, this is largely explained by a higher probability of colonizations and host shifts while feeding on trees than on other growth forms.
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In this study we used reciprocal rearing experiments to test the hypothesis that there is a genetic basis for the adaptive differences in host-use traits among host-associated soapberry bug populations (described in Carroll and Boyd 1992). These experiments were conducted on two host races from Florida, in which differences in beak length and development were found between natural populations on a native host plant species and those on a recently introduced plant species (colonized mainly post-1950). Performance was generally superior on the host species from which each lab population originated (i.e., on the "Home" host species): in analysis of variance, there was significant population-by-host interaction for size, development time, and growth rate. These results indicate that the population differences in nature are evolved rather than host induced. Increased performance on the introduced host was accompanied by reduced performance on the native host, a pattern that could theoretically promote further differentiation between the host races.
We hypothesize that the evolution of an ecologically important character, the host associations of specialized phytophagous insects, has been influenced by limitations on genetic variation. Using as a historical framework a phylogenetic reconstruction of the history of host associations in the beetle genus Ophraella (Chrysomelidae), we have employed quantitative-genetic methods to screen four species for genetic variation in larval survival, oviposition (in one species only), and feeding responses to their congeners' host plants, in the Asteraceae. We here report results of studies of one species and evaluate the results from all four. Analysis of half-sib/full-sib families and of progenies of wild females of O. notulata, a specialist on Iva (Ambrosiinae), provided evidence of genetic variation in larval consumption of five of six test plants and in adult consumption of four of six. Larval mortality was complete on five plants; only on Ambrosia, a close relative of the natural host, was there appreciable, and genetically variable, survival. Oviposition on Ambrosia showed marginally significant evidence of genetic variation; a more distantly related plant elicited no oviposition at all. In compiling results from four Ophraella species, reported in this and two other papers, we found no evidence of genetic variation in 18 of 39 tests of feeding responses and 14 of 16 tests of larval survival on congeners' hosts. This result is consistent with the hypothesis that absence or paucity of genetic variation may constrain or at least bias the evolution of host associations. The lower incidence of genetic variation in survival than in feeding behavior may imply, according to recent models, that avoidance is a more common evolutionary response to novel plants than adaptation. The usually great disparity between mean performance on congeners' hosts and the species' natural hosts, and an almost complete lack of evidence for negative genetic correlations, argue against the likelihood that speciation has occurred by sympatric host shift. The presence versus apparent absence of genetic variation in consumption was correlated with the propinquity of relationship between the beetle species tested and the species that normally feeds on the test plant, suggesting that the history of host shifts in Ophraella has been guided in part by restrictions on genetic variation. It was also correlated with the propinquity of relationship between a test plant and the beetle's natural host. The contributions of plant relationships and insect relationships, themselves correlated in part, to the pattern of genetic variation, are not readily distinguishable, but together accord with phylogenetic evidence that these and other phytophagous insects adapt most readily to related plants. In this instance, therefore, the macroevolution of an ecologically important character appears to have been influenced by genetic constraints. We hypothesize that absence of the structural prerequisites for genetic variation in complex characters may affect genetic variation and the trajectory of evolution.
Ecological explanations for the prevalence of resource specialists are abundant, whereas phylogenetic evidence on their origins is scarce. In this paper, we provide a molecular phylogenetic study of the 19 specialist or generalist species in the bark beetle genus Dendroctonus, which collectively attack species in four different genera in the conifer family Pinaceae. Given substantial variation in diet breadth, we asked two general questions concerning the evolution of resource use in this group. How conservative is the evolution of host use in these insects? Does specialization tend to be derived (i.e., a “dead end”)?