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AimGeographic spread and range expansion of species into novel environments may merge originally separated species assemblages, yet the possible drivers of geographic heterogeneity in host-parasite associations remain poorly understood. Here, we examine global patterns in the parasite assemblages of two rat species and explore the role of parasite acquisition from local pools of host species.LocationGlobal.Methods We compiled a global data set of helminth parasites (n = 241 species) from two rat species (Rattus rattus species complex, R. norvegicus) and, concomitantly, from all other mammal species known to be infected by the same parasites. We used an inverse Bayesian modelling approach to explicitly link species-level to community-level infestation probabilities at different geographic scales and alleviate the shortcoming of sampling bias.ResultsPatterns of species richness and turnover of parasites in the two focal rat species revealed clear biogeographic structure with lowest species richness and most distinct assemblages in Madagascar and highest species richness and least distinct assemblages in the Palaearctic region. Parasite species richness and turnover across regions were correlated for the two focal hosts, although they were associated with distinct assemblages within regions. Infection probability of a focal host with any given parasite was clearly related to infection probability of the local species pool of wildlife hosts with that same parasite. Infection probability of other mammal species infected with these parasite species, in turn, decreased with their taxonomic distance to the genus Rattus.Main conclusionsOur study demonstrates the importance of spillover of parasites from local wildlife hosts to invasive rats on global patterns of host-parasite associations. Considering both changes in local pools of host species and the global distributions of parasite and pathogen diversity in consistent model frameworks may therefore advance the forecasting of species-level infestation patterns and the possible risk of disease emergence from local to global scale.
Illustration of the inverse Bayesian model for inferences on parasite geography and spillover effects from global species lists. The illustration represents a focal host species (dark rat) in three different regions (R1–R3; illustrated wildlife species are examples from the Palaearctic, Afrotropical and Australian zoogeographic regions), which can be divided into any number of different locations (R1: l1 and l2; R2: i1 and i2). Rats and also other mammals species have been sampled for a parasite species, which has been only found in a few species and localities, with presence recorded as ‘1’ (nematode drawn on top of mammals) and absence as ‘0’. Records are considered random draws from a Bernoulli distribution (blue arrows) with probabilities ψ for the focal host species and probability ϑ for all other host species. Estimates of ϑ for any local host assemblage are used for the estimation of ψ, linking infection probability of local wildlife hosts to the focal host species (green arrows). The parasite has not been sampled from the focal host species in location i2 and R3. However, given the overall model framework, there is a certain probability that the focal species is also infected by the parasite in these areas: the intercept μψ denotes an average global infection risk independent of region and location, while the parameter μΦ estimates regional infection probability independent of location. Thus, μΦ R2 > 0 (parasite is recorded in i1 in R2) and μΦ R3 = 0 (no parasite recorded in R3), and there is a higher probability that the parasite is present in i2 than in R3 given the data and parameter estimates.
… 
Illustration of the inverse Bayesian model for inferences on parasite geography and spill-over effects from global species lists. The illustration represents a focal host species (dark rat) in three different regions (R1 – R3; illustrated wildlife species are examples from the Palearctic, Afrotropical and Australian zoogeographic regions), which can be divided into any number of different locations (R1: l1 and l2; R2: i1 and i2). Rats and also other mammals species have been sampled for a parasite species, which has been only found in a few species and localities, with presence recorded as ‘1’ (nematode drawn on top of mammals) and absence as ‘0’. Records are considered random draws from a Bernoulli distribution (blue arrows) with probabilities  for the focal host species and probability  for all other host species. Estimates of  for any local host assemblage are used for the estimation of , linking infection probability of local wildlife hosts to the focal host species (green arrows). The parasite has not been sampled from the focal host species in location i2 and R3. However, given the overall model framework, there is a certain probability that the focal species is also infected by the parasite in these areas: the intercept  denotes an average global infection risk independent of region and location, while the parameter  estimates regional infection probability independent of location. Thus,  R2 > 0 (parasite is recorded in i1 in R2) and  R3 = 0 (no parasite recorded in R3) and there is a higher probability that the parasite is present in i2 than in R3 given the data and parameter estimates.
… 
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BIODIVERSITY
RESEARCH
The importance of parasite geography
and spillover effects for global patterns
of hostparasite associations in two
invasive species
Konstans Wells
1
*, Robert B. O’Hara
2
, Serge Morand
3
,
Jean-Philippe Lessard
4,5
and Alexis Ribas
6
1
The Environment Institute, School of Earth
and Environmental Sciences, The University
of Adelaide, Adelaide, SA, Australia,
2
Biodiversity and Climate Research Centre
(BiK-F), Frankfurt, Germany,
3
Centre
d’Infectiologie Christophe M
erieux du Laos,
CIRAD AGIRs, CNRS ISEM, Vientiane, Lao
People’s Democratic Republic,
4
Qu
ebec
Centre for Biodiversity Science, McGill
University, Montr
eal, QC, Canada,
5
Department of Biology, Concordia
University, Montr
eal, QC, Canada,
6
Biodiversity Research Group, Faculty of
Science, Udon Thani Rajabhat University,
Udon Thani, Thailand
*Correspondence: Konstans Wells, School of
Earth & Environmental Sciences and the
Environment Institute, The University of
Adelaide, North Terrace, Adelaide SA 5005,
Australia.
E-mail: konstans.wells@adelaide.edu.au
ABSTRACT
Aim Geographic spread and range expansion of species into novel environ-
ments may merge originally separated species assemblages, yet the possible
drivers of geographic heterogeneity in hostparasite associations remain poorly
understood. Here, we examine global patterns in the parasite assemblages of
two rat species and explore the role of parasite acquisition from local pools of
host species.
Location Global.
Methods We compiled a global data set of helminth parasites (n=241 spe-
cies) from two rat species (Rattus rattus species complex, R. norvegicus) and,
concomitantly, from all other mammal species known to be infected by the
same parasites. We used an inverse Bayesian modelling approach to explicitly
link species-level to community-level infestation probabilities at different geo-
graphic scales and alleviate the shortcoming of sampling bias.
Results Patterns of species richness and turnover of parasites in the two focal
rat species revealed clear biogeographic structure with lowest species richness
and most distinct assemblages in Madagascar and highest species richness and
least distinct assemblages in the Palaearctic region. Parasite species richness and
turnover across regions were correlated for the two focal hosts, although they
were associated with distinct assemblages within regions. Infection probability
of a focal host with any given parasite was clearly related to infection probabil-
ity of the local species pool of wildlife hosts with that same parasite. Infection
probability of other mammal species infected with these parasite species, in
turn, decreased with their taxonomic distance to the genus Rattus.
Main conclusions Our study demonstrates the importance of spillover of par-
asites from local wildlife hosts to invasive rats on global patterns of hostpara-
site associations. Considering both changes in local pools of host species and
the global distributions of parasite and pathogen diversity in consistent model
frameworks may therefore advance the forecasting of species-level infestation
patterns and the possible risk of disease emergence from local to global scale.
Keywords
Biogeographic regions, biological invasions, geographic mosaics, global diver-
sity, helminths, hostparasite associations, inverse modelling, parasite spread,
species distribution, zoonoses.
DOI: 10.1111/ddi.12297
ª2014 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/ddi 477
Diversity and Distributions, (Diversity Distrib.) (2015) 21, 477–486
A Journal of Conservation Biogeography
Diversity and Distributions
INTRODUCTION
As much as 60% of human diseases are of zoonotic origin
(Taylor et al., 2001), but our knowledge of how parasites
are distributed and shared among wildlife, commensal and
domestic animal species is inevitably incomplete given the
challenge to exhaustively document possible hostparasite
combinations for thousands of species. Moreover, while it is
evident that environmental change alters conditions for para-
site persistence and transmission (Patz et al., 2000), we lack
a solid understanding of how global patterns in hostparasite
associations are shaped by geographic range limits of para-
sites and interactions between invasive hosts and native
assemblages of wildlife hosts (Morand & Krasnov, 2010;
Estrada-Pe~
na et al., 2014).
