Evolution of host-parasite
interactions
Coevolution
► Mode (1958) – mathematical model for host-parasite
coevolution
► Janzen (1980) - process between interacting species,
where each of the interacting species changes its genetic
structure in response to a genetic change in its partner
► Thomspon (1994) - process of reciprocal evolutionary
changes of interacting species
► coevolutionary processes at the level of molecules, cells,
genes, males-females, parents-offspring, species
► Its importance depends on the frequency of interactions
between partners and the impact on their reproductive
success
Coevolution
► Woolhouse et al. (2002). Nature Genetics 32: 569–577
Reciprocal, adaptive genetic changes between interacting
species
Host-parasite coevolution can be studied from the
following perspectives:
- mutual phenotypic characteristics (resistance and
infectivity)
- interacting parasite and host molecules
- genes or nucleotide sequences
Coevolution of host-parasite interactions
Schematic representation of
coevolution with emphasis on
reciprocity:
Changes in allele frequency due
to selection in one species have
a selective effect on the other
species - changes in allele
frequency in another species
Coevolution
► From the point of view of evolutionary parasitology
coevolution = common evolution of parasites and their
host species, during which they interact
► In the strict sense - the evolution of associated groups,
expressed as reciprocal adaptations
► Association with macroevolutionary (cospeciation) and
microevolutionary (coadaptation) components
Macroevolution versus microevolution
► Macroevolution - the origin and evolution of higher taxa
than the species
- rules that determine the origin of a certain form and
adaptive changes
- changes in species diversity within and between
evolutionary groups, rate of speciation and extinction in
the long term (historical, unrepeatable, unique)
► Microevolution - evolutionary processes within a species
- short-term, recent, ongoing changes, experimentally
studyable
- population genetics, ecology, ethology
Cospeciation and coadaptation
► Cospeciation
- macroevolutionary process
- may reflect the degree of congruence or incongruence
between the phylogenies of hosts and parasites
► In the strict sense: topological congruence and the same
rate of molecular divergence (same branch lengths) in the
associated groups
► Known examples: Figs and their wasps, Buchnera
aphidicola (symbiont) and aphids, Australian mistletoe and
pine, pocket gophers (Geomyidae) and their lice
Coadaptation
► originally co-accommodation
► microevolutionary processes
► includes anagenesis and reciprocal adaptation (arms race
scenario)
► associated with host specificity
Coevolution models in host-parasite systems
1. model of allopatric cospeciation
► parasites and hosts share common space and energy
► disruption of gene flow between host populations 
allopatric speciation of hosts and parasites
► synchronous cospeciation - speciation of parasites and
hosts takes place simultaneously
► delayed cospeciation - a host or parasite speciation is
delayed after speciation of the other
Coevolution models in host-parasite systems
2. Resource tracking model
► based on the ecological concept
► parasites track resources over evolutionary time
► the evolution of a parasite is a response to a change in the
resources provided by the host
► the host changes the resources that the parasite is looking
for  the parasite undergoes evolutionary changes that
allow it to use new resources
► changes in the parasite occur after changes that have
taken place in the resources provided by the host
Coevolution models in host-parasite systems
3. Model of an evolutionary arms race
► the most strict view of coevolution - mutual adaptive
responses between hosts and parasites
► permanent evolution between parasites and hosts aggressive
targeting of each other
► parasite selection - higher host utilization, host selection more
successful parasite elimination
► This model is part of the concept of the hypothesis gene
for the gene
Coevolutionary models in host-parasite
systems - gene for gene
► for each gene conferring resistance in a host, there is a
corresponding suitable gene for avirulence in the parasite
► host resistance is dependent on the presence of the
resistance gene and the corresponding avirulence gene in
the parasite
► resistance genes and avirulence genes = dominant genes
Host genotype
Parasite genotype RR Rr rr
AA Resistant Resistant Susceptible
Aa Resistant Resistant Susceptible
aa Susceptible Susceptible Susceptible
Coevolutionary models in host-parasite
systems - arms race
► 1. parasites reduce a host's fitness
► 2. the host creates defense mechanisms against parasites
= mutations or gene recombinations
► 3. the host with a new defense mechanism increases
fitness and expands in the population
► 4. a new mutant or recombinant appears in the parasite
population - it resists the host's defense mechanisms
► 5. a new mutant spreads in a population of parasite, it is
able to enter the host
► 6. cycle is repeated
Coevolutionary models in host-parasite
systems - arms race
Coevolution
► 4 rules
► Fahrenholz's rule (Stammer 1957, Dogiel 1964) - the
phylogeny of parasites is a mirror of the phylogeny of hosts
► Szidat's rule (Szidat 1956, 1960) - the more "primitive" the
host is - the more "primitive" are its parasites
► Eichler's rule (Eichler 1941, 1948) - species-rich group of
hosts - a larger number of parasite species
Coevolution
► Manter's rule (Manter 1955, 1966)
a) parasites evolve more slowly than their hosts
b) longer association to a certain host group  higher
specificity of parasites
c) the host species are parasitized by the higher number
of parasite species in the area where they have resided
for the longest time.
