Behavioral Ecology Vol. 11 No. 1: 19-26
© 2000 International Society for Behavioral Ecology
Ecological immunology: life history trade-offs and immune defense in birds
a School of Animal and Microbial Sciences, University of Reading, Whiteknights, PO Box 228, Reading, RG6 6AJ, UK, b Department of Biological and Molecular Sciences, University of Stirling, Stirling, FK9 4LA, UK
Address correspondence to K. Norris. E-mail: k.norris{at}reading.ac.uk .
Received 2 March 1999; revised 28 April 1999; accepted 21 May 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMeasuring immunocompetenceTrade-offs and immune defenseFuture prospectsConclusionsACKNOWLEDGEMENTSREFERENCES |
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There has been considerable recent interest in the effects of life-history decisions on immunocompetence in birds. If immunocompetence is limited by available resources, then trade-offs between investment in life-history components and investment in immunocompetence could be important in determining optimal life-history traits. For this to be true: (1) immunocompetence must be limited by resources, (2) investment in life-history components must be negatively correlated with immunocompetence, and (3) immunocompetence must be positively correlated with fitness. To gather such empirical data, ecologists need to be able to measure immunocompetence. We review techniques used to measure immunocompetence and how they are applied by ecologists. We also consider the components of the immune system that constitute immunocompetence and evaluate the possible consequences of measuring immunocompetence in different ways. We then review the empirical evidence for life-history trade-offs involving immune defense. We conclude that there is some evidence suggesting that immunocompetence is limited by resources and that investment in certain life-history components reduces immunocompetence. However, the evidence that immunocompetence is related to fitness is circumstantial at present, although consistent with the hypothesis that immunocompetence and fitness are positively correlated. We argue that future work needs to examine the fitness effects of variation in immunocompetence and suggest that artificial selection experiments offer a potentially important tool for addressing this issue.
Key words: fitness, immune system, immunocompetence, life-history trade-offs.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMeasuring immunocompetenceTrade-offs and immune defenseFuture prospectsConclusionsACKNOWLEDGEMENTSREFERENCES |
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Since the publication of Hamilton and Zuk's seminal paper on the role of parasites in sexual selection in 1982, there has been considerable interest in ecological and evolutionary relationships between parasites and their hosts (reviewed by Clayton and Moore, 1997
; Lochmiller,
1996; Loye and Zuk,
1991; Sheldon and Verhulst,
1996; Zuk, 1996).
Several studies have shown a trade-off between investment in life-history
components, such as reproductive effort or sexual ornaments, and infection
with parasites; increasing investment in such life-history components often
increases the prevalence or intensity of parasitic infections (e.g.,
Møller, 1994,
1997;
Norris et al., 1994;
Richner et al., 1995;
Sheldon and Verhulst, 1996).
More recently, interest has focused on the possibility that the relationship
between life-history decisions and parasitism may be mediated by a trade-off
between investment in life-history components and immune defense by hosts
(i.e., the prevention or control of an infection by pathogens or parasites)
(Deerenberg et al., 1997;
Folstad and Karter, 1992;
Saino and Møller, 1996;
Saino et al.,
1997a,b).
If resources (e.g., energy, protein, nutrients) are limiting, it is reasonable
to assume that investment of resources in, for example, a larger family or a
more elaborate sexual ornament, might reduce the resources available to invest
in immune defense (Sheldon and Verhulst,
1996). Because the immune system plays such a pivotal role in
defending an animal against attack by pathogens and parasites
(Roitt et al., 1998;
Wakelin, 1996), such a
reduction in immunocompetence (i.e., an animal's ability to mount an effective
immune defense) is likely to reduce fitness, so trade-offs involving immune
defense could be crucial in determining optimal life-history decisions. We
define "immunocompetence" as the ability of a host to prevent or
control infection by pathogens and parasites. To demonstrate that a trade-off between life-history decisions and immunocompetence is evolutionary significant, three pieces of empirical evidence are required: (1) immunocompetence must compete with life-history components for access to limiting resources, (2) increasing investment in a particular life-history component must reduce immunocompetence, and (3) a reduction in immunocompetence must cause a reduction in fitness. If these conditions are fulfilled, it is then important to describe how life-history decisions and immunocompetence relate to fitness in order to understand optimal levels of investment in life-history decisions and immunocompetence. To gather such empirical data, it is clearly important to be able to measure immunocompetence. Therefore, the main aims of this review are to critically examine the techniques employed by ecologists to measure immunocompetence and the limitations of the techniques and the evidence for trade-offs of evolutionary significance between investment in life-history components and immunocompetence.
