Disease or pathogen risk prioritisations aid understanding of infectious agent impact within surveillance or mitigation and biosecurity work, but take significant development. Previous work has shown the H-(Hirsch-)index as an alternative proxy. We present a weighted risk analysis describing infectious pathogen impact for human health (human pathogens) and well-being (domestic animal pathogens) using an objective, evidence-based, repeatable approach; the H-index. This study established the highest H-index European pathogens. Commonalities amongst pathogens not included in previous surveillance or risk analyses were examined. Differences between host types (humans/animals/zoonotic) in pathogen H-indices were explored as a One Health impact indicator. Finally, the acceptability of the H-index proxy for animal pathogen impact was examined by comparison with other measures. 57 pathogens appeared solely in the top 100 highest H-indices (1) human or (2) animal pathogens list, and 43 occurred in both. Of human pathogens, 66 were zoonotic and 67 were emerging, compared to 67 and 57 for animals. There were statistically significant differences between H-indices for host types (humans, animal, zoonotic), and there was limited evidence that H-indices are a reasonable proxy for animal pathogen impact. This work addresses measures outlined by the European Commission to strengthen climate change resilience and biosecurity for infectious diseases. The results include a quantitative evaluation of infectious pathogen impact, and suggest greater impacts of human-only compared to zoonotic pathogens or scientific under-representation of zoonoses. The outputs separate high and low impact pathogens, and should be combined with other risk assessment methods relying on expert opinion or qualitative data for priority setting, or could be used to prioritise diseases for which formal risk assessments are not possible because of data gaps.
Genes of the major histocompatibility complex (MHC) encode proteins that recognize foreign antigens and are thus crucial for immune response. In a population of a single host species, parasite-mediated selection drives MHC allelic diversity. However, in a community-wide context, species interactions may modulate selection regimes because the prevalence of a given parasite in a given host may depend on its prevalence in other hosts. By combining network analysis with immunogenetics, we show that host species infected by similar parasites harbour similar alleles with similar frequencies. We further show, using a Bayesian approach, that the probability of mutual occurrence of a functional allele and a parasite in a given host individual is nonrandom and depends on other host-parasite interactions, driving co-evolution within subgroups of parasite species and functional alleles. Therefore, indirect effects among hosts and parasites can shape host MHC diversity, scaling it from the population to the community level.
Interest in bat-borne diseases and parasites has grown in the past decade over concerns for human health. However, the drivers of parasite diversity among bat host species are understudied as are the links between parasite richness and emerging risks. Thus, we aimed at exploring factors that explain macro and microparasite species richness in bats from Southeast Asia, a hotspot of emerging infectious diseases. First, we identified bat species that need increased sampling effort for pathogen discovery. Our approach highlights pathogen investigation disparities among species within the same genus, such as Rhinolophus and Pteropus. Secondly, comparative analysis using independent contrasts method allowed the identification of likely factors explaining parasite and viral diversity of bats. Our results showed a key role of bat distribution shape, an index of the fragmentation of bat distribution, on parasite diversity, linked to a decrease for both viral and endoparasite species richness. We discuss how our study may contribute to a better understanding of the link between parasite species richness and emergence.
Southeast Asia is a biodiversity hotspot that harbours many species of rodents, including some that live in close contact with humans. They host helminth parasites, some of which are of zoonotic importance. It is therefore important to understand the factors that influence the richness of the helminths parasitizing rodents. The specific objectives of this study were to evaluate rodent species as a factor determining helminth richness in rodent assemblages, to identify the major rodent helminth reservoir species and to explore the influence of habitat on helminth richness. We estimated helminth species richness using a large dataset of 18 rodent species (1,651 individuals) originating from Southeast Asia and screened for helminth parasites. The use of an unbiased estimator shows that the helminth species richness varies substantially among rodent species and across habitats. We confirmed this pattern by investigating the number of helminth species per individual rodent in all rodent species, and specifically in the two mitochondrial lineages Rattus tanezumi and R. tanezumi R3, which were captured in all habitats.
