Evolutionary Ecology of Parasites: From Individuals to
Communities
Author: Joly, Damien O.
Source: Journal of Wildlife Diseases, 37(1) : 212-214
Published By: Wildlife Disease Association
URL: https://doi.org/10.7589/0090-3558-37.1.212
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212
Journal of Wildlife Diseases, 37(1), 2001, pp. 212–214
䉷
Wildlife Disease Association 2001
BOOK REVIEW . . .
Evolutionary Ecology of Parasites: From
Individuals to Communities. By R. Poulin,
Chapman & Hall, New York. 1998. 212 pp. US
$107.00 (hardcover), US $54.00 (paperback)
from amazon.com.
Ecology is the study of organisms and their
environments (Begon et al., 1996); therefore, if
animal hosts can be viewed as part of the en-
vironment for their parasites, the synthesis of
ecology and parasitology is a logical extension
of each discipline. In this book Robert Poulin
laments the lack of crossover between the two
sciences. Intended as a reference to parasitol-
ogists, this book bridges this gap and stimulates
the kind of cross-fertilization that has so often
in the past led to new insights when two dis-
ciplines intermingle. Poulin approaches this
task from an evolutionary framework that neat-
ly encapsulates his arguments. Poulin describes
the ecology of parasites at three scales: the in-
dividual, the population, and the community.
He begins by discussing the evolution of para-
sitism and the processes that guide its struc-
ture. Concepts of population ecology are then
introduced, particularly in light of the unique
circumstances that parasite populations expe-
rience. Finally, he expands to the level of par-
asite communities and the interspecies inter-
actions through which they develop. The re-
sulting monograph is a cohesive introduction to
ecological principles for parasitologists, as well
as a guide to the parasite niche for ecologists.
The most fundamental question any evolu-
tionary ecologist must ask when confronted
with a particular behavioural or morphological
trait is, ‘‘what is its evolutionary significance?’’
Poulin repeatedly returns to this foundation.
When describing the ecology of parasites at the
scale of the individual, Poulin never deviates
far from a evolutionary perspective. For ex-
ample, Poulin asserts that two conditions are
required in order for parasitism to evolve: (1)
morphological and behavioural mechanisms
must have existed that allowed a protoparasite
to take advantage of the parasite niche, and (2)
the fitness benefits of such a change in life style
would have to outweigh the costs. Further, he
argues at length that the evolution of complex
life cycles (i.e., addition of one or more inter-
mediate hosts) was an adaptive, rather than ac-
cidental, modification to the life history of var-
ious parasites.
The most interesting application of an evo-
lutionary perspective is the discussion of the
evolution of virulence, which is usually associ-
ated with parasite fecundity. Poulin argues that
virulence should be a parasite-centred concept,
as ‘‘from the parasite’s perspective...what
happens to the host as a consequence of its
exploitation by the parasite may be of no im-
portance.’’ (p. 67). In the same paragraph, he
continues this argument: ‘‘Our notion of viru-
lence originates from medical science and is fo-
cused on impact on host fitness, whereas selec-
tion in parasites acts on rates of host exploita-
tion irrespective of effects on host fitness.’’
Poulin reviews extensive evidence that suggests
virulence (whether it is defined as fecundity of
the parasite or effect on host productivity) does
not necessarily attenuate with common evolu-
tionary history among parasite and host as pre-
viously thought. A parasite-centred concept of
virulence does not preclude a positive correla-
tion between parasite virulence and fecundity;
however, the relationship should not be defined
by such a correlation.
Poulin also addresses the widespread as-
sumptions that transition from free-living to
parasitic life styles incurs a concurrent reduc-
tion in body size and an increase in fecundity.
He points out methodological biases that have
prevented proper comparison among parasites
and their free-living sister taxa (i.e., lack of cor-
rection for phylogeny during analysis and in-
completely described taxa). Further, he pro-
vides extensive empirical evidence suggesting
that both body size and fecundity are life his-
tory traits that can increase or decrease during
this transition, depending on the particular se-
lection pressures. This is an example of Poulin’s
meticulous attack of incorrect assumptions that
is refreshing and brings this book to a higher
level than simply a review text.
Poulin does an admirable job of bringing
ecological tools for describing the distribution
and demography of populations to parasitology.
Concepts such as the causes and consequences
of aggregation, population persistence, stan-
dard epidemiological models, and density de-
pendence are described coherently and com-
prehensively.
Poulin describes how terminology differs
among disciplines. For example, he notes that
an ‘‘overdispersed’’ distribution is clumped or
aggregated to parasitologists, but to ecologists
overdispersion describes a uniform distribu-
tion. Unfortunately, Poulin fails to explicitly de-
fine ‘‘regulation,’’ a fundamental term in ecol-
ogy. A regulating factor is any density-depen-
dent process that keeps populations within pre-
dictable density ranges. Regulating factors are
a density-dependent subset of limiting factors
that quantifiably affect population growth.
There has been much confusion in ecological
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BOOK REVIEWS 213
literature as a result of vague or inaccurate use
of the term regulation (e.g., Sinclair, 1991). An
explicit definition in this volume would have
prevented this misunderstanding in ecological
parasitology.