Our discussion is taxonomically biased toward studies involving birds because birds have a relatively complex immune system and are ideal subjects for the experimental manipulation of life-history decisions. Birds provide a unique opportunity to manipulate life-history decisions and immunocompetence in wild populations, and, as a result, the majority of experimental studies on wild populations have involved birds. However, our arguments are general and relate to any taxon within which the question of immunocompetence trade-offs is being considered.
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Measuring immunocompetence |
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TOPABSTRACTINTRODUCTIONMeasuring immunocompetenceTrade-offs and immune defenseFuture prospectsConclusionsACKNOWLEDGEMENTSREFERENCES |
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To examine trade-offs between life-history decisions and immune defense, ecologists need to be able to measure an individual's immunocompetence; that is, it is necessary to be able to quantify how immunocompetence changes as investment in a life-history component changes. There are basically two different types of technique available for assessing immunocompetence that have been used by ecologists interested in life-history trade-offs: (1) monitoring techniques and (2) challenge techniques (Table 1). Monitoring techniques provide a measure of an individual's health and the status of its immune system at the time it was sampled. As a result, such techniques provide some information on an individual's immunocompetence but also reflect the immune response to current infections. This potentially makes certain techniques difficult to interpret if used as a measure of immunocompetence. For example, one monitoring technique used simply involves counting different types of leukocytes present in blood samples—heterophils (phagocytosing cells of the innate immune system) and lymphocytes (mainly T- and B-cells of the acquired immune system) (e.g., Dufva and Allander, 1989
; Ots and
Hõrak, 1996;
Zuk and Johnsen, 1998).
Although it is possible that low lymphocyte numbers, for example, represent
poor immunocompetence, such data could also reflect the lack of current
infections requiring a specific immune response from the host. Conversely,
high lymphocyte numbers could reflect high immunocompetence, the status of
current infections, or a combination of both.
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Such effects make it difficult to predict a priori the direction of correlations between investment in life-history components and immunocompetence measured using a monitoring technique. For example, reproductive effort in a hypothetical host is known to be positively correlated with the risk of parasitism. If we assume that this is caused by increased contact with vectors carrying the parasite rather than reduced immunocompetence, then we might expect the abundance of leukocytes in blood smears, for example, to be positively correlated with reproductive effort because birds experiencing high levels of effort also have a high current infection status. Conversely, assume that the relationship between parasitism and reproductive effort is caused by reduced immunocompetence. Under these circumstances we might expect a negative correlation between leukocyte abundance and reproductive effort. In reality, a combination of both possibilities is likely, so negative, positive, or nonsignificant correlations are possible depending on the mechanism linking parasitism and reproductive effort and the relative importance of immunocompetence and current infection status in influencing the abundance of leukocytes in peripheral blood. In our opinion, therefore, the validity of certain monitoring methods as measures of immunocompetence per se is questionable.
For these reasons, ecologists have recently used challenge techniques, in
which a component of the immune system, usually the humoral or cell-mediated
acquired immune system, is exposed to a novel antigen and the subsequent
immune response quantified (Table
1). The advantage of these techniques is that each individual in
the study is exposed to a standardized challenge to their immune system, and
the response of the immune system is quantified in a standardized way.
Variation between individuals in the strength of the response to such a
challenge is then taken as a measure of immunocompetence that can be related
to life-history components or experimental manipulations of these components
(e.g., Deerenberg et al., 1997;
Saino et al.,
1997a,b;
Christe et al., 1998;
Nordling et al., 1998).
Although challenge techniques provide a potentially powerful way of examining
trade-offs involving immune defense, the relatively simplistic approach to
measuring immunocompetence used by ecologists contrasts with that advocated by
immunologists interested in human health or the health of domestic birds
(e.g., Dietert et al., 1994,
1996;
Luster et al., 1992).