The prion protein (PrP) when misfolded into the pathogenic conformer PrP(Sc) is the major causative agent of several lethal transmissible spongiform encephalopathies in mammals. Studies of evolutionary pressure on the corresponding gene using different datasets have yielded conflicting results. In addition, putative PrP or PrP interacting partners with strong similarity to PrP such as the doppel protein have not been examined to determine if the same evolutionary mechanisms apply to prion paralogs or if there are coselected sites that might indicate how and where the proteins interact. We examined several taxonomic groups that contain model organisms of prion diseases focusing on primates, bovids, and an expanded dataset of rodents for selection pressure on the prion gene (PRNP) and doppel gene (PRND) individually and for coevolving sites within. Overall, the results clearly indicate that both proteins are under strong selective constraints with relaxed selection on amino acid residues connecting ?-helices 1 and 2.
Leptospirosis is the most common bacterial zoonoses and has been identified as an important emerging global public health problem in Southeast Asia. Rodents are important reservoirs for human leptospirosis, but epidemiological data is lacking.
The emergence of colistin-resistant Klebsiella pneumoniae (CRKP) is a major public health concern worldwide. In this study, the prevalence and molecular basis of colistin resistance in CRKP isolated from healthy individuals and patients in Lao PDR, Thailand, Nigeria and France were investigated. Stool samples were screened by culture for the presence of colistin-resistant Klebsiella spp. Whole-genome sequence analysis was used to decipher the molecular mechanism of colistin resistance in a blaNDM-1-positive in vitro-selected CRKP mutant. PCR amplification and sequencing of the mgrB genetic environment was performed for all CRKP isolates as well as control colistin-susceptible K. pneumoniae (CSKP) isolates recovered from the same stools. A total of 869 stool samples were screened for colistin-resistant Klebsiella spp., yielding 32 CRKP and 2 colistin-resistant Klebsiella oxytoca. Comparative whole-genome sequence analysis revealed that an in vitro-selected CRKP mutant had an insertion sequence in its mgrB gene, as well as missense mutations in other selected clones. Of the 34 colistin-resistant Klebsiella spp. isolates, 14 (41.2%; 13 CRKP and 1 K. oxytoca) from the four countries also had various defects in their mgrB genes, but no such defects were found in the CSKP controls (P<10(-4)). Few mutations were observed in pmrAB compared with mgrB among the CRKP isolates. The worldwide emergence of CRKP is a major public health concern. Detection and surveillance of such strains are warranted to prevent an uncontrollable pandemic. Inactivation of the PhoP/PhoQ regulator gene mgrB is associated with ?40% of colistin resistance among the CRKP isolates observed in this study.
We studied the effect of host gender and body mass on species richness of flea infracommunities in nine rodent host species from three biomes (temperate zone of central Europe, desert of the Middle East and the tropics of East Africa). Using season- and species-specific generalized linear mixed models and controlling for year-to-year variation, spatial clustering of rodent sampling and over-dispersion of the data, we found inconsistent associations between host characteristics and flea species richness. We found strong support for male-biased flea parasitism, especially during the reproductive period (higher species richness in male hosts than in females) in all considered European rodents (Apodemus agrarius, Myodes glareolus and Microtus arvalis) and in one rodent species from the Middle East (Dipodillus dasyurus). In contrast, two of three African rodent species (Lophuromys kilonzoi and Praomys delectorum) demonstrated a trend of female-biased flea species richness. Positive associations between body mass and the number of flea species were detected mainly in males (five of nine species: A. agrarius, M. glareolus, M. arvalis, D. dasyurus and Mastomys natalensis) and not in females (except for M. natalensis). The results of this study support earlier reports that gender-biased, in general, and male-biased, in particular, infestation by ectoparasites is not a universal rule. This suggests that mechanisms of parasite acquisition by an individual host are species-specific and have evolved independently in different rodent host-flea systems.
