Article available at http://www.parasite-journal.org or http://dx.doi.org/10.1051/parasite/1994014291
PARASITIC EFFECTS ON HOST LIFE-HISTORY TRAITS :
A REVIEW OF RECENT STUDIES
MICHALAKIS Y.* AND HOCHBERG M. E.**
Summary :
Résumé
W e review empirical studies bearing on the effects of parasites on
LEURS HOTES : UNE REVUE DES ÉTUDES RÉCENTES
the age of maturity of their hosts. The few cases already published
support theoretical predictions, namely a decrease of host prereproductive life-span unless parasites are benign. Host responses
may be due either to phenotypic plasticity or to genetic diffealready been published both mechanisms occur. Promising areas
of research include the distribution of age-specific potential costs
of resistance to parasitism, as well as the evolution of age-specific
parasite preferences under the concomitant evolution of host lifehistory traits.
publiées confirment des prédictions théoriques, en particulier un
les parasites sont bénins. Les réponses des hôtes aux parasites peuvent être expliquées ou bien par une plasticité phénotypique ou bien
par des différences génétiques, les deux types de mécanismes
ayant été rencontrés bien que très peu d'études aient abordé ce
sujet. Des champs de recherche prometteurs seraient la distribution
en fonction de l'âge de l'hôte d'éventuels coûts de résistance aux
KEY W O R D S : host-parasite interactions, life-history evolution, age at maturity.
M O T S CLES : interactions hôtes-parasites, évolution des traits biodémographiques, âge à la maturité.
parasites, ainsi que l'évolution des préférences parasitaires pour des
hôtes d'âge donné sous l'évolution concomitante des traits biodémographiques des hôtes.
G
iven the fundamental importance o f life-hist o r y t h e o r y to e v o l u t i o n a r y b i o l o g y it is
s o m e w h a t s u r p r i s i n g that a p p l i c a t i o n s to
h o s t - p a r a s i t e s y s t e m s h a v e o n l y started to a p p e a r
o v e r the past d e c a d e , and are almost all empirical
(Minchella, 1 9 8 5 ; Thornhill et a l . , 1986). Rather, most
research involving the evolution of host-parasite syst e m s has b e e n c o n c e r n e d with c h a n g e s in parasite
virulence, d e v e l o p m e n t s b e i n g both empirical and
theoretical (for reviews s e e May and Anderson, 1 9 9 0 ;
Toft and Karter, 1990).
Recently, H o c h b e r g et al. ( 1 9 9 2 ) investigated in detail
with the aid o f a mathematical model just h o w parasites could affect the most fundamental o f their host's
l i f e - h i s t o r y t r a i t s , t h e t i m e to first r e p r o d u c t i o n
( P r o m i s l o w and Harvey, 1 9 9 0 ) . T h e y s h o w e d that
hosts s u b j e c t e d to virulent parasites and u n a b l e to
resist by other means [e.g. immunological resistance
( K l e i n , 1 9 8 2 ) or i n d u c i b l e d e f e n s e s (Harvell, 1 9 9 0
a,b)] w o u l d b e favoured b y s e l e c t i o n if they w e r e
able to reproduce earlier. Only in cases w h e r e para-
* Institut d'Ecologie CNRS IRA 258, HNS, University P. et M. Curie,
Bat. A 7 et. CC 2.37. 7 quai St. Bernard. 75252 Paris Cedex 05,
France.
** Institut d'Ecologie CNRS URA 258, Université P. et M. Curie, ENS,
46 rue d'Ulm, 75230 Paris Cedex 05, France.
Parasite, 1994, 1, 291-294
Nous proposons une revue des étudesportant sur les effets des
parasites sur l'âge de maturité de leurs hôtes. Les quelques études
délai de la maturité de l'hôte dans la majorité des cas sauf lorsque
rences, and even though very few studies on this topic have
e
: EFFETS DES PARASITES SUR LES TRAITS BIODÉMOGRAPHIQUES DE
sites w e r e relatively benign could parasitism select for
longer pre-reproductive life spans.
Here w e review empirical e v i d e n c e relating to the
theoretical propositions o f Hochberg et al. ( 1 9 9 2 ) . W e
address two principal questions. First, whether their
predictions have b e e n met and, s e c o n d , whether the
responses o f the hosts to parasitism are attributable to
phenotypic plasticity or rather to genetic differentiation. In addressing these questions w e e x a m i n e analogous e x a m p l e s involving prey-predator interactions.
