The historical biogeography of co-evolution: Emerging infectious diseases are evolutionary accidents waiting to happen

Abstract

Ecological fitting refers to interspecific associations characterized by ecologically specialized, yet phylogenetically conservative, resource utilization. During periods of biotic expansion, parasites and hosts may disperse from their areas of origin. In conjunction with ecological fitting, this sets the stage for host switching without evolving novel host utilization capabilities. This is the evolutionary basis of emerging infectious diseases (EIDs). Phylogenetic analysis for comparing trees (PACT) is a method developed to delineate both general and unique historically reticulated and non-reticulated relationships among species and geographical areas, or among parasites and their hosts. PACT is based on ‘Assumption 0’, which states that all species and all hosts in each input phylogeny must be analysed without modification, and the final analysis must be logically consistent with all input data. Assumption 0 will be violated whenever a host or area has a reticulated history with respect to its parasites or species. PACT includes a Duplication Rule, by which hosts or areas are listed for each co-evolutionary or biogeographical event affecting them, which satisfies Assumption 0 even if there are reticulations. PACT maximizes the search for general patterns by using Ockam's Razor – duplicate only enough to satisfy Assumption 0. PACT applied to the host and geographical distributions of members of two groups of parasitic helminths infecting anthropoid primates indicates a long and continuous association with those hosts. Nonetheless, c. 30% of the host associations are due to host switching. Only one of those involves non-primate hosts, suggesting that most were constrained by resource requirements that are phylogenetically conservative among primates (ecological fitting). In addition, most of the host switches were associated with episodes of biotic expansion, also as predicted by the ecological fitting view of EIDs.

Full text

GUEST
EDITORIAL
The historical biogeography
of co-evolution: emerging infectious
diseases are evolutionary accidents
waiting to happen
Daniel R. Brooks* and Amanda L. Ferrao
INTRODUCTION
The biodiversity crisis is not just a crisis of extinction; it is also
a crisis of introduced species and emerging diseases (Grenfell &
Gulland, 1995; Daszak et al., 2000; Harvell et al., 2002). Such
events produce complex geographical distributions and host–
pathogen relationships. How do these anthropogenic phe-
nomena compare with area and host relationships produced
on evolutionary time scales? Do they differ in degree or in
kind? Answering such questions requires that we assess both
the geographical and the host context of pathogen/host
co-evolution.
Studies of co-evolution emerged from consideration of host
and geography, beginning with von Ihering’s (1891, 1902)
observations about the similarities between some temnocepha-
lidean (flatworm) parasites inhabiting freshwater crayfish in
New Zealand and in the mountains of Argentina. He
postulated that the species in the two disjunct areas were
derived from ancestral crayfish and flatworms that were
themselves associated, and therefore South America and New
Zealand must once have been connected by fresh water.
A generation later, biogeographical considerations had largely
disappeared from discussions of co-evolution. Fahrenholz
(1913) postulated that the occurrence of related blood-sucking
Department of Zoology, University of
Toronto, Toronto, Canada
*Correspondence: Daniel R. Brooks,
Department of Zoology, University of Toronto,
Toronto, ON M5S 3G5, Canada.
E-mail: dbrooks@zoo.utoronto.ca
ABSTRACT
Ecological fitting refers to interspecific associations characterized by ecologically
specialized, yet phylogenetically conservative, resource utilization. During periods
of biotic expansion, parasites and hosts may disperse from their areas of origin. In
conjunction with ecological fitting, this sets the stage for host switching without
evolving novel host utilization capabilities. This is the evolutionary basis of
emerging infectious diseases (EIDs). Phylogenetic analysis for comparing trees
(PACT) is a method developed to delineate both general and unique historically
reticulated and non-reticulated relationships among species and geographical
areas, or among parasites and their hosts. PACT is based on ‘Assumption 0’,
which states that all species and all hosts in each input phylogeny must be ana-
lysed without modification, and the final analysis must be logically consistent
with all input data. Assumption 0 will be violated whenever a host or area has a
reticulated history with respect to its parasites or species. PACT includes a
Duplication Rule, by which hosts or areas are listed for each co-evolutionary or
biogeographical event affecting them, which satisfies Assumption 0 even if there
are reticulations. PACT maximizes the search for general patterns by using
Ockam’s Razor – duplicate only enough to satisfy Assumption 0. PACT applied to
the host and geographical distributions of members of two groups of parasitic
helminths infecting anthropoid primates indicates a long and continuous
association with those hosts. Nonetheless, c. 30% of the host associations are due
to host switching. Only one of those involves non-primate hosts, suggesting that
most were constrained by resource requirements that are phylogenetically con-
servative among primates (ecological fitting). In addition, most of the host
switches were associated with episodes of biotic expansion, also as predicted by
the ecological fitting view of EIDs.
Keywords
Co-evolution, ecological fitting, emerging infectious diseases, evolution, histor-
ical biogeography, PACT, phylogeny.
Journal of Biogeography (J. Biogeogr.) (2005) 32, 1291–1299
ª2005 Blackwell Publishing Ltd www.blackwellpublishing.com/jbi doi:10.1111/j.1365-2699.2005.01315.x 1291

lice on different primates demonstrated that the catarrhines
were more closely related to hominoids than to any other
primates. By the late 1930s, the orthogeneticists had produced
an integrated view of co-evolution: parasites are highly host
specific, so they coevolve with their hosts, and because they
coevolve with their hosts, they become highly host specific.
Since host specificity was the ‘cause’ of co-evolution, rather
than a function of the ecological interaction between lineages,
any conflicting or inconsistent observations were erroneous or
irrelevant because they failed to conform to the orthogenetic
view of co-evolution.
