Parasite diversity
1 000 000 described species
of eukaryotes
100 000 described species of
parasites
(Poulin & Morand, 2004)
Parasite diversity
Parasite diversity
> 70 transitions from free-living
strategy to parasitic life strategy
(Poulin & Morand, 2004)
Parasite diversity
► What are our knowledge?
► Rate of description of new species as an indicator of
diversity (in a given geographical area)
► Ex. Cumulative number of Cestoda species from vertebrates
of Australia over time
Many parasites are waiting to be discovered and described
Parasite diversity
Ex. Average body size of monogeneans (A) and female nematodes parasitizing
vertebrate animals (B) decreases over time with increasing number of species
discovered
(A) (B)
Parasite diversity
Numberofparasitespecies
(Combes & Morand, 1999)
Mammals and birds have a high number of
species of parasites
At all levels from the host's point of view:
- Host individual (infracommunity)
- Host population (metacommunity)
- Host species (parasitofauna)
At all levels of the geographical scale:
- local, regional, global
Determinants of parasite diversity
Effect of sample size on estimation of parasite
diversity
► Many parasites are not detected in the host sample studied
due to their low prevalence
► Ex. Prevalence of parasites in birds and mammals ≤ 5%, in
fish <20%
167 species og
gastrointestinal
helminths from 20
metacommunities
644 species of
helminths from 77
metacommunities
60 species of
metazoan
ectoparasites
128 species of
gastrointestinal
helminths
both from 88
metacommunities
of freshwater fish
Effect of sample size on estimation of parasite
diversity
Number of metazoan parasite species
versus the number of studies per host
species during 10 years
49 freshwater fish species of North
America
Number of gastrointestinal helminth
species versus the number of
examined host individuals in 79
mammalian species
Effect of sample size on estimation of parasite
diversity
Sample size
Host species 1
Host species 2
Host species 3
Cumulativenumberofparasitespecies
Correction for sample size
► Use of residues
► - residues of the number of parasite species (i.e. the
number of parasite species is corrected for the size of the
host sample (Gregory, 1990))
► Use of estimators of the number of parasite species
- individual data (Walther & Morand, 1997, Poulin 1998)
- 3 non-parametric methods (or their modifications) for
estimating the number of species:
Jacknife estimator, Chao estimator, bootstrap estimator
Estimators of the number of parasite species
Sjack1 = Sobs + Qj(m-1/m)
where Sobs is the total number of parasite species recorded on all
examined hosts, Qj is the number of parasite species occurring on the
number j of randomly selected individuals and m is the total number of
sampled hosts
Sb = S0 + ∑So[1-(hj/H)]H
j=1
where S0 is the number of species observed, i.e. the number of species
currently present in the sample, H is the number of host individuals in
the sample, hj is the number of host individuals on which the parasite
species j was found
Y
XError 2nd order Error 1st order X
Y
Wrong acceptence of HO
Wrong rejection of HO
Effect of host phylogeny on parasite diversity
HO – no relationship
between X and Y
Method of phylogenetically independent
contrasts
(1) Independent contrasts
compare values ​​corresponding
to sister taxa (2) Calculation of values ​​for
a common ancestor
(3) Three independent contrasts (d1, d2, d3)
were obtained by calculation
Ex. calculation d1(X) = 10-8, d1(Y) = 24-20,
d2(X)=9-5, d2(Y)=22-12
9 = (10+8)/2
22 = (24+20)/2
7
17
(4) The regression line passes
through 0
Method of phylogenetically independent
contrasts
Interspecies comparison without phylogenetic recontrusction Interspecies comparison without phylogenetic recontrusction
Interspecies comparison with phylogenetic recontrusction Interspecies comparison with phylogenetic recontrusction
Parasite diversity and host diversity
Variability in the number of ectoparasite
species between taxa
e.g. number of ectoparasite species
in major orders of mammals
0
20
40
60
80
00
20
Parasite diversity and host diversity
Ex. Relationship between mite
diversity on host taxon and
mammalian diversity (number of
mammal species per order)
Positive relationship between number of parasites and number of hosts result
of coevolution and codiversification (host-specific parasites)
Ex. malaria-causing parasites - Plasmodium and Haemoproteus in birds
Ex. Relationship between ectoparasie
diversity (arthropods) and mammalian
diversity
Corrections for phylogeny and body size
Parasites and habitat type of hosts: aquatic versus terrestrial
Parasite diversity and host habitat type
Comparison of the number of intestinal helminth species
between different groups of vertebrates
Parasite diversity and type of host food
Carnivora Cetartiodactyla
mammals: carnivores versus herbivores
0
20
40
60
80
100
120
O
visC
apraEquus
Bos
SusLepusC
am
elusRattusSciurus
C
anis
Felis
M
ustelids
Hom
o
Monoxenous
Heteroxenous
Classical views on determinants of parasite
diversity
1) Latitude gradient
Low latitudes lead to greater diversification
- Host species living in low latitudes (tropics) have more parasite
species
2) The relationship between area size and diversity
Hosts considered islands for parasites
- Larger host species and/or host species with wider geographical
distribution show higher parasite diversity
3) Theory of epidemiology (Anderson & May, 1978, 1991)
The transmission of parasites depends on the exposure of the hosts
and the frequency of contacts
- higher survival, population density and size lead to higher parasite
diversity
Latitude gradient of parasite diversity
No: Mammals and helminths (Poulin, 1995)
No: Primates and helminths (Nunn et al., 2005)
No: North American mammals and helminths (Morand, 2002)
Yes: Rodents and fleas (Krasnov et al., 2004), but the opposite trend!