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 favor 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.
Solution hybridization capture methods utilize biotinylated oligonucleotides as baits to enrich homologous sequences from next generation sequencing (NGS) libraries. Coupled with NGS, the method generates kilo to gigabases of high confidence consensus targeted sequence. However, in many experiments, a non-negligible fraction of the resulting sequence reads are not homologous to the bait. We demonstrate that during capture, the bait-hybridized library molecules add additional flanking library sequences iteratively, such that baits limited to targeting relatively short regions (e.g. few hundred nucleotides) can result in enrichment across entire mitochondrial and bacterial genomes. Our findings suggest that some of the off-target sequences derived in capture experiments are non-randomly enriched, and that CapFlank will facilitate targeted enrichment of large contiguous sequences with minimal prior target sequence information.
The rising incidence of emerging infectious diseases (EID) is mostly linked to biodiversity loss, changes in habitat use and increasing habitat fragmentation. Bats are linked to a growing number of EID but few studies have explored the factors of viral richness in bats. These may have implications for role of bats as potential reservoirs. We investigated the determinants of viral richness in 15 species of African bats (8 Pteropodidae and 7 microchiroptera) in Central and West Africa for which we provide new information on virus infection and bat phylogeny. We performed the first comparative analysis testing the correlation of the fragmented geographical distribution (defined as the perimeter to area ratio) with viral richness in bats. Because of their potential effect, sampling effort, host body weight, ecological and behavioural traits such as roosting behaviour, migration and geographical range, were included into the analysis as variables. The results showed that the geographical distribution size, shape and host body weight have significant effects on viral richness in bats. Viral richness was higher in large-bodied bats which had larger and more fragmented distribution areas. Accumulation of viruses may be related to the historical expansion and contraction of bat species distribution range, with potentially strong effects of distribution edges on virus transmission. Two potential explanations may explain these results. A positive distribution edge effect on the abundance or distribution of some bat species could have facilitated host switches. Alternatively, parasitism could play a direct role in shaping the distribution range of hosts through host local extinction by virulent parasites. This study highlights the importance of considering the fragmentation of bat species geographical distribution in order to understand their role in the circulation of viruses in Africa.
A growing number of studies are reporting simultaneous infections by parasites in many different hosts. The detection of whether these parasites are significantly associated is important in medicine and epidemiology. Numerous approaches to detect associations are available, but only a few provide statistical tests. Furthermore, they generally test for an overall detection of association and do not identify which parasite is associated with which other one. Here, we developed a new approach, the association screening approach, to detect the overall and the detail of multi-parasite associations. We studied the power of this new approach and of three other known ones (i.e., the generalized chi-square, the network and the multinomial GLM approaches) to identify parasite associations either due to parasite interactions or to confounding factors. We applied these four approaches to detect associations within two populations of multi-infected hosts: (1) rodents infected with Bartonella sp., Babesia microti and Anaplasma phagocytophilum and (2) bovine population infected with Theileria sp. and Babesia sp. We found that the best power is obtained with the screening model and the generalized chi-square test. The differentiation between associations, which are due to confounding factors and parasite interactions was not possible. The screening approach significantly identified associations between Bartonella doshiae and B. microti, and between T. parva, T. mutans, and T. velifera. Thus, the screening approach was relevant to test the overall presence of parasite associations and identify the parasite combinations that are significantly over- or under-represented. Unraveling whether the associations are due to real biological interactions or confounding factors should be further investigated. Nevertheless, in the age of genomics and the advent of new technologies, it is a considerable asset to speed up researches focusing on the mechanisms driving interactions between parasites.