During historical dispersal and invasions of new environ-
ments, host species are likely to escape from some associated
parasite species and thus harbour fewer parasites in newly
colonized regions compared to the associated parasite assem-
blages in their native range (Poulin & Mouillot, 2003;
Torchin et al., 2003). Moreover, a local assemblage of para-
sites (i.e. all parasites found in a host species in a region)
infecting a widely distributed host species (e.g. commensal
rat) may be strongly influenced by acquisition from the local
pool of wildlife hosts, that is a gain of parasites that origi-
nated in local wildlife species (Daszak et al., 2000). Geograph-
ical structure in hostparasite associations is thus likely to
track patterns of wildlife diversity such as those observed
along broad-scale environmental gradients (Jenkins et al.,
2013) and on global maps of zoogeographic regions (Holt
et al., 2013). The total species richness of parasites in local
host communities often correlates positively with the species
richness of hosts (Krasnov et al., 2004; Thieltges et al., 2011).
As such, an invasive host species colonizing an area with a
high diversity of wildlife species is likely to be exposed to a
high diversity of potentially suitable parasite species. How-
ever, increasing the diversity of host species may also cause
unfavourable conditions for parasites if host species differ in
quality. In such cases, increasing host species richness can
reduce parasite transmissibility due to more encounters with
unfavourable hosts (Ostfeld & Keesing, 2012). The strength
and generality of the relationship between the number of par-
asites in an invasive host species and the diversity of local
wildlife assemblages as potential reservoirs over large geo-
graphic scales remain therefore elusive (Morand, 2012).
Uncertainty persists as to whether parasite diversity on
any given species of host in a local community is positively
related to local host diversity. Presumably, the parasite spe-
cies richness of any given host species should be highest in
its ancestral centre of origin (i.e. South and Southeast Asia
for commensal rats of the genus Rattus; Robins et al., 2008;
Aplin et al., 2011). The sharing of parasite species with other
species from local host species pools can be expected to be
highest if species have a long history of sharing the same
biogeographical space: the longer domestic and commensal
animals are associated with humans, for example the more
parasites they share with them (Morand et al., 2014).
In this study, we explored changes in parasite species rich-
ness and turnover at global scale and the role of parasite
acquisition from local pools of wildlife hosts of two of the
most cosmopolitan invaders and important commensal rat
species. The black rat Rattus rattus (species complex) and the
Norway rat Rattus norvegicus have been introduced in most
regions of the world as a result of human activities (Aplin
et al., 2011), have a long history of disease transmission to
humans (Meerburg et al., 2009) and cause considerable eco-
nomic loss (Singleton et al., 2003; Stenseth et al., 2003).
R. rattus invades a large range of semi-natural and natural
environments, where it is likely to interact with various wild-
life species (Goodman, 1995; Harris et al., 2006; Wells et al.,
2014). Such human-induced mixture of anthropogenic and
natural habitats and animal species are likely to enhance the
exchange of parasite species across environments (Hoberg,
2010). R. norvegicus is more strongly associated with urban
environments that generally harbour fewer wildlife species
(Wells et al., 2014). We may therefore expect parasite assem-
blages of R. rattus to reflect the higher richness of reservoir
hosts in their environment relative to that of R. norvegicus.
The two rat species could be expected to share similar parasite
assemblages and exhibit similar patterns of spatial turnover
across zoogeographic regions if we take into account that they
occur in sympatry in urban environments and parasite may
frequently shift between these two closely related species.
Not only do we know very little about global geographic
trends of hostparasite associations; there are important
methodological obstacles that can preclude obtaining a clear
picture. Species distributional data commonly include bias
towards heterogeneous sampling efforts and incomplete sam-
pling (Lomolino, 2004; Hortal et al., 2007; Boakes et al.,
2010). Incomplete inventories introduce ‘false’ zeros into
data (Martin et al., 2005), and there is uncertainty as to
whether hostparasite associations are lacking or have simply
been unobserved (Hopkins & Nunn, 2007). Especially in
comparative studies, sampling bias and incomplete invento-
ries may lead to misleading conclusions about hostparasite
associations if not accurately accounted for in analyses (Wells
et al., 2013). We must therefore develop analytical tools that
will minimize how sampling biases influence our perception
of geographic patterns in hostparasite associations.
Addressing our study question with incomplete observa-
tions inevitably calls for statistical approaches that take
uncertainty and unknown measures into account (Keating &
Cherry, 2004; Reese et al., 2005; Ward et al., 2009). We fitted
an inverse modelling approach in a Bayesian hierarchical
framework to estimate possible hostparasite associations
from a limited set of observations, while also accounting for
the possible links between parasite species and local species
pools of wildlife hosts.
We therefore used the flexibility of a hierarchical Bayesian
approach for estimating parasite occurrence at poorly sampled
478 Diversity and Distributions, 21, 477–486, ª2014 John Wiley & Sons Ltd
K. Wells et al.
locations by ‘borrowing strength’ from more intensively sam-
pled locations, while also acknowledging that locations are not
identical in all aspects. The hierarchical model structure fur-
ther allows to model the variation of parasite occurrence in
wildlife hosts according to species and population attributes
and environmental variables (Fig. 1). For example, we can ask
whether species of conservation concern are particularly sensi-
tive to share parasites with invasive (focal) species, fostering
our understanding for informed wildlife management and pest
control (Daszak et al., 2000). We systematically combined
information at the species level (i.e. parasite associations in
the focal rats species) with those at the community level (i.e.
wildlife hosts linked to rats by sharing the same parasites) into
a hierarchical model that optimizes inference by maximizing
the use of all available information and simultaneously assess-
ing the influence of ecological processes expected to operate
across levels of organization.
METHODS
Database on hostparasite records
We compiled a database of recorded associations between
the focal rat species and their helminth parasites from the
hostparasite database of the Natural History Museum Lon-
don (NHML) (Gibson et al., 2005), which includes hostpar-
asite records from more than 28,000 references up to 2003
(accessed in June 2013).
For each field record (excluding experimental and captive
records), we characterized the geographic location based on
current country-level geographic borders. We specified this
characterization in subregions for some locations such as
China (which encompasses multiple zoogeographic regions;
for all records from China which could not be identified to
subregion, we used an extra category that specified zoogeo-
graphic region as missing data). Additionally we separated
records from different islands in Indonesia (e.g. we consid-
ered Borneo as a separate location irrespective of whether
records were made in the Indonesian or Malaysian part of
the island). For countries with few records, we merged
neighbouring countries into larger units such as Scandinavia
(Finland, Norway, Sweden). We are aware that this classifica-
tion is coarse and arbitrary. Nevertheless, we consider this
approach to be acceptable in order to systematically assign
all records to geographical units while accounting for the
global topography and zoogeographic structure of a large set
of records with no detailed geographic positions available.
Our data set for analysis included 144 geographic locations.
Figure 1 Illustration of the inverse Bayesian model for inferences on parasite geography and spillover effects from global species lists.
The illustration represents a focal host species (dark rat) in three different regions (R1R3; illustrated wildlife species are examples from
the Palaearctic, Afrotropical and Australian zoogeographic regions), which can be divided into any number of different locations (R1: l1
and l2; R2: i1 and i2). Rats and also other mammals species have been sampled for a parasite species, which has been only found in a few
species and localities, with presence recorded as ‘1’ (nematode drawn on top of mammals) and absence as ‘0’. Records are considered
random draws from a Bernoulli distribution (blue arrows) with probabilities wfor the focal host species and probability ϑfor all other
host species. Estimates of ϑfor any local host assemblage are used for the estimation of w, linking infection probability of local wildlife
hosts to the focal host species (green arrows). The parasite has not been sampled from the focal host species in location i2 and R3.
However, given the overall model framework, there is a certain probability that the focal species is also infected by the parasite in these
areas: the intercept l
w
denotes an average global infection risk independent of region and location, while the parameter l
Φ
estimates
regional infection probability independent of location. Thus, l
Φ
R2>0 (parasite is recorded in i1inR2) and l
Φ
R3=0 (no parasite
recorded in R3), and there is a higher probability that the parasite is present in i2 than in R3 given the data and parameter estimates.
Diversity and Distributions, 21, 477–486, ª2014 John Wiley & Sons Ltd 479
Parasite geography and spillover effects
We assigned all locations to one of the 11 zoogeographic
regions recently defined by Holt et al. (2013). We further
assigned locations to the main climate zones (equatorial,
arid, warm-temperate, snow, polar) based on an updated
world map of the K
oppenGeiger climate classification (Kot-
tek et al., 2006); if locations were covered by various climate
zones (28 of 144), we assigned the relative proportion of the
area covered by each climate zone and considered the uncer-
tainty in which climate zones parasites were recorded with
multiple data imputation as part of the Bayesian analysis and
sampling procedure.