Immunologists argue that, due to the numerous components in the immune system,
several immune tests are required to measure immunocompetence effectively
(Table 2). What are the
possible consequences of an oversimplified view of the immune system, and what
needs to be measured and why?
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Most ecological studies that have used a challenge technique have employed
a single technique that quantifies one component of the immune system, usually
either the humoral or cell-mediated immune response (e.g.,
Deerenberg et al., 1997; Saino
et al.,
1997a,b;
Christe et al., 1998;
Nordling et al., 1998). For
simplicity, consider the immune system as being composed of three primary
components: innate immunity, humoral immunity, and cell-mediated acquired
immunity. This classification approximates the components assessed using the
immune assays proposed by Dietert et al.
(1994,
1996) for domestic poultry
(Table 2), the major components
of immunocompetence identified by Luster et al.
(1992) (see also
Table 2 in
Dietert et al., 1994), and
those recognized by researchers examining immunocompetence in poultry (e.g.,
Cheng and Lamont, 1998). By
using a single technique to assess only one of these components as a measure
of overall immunocompetence, ecologists implicitly assume that there is a
correlated response in the other components of the immune system not measured.
That is, there is a reduction in investment in each component of the immune
system as a result of resource limitation. If this assumption is correct,
using a single challenge technique to measure immunocompetence would be
adequate because it would provide an index of overall immunocompetence.
It is possible that resource limitation has a differential effect on the
different components of the immune system (i.e., there is no correlated
response). This could occur if individuals invested strategically in the
different components of their immune systems. There could be sensible
evolutionary reasons for doing this. There is evidence that limiting access to
resources, such as energy or protein, compromises immune defense (e.g., Glick
et al., 1981,
1983;
Lochmiller et al., 1993;
Saino et al., 1997b). As a
result, it is possible that investment in one component of the immune system
could compromise an animal's ability to invest in other components. Under
these circumstances, animals could be forced to optimize their investment in
each component, based on selection pressures generated by the important
pathogens and parasites their immune systems have to combat. Investment of
limited resources in immune system components should reflect the fitness
effects on the host imposed by pathogens and parasites controlled by each
component. How might such strategic investment influence the relationship
between immunocompetence measures and resource limitation?
As resource limitation becomes more severe, investment in immune system components should be altered to maximize fitness for a given resource availability. This could conceivably mean that, as resource limitation increases, investment is initially reduced in one component (A) to maintain the effectiveness of another component (B), especially if component B is crucial in controlling potentially pathogenic infections. Clearly, if the immunocompetence of the host was measured by assessing a single component of the immune system under these circumstances, two different conclusions might be reached. If component A were assessed, it would be concluded that resource limitation reduced immunocompetence. However, if component B were assessed, it would be concluded that resource limitation had no significant effect on immunocompetence.
There is evidence that selection can influence investment in one component
of the immune system to the detriment of other components. Artificial
selection can be used to produce domestic fowl lines that exhibit high (HA) or
low (LA) antibody titers when immunized with sheep erythrocytes
(Seigel and Gross, 1980).
Gross et al. (1980) showed
that HA birds were significantly less effective at controlling bacterial
infections compared with LA birds. Bacterial infections are generally
controlled by phagocytosing cells such as heterophils (i.e., innate immunity;
Roitt et al., 1998), so these
results suggest that selection for an improved immune response from a
component of the acquired immune system could reduce investment in innate
immunity. That is, there could be a trade-off between investment in different
immune system components.
If investment in immune system components is shaped by selection in a similar way in wild bird populations, then ecological studies that examine the competence of only a single immune system component run an increased risk of type II statistical errors—failing to reject the null hypothesis that there is no relationship between immunocompetence and life-history decisions. This means that ecologists assessing only a single immune system component should be wary of nonsignificant results. However, significant results can be regarded as reliable evidence that life-history decisions do have consequences for immunocompetence.
Ecologists also implicitly assume that challenging a particular immune
system component with a novel antigen produces a similar immune response,
irrespective of the specific antigen used. Although this assumption has not
been rigorously tested in wild bird populations, data from domestic fowl
suggest that, indeed, immunocompetence measurements might not be antigen
specific. For example, Gross et al.