An opportunity for further bridging the gap
between the terminology of ecology and para-
sitology was missed in this text. Poulin uses the
term ‘‘infrapopulation’’ to define all the para-
sites of a particular species occurring within the
body of a single host individual (Margolis et al.,
1982). This is in contrast to the ‘‘suprapopula-
tion,’’ which encompasses all the parasites of a
single species, regardless of developmental
stage, that occur within hosts within an ecosys-
tem (Margolis et al., 1982). If an individual host
is viewed as ‘‘habitat’’ for a parasite infrapopu-
lation, these terms are directly analogous to the
ecological terms, ‘‘local population’’ (a set of in-
dividuals living in the same habitat patch) and
‘‘metapopulation’’ (set of local populations
which interact via dispersing individuals among
local populations; Hanski, 1996), respectively.
The analogy of metapopulation dynamics has
been used extensively to describe the epide-
miology of measles in humans (e.g., Grenfell
and Harwood, 1997; Finkensta¨dt and Grenfell,
1998) and the distribution of strongylid nema-
todes in mammals (Arneberg et al., 1998; see
review by Begon et al., 1996 for other exam-
ples). The metapopulation concept brought
many innovations to ecology, and the opportu-
nity to generate new ideas may have been be-
cause the concept was excluded here. For ex-
ample, Poulin (1998) emphasizes that regula-
tion occurs via processes acting within infra-
populations. Regulation of metapopulation size
is a function of the colonization rate of new
habitats, the proportion of habitats occupied,
and the extinction rate within each habitat. The
respective processes of infection, prevalence,
and recovery or mortality of host individuals are
analogous in light of the metapopulation con-
cept. Dispersal among habitats (hosts) clearly
affects both colonization (infection) and extinc-
tion (host recovery or mortality), and density of
habitat patches (hosts) is a major determinant
of dispersal. Therefore, density of hosts should
be a primary determinant of parasite abun-
dance. In fact, Arneberg et al. (1998) demon-
strated that density of mammalian hosts influ-
ences strongylid nematode abundance, in con-
trast to the common view that regulationoccurs
primarily through infrapopulation density-de-
pendence (Poulin, 1998).
A community is a collection of species in the
same place and time. Poulin effectively de-
scribes interspecific interactions (e.g., compe-
tition, facilitation etc.) that serve to modify the
abundance and distribution of parasites within
a community. Further, Poulin provides a com-
prehensive review of the evidence surrounding
creation of community structure, effectively
whether, ‘‘the structure of parasite infracom-
munities differs from that of random assem-
blages.’’ (p. 145). This has been a central ques-
tion in ecology since Frederic Clements pro-
posed in 1916 that plant community succession
results in an ‘‘organic entity’’ or functional su-
per-organism (Clements, 1916). Gleason (1926)
vehemently opposed this thesis, and proposed
that associations among plants were coinci-
dences driven by similar resource needs. Pou-
lin’s review suggests that infracommunity de-
velopment also may be the result of similar re-
source needs.
Poulin concludes the book by discussing the
influence of human activities, namely habitat
alteration and parasite control (which he points
out is merely changing the parasites’ habitat).
As with all ecology, it is evident that our ana-
lytical toolbox suffers from a severe lack of pre-
dictive power, consequently the consequences
of our actions are largely unknown. Maybe, as
Poulin predicts, the use of comparative studies
to develop testable hypotheses will allow the
development of a ‘‘holistic, evolutionary per-
spective of parasite biology.’’
LITERATURE CITED
A
RNEBERG
, P., A. S
KORPING
,B.G
RENFELL
,
AND
A.
F. R
EAD
. 1998. Host densities as determinates of
abundance in parasite communities. Proceedings
of the Royal Society of London B. 265: 1283–
1289.
B
EGON
,M,J.L.H
ARPER
,
AND
C. R. T
OWNSEND
.
1996. Ecology: Individuals, populations, and
communities. 3rd Edition. Blackwell Science
Ltd., Oxford, 1068 pp.
C
LEMENTS
, F. E. 1916. Plant succession: An analysis
of the development of vegetation. Carnegie In-
stitution of Washington Publication 520, Wash-
ington, D.C., 512 pp.
F
INKENSTA
¨
DT
,B.,
AND
B. G
RENFELL
. 1998. Empir-
ical determinants of measles metapopulation dy-
namics in England and Wales. Proceedings ofthe
Royal Society of London B. 265: 211–220.
G
LEASON
, H. A. 1926. The individualistic concept of
the plant association. Bulletin of the Torrey Bo-
tanical Club 53: 1–20.
G
RENFELL
,B.,
AND
J. H
ARWOOD
. 1997.
(Meta)population dynamics of infectious diseas-
es. Trends in Ecology and Evolution 12: 395–
399.
H
ANSKI
, I. 1996. Metapopulation ecology. In Popu-
lation dynamics in ecological space and time. O.
E. Rhodes, R. K. Chesser, and M. H. Smith
(eds.). University of Chicago Press, Chicago, Il-
linois, pp. 13–41.
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214 JOURNAL OF WILDLIFE DISEASES, VOL. 37, NO. 1, JANUARY 2001
M
ARGOLIS
, L., G. W. E
SCH
,J.C.H
OLMES
,A.M.
K
URIS
,
AND
G. A. S
CHAD
. 1982. The use of eco-
logical terms in parasitology (report of an ad hoc
committee of the American Society of Parasitol-
ogists). The Journal of Parasitology 68: 131–133.
P
OULIN
, R. 1998. Evolutionary ecology of parasites:
from individuals to communities. Chapman and
Hall, New York, New York, 212 pp.
S
INCLAIR
, A. R. E. 1991. Science and the practice of
wildlife management. The Journal of Wildlife
Management 55: 767–773.
Damien O. Joly, Department of Biology, University of
Saskatchewan, 112 Science Place, Saskatoon, Sas-
katchewan S7N 5E2 Canada.
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