If the distribution of one or two closely related host
species is disjunctive and yet the same parasites are
found in these hosts, then the range of their distribution
was overlapped in the past.
Speciation of parasite species
► Speciation - the evolutionary process of the origin of one or
more species from an ancestral species
► 2 types of geographical speciation in parasites
► Allopatric speciation - in conditions of non-overlapping host
areas
► Sympatric speciation - in conditions of overlapping host
areas
► Cospeciation - parasite speciation follows host speciation
► geographical isolation, reproductive isolation, genetic
divergence of host populations
► Identical topology of phylogenetic reconstructions of hosts
and parasites (Fahrenholz's rule)
Allopatric speciation of parasites
Cospeciation
► pocket gophers (Geomyidae) and
ectoparasitic lice
► Aphids and endosymbiotic
bacteria
Sympatric speciation of parasites
► host switching = colonization of different host species,
evolution of multihost parasite species
► intrahost speciation = parasite duplication
cospeciation
duplication
failure do diverge
host switching
sorting event
sorting event
Other coevolution events in host-parasite
systems
Host speciation without corresponding parasite speciation:
- Failture to diverge
- Sorting event - extinction of the parasite following cospeciation
- „missing the boat“
cospeciation
duplication
failure do diverge
host switching
sorting event
sorting event
Speciation of congeneric parasites
► Speciation of monogeneans
- highly host-specific
- direct life cycle
- high morphological diversity
- high species diversity
- adaptation
- high number of congeneric species (within some genera)
- high number of congeneric species per host
Speciation of congeneric parasites
► Ex. Lamellodiscus (Monogenea) parasitizing marine fish of the
Sparidae
- old genus
- high intraspecific morphological variability of the sclerotized
parts of the attachment apparatus
- high dispersibility of host species
fast speciation by
host switch
► Ex. Dactylogyrus (Monogenea)
- freshwater fish of Cyprinidae
- high number of host-specific
parasites
- high number of species
coexisting on 1 host species
Speciation of congeneric parasites
intrahost speciation
- evolution of different positions
of preferred niches
► Gyrodactylus (Monogenea)
- viviparous, capable to colonize a wide range of
freshwater and some marine fish species
- speciation by host switch, adaptive radiation
Speciation of congeneric parasites
► Ex. Polystomes (Monogenea)
- a special group of endoparasitic monogeneans
- infect mainly amphibians and freshwater turtles
Speciation of congeneric parasites
Speciation of congeneric parasites
► Ex. Polystomes (Monogenea)
- high morphological similarity
- highly host specific
- preferences for different
niches within the host
Host switch and cospeciation
Parasites affecting the evolutionary biology of
hosts
► Evolution of interactions between hosts and parasites from
a perspective other than coevolution
► Role of parasites in:
1. the evolution of sexual reproduction of the host
2. the sexual selection of the host
3. the evolution of host genetic polymorphism
The role of the parasites in the evolution of
sexual reproduction of the host
► Red Queen hypothesis
► „Now you run to stay in the same place.” (Lewis Carroll,
1872. Through the Looking-Glass, and What Alice Found
There)
► “In the beginning, it was a fragile plant that someone
sometimes ate; at the end there is a thorny and poisonous
monster, which is also sometimes eaten by someone.” (Jan
Zrzavý et al. 2004. How evolution is done: from the selfish
gene to the diversity of life)
► The Red Queen Hypothesis - a specific type of evolutionary
arms race hypothesis
► the benefit of sexual reproduction by frequency-dependent
selection directed against a common host genotype
► sexual reproduction and recombination  rare genotypes