With the same approach, for each helminth species in our
database we compiled the full range of host species for all
locations from the NHML hostparasite database. For all
mammal species in our database, we calculated the taxonomic
distance to the genus ‘Rattus’ based on the number of nodes
in a taxonomic tree (Wilson & Reeder, 2005) resulting from
the species’ genus, family and order classification, indexed
between 1 and 5. We further classified the IUCN conservation
status of all mammal species (categories: least concern, near
threatened, vulnerable, endangered, critically endangered)
based on the 2001 assessment (version 3.1, http://www.
iucnredlist.org). Note that we termed regional assemblages of
mammals as ‘wildlife hosts’ in this study, but these assem-
blages also included humans and domestic mammals.
For data cleaning, all records not identified to species level
were excluded, except those genera for which only single
unidentified species were recorded. Scientific names were
revised and standardized with the aid of a literature search
in Thompson Reuters Web of Science (http://apps.webof-
knowledge.com/; latest searches performed in September
2013), personal literature collections and the mammal online
database at http://vertebrates.si.edu/msw/mswCFApp/msw/
index.cfm (Wilson & Reeder, 2005).
Our final data set for analysis included a total of 12,405
records of hostparasite association from different locations.
Missing data were handled in our model approach by multi-
ple data imputation. We are aware that our database is
incomplete and lacks recently discovered helminth species.
However, we do not consider this to be a problem, as we
were interested in inference on geographic structure in host
parasite interactions from a finite data set, rather than
complete lists of records. Species lists and classification of
sampling locations are provided in Appendix S1 in the
Supporting Information.
Inferring hostparasite associations with an inverse
modelling approach
We used an inverse hierarchical modelling approach in a
Bayesian framework to ask how likely it was for any parasite
species to occur in a focal host species (Rattus rattus and
R. norvegicus) in different locations inferred from a finite set
of observations. To make inferential summary statistics on
modelled estimates rather than observations, we estimated
the probability of having a parasite species associated with a
host species in any sampled location.
For all locations l, at which at least one parasite species p
has been recorded in at least one focal host species h,we
assumed that all records y(h, p, l) of hostparasite associa-
tions were random draws based on the true but unknown
distribution of hostparasite associations such that
yðh;p;lÞBernoulliðwðh;p;lÞÞ (1)
The probability of local hostparasite association w(h, p, l)
can be modelled further. In particular, we assumed w(h, p, l)
to be linked to the odds of the average occurrence probabil-
ity of the respective parasite species Φ(p, r) within the zoo-
geographic region rwhere lis located (based on records
from all kind of host species, irrespective of host species
identity), given that locations from the same region are likely
to harbour similar parasite assemblages. Likewise, we
assumed w(h, p, l) to be linked to the odds of the average
occurrence probability of the respective parasite species Ω(p,
c) within the climate zone cwhere lis located. We also
assumed w(h, p, l) to vary with the average infestation prob-
ability of any mammal species from local assemblages with
the same parasite, given as l
ϑ
(p, l) (the odds of the infesta-
tion probability ϑ(p, l)). Using a logit-link function, this
gives:
logitwðh;p;lÞ¼lwðh;pÞþa1ðh;pÞlUðp;r½lÞ
þa2ðh;pÞlXðp;c½lÞ þ a3ðh;pÞl0ðp;lÞ(2)
where l
w
(h, p) is the species-specific intercept and a
1
to a
3
are coefficient estimates.
The covariates l
Φ
(p, r), l
Ω
(p, c) and l
ϑ
(p, l) are them-
selves considered as random variables (i.e. modelled proba-
bilities from finite sets of observations), for which we
assumed all observations, Φobs and ϑobs respectively, as
random draws out of the true but unknown parasite distri-
butions and host associations. We thus assumed
Uobsðp;lÞBernoulliðUðp;lÞÞ and
0obsðp;l;xlÞBernoullið0ðp;lÞÞ (3)
where x
l
indexes all mammal species examined in location l
for parasites.
We assumed again logit-link functions to model Φ(p, l)
and ϑ(p, l) based on random intercepts such as
logitUðp;lÞ¼lUðp;r½lÞ þ lXðp;c½lÞ and
logit0ðp;lÞ¼l0ðp;lÞþc1TðmÞþc2CðmÞ:(4)
Here, we modelled ϑ(p, l) further as a function of species-
specific taxonomic distance Tand their IUCN conservation
status Cof mammal species m;c
1
and c
2
are the respective
coefficient estimates.
Given the estimated probability of local hostparasite asso-
ciation w(h, p, l), we can express our uncertainty in the
derived state variable z(h, p, l) of whether a host species his
480 Diversity and Distributions, 21, 477–486, ª2014 John Wiley & Sons Ltd
K. Wells et al.
We assigned all locations to one of the 11 zoogeographic
regions recently defined by Holt et al. (2013). We further
assigned locations to the main climate zones (equatorial,
arid, warm-temperate, snow, polar) based on an updated
world map of the K
oppenGeiger climate classification (Kot-
tek et al., 2006); if locations were covered by various climate
zones (28 of 144), we assigned the relative proportion of the
area covered by each climate zone and considered the uncer-
tainty in which climate zones parasites were recorded with
multiple data imputation as part of the Bayesian analysis and
sampling procedure.
With the same approach, for each helminth species in our
database we compiled the full range of host species for all
locations from the NHML hostparasite database. For all
mammal species in our database, we calculated the taxonomic
distance to the genus ‘Rattus’ based on the number of nodes
in a taxonomic tree (Wilson & Reeder, 2005) resulting from
the species’ genus, family and order classification, indexed
between 1 and 5. We further classified the IUCN conservation
status of all mammal species (categories: least concern, near
threatened, vulnerable, endangered, critically endangered)
based on the 2001 assessment (version 3.1, http://www.
iucnredlist.org). Note that we termed regional assemblages of
mammals as ‘wildlife hosts’ in this study, but these assem-
blages also included humans and domestic mammals.
For data cleaning, all records not identified to species level
were excluded, except those genera for which only single
unidentified species were recorded. Scientific names were
revised and standardized with the aid of a literature search
in Thompson Reuters Web of Science (http://apps.webof-
knowledge.com/; latest searches performed in September
2013), personal literature collections and the mammal online
database at http://vertebrates.si.edu/msw/mswCFApp/msw/
index.cfm (Wilson & Reeder, 2005).
Our final data set for analysis included a total of 12,405
records of hostparasite association from different locations.
Missing data were handled in our model approach by multi-
ple data imputation. We are aware that our database is
incomplete and lacks recently discovered helminth species.
However, we do not consider this to be a problem, as we
were interested in inference on geographic structure in host
parasite interactions from a finite data set, rather than
complete lists of records. Species lists and classification of
sampling locations are provided in Appendix S1 in the
Supporting Information.
Inferring hostparasite associations with an inverse
modelling approach
We used an inverse hierarchical modelling approach in a
Bayesian framework to ask how likely it was for any parasite
species to occur in a focal host species (Rattus rattus and
R. norvegicus) in different locations inferred from a finite set
of observations. To make inferential summary statistics on
modelled estimates rather than observations, we estimated
the probability of having a parasite species associated with a
host species in any sampled location.
For all locations l, at which at least one parasite species p
has been recorded in at least one focal host species h,we
assumed that all records y(h, p, l) of hostparasite associa-
tions were random draws based on the true but unknown
distribution of hostparasite associations such that
yðh;p;lÞBernoulliðwðh;p;lÞÞ (1)
The probability of local hostparasite association w(h, p, l)
can be modelled further. In particular, we assumed w(h, p, l)
to be linked to the odds of the average occurrence probabil-
ity of the respective parasite species Φ(p, r) within the zoo-
geographic region rwhere lis located (based on records
from all kind of host species, irrespective of host species
identity), given that locations from the same region are likely
to harbour similar parasite assemblages. Likewise, we
assumed w(h, p, l) to be linked to the odds of the average
occurrence probability of the respective parasite species Ω(p,
c) within the climate zone cwhere lis located. We also
assumed w(h, p, l) to vary with the average infestation prob-
ability of any mammal species from local assemblages with
the same parasite, given as l
ϑ
(p, l) (the odds of the infesta-
tion probability ϑ(p, l)). Using a logit-link function, this
gives:
logitwðh;p;lÞ¼lwðh;pÞþa1ðh;pÞlUðp;r½lÞ
þa2ðh;pÞlXðp;c½lÞ þ a3ðh;pÞl0ðp;lÞ(2)
where l
w
(h, p) is the species-specific intercept and a
1
to a
3
are coefficient estimates.