For most of the twentieth century, parasitologists continued
to study co-evolution within an orthogenetic framework
despite calls to integrate with mainstream evolutionary biology
(e.g. Mayr, 1957; Manter, 1966; Janzen, 1985a; Brooks &
McLennan, 1993, 2002). Vestiges of orthogenetic thinking
persist today; this is especially true for the assumption that
hosts and parasites ‘ought’ to have congruent phylogenies,
embodied in the maximum co-speciation research programme
(Page, 2002; see also Brooks, 2003).
There is a second tradition of thought about the nature of
co-evolution. Kellogg (1896, 1913) suggested that while some
host–parasite systems might show strong phylogenetic associ-
ations, there were substantial cases of what he termed
‘straggling’, referring in some cases to hosts speciating when
the parasites did not and in other cases to parasites switching
hosts. Kellogg cast his observations about the relationship
between birds and their biting lice in a Darwinian framework,
which helped initiate a different approach to co-evolution.
Most researchers who adopted this perspective were interested
in studying the interactions between plants and phytophagous
insects (e.g. Verschaffelt, 1910; Brues, 1920, 1924). Because
those associations often showed no clear phylogenetic com-
ponent with respect to host species (though they often were
extremely specific), researchers in this tradition focused on
discovering the ecological ties between organisms, particularly
the cues insects used to locate their host plants.
The modern version of this second perspective emerged in
the early 1960s. Following a mathematical model proposed by
Mode (1958), Ehrlich & Raven (1964) hypothesized that the
evolutionary diversification of plants and insects had been
fuelled by complex co-evolutionary interactions involving
mutual modification. Such co-evolutionary dynamics might
have a general phylogenetic context, but the fine details need
not parallel the evolutionary history of the specific taxa
involved. The distribution of insects among plants followed the
evolution of host resources and the evolution of insects’
abilities to utilize those resources, rather than the evolution of
host species themselves. Janzen (1968, 1973a,b, 1980, 1981,
1983, 1985a,b) reintroduced an explicit biogeographical
element to this discussion. He argued that the appearance of
tight co-evolutionary associations at any single locality could
be misleading. No matter where a given species evolved in the
first place, its inherited functional abilities may allow it to
survive in a variety of places under a variety of conditions
through arbitrary amounts of time. In other words, species and
their phylogenetically conservative traits may disperse readily
through time and space. He termed this interaction between
the past history of the species and their present day associ-
ations ‘ecological fitting’. One particularly critical manifesta-
tion of ecological fitting is that any given species may be a
resource specialist but may also share that specialist trait with
one or more close relatives. That is, specialization on a
particular resource can be plesiomorphic. In a complementary
manner, the resources themselves may be very specific and yet
still be taxonomically and geographically widespread, if they
are persistent plesiomorphic traits of the hosts.
The phylogenetic revolution has given rise to modern
versions of these two traditional schools of thought. The
maximum co-speciation, or co-phylogeny, school has been
based on the belief that host–parasite associations are so
ecologically specialized that parasites have few opportunities to
switch hosts. Various models or assumptions are invoked to
‘reconcile’ portions of parasite phylogenies that are incongru-
ent with host phylogeny to the host phylogeny. This can be
accomplished for every case of incongruence by postulating
that each one actually represents at least two past episodes, one
of sympatric speciation by the parasite (which the maximum
co-speciation school calls ‘lineage duplication’) coupled with
one or more episodes of particular extinctions (which the
maximum co-speciation school calls ‘lineage sorting’). This
methodology, sometimes called ‘tree reconciliation’, can make
every putative case of host switching disappear (Van Veller &
Brooks, 2001). It is then up to the discretion of the investigator
to decide if any cases of host switching will be permitted.
Although generally unacknowledged by its advocates, the
theoretical basis for this approach can be found in orthoge-
netic theory (for a historical discussion, see Brooks &
McLennan, 1993, 2002), in which parasites are evolutionarily
tied to their host species.
The alternative approach is based on the assumption that
the extent to which host–parasite associations are specialized is
decoupled from the extent to which there might be host
switching. Brooks (1979) made this point in distinguishing
between co-speciation and co-accommodation (more recently
co-adaptation), arguing that one could not extrapolate from
one to the other. This sentiment has also been formalized as
diffuse co-evolution (Futuyma & Slatkin, 1983), and, as noted
above, ecological fitting (Janzen, 1985b). Brooks & McLennan
(2002) suggested that ecological fitting be used as the general
term, as it best embodies the envisioned process. Basically, no
matter how ecologically specialized an association between
species at any particular place and time, the traits (resources)
characterizing the association may be phylogenetically con-
servative. Therefore, if geographical and/or ecological circum-
stances change, a parasite might easily switch to new host
species simply because they are sources of the same specialized
resources that were previously available only from another
host. Furthermore, if these highly specialized resources are
plesiomorphic, the host switches need not be restricted to hosts
belonging to a single clade, although we might expect them not
to be very distantly related (for a recent example, see Radtke
D. R. Brooks and A. L. Ferrao
1292 Journal of Biogeography 32, 1291–1299, ª2005 Blackwell Publishing Ltd

et al., 2002). As a consequence, Brooks (1979) suggested that
one could not simply extrapolate from the degree of host
specificity, or the perceived degree of specialization of any
host–parasite association to an expectation of the probability
of co-speciation or host switching. Furthermore, co-speciation
patterns might simply be a by-product of allopatric speciation
events experienced by both hosts and parasites (frozen
accidents of history) rather than evidence of strong and
exclusive co-evolutionary interactions (Brooks, 1981; for a
review with numerous references, see Brooks & McLennan,
2002).