(1980) showed that chicken
lines selected for a high-level antibody response to sheep erythrocytes also
displayed higher immunocompetence when challenged with other antigens (e.g.,
Newcastle's disease virus vaccine).
Given these complexities, how should ecologists measure immunocompetence?
There are two obvious differences between the approach to measuring
immunocompetence advocated by immunologists (e.g.,
Table 2) and that used by
ecologists. First, to our knowledge no ecological study has assessed more than
one immune system component during a particular experiment on a wild
population (see Dabbert et al.,
1997; Lochmiller et al.,
1993, for examples of a panel of assays applied to a captive
population). Second, no direct assessment has been made of innate
immunocompetence in any ecological study involving wild birds. In vivo
challenge techniques are available for assessing innate immunity (e.g.,
Cheng and Lamont, 1988).
However, such techniques have not been applied to wild birds, so methods need
to be developed. Alternative monitoring methods are also possible. Heterophils
in blood samples can be isolated and counted (see
Table 1) and their
phagocytosing activity assessed in vitro (e.g.,
Rodriguez and Lea, 1994;
Rodriguez et al., 1997) as a
potential measure of innate immunocompetence. However, this monitoring method
also has the problem of assessing both immunocompetence and the immune
response to current infections.
Humoral and cell-mediated acquired immunity are crucial to controlling a
range of pathogens and parasites, including viruses, intra- and extracellular
parasites, and ectoparasites (Roitt et
al., 1998; Wakelin,
1996). Innate immunity is generally regarded as having an
important role in the control of some of these infections, particularly during
the initial stages, but innate immunity is the primary means of controlling
bacterial infections (Roitt et al.,
1998). Therefore, it seems prudent to suggest that these immune
system components need to be assessed in future studies interested in
immunocompetence trade-offs. This presents practical problems. If different
immune system components are simultaneously challenged, does this influence
the effectiveness of each component compared with a challenge to a single
component? This seems likely if immunocompetence is limited by resources. As a
result, it might be necessary to assess different immune system components in
different individuals experiencing similar experimental treatments. This would
have important implications for sample sizes required in immunocompetence
studies and for the statistical power of feasible field experiments.
Nonetheless, it is important that these methodological issues are addressed. A
more comprehensive assessment of immunocompetence does not preclude a role for
studies focusing on single components of the avian immune system. However,
such an approach has clear limitations if used as a general measure of
immunocompetence, especially if the data suggest no significant effect of
life-history decisions on the competence of the immune system component being
assessed.
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Trade-offs and immune defense |
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TOPABSTRACTINTRODUCTIONMeasuring immunocompetenceTrade-offs and immune defenseFuture prospectsConclusionsACKNOWLEDGEMENTSREFERENCES |
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A number of studies have examined aspects of the potential trade-off between life-history decisions and immunocompetence. Are such trade-offs significant?
Resource limitation and immune defense
The evidence that an immune response is energetically costly is equivocal
(see R
berg
et al., 1998, for a review). There is also evidence that a
short-term increase in food intake can reduce immunocompetence (e.g.,
Klasing, 1998). Furthermore,
some nutrients act as immunomodulators, influencing the specific type of
immune response exhibited by a host (e.g.,
Lessard et al., 1997).
Nevertheless, there is evidence that resources such as energy and protein can
limit immunocompetence. Glick et al.
(1981,
1983) showed that dietary
levels of energy and/or amino acids influenced humoral and cell-mediated
immunocompetence in domestic fowl. The relationship between nutrition and
immunocompetence in domestic fowl is reviewed by Cook
(1991). Lochmiller et al.
(1993) showed that
cell-mediated but not humoral immunocompetence was significantly suppressed in
captive northern bobwhite chicks (Colinus virginianus) raised on a
diet with a low protein content. This study also highlights the importance of
examining different immune system components within a single experiment. The
majority of studies have been conducted on captive birds, but one study has
shown that resource limitation can reduce immunocompetence in a wild bird
population. Saino et al.
(1997b) showed that nestling
barn swallows (Hirundo rustica) provided with a protein-rich food
supplement at regular intervals after hatching had significantly better
cell-mediated immunocompetence than controls.