The covariates l
Φ
(p, r), l
Ω
(p, c) and l
ϑ
(p, l) are them-
selves considered as random variables (i.e. modelled proba-
bilities from finite sets of observations), for which we
assumed all observations, Φobs and ϑobs respectively, as
random draws out of the true but unknown parasite distri-
butions and host associations. We thus assumed
Uobsðp;lÞBernoulliðUðp;lÞÞ and
0obsðp;l;xlÞBernoullið0ðp;lÞÞ (3)
where x
l
indexes all mammal species examined in location l
for parasites.
We assumed again logit-link functions to model Φ(p, l)
and ϑ(p, l) based on random intercepts such as
logitUðp;lÞ¼lUðp;r½lÞ þ lXðp;c½lÞ and
logit0ðp;lÞ¼l0ðp;lÞþc1TðmÞþc2CðmÞ:(4)
Here, we modelled ϑ(p, l) further as a function of species-
specific taxonomic distance Tand their IUCN conservation
status Cof mammal species m;c
1
and c
2
are the respective
coefficient estimates.
Given the estimated probability of local hostparasite asso-
ciation w(h, p, l), we can express our uncertainty in the
derived state variable z(h, p, l) of whether a host species his
480 Diversity and Distributions, 21, 477–486, ª2014 John Wiley & Sons Ltd
K. Wells et al.
occurrence probability of parasites across climate zones l
Ω
(p,
c) had a positive impact on the infection probability for only
7 of 241 parasite species in R. rattus and for eight parasite
species in R. norvegicus (lower limits of CI >0 for a
2
).
Average infection probability of other mammal species
with helminths decreased considerably with taxonomic dis-
tance from the genus Rattus (Fig. 4), and it also decreased
with increasingly endangered status (according to their IUCN
status) (Fig. 4). However, the species turnover in overall
mammal assemblages in different zoogeographic regions was
not correlated with the species turnover of parasite assem-
blages in the two rat species (both Mantel tests with Pear-
son’s correlation coefficients r<0.27).
DISCUSSION
Inferring hostparasite associations for two of the most com-
mon and invasive commensal rat species at a global scale
showed that species richness and assemblage composition of
parasitic helminths varied over zoogeographic regions. Geo-
graphic variation in parasite species richness and assemblage
composition was correlated between the two focal host
species (Rattus rattus and R. norvegicus), although locally
they were associated with distinct parasite assemblages. Fur-
ther, our hierarchical model framework showed a clear influ-
ence of local species pools of wildlife hosts on parasite
Table 1 Summary of species richness and spatial turnover
(meanb
sim
) of helminth parasite assemblages in the two host
species Rattus rattus and R. norvegicus in different zoogeographic
regions as defined by (Holt et al., 2013). For species richness,
recorded numbers are given as S
Rec
, while posterior estimates are
given as S
Est
. Spatial turnover estimates of meanb
sim
are
calculated as the mean of all pairwise b
sim
values from different
locations within regions. 95% credible intervals for posterior
estimates are given in parenthesis
Region S
Rec
S
Est
Meanb
sim
R. rattus
Afrotropical 27 40 (3547) 0.47 (0.340.53)
Australian 11 17 (1421) 0.49 (0.380.56)
Madagascan 0 1 (03) 0.99 (0.21)
Nearctic 3 15 (921) 0.55 (0.40.67)
Neotropical 16 24 (1930) 0.51 (0.380.58)
Oceanian 9 15 (1119) 0.58 (0.460.68)
Oriental 64 71 (6776) 0.38 (0.240.43)
Palaearctic 48 67 (5974) 0.39 (0.250.45)
Panamanian 6 15 (922) 0.61 (0.470.69)
Saharo-Arabian 25 30 (2736) 0.53 (0.40.59)
Sino-Japanese 15 28 (2234) 0.56 (0.420.63)
R. norvegicus
Afrotropical 0 24 (1733) 0.58 (0.450.68)
Australian 13 19 (1623) 0.49 (0.360.55)
Madagascan 0 1 (03) 0.99 (0.31)
Nearctic 27 34 (3043) 0.54 (0.410.59)
Neotropical 19 29 (2435) 0.59 (0.440.65)
Oceanian 0 11 (516) 0.54 (0.380.69)
Oriental 21 41 (3348) 0.54 (0.40.62)
Palaearctic 97 100 (95107) 0.26 (0.210.4)
Panamanian 6 14 (920) 0.58 (0.440.67)
Saharo-Arabian 26 33 (2838) 0.53 (0.40.58)
Sino-Japanese 30 43 (3649) 0.55 (0.410.61)
020406080
020406080100
R. rattus parasite number
R. norvegicusparasite number
Helminth species richness
Figure 2 Relationship in the estimated numbers of helminth
species associated with the two host species Rattus rattus and
R. norvegicus in different zoogeographic regions given as
posterior estimates of modes (points) and 95% credible intervals
(bars). The dashed line indicates a 1 : 1 relationship.
0.2 0.4 0.6 0.8 1.0
0.2 0.4 0.6 0.8 1.0
R. rattus −β
Sim
R.norvegicus −β
Sim
Uniqueness of helminth assemblages
Figure 3 Distinctness of parasitic helminth assemblages
associated with the two host species Rattus rattus and
R. norvegicus in different zoogeographic regions as calculated
from averaged spatial turnover estimates (modes of posterior
samples are plotted as points and 95% credible intervals as
bars). The dashed line indicates a 1 : 1 relationship.
482 Diversity and Distributions, 21, 477–486, ª2014 John Wiley & Sons Ltd
K. Wells et al.
associations in the two focal host species, which supports the
importance of spillover effects (Daszak et al., 2000). More-
over, in non-focal host species, taxonomic distance to the
genus ‘Rattus’ and conservation status was related to the
probability of being infected with a parasite species that had
also infected one of the focal hosts.
Commensal rats have escaped several helminth parasites in
regions such as Madagascar or Australia, where estimates of
the species richness of parasites associated with the focal
hosts are very small (see also Torchin et al., 2003). Only in
the Palaearctic region were estimates of parasite species rich-
ness higher (R. norvegicus) than in the Oriental region, where
the host genus Rattus originated and diversified (Robins
et al., 2008; Aplin et al., 2011). At a global scale, total num-
bers of recorded parasite species were considerably higher
than those in the Oriental region for both focal host species,
emphasizing that a considerable proportion of parasite spe-
cies are linked to non-focal host species and were likely to
have been acquired by the focal rat species during their inva-
sion and colonization history. However, despite the clear link
between focal and non-focal hostparasite associations, we
do not know specifically which parasite species co-evolved
with the rat species or any other host species. Moreover, with
only general relationships in species richness and turnover
examined, the underlying mechanisms that cause loss and
acquisition of hostparasite association across geographic
gradients remain unexplored.
Besides the likely impact of geographically varying regional
wildlife host assemblages on parasites, there are likely to be
other factors impacting parasite transmission and survival
according to parasites’ life histories. Parasitic helminths with
either free-living stages in their life cycles or indirect trans-
mission (e.g. via vectors) may be particularly sensitive to cli-
mate changes and other ecological perturbations (Brooks &
Hoberg, 2007), and variable conditions may result in geo-
graphic mosaics of species associations in time and space
(Thompson & Cunningham, 2002). Geographic patterns in
hostparasite associations and other species interactions are
most likely structured by multiple drivers of species and
environmental attributes (Sheppard et al., 2010; Guilhaumon
et al., 2012). Correlations in species richness and spatial
turnover of parasites in the two focal host species, despite
different associated assemblages, is an important result.
However, additional studies are required to explore possible
drivers of such relationships.