Empirically, advocates of the maximum co-speciation
school assert that maximum co-speciation should be the
preferred explanation even when there is incongruence
between host and parasite phylogenies because it is a simpler
a priori theory, and worry that ecological fitting permits too
many a priori possibilities. Advocates of ecological fitting argue
that host switching should be preferred for such cases, because
one host switch is simpler than one sympatric speciation event
and one or more extinction events, and argue that maximum
co-speciation prohibits too many possibilities a priori. Thus,
the two approaches invoke parsimony differently, ontologically
and epistemologically respectively. This parallels the case of
cladistic and phylogenetic approaches to historical biogeogra-
phy, previously presented in this journal (Van Veller & Brooks,
2001; see also Brooks, 2003; Brooks et al., 2004).
Happily, there are signs of a synthesis. Brooks & McLennan
(2002) suggested that the evolutionary basis for such fitting is
simple and its manifestations are ubiquitous. If specific
environmental cues/resources are widespread or if traits can
have multiple functions (or both), then the stage is set for the
appearance of ecological specialization and close (co)evolu-
tionary tracking, without losing the ability to establish novel
associations. In this context, it is important to remember that
resource availability is not the same as resource distribution.
Trophic segregation and allopatry are two powerful ‘indirect
effects’ that may limit actual (vs. potential) host utilization
(the observed host range) at any given time. These effects
actually lower the long-term evolutionary cost of specialization
(i.e. increased risk of extinction over time) for a given
pathogen by increasing the chances that it will come into
contact with additional susceptible hosts if there is a change in
the environment, leading to altered trophic interactions or to
geographical dispersal.
Less than 2 years later, Systematic Biology published the
proceedings of a symposium by the maximum co-speciation
school that marked a singular change in their perspective.
Parasitologists and zoo veterinarians have long known that
parasites switch hosts under conditions of close confinement
(and stress). Noting this, Johnson & Clayton (2004) and
Clayton et al. (2004) suggested that host switches are not
limited by inherent inability to establish on new hosts but by
lack of opportunity, and called for more study of the ecology of
host–parasite associations, not just to understand systems that
appear to show high degrees of co-speciation but also to gain
more insight into those that show substantial amounts of host
switching, such as those reported in the symposium (Degnan
et al., 2004; Percy et al., 2004; Ricklefs et al., 2004; Sorenson
et al., 2004; Weiblen, 2004). Interestingly, Johnson & Clayton
(2004) and Clayton et al. (2004) suggested that avian lice, the
model system used by Kellogg (1896, 1913) to study straggling,
would be an excellent system to study …straggling!
Notable among those contributions was the one by
Weckstein (2004), who concluded that historical biogeo-
graphical phenomena might play a role in mediating both
co-speciation and host switching, an idea first proposed by
Brooks (1979, 1980, 1981), consistent with the results of many
published studies ranging from particular parasite groups, such
as malaria (Escalante & Ayala, 1994; Escalante et al., 1995) and
some human tapeworms (Taenia spp.) (Hoberg et al., 2000),
to entire biotas, such as the host–parasite assemblage of the
Arctic (Hoberg, 1986, 1989, 1992, 1995, 1996, 1997a,b, 2002,
2005; Hoberg & Adams, 1992, 2000; Hoberg et al., 1995,
1999a,b, 2000, 2001, 2002, 2003, 2004; Hoberg & Klassen,
2002), and summarized for vertebrate parasites in book form
by Brooks & McLennan (1993). This list is only representative,
not exhaustive, as virtually all phylogenetic studies of insect–
plant systems also show extensive host-switching, as first
suggested by Mitter & Brooks (1983).
In the context of emerging infectious disease, the traditional
distinction between these two schools of thought is striking.
For traditional advocates of maximum co-speciation, the
co-evolutionary process itself provides a safeguard against emer-
ging diseases, which should be rare, if not ruled out altogether.
For advocates of ecological fitting, and the emerging modifi-
cation of the maximum co-speciation school, however, the
world is a mosaic of specialized but evolutionarily conservative
ecologies, into which large numbers of pathogens could fit,
given the right circumstances. And those circumstances involve
geographical and/or climatological alteration of ecosystems,
such that hosts and pathogens are able to move out of their
areas of origin, coming into contact with novel hosts and
pathogens as a result of dispersal with or without modifica-
tions of trophic structure. If observed incongruence between
host and parasite phylogenies were due to lineage duplication
plus extinction, there would be no particular biogeographical
signature of the event (duplications being due to sympatric
speciation). Emerging diseases imply that there has been host
switching coupled with geographical movement. Either new
hosts have moved into the area of origin of a given pathogen,
which has incorporated them into its host range, or the
pathogen has moved out of its area of origin into an area where
susceptible hosts live, and has added them to its host range.
Thus, we would expect to find a preponderance of cases of host
switching associated with episodes of geographical dispersal.
METHODOLOGY
The ecological fitting perspective is based on the notion that
evolution has been complex and historically contingent;
however, that history includes both general (law-like)
and unique (contingent) phenomena. Extending this to
Guest Editorial
Journal of Biogeography 32, 1291–1299, ª2005 Blackwell Publishing Ltd 1293

co-evolutionary studies leads us to predict that phylogenetic
comparisons of parasite–host cladograms (i.e. parasite phylo-
genies in which the parasite species names have been replaced
by the names of their hosts) should be historically unique
combinations of phenomena that are congruent with host
phylogeny (co-speciation, extinction, sympatric speciation and
extinction) as well as episodes of host switching. Furthermore,
we would predict that our ability to document those patterns
would be obscured most by the use of models and methods
that over-simplify the process by invoking a priori assumptions
or prohibitions. This leads us to recognize several essential
elements of the analytical method required to study host–
parasite evolution, which together form the basis for the new
algorithm PACT (phylogenetic analysis for comparing trees;
Wojcicki & Brooks, 2004, 2005).