capable to escape parasites
► selection favors hosts with rare genotypes
► rare genotypes become common, parasites are able to
trace these genotypes due to frequency-dependent
selection
The role of the parasites in the evolution of
sexual reproduction of the host
The role of the parasites in the evolution of
sexual reproduction of the host
► Sexual reproduction produces offspring with new
genotypes - resistance to parasites
► Asexual reproduction produces offspring with the same
combination of resistance genes as in parents - the target
of increased parasitism
► Ex. Poeciliopsis monacha - parthenogenetic form
accumulated parasites much faster than sexually
reproducing forms
► Ex. The most common genotypes of the triploid form of
Carassius gibelio - a higher number of parasite species
than in sexually reproducing form
The role of the parasites in the sexual
selection of the host
Sexual selection
- natural selection affecting the expression of certain
phenotypes in one sex (most often in males), which
determine the success in selecting a partner by the other
sex (mostly by females) -> sexual dimorphism
e. g. body size, tail size, color, antlers, vocal expressions
Sexual selection leads to the evolution of secondary sexual
traits (sexual ornamentation) Darwin (1971)
Two causes of sexual selection:
1. competition between males (at the level of individuals,
at the level of sperm)
2. female preferences (females invest more in
reproduction)
The role of the parasites in the sexual
selection of the host
The role of the parasite in the sexual selection
of the host
► Handicap hypothesis (Zahavi, 1975)
► Expression of a secondary sexual trait
- represents a handicap for males
- a male with a good genetic predisposition can cope with
a handicap
- indicates the quality of the male
- expression of a trait is expensive (energetically, predation)
- males with higher genetic quality have lower costs and
greater benefits associated with the expression of a trait
► Hamilton-Zuk hypothesis (1982)
► Secondary sexual trait - an indicator of the effectiveness of
resistance genes against parasites
► Females prefer resistant males - selection of suitable genes
for offspring (hypothesis of good genes)
► 3 assumptions of the hypothesis:
1. expression of secondary sexual characteristics in males is
associated with overall good health and vitality
2. inherited parasite resistance in hosts (consequence of
coevolution)
3. negative effect of parasites on host viability (selection of
resistant males)
The role of the parasite in the sexual selection
of the host
The role of the parasites in sexual selection of
the host
Poecilia reticulata
Infection with the parasite Gyrodactylus
turbulli decreases with the intense
ornamentation of males - more attractive
for females
Females select colored males
(resistance or prevention of parasite
transmission)
Females infected with the parasite show a
lower tendency toward male preferences
Intraspecific test of the Hamilton-Zuk hypothesis
The role of the parasites in sexual selection of
the host
Barn swallow (Hirundo rustica) and mites
1. The expression of ornamentation is associated
with the parasite intensity
Males with a long tail have fewer mites
Females prefer males with a long tail
2. The parasite affects the fitness of the host
Offspring with high parasite intensity are smaller
and have lower survival
3. Heredity in parasite resistance
The offspring of long-tailed males showed hereditary resistance to mites
Intraspecific test of the Hamilton-Zuk hypothesis
Intraspecific tests of the Hamilton-Zuk hypothesis
Reference Organism Parasite
Costly
Heritable
variation
Ornament depends
on parasite
Females choose males with
fewer parasites
Unique
prediction tested
Parasite
aggregation known
Zuk 1987, 1988 cricket YES NO NO NO NO
Jaenike 1988 octomilka YES YES NO NO
Kennedy et al 1987 živorodka YES YES YES NO
