Parasitic strategies of host
utilization
Evolution of virulence
► Virulence
- the ability of the parasite to reduce the biological fitness of the host
- individual property
- the degree of virulence of individual populations of the parasite is
variable
- parasite-induced host mortality
- in some host-parasitic systems, manifestations of virulence beneficial to
parasites
► Evolution of virulence associated with the fecundity and rate of
transmission of the parasite
► a compromise between parasite reproduction rate and host survival
- prevents uncontrollable fluctuations in virulence
- does not prevent high virulence values
- is analyzed using mathematical models
- for each host-parasite system - optimal strategies of host utilization =
maximization of parasite fecundity
- optimal value of virulence at the local level
Evolution of virulence
Evolution of virulence
 




N
R0
Epidemiological model (Anderson & May, 1982, 1991)
Fitness parasite = reproductive success during life
β is the rate at which infected hosts transmit parasites to susceptible ones
μ is the natural mortality
α is the parasite-induced rate of host mortality
v is the time of host recovering
Evolution of virulence
► Optimal virulence of the parasite derived from the application of the
marginal value theorem for the functional relationship between the
rate of transmission (β) and parasite-induced mortality (α)
Transmission
Natural mortality Parasite-induced mortality
Optimal virulence
Models of virulence evolution
► Prediction of virulence evolution in different conditions
TransmissionTransmission
Natural mortality Parasite-induced mortality
Evolution of virulence in the case of multispecies
infection
► Competition of two types → selection for higher host utilization and
higher virulence within the host
the virulent parasite kills the host quickly
► The coexistence of two species → selection between hosts favours a
lower rate of host utilization and a lower degree of virulence
parasites allow the host a longer life, have a higher reproductive potential
Evolution of virulence: empirical support of
theoretical models
► 2 assumptions of the virulence model empirically supported:
► 1. evolution of high virulence limited by a compromise between the
rate of host utilization by the parasite and host survival
► 2. high virulence leads to higher replication of the parasite
Relationship between virulence (measured as
a reduction in host reproductive success) and
spore production of Pleistophora intestinalis
(Microsporidia) infecting planktonic crustacean
Daphnia magna
Evolution of virulence: empirical support of
theoretical models
► Influence of transmission on the evolution of parasite virulence
► Ex. Study of virulence of protozoa, bacteria and viruses - pathogens in
humans (Ewald 1983, 1994)
virulence = the probability of infection leading to the death of the host
empirical support of theoretical models:
- pathogen virulence using aquatic systems for transmission >
pathogen virulence using host contacts
- virulence of vector-borne pathogens > virulence of pathogens
using host contacts
- virulence of pathogens surviving for a long time in the
external environment > virulence of short-living pathogens in the
external environment
Evolution of virulence in parasites with a
complex life cycle
► high degree of virulence in one host, low degree of virulence in the
other host
► Helminths with predation to the DH - high virulence in IH (source,
specialization) - aggressive strategy of the parasite using IH, low
virulence in DH (dispersion)
► Helminths - without predation to the DH - virulent (inflammatory
reaction caused by eggs in the host tissue)
► Schistosomes eg Schistosoma mansoni - virulent in IH and DH
► parasite virulence in DH (mouse) positively correlates with egg
production rate
► parasite virulence in IH (snail) negatively correlates with the rate of
cercariae production
► Multiple strains at the same IH → strain with low virulence competitively
favoured
► Parasite success in both hosts - genetic compromise = selection of
intermediate virulence's in both hosts
Evolution of virulence in parasites with a
complex life cycle
negative genetic correlation between parasite success in IH and DH
Influence of horizontal and vertical
transmission on the evolution of virulence
► Horizontal transmission - high virulence
► Vertical transmission - low virulence
► Ex. Comparison of ectoparasitic arthropods in birds with different types
of transmission
► Ex. Parasites with stages of horizontal and vertical transmission
► Edhazardia eadis (Microsporidia):
- horizontally transmitted spores - high virulence
in mosquitoes
- vertically transmitted spores - low virulence
Manipulating host behaviour
► targeted intervention in the functioning of the host organism
► modification of host properties - morphology, regulation of metabolism,
specific interventions in the nervous system → changes in the
behaviour of the infected host
► Virulent parasites, i.e. behavioural changes often maximize the
transmission of parasites and increase the probability of host death
Adaptive vs. non-adaptive manipulation of hosts
► Parasites induced changes in host behaviour
► 1. the result of adaptation - higher rate of transmission to DH and/or an
increase in the fitness parasite
► 2. non-adaptive accidental effects of parasitic infection
- accidental changes or side effects of parasite pathology
- parasitism in IH does not increase the predation rate of DH
- increasing the host susceptibility to predation, which is not necessary
for the life cycle
Adaptive vs. non-adaptive manipulation of hosts
► 3. benefits (?) for both the host and the parasite
► e.g. Moniliformis moniliformis (Acanthocephala) influences the
behaviour of intermediate cockroach hosts
Non-adaptive effects of parasitic infection
► Changes in host activity caused by the parasite in the opposite
direction and have different effects on parasite transmission (in similar
host-parasite systems)
Effect of infection of 4
cestodean species on the
activity of Cyclops spp.