First, it is not permissible to remove or modify data. Wiley
(1986a,b,c, 1988a,b) and Zandee & Roos (1987) already
formalized this as ‘Assumption 0’, which states that you must
analyse all species and all hosts in each input phylogeny
without modification, and your final analysis must be logically
consistent with all input data. Recognition of the fundamental
importance of Assumption 0 was obscured by Page (1990),
who used ‘Assumption 0’ to refer to the protocol of coding
‘absence’ as ‘0’ in preparing a matrix of data for analysis.
Brooks (1981) proposed that protocol because computer
programs at that time did not accept missing data. It was
eliminated when Wiley (1986a) proposed using missing data
coding for absences for analyses using Brooks’ method, which
Wiley dubbed Brooks Parsimony Analysis (BPA). Assumption
0 does not imply that the input phylogenies are true or
complete. It does imply, however, that the method of analysis
for biogeographical or co-evolutionary studies cannot be used
to assess the accuracy of the phylogenies, as that would
introduce an unacceptable degree of subjectivity, or even
circularity, into the process. Therefore, if one is dissatisfied
with the results of a co-evolutionary analysis, and suspects that
this is due to a poor phylogenetic hypothesis or un-sampled
species, the solution is to get more data, improve the input
phylogeny, and re-do the co-evolutionary analysis.
Second, host cladograms based on many parasites inhabiting
the same hosts must include reticulated host relationships. If
each host species on this planet had a singular history with
respect to all the species living in association with it, either
there would be one parasite species per host species or one
parasite clade per host species. Nowhere on earth does this
occur, so we must assume that reticulated host relationships
have been common. If we use a method of analysis that
produces simple host cladograms (i.e. ones in which parasite
data are reconciled to the host phylogeny), Assumption 0 will
be violated whenever a host has a reticulated history with
respect to any of its parasites. Assumption 0 can be satisfied in
such cases by duplicating hosts with reticulated histories.
Therefore, a method of analysis for handling complexity
requires a Duplication Rule, a mechanism by which hosts are
listed for each co-evolutionary event affecting them (see also
Brooks & McLennan, 2002).
Finally, if no possibilities, including host reticulations,
are prohibited a priori, and if co-evolutionary patterns are
combinations of unique and general phenomena, how are
general patterns found? PACT employs Ockam’s Razor as an
epistemological corollary of the Duplication Rule – duplicate
only enough to satisfy Assumption 0. Simplicity is used only to
determine if there are general patterns, so the ecological fitting
perspective is not a ‘maximum host-switching’ analogue of the
maximum co-speciation school. PACT searches for the maxi-
mum allowable general patterns as well as unique events and
reticulated relationships. In this regard, it is most similar to
secondary BPA (Brooks, 1990; Brooks & McLennan, 2002), but
has been shown to be an improvement on that method
(Wojcicki & Brooks, 2004, 2005). PACT produces a simple
result when the data warrant it, but is capable of producing
complex results when the data demand.
We illustrate the ecological fitting perspective on under-
standing EIDS using the most recent phylogenetic hypotheses
for pinworms (Enterobius spp.; Hugot, 1999) (Fig. 1) and
hookworms [Oesophagostomum (Conoweberia) spp.; Glen &
Brooks, 1985] (Fig. 2) inhabiting the Great Apes. For details of
the phylogenetic analyses of the parasite clades and their
sources, see Brooks & McLennan (2003) and references
therein. We used PACT to generate (1) a host cladogram, a
branching diagram listing hosts as terminal taxa, providing a
visual summary of the host context of speciation events
implied by the parasite phylogenies; and (2) an area clado-
gram, a branching diagram listing areas as terminal taxa,
providing a visual summary of the geographical context of
speciation events implied by the parasite phylogenies. For
details of PACT, see Wojcicki & Brooks (2004, 2005).
7
65
10
4
9
3
8
21
11
12
Colobenterobius
bipapillatus+brevicauda+macaci
buckleyi
lerouxi
anthropopitheci
vermicularis
gregorii
Figure 1 Phylogenetic tree of species of Enterobius. All branches
are numbered for ease of interpreting the host cladogram (Fig. 3).
D. R. Brooks and A. L. Ferrao
1294 Journal of Biogeography 32, 1291–1299, ª2005 Blackwell Publishing Ltd

RESULTS
The heavy branches on the PACT host cladogram (Fig. 3)
indicate instances of congruence between host and parasite
phylogeny (co-speciation; Brooks, 1981). This includes one
case (the common ancestor [8] of Enterobius gregorii [1] +
E. vermicularis [2]) in which a parasite clade speciated but the
host did not, and another (Oesophagostomum stephanostomum
[18]) in which the host clade speciated but the parasite did not.
These findings suggest that the association between pinworms
and hookworms and the Great Apes and their relatives has
been a long and continuous one. Despite the substantial
amount of co-speciation, the PACT analysis suggests that,
among the 28 lineages of Enterobius and Oesophagostomum
included, there have been eight events (29%) that are not
congruent with host phylogeny. Only one of those host
switches, that giving rise to the common ancestor of
O. xeri +O. susannae (18 in Fig. 3), represents a switch to a
non-primate host (in this case rodents), suggesting phylo-
genetic conservatism in host specificity among these parasites
in accordance with the expectations of ecological fitting. The
remaining switches include the acquisition of parasites that are
more or less the same age (Oesophagostomum brumpti (20 in
Fig. 3), O. aculeatum (19 in Fig. 3), and the common ancestor
of Enterobius bipapillatus +E. brevicaudatum +E. macaci (six
in Fig. 3)), that are younger (O. pachycephalum (14 in Fig. 3)),
and that are older (O. bifurcum (21 in Fig. 3), O. raillieti (16 in
Fig. 3), and O. blanchardi (17 in Fig. 3)) than their hosts, again
suggesting ecological fitting.