Life-history decisions and immune defense
Over the past 10 years, two life-history decisions have been studied in
detail with respect to whether investment increases the risks of parasitism:
reproductive effort and sexual ornamentation. There is now compelling evidence
that there is a trade-off between the risk of parasitism and these
life-history decisions (reviewed by
Møller, 1997;
Sheldon and Verhulst, 1996).
However, this evidence, in isolation, is not sufficient to show that these
life-history decisions have consequences for immune defense. This is because
parasitism not only depends on the host's ability to control an infection
using its immune system, but also on the chances of a host being infected with
the parasite, which might be unrelated to immunocompetence (see also
Norris et al., 1994).
Therefore, it is important to show that life-history decisions have a direct
effect on immunocompetence.
Fewer studies have explicitly examined the link between life-history
decisions and immune defense in birds. However, there is evidence that
life-history decisions can have a direct effect on immunocompetence. Increased
reproductive effort reduces immunocompetence. Deerenberg et al.
(1997) conducted a number of
experiments that examined the relationship between reproductive effort and
humoral immunocompetence in zebra finches (Taeniopygia guttata) by
quantifying the production of antibodies toward sheep erythrocytes. They
showed that all nonbreeding birds produced antibodies but that only 47% of
breeding birds produced antibodies. There was also a reduction in antibody
response with increasing brood size, suggesting that increasing reproductive
effort progressively reduced humoral immunocompetence
(Figure 1a). Furthermore, birds
showed a reduced antibody response if they were forced to undertake
energetically costly tasks, implying that the increased work required during
breeding could directly result in reduced immunocompetence. Nordling et al.
(1998) conducted a comparable
brood manipulation experiment on a wild population of collared flycatchers
(Ficedula albicollis) (Figure
1b). They quantified humoral immunocompetence by quantifying
antibody production toward Newcastle disease virus (NDV) vaccine and showed
that female birds raising larger broods (i.e., having greater reproductive
effort) had reduced immunocompetence.
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The reproductive effort of parents also appears to have consequences for
immune defense of offspring. Saino et al.
(1997b) showed that there was
a negative correlation between cell-mediated immunocompetence in nestling barn
swallows and the size of the brood. A brood manipulation experiment showed
that this relationship was causal: chicks in broods enlarged by one nestling
had significantly lower cell-mediated immunocompetence compared with broods
reduced by one nestling (Figure
1c). Saino et al.
(1997b) argued that this
resulted from a lower per capita feeding rate in larger broods, so chicks in
such broods were more likely to be resource limited. This interpretation was
supported by an experiment in which chicks in a number of different broods
were provided with a protein-rich food supplement. Food-supplemented chicks
had significantly higher immunocompetence compared with controls.
Investment in sexual ornamentation also appears to affect humoral
immunocompetence. Male barn swallows have elongated tail ornaments that are
important in mate choice by females; males with long tails are more likely to
obtain a mate, mate earlier in the season and are more successful at mating
with extrapair females (Møller,
1994). There is evidence that investment in this sexual ornament
by males can reduce immunocompetence. Saino et al.
(1997a) experimentally
manipulated the tail length of male swallows and examined the impact of this
manipulation on antibody production toward sheep erythrocytes. They showed
that males with elongated tails had reduced 
-globulin levels, compared
with control males (i.e., no change in tail length) or males with shortened
tials (Figure 1d). This implies
that humoral immunocompetence is compromised by increasing investment in tail
ornaments.
Direct evidence of a trade-off between sexual ornamentation in male birds
and immunocompetence comes from a recent study on selected lines of domestic
fowl. Verhulst et al. (1999)
produced lines of domestic fowl selected for different levels of antibody
response to sheep erythrocytes (low or high response) and control lines. They
showed that lines selected for a high antibody response had significantly
smaller sexual ornaments (i.e., comb size) than the lines selected for a low
antibody response, with control lines intermediate. This is consistent with
the idea that investment in immunocompetence reduces a male's ability to
invest in his sexual ornaments, but the study also elegantly demonstrates a
negative genetic correlation between immunocompetence and this life-history
component.
Immune defense and fitness
Although there is experimental evidence that immunocompetence is influenced
by resource availability and that investment in life-history components, such
as reproductive effort and sexual ornaments, has consequences for
immunocompetence, reduced immunocompetence must reduce fitness for these
trade-offs to be evolutionarily significant. That is, changes in
immunocompetence of the magnitude recorded in experimental studies in relation
to changes in investment in life-history components must affect fitness. This
distinction is important because it is not sufficient simply to argue that a
reduction in immunocompetence must have fitness consequences because the
immune system is so important in pathogen and parasite prevention and control.