Adaptive host manipulation
► parasites manipulate IH behaviour → higher tranmission rate to DH
- infected IH is more susceptible to predation by DH than uninfected IH
DH starlings DH kestrels DH piscivorous birds
Adaptive host manipulation
► parasite-induced changes in hosts affect the fitness of parasites
► When is it an adaptation?
1. time synchronization between parasite infection and behavioural
change expression in hosts
2. a certain degree of host specificity of adaptive manipulation of host
behaviour
Adaptive host manipulation
► Ex. Freshwater snail Potamopyrgus antipodarum infected with the
parasite Microphallus sp. (Digenea)
- modified behaviour to increase predation by waterfowl
(DH) and reduce predation by fish
Parasites induced changes in host behaviour
► Changes positively affect the transmission of the parasite
1. Direct, e.g. infection of the host neuroendocrine system
2. Indirect, e.g. change in the host physiology, which evokes
a specific response in the behaviour of the infected host
► Host visibility (aggressive mimicry)
- parasite-induced color changes in the intermediate host,
formation of white or dark spots or swelling
- increase the predation success of the final host
Parasites induced changes in host behaviour
e.g. colored sporocysts of Leucochloridium
macrostomum pulsating in tentacles of the
terrestrial snail of the genus Succinela
http://www.youtube.com/watch?v=EWB_COSUXMw
Parasites induced changes in host behaviour
► E.g. black spots on the skin of
freshwater fish ("black spot
disease") caused by some digenean
species
► Posthodiplostomum cuticola
Parasites induced changes in
host behaviour
► Altered feeding behaviour
- parasite-induced change of host feeding
behaviour - long search for food near
the predator
- e.g. plerocercoids of the tapeworm
Schistocephalus solidus in three-spined
stickleback (Gasterosteus aculeatus)
ForagingintensityForagingintensity
► Altered ability to move -> disorientation of the host
- the parasitized host shows an atypical movement
- e.g. metacercariae of Diplostomum spathaceum in freshwater fish
(intermediate host) - localization in the lens of the eye
Parasites induced changes in host behaviour
Parasites induced changes in host behaviour
► Altered behaviour in the presence of a predator
► the parasitized host has a reduced susceptibility to the presence of a
predator
► the escape distance between the predator and the infected host is
shortened
► the reaction of the infected host to the predator's attack is stiffness
► Ex. plerocercoids of tapeworm Schistocephalus solidus in Gasterosteus
aculeatus
Parasites induced changes in host behaviour
► Toxoplasma gondii in rodents (intermediate hosts)
- affects transmission to the final host (cats)
- congenital aversion of rats to cats
- parasite modification of host behavior - cat odour is an attractant to rats
http://www.youtube.com/watch?v=__K104jSGzs
Parasites induced changes in host behaviour
► metacercariae of Apatemon (<15) in the fish brain
Nothobranchius furzeri
- "jumps" above the surface - the probability of catching an infected
fish with a heron 30 times higher than in the case of a healthy fish
Infikovaný jedinecKontrola
Parasites induced changes in host behaviour
► Habitat preferences
► The parasitized host moves to an environment where DH is more
conspicuous and easier to reach
► Ex. Metacercariae of Dicrocoelium dendriticum in ants (Formica
praetensis)
http://www.youtube.com/watch?v=lGSUU3E9ZoM
Parasites induced changes affecting host
reproduction
► Modification of sexual behaviour
1. parasites directly use reproductive organs (feed on gonads)
2. indirect use of the host - the host's reproductive effort to its
advantage (host energy to reproduce or prevent sexual
maturation of the host - castration)
► production of hormones that prevent sexual maturity of the host
Ex. the tapeworm Hymenolepis diminuta suppresses vitelogenesis in the
insect intermediate host (Tribolium confusum and Tenebrio molitor) smaller
size and viability of eggs
Ex. Plerocercoids of tapeworm Ligula intestinalis prevents the
development of gonads and reaching sexual maturity of fish IH
Parasites induced changes affecting host
reproduction
► the parasite uses the energy intended for host reproduction to benefit
its own growth through castration of the host
Ex. Digenea castrating snails
Ex. Sacculina carcini (Cirripedia) parasitizing crabs - castration of males
and females + hormonal interference - feminisation of males
Parasites induced changes affecting host
reproduction
http://www.youtube.com/watch?v=LFaqeTauVhA
Parasites induced changes affecting host
reproduction
► Castration of hosts - ideal parasite strategies for host utilization
- the parasite does not reduce the lifespan of the host
- energy not used for reproduction, the host invests energy in somatic
growth
Cumulative host investment in
reproduction and body weight
in the case of an uninfected and
infected individual by a parasitic
castrator
► Host gigantism
- growth factor secretion, excessive food intake, inability to
metamorphosis
- secretion of analogues by parasites which mimic the growth factor host
Parasites induced change - host gigantism
Plerocercoids of Spirometra mansonoides
in rodents produce a growth factor which
mimics mammalian growth hormone
Parasites induced change - host gigantism
► Hypotheses
1. Parasite strategies to exploit the host
- later benefit for longer-lived parasites with intermediate growth rate
(e.g. for larval stages of digeneans parasitizing snails)
- resources released by castration are invested in the body weight of
the host for later use of the parasite, the parasite induces very low or no
host mortality
2. Adaptive response of the infected host
- compensation of the parasite effect
Parasites induced change - host gigantism
► Host gigantism
► Experiment: gigantism as a strategy of a parasite using a host or
gigantism as a host adaptation to compensate for the effect of
parasitism?