The biogeographical analysis of Enterobius and Oesophago-
stomum (Conoweberia) (Fig. 4) suggests a history of speciation
involving alternating episodes of isolation in, and then
movements between, Africa and Asia. This supports a taxon
pulse dynamic rather than a simple vicariance scenario (Erwin,
1979; for recent studies of taxon pulses, see Spironello &
Brooks, 2003; Bouchard et al., 2004; Halas et al., 2005).
Furthermore, five of the eight (63%) host switches discovered
in Fig. 3 occurred during periods of biotic expansion discov-
ered in Fig. 4, the exceptions being the switch from primates to
rodents in the common ancestor of O. xeri +O. susannae,
which took place in Africa, and O. blanchardi in Pongo and
O. raillieti in Hylobates (perhaps representing an actual case of
sympatric speciation), which took place in Asia. These data
clearly support ecological fitting more than maximum
co-speciation.
DISCUSSION
We began by pointing out that the phenomenon of emerging
infectious diseases is the result of species being moved from
their areas of origin into novel places, leading to host switches,
and we asked if this was a difference in degree or kind from the
evolution of host–parasite relationships in the past. Nearly
21
20
19
18
17
16 15
14 13
22
23
24
25
26
27
28
29
bifurcum
brumpti
aculeatum
xeri+susannae
balanchardi
raillieti
ovatum
pachycephalum
stephanostomu
m
Figure 2 Phylogenetic tree of species of Oesophagostomum
(Conoweberia). All branches are numbered for ease of interpreting
the host cladogram (Fig. 3).
21
28
27
20 19
18
26
25
17 16
24
23
15 10
22
6
5
13
49
38
7
12
14
11
Cercopithecines
Colobines
Colobines
Colobines
Homo
Homo
Gorilla
Gorilla
Cercopithecines
Cercopithecines
Rodents
Pongo
Pongo
Pan
Hylobates
Hylobates
1,2,
Figure 3 Host cladogram produced by
PACT, indicating host context of speciation
events implied by phylogenies for Enterobius
and Oesophagostomum (Conoweberia) (Figs 1
& 2). Thick lines indicate associations con-
gruent with host phylogeny; thin lines indi-
cate host-switching events. Numbers on
branches refer to particular branches on the
parasite phylogenetic trees.
Guest Editorial
Journal of Biogeography 32, 1291–1299, ª2005 Blackwell Publishing Ltd 1295

one-third of the host associations for members of two groups
of parasites arose by host switching, despite a long history of
association with Great Apes. Approximately 60% of those
ancient EIDs were associated with post-speciation biotic
expansion from the area of origin. This indicates that the
contemporary EID crisis is different in degree rather than kind.
EIDs are not rare accidents but are rather common evolution-
ary accidents waiting to happen. The analysis of the hominoid
nematodes above is but an illustration. All but one of the host
switches discovered in this analysis occur among primates. In
addition, more than 60% of the host switches are associated
with episodes of biotic expansion, or post-speciation dispersal
by hosts and parasites from their areas of origin. Together,
these observations suggest that these host switches, all of which
would have been called EIDs at the time of their origins, are
the result of the intersection of ecological fitting and
geographical dispersal.
CONCLUSIONS
If we could be confident that EIDs were rare phenomena,
perhaps it would be cost-effective to engage in the kind of crisis
response we have seen globally to this point in time.
Unfortunately, we believe the results of our analysis above
are typical, in which case we must assume that the potential
number of EIDs is very large; there are many ‘accidents waiting
to happen’ as a result of continued anthropogenic activities,
including the introduction of non-native species for biological
control.
The good news is that if EIDs are a regular feature of
biogeographical dispersal, we can hope to understand the
contemporary EID crisis and learn from the lessons of
(evolutionary) history, and move from being ignorant-reactive
to being informed-proactive. In that regard, our lack of a
comprehensive taxonomic inventory of pathogen on this
planet, and of phylogenetic assessments of their co-evolution-
ary and biogeographical histories, are major hindrances to
dealing with the current EID crisis. One cannot perform
co-evolutionary and biogeographical analyses on species whose
existence has not yet been documented. Society, through its
public, wildlife and livestock health managers, must decided
whether to expend its funds continuing to manage the EID
crisis, or to solve it.
ACKNOWLEDGEMENTS
Funds for this study were provided through a grant from the
Natural Sciences and Engineering Research Council (NSERC)
of Canada to DRB. We thank Rob Whittaker for the invitation
to contribute this Guest Editorial.
REFERENCES
Bouchard, P., Brooks, D.R. & Yeates, D.K. (2004) Mosaic
macroevolution in Australian wet tropics arthropods:
Community assemblage by taxon pulses. Rainforest: past,
present, future (ed. by C. Moritz and E. Bermingham),
pp. 425–469. University of Chicago Press, Chicago.
Brooks, D.R. (1979) Testing the context and extent of host–
parasite coevolution. Systematic Zoology,28, 299–307.
Brooks, D.R. (1980) Allopatric speciation and non-interactive
parasite community structure. Systematic Zoology,29, 192–
203.
Brooks, D.R. (1981) Hennig’s parasitological method: a pro-
posed solution. Systematic Zoology,30, 229–249.
Brooks, D.R. (1990) Parsimony analysis in historical bioge-
ography and coevolution: methodological and theoretical
update. Systematic Zoology,39, 14–30.
Brooks, D.R. (2003) The new orthogenesis. Cladistics,19, 443–
448.
Brooks, D.R. & McLennan, D.A. (1993) Parascript: parasites
and the language of evolution. Smithsonian Institution Press,
Washington, D.C.
Brooks, D.R. & McLennan, D.A. (2002) The nature of diversity:
an evolutionary voyage of discovery. University of Chicago
Press, Chicago.