How fitness changes in relation to changes in immunocompetence needs to be
quantified to investigate optimal life-history decisions empirically.
Because the immune system is designed to prevent and control infection by
pathogens and parasites, it is reasonable to expect that a reduction in
immunocompetence might lead to an increased risk of infection. There is
evidence consistent with this idea. For example, studies on reproductive
effort have shown that increased effort is associated with reduced
immunocompetence (e.g., Deerenberg et al.,
1997; Nordling et al.,
1998) and increased parasitism
(Møller, 1997;
Norris et al., 1994;
Oppliger et al., 1996;
Ots and
Hõrak, 1996;
Richner et al., 1995).
However, it is possible that correlations between reproductive effort and
parasitism represent the risk of exposure to parasites rather than the
influence of immunocompetence. To our knowledge, only a single study has
reported the effects of reproductive effort on both immunocompetence and
parasitism within a single experiment. Nordling et al.
(1998) showed that female
collared flycatchers raising enlarged broods had reduced humoral
immunocompetence and an increased intensity of infection by
Haemaproteus parasites. This is consistent with the hypothesis that
reproductive effort influences immunocompetence, which in turn influences
parasitism, although these data are, in isolation, insufficient to demonstrate
a causal link (see below for discussion).
Even if individuals with low immunocompetence were more likely to be
infected with pathogens and parasites, it would still be necessary to show
that such infections reduce fitness. Although it is generally accepted that
parasites can reduce the fitness of their hosts
(Clayton and Moore, 1997;
Loye and Zuk, 1991), links
among life-history decisions, immunocompetence, parasitism, and fitness must
be established to show that immunocompetence trade-offs are likely to be of
evolutionary significance. It is possible that life-history decisions
influence immunocompetence, which in turn influences parasitism, but that
increased parasitism has negligible fitness consequences in specific cases.
For example, Norris et al.
(1994) showed that increased
reproductive effort by male great tits increased the prevalence of their
hematozoan parasites. If we assume this was due to reduced immunocompetence,
is this sufficient evidence of a significant trade-off? Circumstantial
evidence would suggest not, as a number of studies have failed to show that
increased reproductive effort in great tits causes a reduction in adult
survival or future fecundity (e.g.,
Pettifor et al., 1988;
Tinbergen and Daan, 1990),
which would be expected if reduced immunocompetence and increased parasitism
reduced the fitness of males.
There is experimental evidence from work on domestic fowl of direct links
among immunocompetence, pathogens and parasites, and fitness. Gross et al.
(1980) investigated the
ability of lines of domestic fowl, selected for aspects of humoral
immunocompetence, to control experimental infections with a range of pathogens
and parasites. Two specific types of selection were included in the study with
respect to humoral immunocompetence: (1) lines selected for high (HA) and low
(LA) antibody response toward sheep erythrocytes, and (2) lines selected for
persistent (PA) and nonpersistent (NPA) antibody responses to sheep
erythrocytes. With the exception of bacterial infections, the HA and PA
selected lines had higher fitness than the LA and NPA lines when exposed to a
range of viral and parasitic infections. This implies a link between
immunocompetence and fitness. However, it could be argued that differences in
fitness between strains (i.e., HA and LA or PA and NPA) could have arisen for
reasons other than immunocompetence. This explanation seems unlikely because,
for certain infections that could be treated, the administration of drugs
removed the fitness difference between strains
(Gross et al., 1980).
If a reduction in immunocompetence has fitness consequences because it
renders hosts more susceptible to infection with pathogens or parasites, then
immunocompetence should be positively correlated with survival. There is some
evidence to support this idea. Saino et al.
(1997a) showed that male barn
swallows surviving to a subsequent breeding season showed a significantly
stronger antibody response toward sheep erythrocytes than nonsurviving males.
Christe et al. (1998) showed
that nestling house martins (Delichon urbica) of low rank within the
brood hierarchy, which also had poor cell-mediated immunocompetence, were less
likely to survive the prefledging period than higher ranking, more
immunocompetent siblings. Nordling et al.