After discussing the e v i d e n c e , w e p r o p o s e several
directions for further research. W e emphasize that the
experimental literature on effects of parasites on host
life-history traits is still in its infancy, and therefore it
is too early to reach firm conclusions. T h e few e x p e riments discussed, however, show that this research
area is promising.
PRE-REPRODUCTIVE LIFE SPAN
T
o our k n o w l e d g e three experimental studies
closely related to this topic have b e e n publis h e d r e c e n t l y in t h e p r i m a r y l i t e r a t u r e .
Interestingly, these studies have e x p a n d e d the taxonomic range o f organisms usually covered in life-his-
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291
MICHALAKIS Y. AND HOCHBERG M. E
tory i n v e s t i g a t i o n s ; virtually all past s t u d i e s h a v e
c o n c e r n e d snails as h o s t s to parasitic w o r m s ( s e e
reviews in Minchella. 1 9 8 5 ; Michalakis et at., 1992).
Indeed, w e start by reviewing a case involving a snail
and its n e m a t o d e parasites.
Lafferty ( 1 9 9 3 ) studied the interaction b e t w e e n the
marine snail Cerithidea
califomica
and several n e m a todes which parasitise it. He attempted to test w h e ther parasitism affects age at maturity o f these snails.
He was unable to study directly age at maturity, instead measuring size at maturity, under the assumption that size is highly c o r r e l a t e d to a g e in t h e s e
organisms. He s h o w e d that there was a negative correlation b e t w e e n size at maturity a n d the level o f
infestation o f the host p o p u l a t i o n . In o t h e r words,
snails matured significantly earlier in populations subj e c t e d to high parasitism. Using transplant e x p e r i ments, he s h o w e d that there was a significant effect
o f the origin o f the population. This result indicates
s o m e g e n e t i c b a s i s for the r e s p o n s e o f the h o s t s ,
though it d o e s not preclude other environmental factors such as maternal effects.
G o m a r i z - Z i l b e r and Thomas-Orillard ( 1 9 9 3 ) studied
the interaction between Drosophila
melanogaster
and
its picornavirus (the "C vims"). Infection by this pathog e n i n d u c e s relatively high pre-adult mortality ( a s
much as 40 % ) . They showed, however, that infected
flies have a significantly decreased developmental time
(from egg to adult), developmental time being influenced by temperature, origin o f the population, and the
viral d o s e applied to the host population. B e c a u s e
temperature was responsible of about 98 % of the total
variance, the authors performed separate analyses at
the two different temperatures assayed. At 25°C, devel o p m e n t a l time significantly d e c r e a s e d in all t h r e e
populations studied, each showing a roughly similar
pattern ( n o population effect). At 20°C. however, the
results depended on the population studied since, in
s o m e p o p u l a t i o n s , d e v e l o p m e n t was a c c e l e r a t e d as
viral dose increased while, in others, development was
retarded. Interestingly the authors also s h o w e d that
infection by the C-virus increased the mean number of
ovarioles for all populations at both temperatures.
B o o t s and B e g o n ( 1 9 9 3 ) studied the interaction betw e e n the Indian meal moth (Plodia
interpunctella)
a n d a g r a n u l o s i s virus. T h e y w e r e a b l e to s e l e c t
strains which were resistant to the virus, the rate o f
r e s i s t a n c e b e i n g 1.96 times that o f the s u s c e p t i b l e
b a s e population. This resistance carried an associated
cost, however, corresponding to an increase in developmental time, a reduction in egg-viability and an
increase in pupal weight. T h e authors further dissected the nature o f the cost and found that d e v e l o p ment w a s delayed only in the fourth and fifth larval
292
instars. T h e authors noted that these moths are susceptible to infection only during the first three instars,
while they are practically immune during the fourth
and fifth instars. In other words, resistance to parasitism c a u s e s a delay o f a g e at maturity. This delay,
h o w e v e r , d o e s not c o n c e r n the s u s c e p t i b l e host
stages but only stages which are i m m u n e .
ANALOGY TO PREDATION
Several
a n a l o g o u s studies on life-history shifts
have b e e n conducted in predator-prey interactions ( r e v i e w e d in Lafferty, 1 9 9 3 ) . S o m e have
s h o w n that u n d e r s t r o n g p r e d a t o r p r e s s u r e , p r e y
reduce their pre-reproductive life-span (e.g. Reznick
et al., 1 9 9 0 ) . More interestingly, the effect o f predators o n prey life-history strategies d e p e n d s on a g e specific predation rates. For e x a m p l e , Reznick et al.