the effect of climatic factors within a given latitude or
specific environmental factors
Numberofspecies
offleas
Latitude
Latitude gradient of parasite diversity
Yes: Primates and microparasites
(Nunn et al., 2005)
Yes : Humans and microparasites
(Guernier et al., 2004)
Concept of area size vs. diversity
Theory of island biogeography (MacArthur & Wilson, 1967)
The number of species on the island reflects the balance
between the degree of colonization and the degree of
extinction of the species
- hosts = islands for parasites (Kuris et al., 1980)
Island size ~ host size
Island age ~ life expectancy of the host species or population
Distance of the island from the mainland ~ geographical
distribution of hosts
► Island size = larger host (length, weight) - more space and
food resources for parasites, higher diversity of
microhabitats
► Positive relationship between host size (length, weight) and
parasite diversity
► The need for correction for sample size and phylogenetic
effects
Parasite diversity and host size
► Ex. Positive relationship between fish size and number of
monogenean species in fish of the Cichlidae or African
members of the Cyprinidae
► Ex. There is no relationship between the number of ecto- or
endoparasites and the weight in mammals
Parasite diversity and host size
-0,8
-0,6
-0,4
-0,2
0
0,2
0,4
0,6
0 0,2 0,4 0,6 0,8 1
Mean Mammal Body Weight
(contrasts in Log kg)
Ectoparasite
Genera (contrasts in number)
► Island size = host biomass per unit area
► Ex. One elephant versus very numerous rodents
► biomass = product of body weight and density
Parasite diversity and host biomass
► Life expectancy of the host - effect on the degree of
colonization by parasite species
► Longer-lived host species have more parasite species than
short-lived hosts (empirical evidence of the relationship is
limited)
Parasite diversity and host life span
Ex. Number of endoparasitic helminth
species and the life expectancy of North
American freshwater fish
Parasite diversity and age of the host population
► New island - without life
~ new host or population
- few parasite species
in the population of the founder
► Over time – colonization of
new species and speciation –
positive relationship between
number of parasite species and age
of population to the stabilization
stage of the number of species
Ex. host crustacean population - Daphnia magna
Parasite diversity and geographical distribution
of the host
The number of flea species
increases with higher geographical
distribution of hosts
Scope of distribution
Numberofspecies
offleas
Scope of distribution
Numberofhelminth
species
Helminth diversity in carnivores (Torres et al., 2006)
The number of helminth species
increases with higher
geographical distribution of hosts
Flea diversity in rodents (Krasnov et al. 2004)
Epidemiology: parasite diversity and density
of host populations
► Epidemiological determinant
► Basic reproduction rate R0
► R0 for microparasites - number of infections produced by the
pathogen entering the susceptible host population
► R0 for macroparasites - the average number of offspring
produced during the life of a female and reaching sexual
maturity under conditions of absence on density-dependent
restrictions
► R0 < 1 - parasite tends to local extinction
► R0 > 1 - the parasite successfully invades the host population,
the number of parasites grows to equilibrium state
Parasite diversity and host population density
► Host density encourages the accumulation of parasite
species in host populations
► A positive relationship is not always strong
Parasite diversity and host population density
Number of parasite
species vs.
host density in fish
of the Chaetodontidae
Number of monogenean species vs.
frequency of fish occurrence (Cyprinidae)
Number of flea species vs.
population density of host
mammals
More recent perspectives on the study of
determinants of parasite diversity
► Classical predictions indicate several universal rules: host
density, geographical distribution
► Some studies show conflicting relationships: latitude, group
size, life expectancy
► The expression of some determinants is inaccurate, e.g.
the size of the group does not reflect host sociality
► Host behavior is rarely studied
► Therefore new approaches, new hypotheses
Parasite diversity and host sociality
► Sociality of rodent hosts (Bordes et al. 2007)
► Sociality index instead of using group size
► Ex. Diversity of helminths and arthropods in 46 rodent species
H1: benefits of host species living in social groups in relation to behavioral
protection of allogrooming
H2: avoidance of parasites through dilution effect
Parasite diversity and host sociality
In Rhabdomys pumilio, the daily energy expenditure is lower in larger
ones groups (Scantlebury et al. 2006)
probably less energy costs for thermoregulation
stored energy used for costly immunity?