(1998) showed that female
collared flycatchers raising enlarged broods had lower humoral
immunocompetence, increased parasitism, and that parasitism was associated
with a reduction in survival probability to a subsequent breeding season.
Although these data are consistent with the hypothesis that
immunocompetence influences fitness, they are also consistent with an
alternative hypothesis (see Sheldon and
Verhulst, 1996). It is possible that both survival and
immunocompetence are condition-dependent traits. That is, an individual in
good condition might have a high survival probability because it is, for
example, better able to escape from predators or less likely to starve. Such
an individual might also be able to invest resources in mounting an effective
immune defense. The converse situation could be true for an individual in poor
condition. Under these circumstances, there would be a correlation between
survival and immunocompetence even if immunocompetence had no direct impact on
survival. If life-history decisions influence condition, then one could
erroneously conclude that there was a significant trade-off between such
decisions and immunocompetence, even through there was no causal link between
immunocompetence and fitness. Although consistent with the hypothesis that
immunocompetence influences fitness, therefore, correlations between fitness
components (e.g., survival and immunocompetence) might not reflect a causal
link.
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Future prospects |
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TOPABSTRACTINTRODUCTIONMeasuring immunocompetenceTrade-offs and immune defenseFuture prospectsConclusionsACKNOWLEDGEMENTSREFERENCES |
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There is clearly a need for more studies on life-history decisions and immunocompetence in wild bird populations, both from a methodological perspective and to provide further empirical information on life-history trade-offs involving immune defense. There are few studies on wild birds that examine the impact of resource limitation on immune defense; further field experiments are required. This is especially important given the current debate concerning the extent to which immune defense is resource limited (see R
berg et
al., 1998; Sheldon and
Verhulst, 1996). Furthermore, only a small number of life-history
decisions (reproductive effort and sexual ornaments) have been examined
experimentally. It would be valuable to investigate immune defense trade-offs
in other decisions to see how general immune defense trade-offs might be in
life-history evolution. However, in our opinion, the most pressing issue is to
understand the relationship between immunocompetence and fitness in bird
populations. It is apparent that it is difficult to establish a causal link
using circumstantial evidence due to the possibility of condition dependence
in fitness and immunocompetence. The only way to overcome this problem
directly is to manipulate immunocompetence
(Norris et al., 1994;
Sheldon and Verhulst, 1996).
There appear to be two possible ways of doing this: (1) administration of
immunosuppressive or immuno-enhancing drugs, or (2) use of lines artificially
selected for high and low immunocompetence.
A range of biotic and abiotic factors are known to influence the
immunocompetence of domestic fowl (see
Dietert et al., 1996) and could
potentially be used to experimentally alter immunocompetence. Furthermore,
specific drugs have been used to suppress particular immune system components
in domestic fowl. For example, Arnold and Holt
(1995) used cyclophosphamide
and testosterone propionate to suppress humoral immunity in chickens. These
drugs prevent development of the bursa of Fabricius and so selectively reduce
humoral immunocompetence without influencing macrophages or cell-mediated
immunity. Drugs such as cyclosporine A act on T-cells and can therefore be
used to reduce cell-mediated immunocompetence (e.g.,
Arnold and Holt, 1995). It is
unclear at present whether similar treatments would be suitable for
experimental manipulation of immunocompetence in wild bird populations to
examine subsequent fitness effects. This is because a suitable drug must (1)
only influence immunocompetence and no other physiological or behavioral
mechanism likely to affect fitness and (2) act over a sufficient time to
render the host more susceptible to natural pathogens and parasites. Although
drugs such as cyclophosphamide are likely to have a long-term effect on
humoral immunocompetence, drug treatment using particular protocols can reduce
host survival (Arnold and Holt,
1995). Thus there are significant methodological and ethical
considerations in developing and applying comparable techniques in wild bird
populations.
Selected lines provide an alternative way to establish a link between
fitness and immunocompetence, as well as providing an elegant technique for
examining trade-offs between life-history decisions and immunocompetence
(e.g., Verhulst et al., 1999).
The experiments on domestic fowl reported by Gross et al.