Africa
Africa
Asia
Africa to Asia
Africa to Asia
Africa to Asia
Asia
Asia
Asia to Africa
Africa
Africa to Asia
Africa
Africa
Africa
Asia
Asia
Asia
Asia
Asia
Asia
Africa
Africa
Africa
Africa
Africa-Asia
Africa-Asia
Asia
Figure 4 Area cladogram produced by
PACT, indicating host context of speciation
events implied by phylogenies for Enterobius
and Oesophagostomum (Conoweberia) (Figs 1
& 2). Thick lines indicate associations con-
gruent with host phylogeny; thin lines indi-
cate host switching events. Areas at nodes
indicate episodes of isolation (in either Asia
or Africa) or of biotic expansion (Africa–Asia
or Asia–Africa).
D. R. Brooks and A. L. Ferrao
1296 Journal of Biogeography 32, 1291–1299, ª2005 Blackwell Publishing Ltd

Brooks, D.R. & McLennan, D.A. (2003) Extending phyloge-
netic studies of coevolution: secondary Brooks parsimony
analysis, parasites and the Great Apes. Cladistics,19, 104–
119.
Brooks, D.R., Dowling, A.P.G., Van Veller, M.G.P. & Hoberg,
E.P. (2004) Ending a decade of deception: a valiant failure, a
not-so-valiant failure, and a success story. Cladistics,20, 32–
46.
Brues, C.T. (1920) The selection of food-plants by insects, with
special reference to lepidopterous larvae. The American
Naturalist,54, 313–332.
Brues, C.T. (1924) The specificity of food-plants in the evo-
lution of phytophagous insects. The American Naturalist,58,
127–144.
Clayton, D.H., Bush, S.E. & Johnson, K.P. (2004) Ecology of
congruence: past meets present. Systematic Biology,53, 165,
173.
Daszak, P., Cunningham, A.A. & Hyatt, A.D. (2000) Emerging
infectious diseases of Wildlife – threats to biodiversity and
human health. Science,287, 443–449.
Degnan, P.H., Lazarus, A.B., Brock, C.D. & Wernegreen, J.J.
(2004) Host-symbiont stability and fast evolutionary rates in
an ant-bacterium association: co-speciation of Campanotus
species and their endosymbionts, Candidatus Blochmannia.
Systematic Biology,53, 95–110.
Ehrlich, P.R. & Raven, P.H. (1964) Butterflies and plants: a
study in coevolution. Evolution,18, 586–608.
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
tropical regions. Carabid beetles: their evolution, natural
history, and classification (ed. by T.L. Erwin, G.E. Ball and
D.R. Whitehead), pp. 539–592. W. Junk, The Hague.
Escalante, A.A. & Ayala, F.J. (1994) Phylogeny of the malarial
genus Plasmodium, derived from rRNA gene sequences.
Proceedings of the National Academy of Sciences of the United
States of America,91, 11373–11377.
Escalante, A.A., Barrio, E. & Ayala, F.J. (1995) Evolutionary
origin of human and primate malarias: evidence from the
circumsporozoite protein gene. Molecular Biology and Evo-
lution,12, 616–626.
Fahrenholz, H. (1913) Ectoparasiten unde abstammungslehre.
Zoologische Anzeiger (Leipzig),41, 371–374.
Futuyma, D.J. & Slatkin, M. (1983) Coevolution. Sinauer
Associates, Sunderland, MA.
Glen, D.R. & Brooks, D.R. (1985) Phylogenetic relationships of
some strongylate nematodes of primates. Proceedings of the
Helminthological Society of Washington, DC,52, 227–236.
Grenfell, B.T. & Gulland, F.M.D. (1995) Introduction: ecolo-
gical impact of parasitism on wildlife host populations.
Parasitology,111 (Suppl.),S3–S14.
Halas, D.D., Zamparo, D. & Brooks, D.R. (2005) A protocol
for studying biotic diversification by taxon pulses. Journal of
Biogeography,32, 249–260.
Harvell, C.D., Mitchell, C.E., Ward, J.R., Altizer, S., Dobson,
A.P., Ostfeld, R.S. & Samuel, M.D. (2002) Climate warming
and disease risks for terrestrial and marine biota. Science,
296, 2158–2162.
Hoberg, E.P. (1986) Evolution and historical biogeography of a
parasite-host assemblage: Alcataenia spp. (Cyclophyllidea:
Dilpeididae) in Alcidae (Charadriiformes). Canadian Jour-
nal of Zoology,64, 2576–2589.
Hoberg, E.P. (1989) Phylogenetic relationships among genera
of the Tetrabothriidae (Eucestoda). Journal of Parasitology,
75, 617–626.
Hoberg, E.P. (1992) Congruent and synchronic patterns in
biogeography and speciation among seabirds, pinnipeds and
cestodes. Journal of Parasitology,78, 601–615.
Hoberg, E.P. (1995) Historical biogeography and modes of
speciation across high-latitude seas of the Holarctic: con-
cepts for host–parasite coevolution among the Phocini
(Phocidae) and Tetrabothriidae. Canadian Journal of Zool-
ogy,73, 45–57.
Hoberg, E.P. (1996) Faunal diversity among avian parasite
assemblages: the interaction of history, ecology, and bioge-
ography in marine systems. Bulletin of the Scandinavian
Society of Parasitology,6, 65–89.
Hoberg, E.P. (1997a) Phylogeny and historical reconstruction:
host–parasite systems as keystones in biogeography and
ecology. Biodiversity II: understanding and protecting
our biological resources (ed. by M. Reaka-Kudla, D.E. Wilson
and E.O. Wilson), pp. 243–261. Joseph Henry Press,
Washington, D.C.
