Evolution of life strategies of
parasites
Life strategies
► Combination of physiological and demographic
components: body size, life expectancy, age at sexual
maturity, fecundity, size and number of offspring
► Some combinations are favored by selection because they
lead to higher fitness in a given environment
► Some components are variable at the population level,
others are fixed at a higher taxonomic level
Theory of life history
► To analyze the relationships between life traits
(maintenance, reproduction and survival)
► Total contribution to individual's fitness
► Do organisms with late maturity live longer?
► Do larger organisms have fewer offspring than smaller
organisms?
► Simultaneous maximization in more traits is not possible →
the evolution of life traits is limited and is characterized by
a trade-off between the individual traits
Trade-off
► The connection between the traits of life, leads to the
simultaneous evolution of traits
► A benefit obtained by a change in one trait (component) is
offset by a cost in the other trait (component)
► Negative relationship between two traits, e.g. number and
size of offspring, onset of reproduction and survival
Relationships between parasites and
components of the host's life history
► Parasites can control the evolution of host's life history
traits
► Parasites represent an important selection pressure on the
host
► The trade-off in host energy allocation depends on the
selection pressure of the parasite
► Survival and reproduction
► Immune function
► Age at sexual maturity versus parasite species richness
► Parasites that accumulate with the age of the host reduce
its age in sexual maturity
Relationships between parasites and
components of the host's life history
Ex. Fish species colonized by a higher number of parasitic species (larval
stages) mature earlier
Relationships between parasites and
components of the host's life history
► Age at sexual maturity versus parasite species richness
► Fish with delayed onset of sexual maturity have a higher
number of parasitic species
► Life span versus parasite species richness
► Ex. Long-lived fish are parasitized by a higher number of
endoparasites
Relationships between parasites and
components of the host's life history
Numberofendoparasitespecies
Life expectancy
► Host basal metabolism versus parasite species richness
► BMR - the minimum energy costs needed to ensure the
activity of the organism
► Metabolic costs of immunity
Ex. Mammals at higher risk of parasitism have higher
metabolic requirements to initiate an immune response
Mammals with higher parasitic load have a shorter lifespan
(consequence of physiological losses)
Relationships between parasites and
components of the host's life history
► Mammals with higher metabolic rates have a higher
number of parasitic species
Relationships between parasites and
components of the host's life history
► Host ploidy versus parasitism
chromosomal duplication - an important role in adaptive
immunity
Ex. Positive relationship between parasite species richness
and ploidy of African cyprinid fish
Relationships between parasites and
components of the host's life history
Numberofparasitespecies
2n=50
2n=100
2n=150
► Host genetic diversity versus parasite species richness
Ex. Positive relationship between number of monogenean
species and genetic heterozygosity in cichlid fish (factor of
parasite diversification)
- size of host population is also important factor of parasite
diversification
Relationships between parasites and
components of the host's life history
Phenotypic plasticity and adaptation of parasites
► Adapting the strategy of parasite life history to changes in
environmental conditions
► 1. Phenotypic plasticity
- adaptation to local conditions, small developmental
changes, selection of the best strategy, change in one
generation
- one genotype produces numerous phenotypes
► 2. Adaptation
- selection prioritizes genotypes producing the most
appropriate phenotypes, evolutionary change, spread of
genotypes in a population, adaptive genetic response –
change in multiple generations
► Phenotypic plasticity - body size
Ex. Freshwater fish tapeworm Triaenophorus crassus –
adult weight 5.7 -124 mg, difference in size 20x
Freshwater fish nematode Raphidascaris acus 0.7- 61.2mg,
difference in size 90x,
even higher differences in fecundity
influence of parasite distribution (aggregation)
host immune response generates phenotypic variability in
body size within a parasitic population
Phenotypic plasticity and adaptation of parasites
► How quickly the adaptation appears?