(1980) and Seigel and Gross
(1980) provide an example, as
well as a range of experiments cited by Verhulst et al.
(1999). It is at least
feasible to produce selected lines among bird species that readily breed in
captivity, which could then be released into the wild. It is also feasible to
use artificial selection regimes to generate a range of immunocompetence among
a host population to describe the relationship between immunocompetence and
fitness. However, it would also be necessary to demonstrate that any fitness
differences between strains (i.e., high and low immunocompetence) within
selected lines in the wild was due to immunocompetence differences rather than
other differences that affected fitness caused by the artificial selection
regime. One way to do this would be to study a host population in which
pathogens and parasites were well known and could either be controlled
directly using drugs or varied in occurrence between host populations. This
would allow the fitness of different strains in the presence and absence of
pathogens and parasites to be examined.
Given the obvious difficulties of performing such experiments on wild bird populations, we are not arguing that all studies examining trade-offs between life-history decisions and immunocompetence need to undertake them. Rather, it would be valuable to perform such experiments on a few model systems. Gallinaceous birds seem to be ideal model hosts for this kind of experimental study because wild-caught birds can be bred and raised in captivity and released successfully into wild populations. Furthermore, for certain commercially important species (e.g., red grouse Lagopus lagopus), pathogens and parasites are well known and vary consistently between host populations.
There are also specific methodological issues that require attention. First, it would be valuable to develop methods for assessing the innate immune response, in vivo, in wild bird populations. Using a standardized challenge would provide a comparable technique to those used by ecologists to assess humoral and cell-mediated immunity. However, counts of heterophils in peripheral blood and assessment of phagocytic activity in vitro may be a feasible alternative. Second, studies are required to examine how selection influences investment in immune system components; studies on the evolutionary ecology of the avian immune system are needed. Selection experiments on domestic fowl clearly show that the immune system could potentially be influenced by selection in wild populations mediated by the fitness effects of the range of pathogens and parasites experienced by particular hosts. It would be interesting to experimentally expose hosts to particular parasites over a number of generations against which the immune response is well documented to see whether such exposure alters the competence of the particular immune system components involved in defense to the detriment of other immune system components. Selected lines could also be used to examine the consequences of selection for high and low immunocompetence in one immune system component on the competence of other immune system components. It would also be interesting to see how the competence of different immune system components (e.g., innate, humoral, and cell-mediated) change along a gradient in resource availability within a population of hosts. Finally, it would be valuable to investigate experimentally whether there are interactions between immune responses to different challenges. If different immune system components are simultaneously challenged, does this influence the effectiveness of each component when compared with a challenge to a single component?
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Conclusions |
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TOPABSTRACTINTRODUCTIONMeasuring immunocompetenceTrade-offs and immune defenseFuture prospectsConclusionsACKNOWLEDGEMENTSREFERENCES |
|---|
There is evidence to show that immunocompetence in birds can be limited by resources and that life-history decisions can have consequences for immune defense. However, field experiments on wild populations are still limited. Only one study has examined the relationship between resource limitation and immunocompetence in the wild, and experimental studies on the relationship between life-history decisions and immunocompetence have only focused on reproductive effort and sexual ornamentation. Furthermore, the evidence that immunocompetence correlates with fitness is, at present, only circumstantial. It is a substantial future challenge for ecologists to devise experiments that directly manipulate immunocompetence, thereby allowing them to examine fitness effects. Until such experiments are undertaken, it will remain uncertain whether trade-offs involving immune defense are significant in terms of determining optimal life-history strategies, even though evidence consistent with this view is steadily growing.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMeasuring immunocompetenceTrade-offs and immune defenseFuture prospectsConclusionsACKNOWLEDGEMENTSREFERENCES |
|---|
We would like to thank Joe Kools on the seafront at Durban, South Africa, for providing an appropriate environment for designing this paper. The paper benefited greatly from discussions with Andrew Read, Bob Lochmiller, Richard Sibly, participants of the ESF workshop on ecological immunology held in Uppsala, Sweden, in October 1998 and three anonymous referees. Victor Apanius provided valuable advice on how innate immunocompetence could be assessed.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMeasuring immunocompetenceTrade-offs and immune defenseFuture prospectsConclusionsACKNOWLEDGEMENTSREFERENCES |
|---|
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