McMinn 1990 živorodka YES NO
Milinski and Baker 1990 koljuška YES YES YES NO NO
Hausfater et al. 1990 tree frog YES YES NO NO
Tinsley 1990 toad YES NO NO NO
Ressel and Schall 1989 iguana YES YES NO NO
Hilgarth 1990 pheasant YES YES YES YES NO NO
Zuk et al . 1990 hen YES YES YES YES NO NO
Johnson and Boyce
1990
capercailli
e
MAYBE YES YES NO NO
Gibson 1990 capercailli
e
NO NO NO NO NO
Clayton 1990 pigeon YES NO NO
Moller1990 swallow YES YES YES YES NO NO
Borgia1986; Borgia and
Collis 1989
Silk hem YES YES YES NO NO
Pruett-Jones et al. 1990 paradise YES YES NO NO
Interspecific tests of the Hamilton-Zuk hypothesis
Correlation Observed Between Brightness And
Reference Organism Prevalence Intensity Diversity Phylogenetic
Effects
Contolled
Alternative
Factors
Considered
Info On H-p
Interaction
Hamilton and
Zuk 1982
North American passerines
(plumage bright.and song
complexity)
YES NO NO NO
Read 1987 European passerines (plumage
bright.)
YES NO NO NO
Read and
Harvey 1989
North American passerines
(plumage bright.)
NO YES NO NO
Read and
Weary 1990
North American passerines (song
complexity)
NO YES NO NO
Zuk 1990 Neotropical birds (plumage
characters)
YES NO NO
Pruett- Jones
et al. 1991
New Guinea birds (plumage
characters)
YES NO YES YES YES NO
Weathe rhead
et al.
Wood warblers NO NO NO YES NO
Ward 1988 British fish (degree dimorph) YES
Cabana and
Chandler
1991
British + NA fish
Lefcort and
Blaustein
1991
Lizards (brightness) NO (neg correl) NO YES YES NO
► Problem with hypothesis testing in interspecific studies
► Reverse causality: host ornamentation may attract
parasites (more colored species may attract more
ectoparasites, or species that invest more in
orgnamentation invest less in parasitism resistance)
► Ecological correlation: coloration and parasitism may be
associated with another factor (polygyny, type of nests)
► Falsification: if no correlation is recorded, is the data
sufficient to reject the hypothesis?
► The need of control for phylogenetic relationships
Hamilton-Zuk hypothesis in interspecific
studies
3 models of parasite-mediated sexual selection
► 1. females do not select partners infected by parasites
transmitted by direct contacts
► 2. the female selects a healthy and viable male to help her
take care of the offspring
► 3. the female selects a resistant male to obtain resistance
genes for offspring (= higher offspring viability) - a model
of "good genes"
The role of the parasites in the sexual
selection of the host
Why are non-parasitic males better?
The success of
males in
mating
decreases with
increasing
intensity of
parasitism
1. Hamilton & Zuk hypothesis - hereditary resistance to parasites for offspring
2. Hypothesis of parasitism avoidance - no effect of parasites on the expression of
ornamentation, female detects parasites and avoids contact with the parasitized male
3. Hypothesis of indicator of contagion - females avoid contact with parasitized males
to protect themselves and their offspring from infection (infection is transmissible to
offspring)
The role of the parasites in the sexual
selection of the host
► Immunocompetence handicap hypothesis (Fostad and
Kartet, 1992)
- a mechanism for explaining sexual selection
- a trade-off between costs and benefits of high
testosterone level
- the dualistic nature of testosterone
1. increase in the expression of secondary sexual traits
2. reduction in resistance and suppresssion of the
immune defense (induction of immunosuppressive effect)
► Handicap imunocompetence
► Females select males with remarkable secondary sexual
traits, indicating quality of the immune system despite of
testosterone immunosuppression
► Trade-off between expression of secondary sexual traits
and immunity, but strong males are still viable and
resistant to parasitism
The role of the parasites in the sexual
selection of the host
Studies on associations between immune
response and sexual selection