Hoberg, E.P. (1997b) Parasite biodiversity and emerging
pathogens: a role for systematics in limiting impacts on
genetic resources. Global genetic resources: access, ownership
and intellectual property rights (ed. by K.E. Hoaglund and
A.Y. Rossman), pp. 71–83. Association of Systematics Col-
lections, Washington, D.C.
Hoberg, E.P. (2002) Colonization and diversification: historical
and coevolutionary trajectories among cestodes, cetaceans and
pinnipeds. Tenth International Congress for Parasitology.
Monduzzi Editor, Bologna, pp. 65–69.
Hoberg, E.P. (2005) Coevolution and biogeography among
Nematodirinae (Nematoda: Trichostrongylina) Lagomor-
pha and Artiodactyla (Mammalia): exploring determinants
of history and structure for the northern fauna across the
Holarctic. Journal of Parasitology,91, 358–369.
Hoberg, E.P. & Adams, A. (1992) Phylogeny, historical bio-
geography, and ecology of Anophryocephalus spp.
(Eucestoda: Tetrabothriidae) among pinnipeds of the
Holarctic during the late Tertiary and Pleistocene. Canadian
Journal of Zoology,70, 703–719.
Hoberg, E.P. & Adams, A. (2000) Phylogeny, history and
biodiversity: understanding faunal structure and biogeo-
graphy in the marine realm. Bulletin of the Scandinavian
Society of Parasitology,10, 19–37.
Hoberg, E.P. & Klassen, G.J. (2002) Revealing the faunal
tapestry: co-evolution and historical biogeography of hosts
and parasites in marine systems. Parasitology,124, S3–S22.
Hoberg, E.P., Polley, L., Gunn, A. & Nishi, J.S. (1995)
Umingmakstrongylus pallikuukensis gen. nov. et sp. nov.
Guest Editorial
Journal of Biogeography 32, 1291–1299, ª2005 Blackwell Publishing Ltd 1297

(Nematoda: Protostrongylidae) from muskoxen, Ovibos
moschatus, in the central Canadian Arctic, with comments
on biology and biogeography. Canadian Journal of Zoology,
73, 2266–2282.
Hoberg, E.P., Jones, A. & Bray, R. (1999a) Phylogenetic
analysis among families of the Cyclophyllidea (Eucestoda)
based on comparative morphology, with new hypotheses
for co-evolution in vertebrates. Systematic Parasitology,42,
51–73.
Hoberg, E.P., Monsen, K.J., Kutz, S. & Blouin, M.S. (1999b)
Structure, biodiversity, and historical biogeography of
nematode faunas of holarctic ruminants: morphological and
molecular diagnoses for Teladorsagia boreoarcticus n. sp.
(Nematoda: Ostertagiinae), a dimorphic cryptic species in
muskoxen, Ovibos moschatus.Journal of Parasitology,85,
910–934.
Hoberg, E.P., Rausch, R.L., Eom, K.S. & Gardner, S.L. (2000) A
phylogenetic hypothesis for species of the genus Taenia
(Eucestoda: Cyclophyllidea). Journal of Parasitology,86,
89–98.
Hoberg, E.P., Alkire, N.L., de Queiroz, A. & Jones, A. (2001)
Out of Africa: origins of the Taenia tapeworms in humans.
Proceedings of the Royal Society of London. Series B, Biological
Sciences,268, 781–787.
Hoberg, E.P., Kutz, S.J., Nagy, J., Jenkins, E., Elkin, B.,
Branigan, M. & Cooley, D. (2002) Protostrongylus stilesi
(Nematoda: Protostrongylidae): ecological isolation and
putative host-switching between Dall’s sheep and muskoxen
in a contact zone. Comparative Parasitology,69, 1–9.
Hoberg, E.P., Kutz, S.J., Galbreath, K. & Cook, J. (2003) Arctic
biodiversity: from discovery to faunal baselines – revealing
the history of a dynamic ecosystem. Journal of Parasitology,
89 (Suppl.),S84–S95.
Hoberg, E.P., Lichtenfels, J.R. & Gibbons, L. (2004) Phylogeny
for species of Haemonchus (Nematode: Trichos-
trongyloidea): considerations of their evolutionary history
and global biogeography among Camelidae and Pecora
(Artiodactyla). Journal of Parasitology,90, 1085–1102.
Hugot, J.P. (1999) Primates and their pinworm parasite: the
Cameron hypothesis revisited. Systematic Biology,48, 523–
546.
von Ihering, H. (1891) On the ancient relations between New
Zealand and South America. Transactions and Proceedings of
the New Zealand Institute of Biology,24, 431–445.
von Ihering, H. (1902) Die Helminthen als Hilfsmittel der
zoogeographischen Forschung. Zoologische Anzeiger (Leip-
zig),26, 42–51.
Janzen, D.H. (1968) Host plants as islands in evolutionary and
contemporary time. The American Naturalist,102, 592–595.
Janzen, D.H. (1973a) Host plants as islands. Competition in
evolutionary and contemporary time. The American Nat-
uralist,107, 786–790.
Janzen, D.H. (1973b) Comments on host-specificity of tropical
herbivores and its relevance to species richness. Taxonomy
and ecology (ed. by V.H. Heywood), pp. 201–211. Academic
Press, New York.
Janzen, D.H. (1980) When is it coevolution? Evolution,34,
611–612.
Janzen, D.H. (1981) Patterns of herbivory in a tropical deci-
duous forest. Biotropics,13, 271–282.
Janzen, D.H. (1983) Dispersal of seeds by vertebrate guts.
Coevolution (ed. by D.J. Futuyma and M. Slatkin), pp. 232–
262. Sinauer Associates, Sunderland, MA.
Janzen, D.H. (1985a) Coevolution as a process: what parasites
of animals and plants do NOT have in common. Coevolution
of parasitic arthropods and mammals (ed. by K.C. Kim), pp.