Effect of castration by the parasite Diplostomum phoxini (Digenea) on the
growth of the intermediate host Lymnaea peregra
Host manipulation from the perspective of the
concept of multispecies parasite infection
► Many larval helminths share intermediate hosts with other parasite
species
- some manipulate host behaviour, others do not manipulate
- some have the same, others have different life cycles
- same definitive host = cooperation of parasite species
- different definitive host = conflict between parasite species
Host manipulation from the perspective of the
concept of multispecies parasite infection
Host manipulation from the perspective of the
concept of multispecies parasitic infection
► "Hitchhiking" tracking strategy - a larva of a non-manipulating parasite
actively searches for and infects a manipulated host
► Active "hitchhiking" is only beneficial in case of low manipulator
prevalence's
► Ex. Digenea in Amphipoda (IH)
Microphallus papillorobustus - manipulative species - the host swims at
the surface of the water, where it is exposed to predation by a definitive
host - the bird
Maritrema subdolum - a non-manipulative species, actively swims at the
surface of the water
Host manipulation from the perspective of the
concept of multispecies parasitic infection
► double manipulators - copilot strategy at the same IH
- each affects the host phenotype differently
- the effect of both on the rate of transmission is additive (selection
favors synergisme)
Ex. Acanthocephala (Pomphorhynchus laevis and Acanthocephalus
clavula) in Amphipoda (IH), definitive host fish
Ex. Echinostom Digenea (Curtuteria australis and Acanthoparyphium sp.)
Cerastoderma (bivalves) (IH), the definitive host bird
Host manipulation from the perspective of the
concept of multispecies parasitic infection
► "Hijack" strategy - a competitive process to take control on IH
- both parasite species manipulate
- one is stronger (affecting the host phenotype) – with manipulation
mechanisms or which was first in the host
- "arms races" between manipulators (costs associated with loss are
large)
- Ex. Acanthocephala (Pomphorhynchus laevis and Polymorphus
minutus) in Amphipoda (IH), different DH: fish for PL), bird for PM
- stronger PL
Host manipulation from the perspective of the
concept of multispecies parasite infection
► "Co-pilot shooting" strategy
Ex. Cestoda parasitizing beetles (IH) - Hymenolepis diminuta (DH rat) and
Raillietina cesticillus (DH chicken) - both manipulate
- Infection of beetles with R. cesticillus prevents H. diminuta infection
Ex. Acanthocephala in Amphipoda (IH) - Pomphorhynchus bulbocolli and
Leptorhynchoides thecatus (DH for two parasites are different freshwater
fish species)
- The presence of one species negatively affects the growth of the other
(both are host-manipulating species)
Host manipulation from the perspective of the
concept of multispecies parasite infection
► Sabotage hypothesis - neutralization of manipulation
Vertically transmitted parasite Dictyocoela sp. (Microsporidia) and the
horizontally transmitted parasite Polymorphus minutus (Acanthocephala)
in IH Gammarus roeseli (PM modifies IH behaviour)
Manipulation of the sex ratio of the host
► Parasites transmitted vertically: microsporidia, viruses, bacteria
► Wolbachia bacteria - live in the cytoplasm of host gametes, female
infections - transmission for offspring, male infections - evolutionary
end
► parasite manipulation = effect on investment in female offspring
1. kill the male offspring of the host
2. deform the primary sex ratio by changing the expression of host
genes (convert the genotype of males into the genotype of females)
3. feminize male offspring (change of genotypic males to functional
phenotypic females)
Manipulation of the sex ratio of the host
► Ex. Representation of female offspring in the clutch of female
Gammarus duebeni uninfected and infected with the transovarian
transmitted parasite Octosporea effeminas (Microsporidia)
Manipulation of the sex ratio of the host
► The effect of the parasite on the sex ratio depends on:
1. the primary sex ratio of the host
2. the ability to transmit the parasite from mother to offspring
3. on the feminizing effect of the parasite
Risk strategy of using the host !!!
Maximization of transmission and feminization
→ extinction of the host population (elimination of males)
and extinction of the parasite