► Rapid adaptation - Ex. egg production
and the rate of development of the nematode parasites
Heligmosomoides polygyrus in mice - changes observed
after 11 generations from the former population
► Potential for rapid adaptation sometimes limited Moniliformis
moniliformis - changes not observed after 60
generations compared to the former generation
Phenotypic plasticity and adaptation of
parasites
Evolution of parasite life strategies
► Body size
► Age at the time of reaching sexual maturity
► Egg production
► Animal body size - increasing in evolutionary time (Cop's
rule)
► Parasite body size
in general evolution from wild to parasitic = size reduction
(limited habitats)
Resizing as an adaptation to parasitism
Frequency distribution of body size
Copepoda a Isopoda
Nematoda
Isopoda
Copepoda
Nematoda
► Frequency distribution of body size
→ it indicates which size groups have undergone diversification
The evolution of body size differs among parasite groups
→ it does not always lead to reduction
It is asymmetric (in digeneans and nematodes),
log-normal in ectoparasites of fish (selection favors
intermediate sizes)
Evolution of body size of parasites
► The problem of using the body size distribution for
evolutionary conclusions !!
► The polyphyletic origin of the taxon affects the shape of
the distribution
Evolution of body size of parasites
Ex. Frequency distribution of body size among 1131 species of monogeneans
parasitizing on fish or other aquatic vertebrates
► Lack of fossil records
► Use of phylogenetic analyses - comparison of body size of
basal and derived taxa
► Ex. Digenea - no consistent trend
► Ex. Monogenea - reduction of average body size in
evolutionary time (consequence of invasion of spatially
limited microhabitats)
► Recently evolving groups tend to be smaller in size than
their ancestors
The evolution of body size - the transition
from wild to parasitic life strategy
Body size of parasites - wild and parasitic
generations
► Host body size
► Larger parasites on larger hosts (interspecies comparison)
Factors affecting the evolution of the parasite
body size
Host taxon level
- larger host = wider space (elephant vs. mouse)
- larger host = more food sources
- larger host = longer living = more stable environment
→ favors parasites with later sexual maturity and larger
size
► Larger parasites on larger hosts, smaller parasites on a
wide range of host sizes
► Positive relationship between host body size and parasite
body size
► Flea body size and host bird (or mammal) size (Kirk, 1991)
► Lice body size and host rodent body size
► Enterobius (Nematoda) body size and host primate body
size (Harvey & Keymer, 1991)
Factors affecting the evolution of the body
size of parasites
The relationship between the width of
the groove on the head of the lice and
the diameter of rodent hair
(Morand et al. 2000) - the relationship
between parasite body size and host
body size is associated phenomenon
► Oxyurid Nematoda in invertebrates and vertebrates - a
strong relationship between parasite and host body sizes
→ host size an important factor in the evolution of
nematode body size
► Acanthocephala - positive correlation between parasite size
and host vertebrate host weight
► The largest Digenea in the largest hosts
(didymozoid Digenea 12m in Mola mola)
► !!! The positive relationship between host body size and
parasite is not universal, e.g. Copepoda parasitizing in fish
Factors affecting the evolution of the body
size of parasites
Effect of host body size on parasite life
components
► Influence of host body size mediated by other factors
- host life span affects the growth of the parasite
- variability in the immune response limits the size and
sexual maturity of parasites
- availability of nutrients in the host - location in the host
limits the size of parasites
Ex. The size of the tapeworms in the intestine of small
mammals depends on the position of attachment - it
determines the mortality of parasites
Effect of host body size on parasite body size
Oxyuride nematodes in primates
Effect of host immunity on parasite body size
► Ex. Tapeworm body size is linked with position in the
intestine of its mammalian hosts
Effect of attachment position on parasite body
size
Position in the intestine = median position of attachment, the intestine was
divided into 10 same parts for shrews or 3 parts for voles and lemmings
► Ectoparasites - the effect of external conditions on body
size
- Geographical trend (Bergman's rule)
Ex. Monogenea and parasitic Crustacea in higher latitudes
and deeper waters - a tendency for larger body size
- Seasonal variability in body size (Gyrodactylus)
Effect of external factors on parasite body size
► Sexual selection - controlling mechanism of evolution of
sexually determined dimorphism (Nematoda, Acanthocephala)
► Ex. Nematoda (Oxyuridae) - smaller size in males than in
females
- strong competition for food
- sexual selection - rapid maturation of males