( 1 9 9 0 ) s h o w e d that g u p p i e s m a t u r e e a r l i e r w h e n
attacked as adults rather than as juveniles. A longterm e x p e r i m e n t b y the s a m e g r o u p s h o w e d that
these differences have a genetic basis.
T h e r e exist several other cases w h e r e pre-reproductive life-span is increased by predators and in all of
them the delay is related to a higher susceptibility o f
early life s t a g e s . For e x a m p l e , C r o w l a n d C o v i c h
( 1 9 9 0 ) s h o w e d that the freshwater snail Physella
virgata
virgata
i n c r e a s e s its g r o w t h rate a n d d e l a y s
m a t u r i t y in t h e p r e s e n c e o f a p r e d a t o r c r a y f i s h
(Orconectes
virilis).
This d e l a y in maturity can b e
explained by the fact that the predators preferentially
eat small sized prey, s o that there is strong selection
pressure a m o n g t h e s n a i l p o p u l a t i o n t o d i v e r t
resources to growth in order to reduce the duration
o f t h e s t a g e s u s c e p t i b l e to p r e d a t i o n . C r o w l a n d
Covich ( 1 9 9 0 ) w e r e furthermore a b l e to s h o w that
this shift w a s d u e to p h e n o t y p i c plasticity o f t h e
snails, rather than to fixed genetic differences.
PHENOTYPIC PLASTICITY OR GENETIC DETERMINISM ?
N
ot s u r p r i s i n g l y , e v i d e n c e o n this t o p i c is
even more scanty than for the previous two.
T h e few cases available, however, s h o w that
both types o f determinism exist in natural systems.
Cases o f infection of snails by s c h i s t o s o m e s (review e d in Minchella, 1985 and Michalakis et al.,
1992)
indicate that the host r e s p o n s e is due to p h e n o t y p i c
plasticity. T h e s a m e is true for the r e s p o n s e of the
snail P. virgata
s u b j e c t e d to p r e d a t i o n by crayfish
(Crowl and Covich. 1990). T h e d e c r e a s e of maturation size o f the snail C. califomica
Mise au point
w h e n parasitised
Parasite, 1994, 7, 291-294
PARASITIC EFFECTS O N HOST-LIFE H I S T O R Y TRAITS
by trematodes (Lafferty, 1990) d e p e n d s on the origin
o f the population. This latter result d o e s not e x c l u d e
that other factors, such as maternal effects, might b e
responsible for these differences.
In other cases there is certainly a genetic basis in the
host reaction. For e x a m p l e , the resistance and associated developmental delay o f the Indian meal moth
to granulosis virus is definitely due to genetic differences a m o n g strains ( B o o t s and B e g o n , 1 9 9 3 ) . T h e r e
must also b e s o m e g e n e t i c basis in the reaction of
Drosophila
populations to infection b y C-virus, since
at least at s o m e temperatures the various strains react
differently ( s o m e i n c r e a s e and s o m e d e c r e a s e their
developmental t i m e ; Gomariz-Ziber and T h o m a s Orillard, 1993). Finally, Reznick et al. ( 1 9 9 0 ) clearly
s h o w e d that the r e s p o n s e o f g u p p i e s to different
kinds of predators has a genetic basis.
T h e small number of case studies does not enable us
to distinguish any clear trends. O n e potential guide
could be the predictability o f the infection (or predation). Indeed, it s e e m s reasonable to e x p e c t a p h e n o typically plastic r e s p o n s e w h e n e v e r the parasite (or
predator) pressure is highly u n p r e d i c t a b l e in s p a c e
and/or in time. In such i n s t a n c e s , a g e n e t i c b a s i s
would not readily evolve, b e c a u s e the selection pressure i m p o s e d by the parasites c o u l d b e a b s e n t or
highly variable in direction. For example, if parasites
specifically attacking early larval instars are present
only during several generations and then replaced by
parasites preferentially attacking adults o n e w o u l d
e x p e c t any reaction evolved by the hosts to b e plastic.
G e n e t i c determinism w o u l d b e r e a s o n a b l e in those
cases where the trend of the selection pressure imposed by parasites is relatively constant through time.
From the f e w c a s e s studied s o far, w e k n o w that
p a r a s i t i s m l e v e l s a r e g e n e r a l l y w e a k a m o n g snail
populations
and highly variable through time
( A n d e r s o n and May, 1 9 7 9 ) . In a g r e e m e n t with our
verbal argument the responses of snails to parasitism
are plastic (Minchella, 1 9 8 5 ; Michalakis et a l . , 1 9 9 2 ) .