Contrary to our expectations, R. rattus was not associated
with more parasite species than R. norvegicus nor did its
associated parasite assemblages show more zoogeographic
variation. Along with the findings that more closely related
mammalian host species were more likely to be associated
with the same parasite species, we conclude that parasite
assemblages do evidently change with different conditions in
zoogeographic regions but not necessarily with different hab-
itat use of the focal host species, nor with their affinity for
near-natural habitats shared with local wildlife host species.
We found mammal species of least conservation concern
were more likely to be infected with the parasites of the two
rat species than endangered species. Most endangered species
can be found in natural habitats that are at continuous
decline due to human impact (Rondinini et al., 2011),
whereas a large proportion of mammal species of least con-
cern, including domestic species, are well able to persist in
anthropogenic landscapes, where the focal hosts also occur.
The stronger links between wildlife species of least conserva-
tion concern and the parasites recorded from the two com-
mensal rats provide a first indication that habitat overlap
and species ecological traits may impact the sharing of para-
sites between invasive species and local wildlife. However, we
currently lack further detailed information to incorporate
them into our analysis. Likewise, it is desirable to incorpo-
rate more geographic attributes of sample locations in future
analysis to better partition the role of geography and ecology
on the sharing of parasites by different host species (Davies
& Pedersen, 2008; Cooper et al., 2012).
Spillover and acquisition of parasites and pathogen are
important in many ecological systems of wildlife and domes-
tic or commercial species (Colla et al., 2006; Wood et al.,
2012). Understanding the underlying mechanism for better
predicting how particular species are under threat is typically
challenged by disentangling geographical and ecological
aspects. Pathogen transmission and spillover among species
may include complex dynamics of the ‘geographic’ compo-
nent: variation in the attraction of interacting species can
12345
–0.5 0.0 0.5
Taxonomic distance
Effect size
–0.5 0.0 0.5
LC NT VU ED CD
IUCN conservation status
Figure 4 Posterior estimates of the relative impact of
taxonomic distance from the genus ‘Rattus’ and the IUCN
conservation status on the infestation probability of mammal
species with the parasitic helminth species recorded in the two
focal rat species Rattus rattus and R. norvegicus. Posterior modes
are plotted as squares; 95% credible intervals as bars. Taxonomic
distance indexed between 1 and 5 is based on species’ genus,
family and order classification;IUCN conservation status ranges
from least concern (LC) to critically endangered (CD).
Diversity and Distributions, 21, 477–486, ª2014 John Wiley & Sons Ltd 483
Parasite geography and spillover effects
occurrence probability of parasites across climate zones l
Ω
(p,
c) had a positive impact on the infection probability for only
7 of 241 parasite species in R. rattus and for eight parasite
species in R. norvegicus (lower limits of CI >0 for a
2
).
Average infection probability of other mammal species
with helminths decreased considerably with taxonomic dis-
tance from the genus Rattus (Fig. 4), and it also decreased
with increasingly endangered status (according to their IUCN
status) (Fig. 4). However, the species turnover in overall
mammal assemblages in different zoogeographic regions was
not correlated with the species turnover of parasite assem-
blages in the two rat species (both Mantel tests with Pear-
son’s correlation coefficients r<0.27).
DISCUSSION
Inferring hostparasite associations for two of the most com-
mon and invasive commensal rat species at a global scale
showed that species richness and assemblage composition of
parasitic helminths varied over zoogeographic regions. Geo-
graphic variation in parasite species richness and assemblage
composition was correlated between the two focal host
species (Rattus rattus and R. norvegicus), although locally
they were associated with distinct parasite assemblages. Fur-
ther, our hierarchical model framework showed a clear influ-
ence of local species pools of wildlife hosts on parasite
Table 1 Summary of species richness and spatial turnover
(meanb
sim
) of helminth parasite assemblages in the two host
species Rattus rattus and R. norvegicus in different zoogeographic
regions as defined by (Holt et al., 2013). For species richness,
recorded numbers are given as S
Rec
, while posterior estimates are
given as S
Est
. Spatial turnover estimates of meanb
sim
are
calculated as the mean of all pairwise b
sim
values from different
locations within regions. 95% credible intervals for posterior
estimates are given in parenthesis
Region S
Rec
S
Est
Meanb
sim
R. rattus
Afrotropical 27 40 (3547) 0.47 (0.340.53)
Australian 11 17 (1421) 0.49 (0.380.56)
Madagascan 0 1 (03) 0.99 (0.21)
Nearctic 3 15 (921) 0.55 (0.40.67)
Neotropical 16 24 (1930) 0.51 (0.380.58)
Oceanian 9 15 (1119) 0.58 (0.460.68)
Oriental 64 71 (6776) 0.38 (0.240.43)
Palaearctic 48 67 (5974) 0.39 (0.250.45)
Panamanian 6 15 (922) 0.61 (0.470.69)
Saharo-Arabian 25 30 (2736) 0.53 (0.40.59)
Sino-Japanese 15 28 (2234) 0.56 (0.420.63)
R. norvegicus
Afrotropical 0 24 (1733) 0.58 (0.450.68)
Australian 13 19 (1623) 0.49 (0.360.55)
Madagascan 0 1 (03) 0.99 (0.31)
Nearctic 27 34 (3043) 0.54 (0.410.59)
Neotropical 19 29 (2435) 0.59 (0.440.65)
Oceanian 0 11 (516) 0.54 (0.380.69)
Oriental 21 41 (3348) 0.54 (0.40.62)
Palaearctic 97 100 (95107) 0.26 (0.210.4)
Panamanian 6 14 (920) 0.58 (0.440.67)
Saharo-Arabian 26 33 (2838) 0.53 (0.40.58)
Sino-Japanese 30 43 (3649) 0.55 (0.410.61)
020406080
020406080100
R. rattus parasite number
R. norvegicusparasite number
Helminth species richness
Figure 2 Relationship in the estimated numbers of helminth
species associated with the two host species Rattus rattus and
R. norvegicus in different zoogeographic regions given as
posterior estimates of modes (points) and 95% credible intervals
(bars). The dashed line indicates a 1 : 1 relationship.
0.2 0.4 0.6 0.8 1.0
0.2 0.4 0.6 0.8 1.0
R. rattus −β
Sim
R.norvegicus −β
Sim
Uniqueness of helminth assemblages
Figure 3 Distinctness of parasitic helminth assemblages
associated with the two host species Rattus rattus and
R. norvegicus in different zoogeographic regions as calculated
from averaged spatial turnover estimates (modes of posterior
samples are plotted as points and 95% credible intervals as
bars). The dashed line indicates a 1 : 1 relationship.
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SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article:
Appendix S1 List of parasite species and sampled locations.
Table S1 List of parasitic helminth species and associated
number of mammal hosts.
Table S2 Assignments of sampled locations to zoogeographic
regions.
Appendix S2 Model code in BUGS language.
BIOSKETCHES
The authors of this study have various interests linked to
biodiversity, parasitology, conservation, species distributions,
ecohealth, biotic interactions, and hierarchical models, and
assembled as a multidisciplinary team. All authors contrib-
uted jointly to this study, mostly by asking na
ıve questions
to each other that helped to critically scrutinize approaches
and synthesize different views into this study.
Editor: Jacqueline Beggs
486 Diversity and Distributions, 21, 477–486, ª2014 John Wiley & Sons Ltd
K. Wells et al.
... Predicting parasitic disease emergence requires identifying host attributes that enable pathogen spillover and host shifting (Wells et al., 2015;Dallas et al., 2017;Wells and Clark, 2019). Parasite range expansion can generally be explained by ecological fitting (Wells and Clark, 2019). ...
... This is understandable, as necessary information on host distributions and reliable prevalence values across regions are difficult to acquire for many parasite lineages and host species. However, such information is necessary for statistical frameworks to explicitly capture the hierarchical nature of host specificity and provide a baseline to understand the spatiotemporal dynamic of parasite shifting (Wells et al., 2015;Wells and Clark, 2019). If realized host specificity has a spatial dynamic, prevalence could be also treated as a labile trait that changes geographically. ...
... immune avoidance, coinfection) will act as major barriers to a parasite's realized host specificity affecting therefore, the proportion of infected individuals in a local host population. Thus, by disentangling contributions of parasite identity and environmental conditions to observed host-parasite interactions, one can gain a better understanding of the geographical basis for avian malaria spread (Wells et al., 2015;Clark et al., 2017;Fecchio et al., 2019b;Wells and Clark, 2019). ...