83–99. Wiley and Sons, New York.
Janzen, D.H. (1985b) On ecological fitting. Oikos,45, 308–310.
Johnson, K.P. & Clayton, D.H. (2004) Untangling coevolu-
tionary history. Systematic Biology,53, 92–94.
Kellogg, V.L. (1896) New Mallophaga, 1. With special refer-
ence to a collection from maritime birds of the Bay of
Monterey, California. Proceedings of the California Academy
of Science,6, 31–168.
Kellogg, V.L. (1913) Distribution and species-forming of
ectoparasites. The American Naturalist,47, 129–158.
Manter, H.W. (1966) Parasites of fishes as biological indicators
of recent and ancient conditions. Host–parasite relationships
(ed. by J.E. McCauley), pp. 59–71. Oregon State University
Press, Corvallis, OR.
Mayr, E. (1957) Evolutionary aspects of host specificity among
parasites of vertebrates. Premier symposium sur la spe
´cificite
´
parasitaire des parasites de verte
´bre
´s(ed. by J.G. Baer),
pp. 7–14. Paul Attinger, Neuchatel (International Union of
Biological Sciences and Universite
´Neuchatel).
Mitter, C. & Brooks, D.R. (1983) Phylogenetic aspects of
coevolution. Coevolution (ed. by D.J. Futuyma and M.
Slatkin), pp. 65–98. Sinauer Associates, Sunderland, MA.
Mode, C.J. (1958) A mathematical model for the co-evolution
of obligate parasites and their hosts. Evolution,12, 158–165.
Page, R.D.M. (1990) Temporal congruence and cladistic ana-
lysis of biogeography and co-speciation. Systematic Zoology,
39, 205–226.
Page, R.D.M. (ed.) (2002) Tangled trees. University of Chicago
Press, Chicago.
Percy, D.M., Page, R.D.M. & Cronk, Q.C.B. (2004) Plant–
insect interactions: double-dating associated insect and
plant lineages reveals asynchronous radiations. Systematic
Biology,53, 120–127.
Radtke, A., McLennan, D.A. & Brooks, D.R. (2002) Evolu-
tion of host specificity in Telorchis spp. (Digenea: Plagi-
orchiformes: Telorchiidae). Journal of Parasitology,88,
874–879.
Ricklefs, R.E., Fallon, S.F. & Bermingham, E. (2004) Evo-
lutionary relationships, co-speciation, and host switching
in avian malaria parasites. Systematic Biology,53, 111–
119.
Sorenson, M.D., Balakrishnan, C.N. & Payne, R.B. (2004)
Clade-limited colonization in brood parasitic finches (Vidua
spp.). Systematic Biology,53, 140–153.
Spironello, M. & Brooks, D.R. (2003) Dispersal and
diversification in the evolution of Inseliellium,an
D. R. Brooks and A. L. Ferrao
1298 Journal of Biogeography 32, 1291–1299, ª2005 Blackwell Publishing Ltd

archipelagic dipteran group. Journal of Biogeography,30,
1563–1573.
Van Veller, M. & Brooks, D.R. (2001) When simplicity is not
parsimonious: a priori and a posteriori approaches in his-
torical biogeography. Journal of Biogeography,28, 1–12.
Verschaffelt, E. (1910) The cause determining the selection of
food in some herbivorous insects. Proceedings of the Acad-
emy of Science Amsterdam,13, 536–542.
Weckstein, J.D. (2004) Biogeography explains cophylogenetic
patterns in toucan chewing lice. Systematic Biology,53, 154–
164.
Weiblen, G.D. (2004) Correlated evolution in fig pollination.
Systematic Biology,53, 128–139.
Wiley, E.O. (1986a) Process and pattern: Cladograms and
trees. Systematics and evolution: a matter of diversity (ed. by
P. Hovenkamp), pp. 233–247. University of Utrecht Press,
Utrecht.
Wiley, E.O. (1986b) Methods in vicariance biogeography.
Systematics and evolution: a matter of diversity (ed. by
P. Hovenkamp), pp. 283–306. University of Utrecht Press,
Utrecht.
Wiley, E.O. (1986c) Historical ecology and coevolution.
Systematics and evolution: a matter of diversity (ed. by
P. Hovenkamp), pp. 331–341. University of Utrecht Press,
Utrecht.
Wiley, E.O. (1988a) Vicariance biogeography. Annual Review
of Ecology and Systematics,19, 513–542.
Wiley, E.O. (1988b) Parsimony analysis and vicariance bio-
geography. Systematic Zoology,37, 271–290.
Wojcicki, M. & Brooks, D.R. (2004) Escaping the matrix: a
new algorithm for phylogenetic comparative studies of
co-evolution. Cladistics,20, 341–361.
Wojcicki, M. & Brooks, D.R. (2005) PACT: an efficient and
powerful algorithm for generating area cladograms. Journal
of Biogeography,32, 755–774.
Zandee, M. & Roos, M.C. (1987) Component-compatibility in
historical biogeography. Cladistics,3, 305–332.
BIOSKETCHES
Daniel R. Brooks is a Professor of Zoology, University of
Toronto, specializing in the systematics and evolution of
parasitic helminths. He is currently coordinating the inventory
of eukaryotic parasites of vertebrates, Area de Conservacion
Guanacaste, Costa Rica. He is the co-author of Phylogeny,
ecology and behavior: a research programme in comparative
biology (1991), Parascript: parasites and the language of
evolution (1993) and The nature of diversity: an evolutionary
voyage of discovery (2002).
Amanda L. Ferrao is a student in the Department of
Zoology, University of Toronto.
Editor: Brett Riddle
Guest Editorial
Journal of Biogeography 32, 1291–1299, ª2005 Blackwell Publishing Ltd 1299