On the other hand, the predation pressure exerted on
g u p p i e s s e e m s to h a v e c o n s i s t e n t t r e n d s t h r o u g h
time, giving sufficient time for genetically-based prey
r e a c t i o n s to e v o l v e ( R e z n i c k a n d E n d l e r , 1 9 8 2 ;
Reznick et a l . , 1 9 9 0 ) .
PERSPECTIVES FOR FUTURE RESEARCH
The predictions of H o c h b e r g et al. ( 1 9 9 2 ) are
generally met in the few cases published so
far.
The
exceptions
come
from
factors
they
did
not model. These are the existence of other modes of
resistance and age-specific parasite infection.
Parasite, 1 9 9 4 . 1. 2 9 1 - 2 9 4
In the first case. Boots and Begon ( 1 9 9 3 ) showed that
in the presence of resistance, associated costs should
b e distributed across stages in such a way that the
costs are preferentially carried by stages immune to
parasitism. Resistance is e x p e c t e d to have associated
c o s t s b e c a u s e , o t h e r w i s e , all individuals would be
expected to be resistant (unless the observed polymorphism is transient; see Frank, 1992, for a discussion of
this topic in the case of plant-pathogen interactions).
As far as w e know, this research area is totally open
both theoretically and experimentally. It would indeed
be very interesting to look at the way resistance costs
are distributed across age (or stage) classes in relation
to age (or stage) specific parasitism rates.
T h e age-specificity o f parasitic infestation (or predator
attack) s e e m s to b e a very important parameter in the
evolution of hosts subjected to parasitism. Hosts pref e r e n t i a l l y a t t a c k e d at y o u n g a g e s w o u l d e v o l v e
towards delayed maturation, while hosts attacked at
late ages should evolve towards accelerated maturation. This result o f life-history theory ( s e e Stearns,
1992 for a review) is, so far, corroborated by all studies o f which w e k n o w . It has not b e e n formalised
though in the c o n t e x t o f host-parasite interactions.
More importantly, it would b e interesting to investig a t e h o w parasite a g e - s p e c i f i c p r e f e r e n c e s s h o u l d
evolve under the concomitant evolution o f host lifehistory traits.
T h e o u t c o m e of these interactions is more complicated if the differential parasitism e f f e c t s are s t a g e d e p e n d e n t and fecundity increases with body size as
is the case for many organisms. If the adult stage is
parasitised preferentially while f e c u n d i t y i n c r e a s e s
with b o d y size, maturity is e x p e c t e d to b e delayed.
This is b e c a u s e animals which will stay longer in the
parasite-immune larval stages will have larger adult
b o d y sizes and therefore a higher potential fecundity
if they can e s c a p e parasitism (reviewed by Roff. 1992.
p. 197).
T h e d e t e r m i n i s m o f t h e h o s t r e a c t i o n to p a r a s i t e
attack is still a matter o f d e b a t e . B o t h p h e n o t y p i c
plasticity and genetic determinism have b e e n found
in e x p e r i m e n t a l c a s e s . It w o u l d b e i n t e r e s t i n g to
relate the nature of the determinism of the host reaction to the predictability o f the direction o f the parasite pressure. This area o f research is still virtually
devoid o f detailed data.
Finally, it would b e interesting to c o m p a r e the fitness
of hosts w h i c h modify their behaviour after parasitism, not only to hosts which do not modify theirs
but also to unparasitised hosts. Indeed, it has b e e n
p r o p o s e d that parasites could actually avoid an arms
race with their host if they were pleitotropic with respect to their host's fitness (Michalakis et al., 1 9 9 2 ) .
Mise au point
293
MICHALAKIS Y . A N DH O C H B E R G M.E
T h e term « pleiotropy », used as an analogy to developmental genetics, m e a n s that a given factor might
have various effects. In the present context, a parasite
could have both benign and detrimental effects. T h e
two kinds o f effect could b e manifested tinder different conditions either in s p a c e (spatial pleiotropy) or
in time ( t e m p o r a l p l e i o t r o p y ) . As an e x t r e m e c a s e ,
p a r a s i t e s c o u l d a c t like s e n e s c e n c e g e n e s ( s e n s u
Williams. 1 9 5 7 ) with beneficial effects at early stages
in the life o f the host and detrimental effects at later
stages.
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93, 443-450.
TOFT OA. and [CARTER A.J. Parasite-host coevolution.
in Ecology and Evolution. 1990. 5.326-329.
Trends
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Parasite, 1 9 9 4 , 1, 2 9 1 - 2 9 4