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Haemosporidian parasites of the genera Plasmodium, Leucocytozoon, and Haemoproteus are one of the most prevalent and widely studied groups of parasites infecting birds. Plasmodium is the most well-known haemosporidian as the avian parasite Plasmodium relictum was the original transmission model for human malaria and was also responsible for catastrophic effects on native avifauna when introduced to Hawaii. The past two decades has seen a dramatic increase in research on avian haemosporidian parasites as a model system to understand evolutionary and ecological parasite-host relationships. Despite haemosporidians being one the best studied groups of avian parasites their specialization among avian hosts and variation in prevalence amongst regions and host taxa are not fully understood. In this review we focus on describing the current phylogenetic and morphological diversity of haemosporidian parasites, their specificity among avian and vector hosts, and identifying the determinants of haemosporidian prevalence among avian species. We also discuss how these parasites might spread across regions due to global climate change and the importance of avian migratory behavior in parasite dispersion and subsequent diversification.
... Given the global distribution of invasive host species from the genus Mus and Rattus, that share parasites with a large range of wildlife in different areas [14], as well as the origin of these host species in Asia, one may expect T. muris to be present in SEA, as broadly assumed. However, geographic or environmental barriers may also disrupt hostparasite interactions and can result in distinct parasite species across geographic space [15,16]. ...
... Nevertheless, important details to conclude of the true presence/absence of T. muris in Asia (including our study region) is currently lacking, including missing molecular information from Chinese Trichuris from rodents, as the location of origin of the host species R. norvegicus before its worldwide expansion including Europe [48], together with lack of molecular information in the far west to corroborate this possible origin [6]. Our results suggest that for species such as the two cosmopolitan invasive rats R. norvegicus and R. rattus (present in SEA), which previously have been assumed to harbour T. muris across all its geographic range [14,44], associations with T. muris and conspecific parasites need to be reconsidered for its taxonomic validity. We report the newly described species from a range of different host species such that T. cossoni n. sp. is currently known to be shared by B. indica and Mus pahari and T. arrizabalagai n. sp. by R. rattus complex, R. norvegicus and Sundamys muelleri. ...
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The whipworm Trichuris muris is known to be associated with various rodent species in the northern hemisphere, but the species identity of whipworm infecting rodents in the Oriental region remains largely unknown. We collected Trichuris of Muridae rodents in mainland and insular Southeast Asia between 2008 and 2015 and used molecular and morphological approaches to identify the systematic position of new specimens. We discovered two new species that were clearly distinct from T. muris, both in terms of molecular phylogenetic clustering and morphological features, with one species found in Thailand and another one in Borneo. We named the new species from Thailand as Trichuris cossoni and the species from Borneo as Trichuris arrizabalagai. Molecular phylogeny using internal transcribed spacer region (ITS1-5.8S-ITS2) showed a divergence between T. arrizabalagai n. sp., T. cossoni n. sp. and T. muris. Our findings of phylogeographically distinct Trichuris species despite some globally distributed host species requires further research into the distribution of different species, previously assumed to belong to T. muris, which has particular relevance for using these species as laboratory model organisms.
... Moreover, parasites play key roles not only on individual hosts, but also on many ecology interactions, host population dynamics and community structure in many ecosystems (Price et al. 1986; Wood et al. 2007). In this scenario, the knowledge of the diversity and geographic distributions of parasite species at various spatial scales and host groups is the rst step towards understanding processes of global epidemiology and species conservation (du Toit et al. 2013; Wells et al. 2015). The phylum Apicomplexa is a highly diverse protist group of obligatory parasitic organisms. ...
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The knowledge of the diversity and geographic distribution of parasite species is the first step towards understanding processes of global epidemiology and species conservation. Despite recent increases in research on reptiles and amphibians haemosporidian and haemogregarine parasites, we still know little about their diversity and parasite-host interactions, especially in the Iberian Peninsula, where a few studies have been conducted. In this study, the haemosporidian and hemogregarine diversity and phylogenetic relationships of southwestern Iberian amphibians and reptiles were assessed using PCR approaches on 145 blood samples. The amphibians did not present any of both groups of parasites studied. Regarding the reptile species, six Hepatozoon and one Haemocystidum haplotypes were found infecting four different species, revealing new host records for these parasites. Among them, we found one new isolate Haemocystidium haplotype and three new isolates and a previously reported Hepatozoon haplotype from a north African snake. This finding suggests that some Hepatozoon parasites may not be host-specific and have large geographic ranges even crossing geographical barriers. These results increased the geographic distribution and the number of known host species of some reptile apicomplexan parasites, highlighting the great unexplored diversity of them in this region.
... Due to augmented accessibility of remote areas by growing human infrastructure and anthropogenic fragmentation of natural habitats, rates of direct interaction between humans and wildlife are increasing. This facilitates the introduction of alien and invasive pathogens to native ecosystems and, in reverse, the spillover of zoonotic pathogens from wild animals to humans (Lymbery et al., 2014;Watsa, 2020;Wells et al., 2015). ...
Article
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The relevance of emerging infectious diseases continues to grow worldwide as human activities increasingly extend into formerly remote natural areas. This is particularly noticeable on the island of Madagascar. As closest relatives to humans on the island, lemurs are of particular relevance as a potential origin of zoonotic pathogen spillover. Knowledge of pathogens circulating in lemur populations is, however, very poor. Particularly little is known about lemur hemoparasites. To infer host range, ecological and geographic spread of the recently described hemoparasitic nematode Lemurfilaria lemuris in northwestern Madagascar, a total of 942 individuals of two mouse lemur species (Microcebus murinus [n = 207] and Microcebus ravelobensis [n = 433]) and two rodent species (the endemic Eliurus myoxinus [n = 118] and the invasive Rattus rattus [n = 184]) were captured in two fragmented forest landscapes (Ankarafantsika National Park and Mariarano Classified Forest) in northwestern Madagascar for blood sample examination. No protozoan hemoparasites were detected by microscopic blood smear screening. Microfilaria were present in 1.0% (2/207) of M. murinus and 2.1% (9/433) of M. ravelobensis blood samples but not in rodent samples. Internal transcribed spacer 1 (ITS‐1) sequences were identical to an unnamed Onchocercidae species previously described to infect a larger lemur species, Propithecus verreauxi, about 650 km further south. In contrast to expectations, L. lemuris was not detected. The finding of a pathogen in a distantly related host species, at a considerable geographic distance from the location of its original detection, instead of a microfilaria species previously described for one of the studied host species in the same region, illustrates our low level of knowledge of lemur hemoparasites, their host ranges, distribution, modes of transmission, and their zoonotic potential. Our findings shall stimulate new research that will be of relevance for both conservation medicine and human epidemiology. A microscopic analysis of 942 blood smears from Microcebus murinus, M. ravelobensis and two rodent species from northwestern Madagascar revealed the presence of an unnamed Onchocercidae species with low prevalence (1.0%−2.1%) in both mouse lemur species, but not in the rodents. This microfilaria species was previously described to infect Propithecus verreauxi about 650 km further south. This pathogen therefore shows a wider geographical distribution than its hosts and a rather low host specificity within lemurs. An undescribed Onchocercidae gen.sp. was detected in the blood of two sympatric mouse lemur species, Microcebus murinus and M. ravelobensis (Cheirogaleidae). This microfilaria species was previously found in Propithecus verreauxi (Indriidae), demonstrating its large geographic distribution and low host specificity within lemurs. An undescribed Onchocercidae gen.sp. was detected in the blood of two sympatric mouse lemur species, Microcebus murinus and M. ravelobensis (Cheirogaleidae). This microfilaria species was previously found in Propithecus verreauxi (Indriidae), demonstrating its large geographic distribution and low host specificity within lemurs.
... The expansion and adaptations of invasive rodents, which can come from distant regions, even different continents, have a wide spectrum of ecological consequences, including the spread of parasites and pathogens. As the title of this Research Topic reflects, the parasites travel to these newly colonized areas as stowaways on a stowaway (1,2). ...
