Immunoecology of host-parasite
relationships
Immunoecology
► Combining immunity and evolutionary ecology
► It examines variability in the immune response between
individuals, populations and species
► It studies the processes that explain this variability and its
maintenance
► Seeks trade-offs if immunity is considered a costly
component of life history (principle of energy allocation cost
versus benefit)
► Evolutionary adaptation of immunity
Immunity in vertebrates
► Non-specific (non-adaptive, innate)
- dendritic cells, macrophages
► Specific (adaptive, acquired)
cellular and humoral responses
intracellular parasites, extracellular parasites
Immunocompetence
► The general ability of an individual to induce an effective
immune response in order to minimize losses due to infection
► How to measure immunocompetence?
1. Intensity of parasite infection
High intensity of parasite infection
=> low immunocompetence
2. Induction of infection
Resistance to infection => good immunocompetence
Resistance or susceptibility
3. Serology
High white blood cell count
=> good immunocompetence
Immunocompetence
► How to measure immunocompetence?
4. Weight of immune organs (spleen, thymus)
5. Injection of mitogens
Lymphocyte proliferation (T or B)
6. Injection of antigens
Antibody production
7. Genetic data
MHC genes
Immunological approaches applied in field
studies
Immunity as a component of the life histories
of hosts
► role of the immune system as an important component of
life history
► the organism makes certain investments in the immune
function responsible for resistance to pathogens and
parasites
► If the evolution of the immune system is controlled by
parasites, then a positive correlation can be expected
between parasitic load and the effectiveness of the
immune system
Costs associated with immune responses in
vertebrates
Investment in reproduction versus investment
in immunity
► investment of females and males in reproduction is
different
► females - production of oocytes, males - formation of
secondary sexual characteristics
► The principle of trade-offs in the distribution of energy reproduction
and immunity
► investment in the development of gonads and investment
in the course of reproduction itself energy-costly =>
reduction of the organism's investment in its immune
defenses
► Immunocompetence handicap hypothesis
- energy devoted to reproduction => increased production
sex hormones at the expense of reduced immune function
(immunosupresive role of testosterone)
 Sperm protection hypothesis (Folstad & Skarstein 1997)
- immunosuppressive effect of testosterone leads to
protection of sperm as sperm are recognized as antigenic,
attacked by autoimmune system
- better males (= better tolerating costs associated with the
negative effect of testosterone) - more pronounced secondary
sexual characteristics and sperm of better quality
Investment in reproduction versus investment
in immunity
Gender-differences in immunity
Cellular response
Humoral response
Inflammation
Males < Females
Auto-immune disease Males < Females
Risk of infection Males > Females
Proximal causes
testosterone
immunosuppression
reproductive success of males
behavior (aggressive, dispersion)
Estrogen = increasing the expression of MHC genes
► Ex. Interspecies study in birds
1. Males with larger gonads invest more in the production of sex
hormones, which is compromised with immune function, the evolution
of the size of testes may be the result of sexual selection
2. Birds affected by higher pressure from parasites invest more in
immunocompetence
Investment in reproduction versus investment
in immunity - an interspecific study
Investment in reproduction versus investment
in immunity - intraspecific studies
► Ex. analysis of trade-offs between investments in immunity and reproduction
=> trade-off between parasite resistance and the expression of primary sexual
characteristics
Arctic char
(Salvelinus alpinus)
Reproduction versus immunity
Relationship between reproduction and specific
immunity
1. Increasing investment in reproduction
reduces humoral immunity
2. Increasing reproductive effort increases the
intensity of Haemoproteus infection associated
with higher mortality
Ficedula albicollis
Nordling et al. 1998
Females immunized with NDV (Newcastle disease virus)
Pup success and immunocompetence
Parus caerulus
Cichon & Dubiec 2005
The immune response doesn't play a
role in unfavourable breeding
conditions
Local recruitement is dependent on
immunity, but also on environmental
factors
Manipulation with increasing offspring in nests
T cell mediated immunity - response to PHA
Positive relationship between immunity and offspring success →
predicted probability of admission of young to the population
Offspring size and activation of humoral immunity
Activation of the immune system
decreases reproductive success
(number and size of offspring)
Ficedula hypoleuca
Ilmonen et al. 2000
Females immunized with non-pathogenic antigen (diphtheria-tetanus vaccine)
Test of activation of the immune response to investment in reproduction
Nunn et al. 2000
White blood cells and sexual promiscuity in primates
Mating promiscuity:
gestation time and size of
testes
Relationship between white blood cell
count and number of sexual partners
=> potential relationship to sexually
transmitted diseases
Multiple helminth infections and basic
investment in immunity
Increasing the number of helminth
species is positively correlated with
increasing the basic investment in
immunity in mammals
Bordes & Morand, 2009, Par Res
Food resources and immunocompetence
Only seeds
Seeds and supplementary diet
Taeniopygia guttata
Birkhead et al. 1999
Improving food quality
accelerates growth and
increases
immunocompetence (cellular
response)
Effect of brood nutrition on growth and T cell immunity
(reaction to mitogen)
Sociability and immunocompetence
Larvae
social
Solitary
(Wilson et al. 2002)
Schistocerca gregaria
The survival of social crickets is higher than that of solitary crickets 
increasing density through phenotypic changes associated with better
immunity
Stress = an event that disrupts homeostasis, increasing energy use
stress
hypothalamus - pituitary gland - adrenal gland
corticoids
adaptive response
suppression of cost functions
(immunity)
mobilizing energy for organs