!!! Schistosomes - gonochorists, hermaphrodite ancestor,
male > female
- evolution for „distribution of tasks" – females for
reproduction, males for movement and obtaining food
Effect of sexual dimorphism on the evolution
of parasite body size
Age of parasites at the time of sexual maturity
► General relationship between body size and age of sexual
maturity
► Helminths - the prepatent period, i.e. the time between
infection of the definitive host and the onset of egg
production
► Early maturation = early egg production, late maturation =
larger size and faster egg production
► Intraspecific plasticity in reaching the age of the first
reproduction
Ex. Tapeworm Schistocephalus solidus
- infection by one individual = displacement
onset of the first reproduction
Age of parasites at the time of sexual maturity
► Optimal age of sexual maturity
- to maximize reproductive success during the life of the
parasite
- it depends on age-related mortality and the relationship
between body size and fecundity
- studied mainly in nematodes - the period of sexual
maturity determines the body size of parasites, which is
related to fecundity
- mathematical models supported empirically - a
compromise between higher fecundity (with increasing body
length) and the risk of death before reaching this length →
parasitic nematodes mature earlier if the mortality of their
larval stages is high
Age of parasites at the time of sexual maturity
► High host mortality → shortened time to sexual maturity
► Low host mortality (longer-lived hosts) → delayed onset of
sexual maturity
Effect of host mortality on the age of
parasites at the time of sexual maturity
Production of eggs and offspring of parasites
► 2 general strategies in animals (K- or r- strategists)
► Parasites - r-strategists (short-lived, early sexual maturity,
small body size, high egg production)
► Evolution of parasite fecundity leads to higher egg
production
► !! Variability in egg production among parasites (some
monogeneas < 100)
► Does the transition to parasitism direct fecundity?
- comparison of wild and parasitic sister taxa
Ex. Copepoda and Isopoda parasitizing in fish - higher
fecundity
Production of parasite eggs
The number of eggs
during an
individual's life
Multiplication of
larval stages
Turbellaria (wild) 10 x1
Monogenea (ectoparasite) 1000 x1
Digenea (endoparasite) 10 million x≥1000
Cestoda (endoparasite) 10 million x(1-1000)
► Fecundity estimates
- egg production
- larval multiplication
- generation time (from egg formation to adult stage)
- small number of eggs/individuals + short generation
time (Gyrodactylus)
- large number of eggs + long generation time
Production of parasite eggs
► Selection pressure from the host and/or environment
► Ex. Copepoda - transition from invertebrate hosts to fish
hosts → tendency to higher eggs production
► Ex. Copepoda - latitude gradient on egg number
independent of body size
Production of parasite eggs
Compromises and strategies for egg
production in parasites
► Larger parasites tend to produce more eggs and/or larger
eggs (Ascothoracida, Digenea)
► In some parasites, intraspecific and interspecific variability
in egg size (Nematoda)
► Selection does not maximize both number and size →
compromise between the number of eggs (fecundity) and
the size of the eggs (schistosomes, Copepoda)
→ two parasite strategies
1. production of a large number of small eggs
2. production of a small number of large eggs
the probability of transmission determines the strategy
Compromises and strategies for egg
production in parasites
Ex. Negative correlation between the number of eggs (fecundity)
and the size of eggs in schistosomes parasitizing mammals
► Compromise - negative relationship between size and
number of eggs, e.g. parasitic Copepoda
Compromises and strategies for egg
production in parasites
Ex. host switch – a situation where one taxon is parasitic in invertebrates,
the sister taxon is parasitic in fish
► Homeothermic vs. poikilothermic hosts
► - homeothermic host - better growth conditions for
endoparasites → small eggs and rapid growth of larvae
Compromises and strategies for egg
production in parasites
Ex. Frequency distribution of egg size in two groups of tapeworms
► Environmental impact
Latitude gradient on reproductive strategy of monogeneans
e.g. Gyrodactylus
- warm waters, tropics - small diversity, few larger ones
descendants
- waters of the northern hemisphere - extremely
diversified, worthy of small offspring
Compromises and strategies for egg
production in parasites
► Endoparasites with
complex developmental
cycles
- compromise between egg
production in the final host
and asexual multiplication of
larval stages in the
intermediate host
Compromises and strategies for egg
production in parasites
Miracidium
Miracidium
Cercaria production (in log)
Cercariaproduction(inlog)
Comparison of life-history traits between wild
and parasitic organisms