Parasite diversity and home range
► Home range
The infectious stages of macroparasites are highly aggregated and
immobile
The home district of hosts is a potential determinant of parasite contacts it
affects the parasite diversity
► From the point of view of the hypothesis for area size
versus parasite diversity
a larger home district provides more opportunities for parasite contacts
and accumulation of higher parasite diversity
(Nunn et al. 2003; Ezenwa et al. 2006; Lindenfors et al. 2007)
► Based on epidemiology, the opposite prediction
Parasite diversity and home range
Great home
district
Low density
host
Low transmission
parasites
Aggregated distribution of
larval stages
Reduced parasite diversity
Parasite diversity and home range
Bordes et al. 2009
Negative relationship between the size of the home district and the
number of parasite species in mammals in accordance with the
epidemiological assumption
Negative relationship between host density and home district size
Diversity of parasites and diversity of host
immune genes
(Goüy de Bellocq et al. 2007)
Number of helminth species
(corrected for sample size)
NumberofMHCalleles
(correctedforsamplesize)
High parasite diversity maintains high genetic diversity of hosts
Immune genes (MHC, major histocompatibility complex)
(Prugnole et al., Current Biology 2005)
Diversity of parasites and diversity of host
immune genes
Parasite diversity and host immunity
► Ex. an increase in the number of parasite species is
associated with an increase in investment in the
mammalian immune response
(Nunn et al. 2000, 2002)
Parasite diversity and host mortality
► Higher diversity of parasites worsens the negative impact of
parasitism to the host
► ex. coinfection of canine distemper virus (CDV) and
heamoparasite (Babesia sp.) leads to high mortality of African
lions in Tanzania
Munson et al. 2008 , Plos One
Babesia
Biogeographical aspects of parasite diversity
► Biogeographical rules - changes of species diversity
applicable to parasites
► Latitude gradient
► Preferred centre model versus local oasis model
► Shift of similarity of parasite diversity with distance, i.e. the
role of geographical distances to similarity of parasite
communities
Latitudinal gradient
► Latitude - the main biogeographical
factor influencing the diversity of
parasites
► High diversity in the tropics due to
higher evolutionary speed
► Some climatic factors (temperature)
show a similar trend in the
relationship to the diversity of
ectoparasites in particular
Latitudinal gradient
Ex. Species diversity of digeneans
and monogeneans in marine fish
depending on latitude
Ex. Representation of marine
Gyrodactylidae (in relation to all gill
Monogenea) on the gills of sea fish
in relation to latitude
Latitudinal gradient
► Causes of latitudinal gradient - multiple mechanisms
► Area size theory: larger area - more species
► Species-area theory: larger tropics - higher diversity
► Species-energy theory: more energy, more biomass in a
given area, higher diversity
► Theory of ecological time
► Climate stability theory
► Mid-domain model - different centre of species distribution
- geographical or climatic centre or marginal centre
► It affects the relationship between host size and parasite
diversity
Latitudinal gradient
A = aWb, W = L3 and b = 0.8
Number of species on the island
D = Sb, b = 0.2-0.3
Number of monogenean species
on the gills of fish
P = ((L3)0.8)0.2 and P = ((L3)0.8)0.3
→ P = L0.48 and P = L0.72
► Preferred centre model
(abundance centre model)
- unimodal distribution of species abundance in
space
- geographical distances between each site
and the reference site (i.e. the site with the
highest abundance of the species)
Preferred centre or local oasis?
► Model of local oases
- multimodal distribution of abundance of
the species in space
Methodologically not yet determined
Preferred centre model
► Study of 8 species of helminths in fish species Perca
flavescens (Poulin & Dick, 2007) - only the prevalence of
Proteocephlaus pearsei
► Study of metazoan parasites in fish species Squalius
cephalus (Seifertová et al., 2008) - Monogenea
► Study of 22 species of fleas and mites in rodents (Krasnov
et al., 2008) - weak relationship
Shift of geographical distances
Geographical distances
Climatic or environmental gradient
Species-specific dispersion limits
Shift of geographical distances
Ex. Flea communities Ex. Mite communities
► similarity between communities of metazoan parasites in
populations Squalius cephalus (Seifertová et al. 2008)
Shift in parasite diversity affected by
host genetic distances