that need it
The effect of stress on immunity
Sexual competition and social stress
Arctic ground squirrel
Spermophilus parryii
Boonstra et al. 2001
Excitation of immunity
Chronic stress in reproductive adults - high
cortisol levels, low ability to bind
corticosteroids, low resistance to
dexamethoson, low haematocrit, low white
blood cell count, low ability to respond to
immune stimulation
Adaptive response to stress during reproduction
Response to adrenocorticotropic hormone
Dexamethosone injection - steroid immunosuppressor
Hormonal induction
Kraaijeveld & Godfray, 1997
Selection
No selection
Selection of Drosophila melanogaster
lines resistant to parasitoids
(encapsulation) leads to reduced
competitiveness
Immune response and competition
ns
Pigeons were injected with sheep red
blood cell suspension (SRBC) or
injected with saline (control)
Effect of immune activation on the
relative rate of basal metabolism in
pigeons
Individuals with a strong immune
response relative to a control that
showed a low immune response
(Eraud et al. 2005)
Immune response and metabolism
Costs associated with the immune response
Increasing activity (e.g. flying, reproduction) reduces
immune response => trade-off in energy and resource allocation
Immunity and successful invasion
Moller and Cassey, 2004
T cell - mediated immune response
in young (measured in response to
mitogenic lectin PHA) determines
the success of population
establishment
The immunity of young birds
increases expansion of the
introduced populations or the
colonization of continents
Costs associated with immune responses
Costs associated with immune responses
Evolution of immune genes
► Major histocompatibility system (MHC) genes
► Evolution of MHC genes and selective factors
► capture peptides and fragments (antigens) and immerse
them in the cell surface => cells offering antigen,
fragments of which are recognized by the T-cell receptor
for antigen
► PBR sites (peptide binding regions) - binding sites of MHC
glycoproteins
Glycoproteins MHC I and MHC II
► MHC class I glycoproteins - present on all nuclear cells of
the organism
- To ensure the presentation of intracellularly derived peptides
formed by the breakdown of proteins derived from viruses
and some species of bacteria
► MHC class II glycoproteins - occur on antigen-presenting
cells - B lymphocytes, monocytes, macrophages and
dendritic cells
- To present peptide fragments derived from extracellular
parasites, e.g. some species of bacteria or metazoan
parasites
MHC polymorphism
► found in all jawed vertebrates from fish to mammals
► highly polymorphic genes
► high number of alleles that provide functional loci
► high number of nucleotide substitutions between individual
alleles
► trans-species polymorphism
Selection leading to high polymorphism of
MHC genes
► Two non-exclusive mechanisms:
1. parasite-mediated selection
2. sexual selection
► Parasite-mediated selection
► 1. advantage of rare MHC genotypes (theory of advantage
of rare allele)
► 2. advantage of MHC heterozygotes (heterozygote
advantage theory)
Heterozygote advantage theory
► heterozygote has a higher ability to distinguish a wide
range of antigenic peptides derived from parasites or
pathogens than homozygote
► heterozygote resistence > homozygote resistance
► Ex. female salmon choose males in terms of increasing the
MHC heterozygosity of their offspring
► Ex. relationship between MHC IIB heterozygosity and
Gyrodactylus (Monogenea) infection in Poeciliopsis
occidentalis
► Ex. advantage of mice MHC heterozygotes in infection with
Salmonella strains
Rare allele advantage theory
► Frequency-dependent selection
► Assumption: host individuals with a rare allele respond
better to the presence of new parasite
► Increasing the frequency of the rare allele in the host
population leads to the allele becoming the target of
parasitic adaptation
► Ex. the relationship between the specific allele of the MHC
IIβ system and parasitism in salmonid fish
The average number of alleles is advantageous for
individuals
► Nowak et al. 1992 – mathematical model
High diversity of MHC alleles in an individual is not advantageous
- recognition of a wide range of antigenic peptides
- elimination of own T cells
► the optimal (= intermediate) number of MHC alleles determines the best
immune response
Ex. Mean number as the optimum of MHC alleles and the lowest parasitism at the
level of the individual in three-spined stickleback
The role of sexual selection in increasing MHC
polymorphism
► the relationship between MHC genotype and sexual selection
► MHC genes = resistance genes - good or compatible genes
► Hypothesis of good genes
► vitale males with genetic predisposition for high resistance to parasites
have strong sexual ornamentation
► the female selects her partner in terms of selecting good genes for
offspring
► the relationship between MHC genotype and fitness-dependent
character
► Good genes of males – parasite load,
secondary sexual traits (body colaration,
breeding tubercles in fish)
► Genetic compatibility hypothesis
► MHC as a genetically incompatible system - prevents inbreeding,
individuals with a similar MHC genotype = related individuals
► the female directs her choice of partner depending on her own MHC
genotype, i.e. she selects a male with a different MHC genotype =
complementary to her MHC genotype = high MHC variability for
offspring
► Ex. three-spined stickleback
The role of sexual selection in increasing MHC
polymorphism
The role of sexual selection in
increasing MHC polymorphism
► How can a female recognize a different or complementary
MHC genotype?
► the choice of a partner is based on olfactory perceptions
► Studies in humans, mice, also documented in fish
Sexual selection and MHC
► Two levels of sexual selection in relation to MHC
► at the level of individuals - certain males with better
condition bound traits
► at the gamete level - the sperm of a certain individual are
selected by female oocytes more than the sperm of
another individual
e.g. Arctic char - sperm of MHC heterozygotes have
higher success in fertilization
Arctic char
(Salvelinus alpinus)
MHC and extinction of species
Arabian oryx
Oryx leucoryx
Protection
program
= maintain all 3
variants
desert bighorn sheep
(Ovis canadensis nelsoni)
MHC and extinction of species