... musculus), which is native to southwestern Asia (65), is an invasive rodent with a dramatic impact on biodiversity, and human health and activities (66). Asian rodents of the genus Rattus have been implicated in the emergence and spread of infectious diseases affecting human health (67,68). In the Mediterranean region, the global prevalence of Leishmania infection in the Norway or brown rat (Rattus norvegicus), and the black or roof rat (Rattus rattus) is below 20% but not negligible (9.9 and 16.4%, respectively) ( Table 3). ...
Article
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Leishmaniosis infection begins when a phlebotomine sand fly vector inoculates pathogenic protozoan parasites of the genus Leishmania into a mammalian host. In the case of Leishmania infantum, the domestic dog is considered to be the main parasite reservoir, and canine leishmaniosis (CanL) has a high mortality rate in untreated dogs. Hundreds of cases of human leishmaniosis (HL) are reported in the world each year, the incidence in Europe being relatively low. Leishmaniosis control is primarily focused on the dog, combining methods that prevent sand fly bites and boost host resistance to infection. However, these measures are only partially effective and new solutions need to be found. One of the main factors limiting CanL and HL control is the existence of a sylvatic Leishmania transmission cycle that interacts with the domestic cycle maintained by dogs. It is suspected that the main reservoir of infection in wildlife are rodents, whose expansion and rapid population growth worldwide is increasing the risk of human and zoonotic pathogen transfer. The aim of this review is therefore to analyze reports in the literature that may shed light on the potential role of rodents in the leishmaniosis transmission cycle in the Mediterranean area. Following the general methodology recommended for reviews, six databases (Google Scholar, Ovid, PubMed, Science Direct, Scopus and Web of Science) were explored for the period January 1995 to December 2020. The results extracted from 39 publications that met the established inclusion criteria were analyzed. It was found that 23 species of rodents have been studied in nine countries of the Mediterranean basin. Of the 3,643 specimens studied, 302 tested positive for L. infantum infection by serology, microscopy and/or molecular techniques.
... Although research regarding biological invasions has expanded extensively in recent decades, less attention has been given to the role of parasites in this phenomenon. However, the interchange of parasites is of major concern, whether the transmission is from introduced to native species (spillover) or vice versa (spillback) (Wells et al. 2015). Parasites can have notable impact on host communities, ultimately shaping the biodiversity distribution and the structure of ecosystems (Tompkins et al. 2011). ...
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Invasive species can carry parasites to introduced locations, which may be key to understand the success or failure of species establishment and the invasive potential of introduced species. We compared the prevalence and infection levels of haemogregarine blood parasites between two sympatric congeneric species in Lisbon, Portugal: the invasive Italian wall lizard (Podarcis siculus) and the native green Iberian wall lizard (Podarcis virescens). The two species had significant differences in their infection levels: while P. virescens had high prevalence of infection (69.0%), only one individual of P. siculus was infected (3.7%), and while P. virescens exhibited an average intensity of 1.36%, the infected P. siculus individual had an infection rate of only 0.04%. Genetic analyses of 18S rRNA identified two different haemogregarine haplotypes in P. virescens. Due to the low levels of infection, we were not able to amplify parasite DNA from the infected P. siculus individual, although it was morphologically similar to those found in P. virescens. Since other studies also reported low levels of parasites in P. siculus, we hypothesize that this general lack of parasites could be one of the factors contributing to its competitive advantage over native lizard species and introduction success.
... The loss of parasites is frequently observed in species introductions and has been implicated as a factor promoting the establishment and spread of introduced species (the enemy/parasite release hypothesis; Keane & Crawley, 2002;Torchin et al., 2003). In their new range, non-natives can acquire unfamiliar parasites Criscione & Font, 2001;Gérard & Le Lannic, 2003;Torchin et al., 1996;Wells et al., 2015; reviewed in Kelly et al., 2009); similarly, introduced species may bring with them exotic parasites that can then infect naïve hosts in the new range (parasite spillover; Daszak et al., 2000;Elsner et al., 2011;Font & Tate, 1994;Miller et al., 2018;Prenter et al., 2004). ...
Article
By shuffling biogeographic distributions, biological invasions can both disrupt long‐standing associations between hosts and parasites and establish new ones. This creates natural experiments with which to study the ecology and evolution of host‐parasite interactions. In estuaries of the Gulf of Mexico, the white‐fingered mud crab (Rhithropanopeus harrisii) is infected by a native parasitic barnacle Loxothylacus panopaei (Rhizocephala), which manipulates host physiology and behavior. In the 1960s, L. panopaei was introduced to the Chesapeake Bay and has since expanded along the southeastern Atlantic coast, while host populations in the northeast have so far been spared. We use this system to test the host’s transcriptomic response to parasitic infection and investigate how this response varies with the parasite’s invasion history, comparing populations representing (1) long‐term sympatry between host and parasite, (2) new associations where the parasite has invaded during the last sixty years, and (3) naïve hosts without prior exposure. A comparison of parasitized and control crabs revealed a core response, with widespread downregulation of transcripts involved in immunity and molting. The transcriptional response differed between hosts from the parasite’s native range and where it is absent, consistent with previous observations of increased susceptibility in populations lacking exposure to the parasite. Crabs from the parasite’s introduced range, where prevalence is highest, displayed the most dissimilar response, possibly reflecting immune priming. These results provide molecular evidence for parasitic manipulation of host phenotype and the role of gene regulation in mediating host‐parasite interactions.
... In a changing world where insects are in severe decline and diseases are spreading faster than ever before, understanding the factors governing the distributions of parasites of insects is of particular interest (e.g. Cable et al., 2017;Vogel, 2017;Wells et al., 2015). ...
Article
The role of biotic interactions in shaping species distributions is a cornerstone of biogeographic theory; yet, it remains elusive. Such interactions are more likely to have an influence on organisms with obligate associations, such as hosts and their parasites. Whereas abiotic conditions may affect the abundance and distribution of parasites in ways similar to free‐living species, attributes of the host could also play a part. Here, we focus on parasitic water mites and their dragonfly and damselfly hosts, and use a hierarchical Bayesian model to examine the relative influence of the abiotic environment and biotic factors such as local host community structure and individual host characteristics on parasite intensity along a broad‐scale environmental gradient. Specifically, we assessed how climate, surrounding vegetation, water chemistry, host community structure as well the relative abundance and body mass of host species affected the intensity of parasitism on individual hosts along a latitudinal gradient. We found that water chemistry and body mass of the host were the best predictors of variation in parasite intensity among hosts. High parasite intensity was observed in hosts sampled from lakes with high pH, dissolved oxygen, and conductivity. Additionally, we found that the intensity of parasitism was strongly influenced by host species identity. In particular, body mass, which shows strong phylogenetic signal, was negatively related to parasite intensity. It may be that larger species, or individuals within species, are more immune to high level of parasitism and/or body mass is correlated with other traits of the host which relate to immunity. Considering both the abiotic environment and attributes of host species is necessary to understand why certain host individuals and locations exhibit more intense parasitism. Amid widespread decline of insect populations worldwide, some of which are attributed to pathogens and parasites, models predicting rates of parasitism in space and time could become an essential tool for guiding management and conservation efforts.
... As noted by Pilosof et al. [75] and Wells et al. [76], the parasite assemblage of a given spreading host species often highly depends on the host-parasite network met by this species in a newly colonised area. Since G. roeselii is a species expanding its range, the comparison with the study of Grabner et al. [5] may help understand if G. roeselii shares parasitic fauna with local hosts. ...
Thesis
Title: Evolutionary histories of symbioses between microsporidia and their amphipod hosts : contribution of studying two hosts over their geographic ranges.Keywords: Symbioses, Phylogeny, Phylogeography, Amphipods, Host-Parasite, MicrosporidiaAbstract: Microsporidia are obligate endoparasites, exploiting their hosts with either vertical or horizontal transmission. While the former may promote co-speciation and host-specificity, the latter may promote shifts between host species. Freshwater amphipods are hosts for many microsporidian species, but no general pattern of host specificity and co-diversification is known.In my PhD work microsporidian infections, identified with SSU rDNA, were assessed in two Gammarus species complexes, G. roeselii and G. balcanicus , over their full geographic ranges (each c. 100 sites and 2000 individuals) in aim of (i) exploring the microsporidian diversity present in both hosts and their phylogenetic relationships; (ii) testing if the host phylogeographic history might have impacted host-parasite association (co-diversifications or recent host-shifts from local fauna); (iii) proposing the host-parasite evolutionary history scenarios to explain the diversity and co-bio-geographical pattern observed in the two host species between using N. granulosis as a model.The SSU rDNA marker revealed a high number of microsporidian variants (i.e. haplogroups, 24 and 54, respectively), clustered into 18 species-level taxa, almost all being shared between the two host species. However, many microsporidian haplogroups within a given parasite species are host-specific, suggesting host-parasite co-variation. Within each host species-complex, while the confrontation between hosts and parasites phylogeography suggested some degrees of co-diversification, these patterns remain to be confirmed, mainly as SSU rDNA reached its limits in phylogenetic information content in that matter.Strikingly, almost all of these microsporidia taxa were previously detected in other gammarids, mainly within the genus Gammarus, but also in other genera of Gammaridae. Some were already clearly recognised parasite taxa associated with amphipods: Nosema granulosis, Dictyocoela roeselum, D. muelleri, D. roeselum, D. duebenum, D. berillonum, Cucumispora roeselum, C. ornata, C. dikerogammari, Microsporidium sp 515 and Microsporidium sp 505). Many times, my results increased host taxonomic spectrums and extended geographic ranges (often widely). Some other taxa were known to be extremely rare, having scarce literature records often with few or even very few geographic records and being not fully described. My PhD work either extend host taxonomic spectrum and/or deeply extend geographic ranges for these taxa. It allowed a reappraisal for such taxa, changing their status from puzzling anecdotic association to potentially overlooked established associations for amphipods.
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Urbanization has paved the way for the spread of commensal rodents at global scale. However, it is largely unknown how these species use tropical anthropogenic landscapes originally covered with forests and inhabited by diverse small mammal assemblages. We surveyed non-flying small mammals in various urban and suburban habitat types and adjacent forest in the tropical town of Kota Kinabalu in Borneo. We used occupancy and polynomial regression models to determine variation in species occurrences along gradients of land-use intensity. Müller’s sundamys (Sundamys muelleri) was the only native small mammal species found in urban and suburban landscapes with a continuous decrease in occurrence probability from forests to urban habitats. The invasive Asian black rat (Rattus rattus species complex) and the invasive Asian house shrew (Suncus murinus) had the highest occurrence probabilities in habitats of intermediate land-use intensity, but Asian black rats are also likely to occasionally invade forested habitats and occupied urban habitats in sympatry with the Norway rat (Rattus norvegicus). In urban and suburban habitats, fallow land possibly favoured the occurrence of S. muelleri and S. murinus. Other native small mammal species (Muridae, Sciuridae, Tupaiidae) were found only in forested areas. Our study shows that native small mammals found in forest are largely replaced by invasive species in urban and suburban habitats. Due to their occurrence in habitats of various land use intensities, S. muelleri and R. rattus comprise central links between forest wildlife and urban species, an association that is important to consider in studies of parasite and disease transmission dynamics.
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Impacts of environmental changes on zoonotic disease risk are the subject of speculation, but lack a coherent framework for understanding environmental drivers of pathogen transmission from animal hosts to humans. We review how environmental factors affect the distributions of zoonotic agents and their transmission to humans, exploring the roles they play in zoonotic systems. We demonstrate the importance of capturing the distributional ecology of any species involved in pathogen transmission, defining the environmental conditions required, and the projection of that niche onto geography. We further review how environmental changes may alter the dispersal behaviour of populations of any component of zoonotic disease systems. Such changes can modify relative importance of different host species for pathogens, modifying contact rates with humans.
Article
1. Using data on the spatial distribution of the British avifauna, we address three basic questions about the spatial structure of assemblages: (i) Is there a relationship between species richness (alpha diversity) and spatial turnover of species (beta diversity)? (ii) Do high richness locations have fewer species in common with neighbouring areas than low richness locations?, and (iii) Are any such relationships contingent on spatial scale (resolution or quadrat area), and do they reflect the operation of a particular kind of species-area relationship (SAR)? 2. For all measures of spatial turnover, we found a negative relationship with species richness. This held across all scales, with the exception of turnover measured as β sim. 3. Higher richness areas were found to have more species in common with neighbouring areas. 4. The logarithmic SAR fitted better than the power SAR overall, and fitted significantly better in areas with low richness and high turnover. 5. Spatial patterns of both turnover and richness vary with scale. The finest scale richness pattern (10 km) and the coarse scale richness pattern (90 km) are statistically unrelated. The same is true of the turnover patterns. 6. With coarsening scale, locations of the most species-rich quadrats move north. This observed sensitivity of richness 'hotspot' location to spatial scale has implications for conservation biology, e.g. the location of a reserve selected on the basis of maximum richness may change considerably with reserve size or scale of analysis. 7. Average turnover measured using indices declined with coarsening scale, but the average number of species gained or lost between neighbouring quadrats was essentially scale invariant at 10-13 species, despite mean richness rising from 80 to 146 species (across an 81-fold area increase). We show that this kind of scale invariance is consistent with the logarithmic SAR.
Article
Pathogen spread or &apos;spillover&apos; can occur when heavily infected, domestic hosts interact with closely-related wildlife populations. Commercially-produced bumble bees used in greenhouse pollination often have higher levels of various pathogens than wild bumble bees. These pathogens may spread to wild bees when commercial bees escape from greenhouses and interact with their wild counterparts at nearby flowers. We examined the prevalence of four pathogens in wild bumble bee populations at locations near and distant to commercial greenhouses in southern Ontario, Canada. Bumble bees collected near commercial greenhouses were more frequently infected by those pathogens capable of being transmitted at flowers (Crithidia bombi and Nosema bombi) than bees collected at sites away from greenhouses. We argue that the spillover of pathogens from commercial to wild bees is the most likely cause of this pattern and we discuss the implications of such spillover for bumble bee conservation. (c) 2005 Elsevier Ltd. All rights reserved.
Article
The rate of emergence for emerging infectious diseases has increased dramatically over the last century, and research findings have implicated wildlife as an importance source of novel pathogens. However, the role played by domestic animals as amplifiers of pathogens emerging from the wild could also be significant, influencing the human infectious disease transmission cycle. The impact of domestic hosts on human disease emergence should therefore be ascertained. Here, using three independent datasets we showed positive relationships between the time since domestication of the major domesticated mammals and the total number of parasites or infectious diseases they shared with humans. We used network analysis, to better visualize the overall interactions between humans and domestic animals (and amongst animals) and estimate which hosts are potential sources of parasites/pathogens for humans (and for all other hosts) by investigating the network architecture. We used centrality, a measure of the connection amongst each host species (humans and domestic animals) in the network, through the sharing of parasites/pathogens, where a central host (i.e. high value of centrality) is the one that is infected by many parasites/pathogens that infect many other hosts in the network. We showed that domesticated hosts that were associated a long time ago with humans are also the central ones in the network and those that favour parasites/pathogens transmission not only to humans but also to all other domesticated animals. These results urge further investigation of the diversity and origin of the infectious diseases of domesticated animals in their domestication centres and the dispersal routes associated with human activities. Such work may help us to better understand how domesticated animals have bridged the epidemiological gap between humans and wildlife.
Article
Several floral microbes are known to be pathogenic to plants or floral visitors such as pollinators. Despite the ecological and economic importance of pathogens deposited in flowers, we often lack a basic understanding of how floral traits influence disease transmission. Here, we provide the first systematic review regarding how floral traits attract vectors (for plant pathogens) or hosts (for animal pathogens), mediate disease establishment and evolve under complex interactions with plant mutualists that can be vectors for microbial antagonists. Attraction of floral visitors is influenced by numerous phenological, morphological and chemical traits, and several plant pathogens manipulate floral traits to attract vectors. There is rapidly growing interest in how floral secondary compounds and antimicrobial enzymes influence disease establishment in plant hosts. Similarly, new research suggests that consumption of floral secondary compounds can reduce pathogen loads in animal pollinators. Given recent concerns about pollinator declines caused in part by pathogens, the role of floral traits in mediating pathogen transmission is a key area for further research. We conclude by discussing important implications of floral transmission of pathogens for agriculture, conservation and human health, suggesting promising avenues for future research in both basic and applied biology.