Despite increasing control measures, numerous parasitic and infectious diseases are emerging, re-emerging or causing recurrent outbreaks particularly in Asia and the Pacific region, a hot spot of both infectious disease emergence and biodiversity at risk. We investigate how biodiversity affects the distribution of infectious diseases and their outbreaks in this region, taking into account socio-economics (population size, GDP, public health expenditure), geography (latitude and nation size), climate (precipitation, temperature) and biodiversity (bird and mammal species richness, forest cover, mammal and bird species at threat). We show, among countries, that the overall richness of infectious diseases is positively correlated with the richness of birds and mammals, but the number of zoonotic disease outbreaks is positively correlated with the number of threatened mammal and bird species and the number of vector-borne disease outbreaks is negatively correlated with forest cover. These results suggest that, among countries, biodiversity is a source of pathogens, but also that the loss of biodiversity or its regulation, as measured by forest cover or threatened species, seems to be associated with an increase in zoonotic and vector-borne disease outbreaks.
Network theory is gaining momentum as a descriptive tool in community ecology. Because organisms with the same lifestyle can still exhibit ecological differences, it is crucial to determine the scale at which networks should be described. Here we show that networks of hosts (mammals) and parasites (ectoparasitic gamasid mites) differ when either facultative or obligatory parasites only are considered. More importantly, the structure of these networks is opposed, with obligatory parasites networks being more modular, and facultative parasites networks being more nested. Our results have consequences for the way we define which species to include in ecological networks, which we discuss in the light of community ecology and epidemiology.
In vertebrates, it has been repeatedly demonstrated that genes encoding proteins involved in pathogen-recognition by adaptive immunity (e.g. MHC) are subject to intensive diversifying selection. On the other hand, the role and the type of selection processes shaping the evolution of innate-immunity genes are currently far less clear. In this study we analysed the natural variation and the evolutionary processes acting on two genes involved in the innate-immunity recognition of Microbe-Associated Molecular Patterns (MAMPs).
During a study of the helminth fauna of 1,643 rodents trapped along the Mekong River (Thailand, Lao Peoples Democratic Republic and Cambodia) in 2008-2011, the spirurid nematode Physaloptera ngoci Le-Van-Hoa, 1961 was recovered with an overall prevalence of 2.8%. Based on the original description, it was identified in nine of 23 different Murinae host species and is here reported for the first time from these three countries. A scanning electron microscopy study provides additional morphological data.
Several studies provide evidence of a link between vector-borne disease outbreaks and El Niño driven climate anomalies. Less investigated are the effects of the North Atlantic Oscillation (NAO). Here, we test its impact on outbreak occurrences of 13 infectious diseases over Europe during the last fifty years, controlling for potential bias due to increased surveillance and detection. NAO variation statistically influenced the outbreak occurrence of eleven of the infectious diseases. Seven diseases were associated with winter NAO positive phases in northern Europe, and therefore with above-average temperatures and precipitation. Two diseases were associated with the summer or spring NAO negative phases in northern Europe, and therefore with below-average temperatures and precipitation. Two diseases were associated with summer positive or negative NAO phases in southern Mediterranean countries. These findings suggest that there is potential for developing early warning systems, based on climatic variation information, for improved outbreak control and management.
The distribution of parasites among individual hosts is characterised by high variability that is believed to be a result of variations in host traits. To find general patterns of host traits affecting parasite abundance, we studied flea infestation of nine rodent species from three different biomes (temperate zone of central Europe, desert of Middle East and tropics of East Africa). We tested for independent and interactive effects of host sex and body mass on the number of fleas harboured by an individual host while accounting for spatial clustering of host and parasite sampling and temporal variation. We found no consistent patterns of the effect of host sex and body mass on flea abundance either among species within a biome or among biomes. We found evidence for sex-biased flea infestation in just five host species (Apodemus agrarius, Myodes glareolus, Microtus arvalis, Gerbillus andersoni, Mastomys natalensis). In six rodent species, we found an effect of body mass on flea abundance (all species mentioned above and Meriones crassus). This effect was positive in five species and negative in one species (Microtus arvalis). In M. glareolus, G. andersoni, M. natalensis, and M. arvalis, the relationship between body mass and flea abundance was mediated by host sex. This was manifested in steeper change in flea abundance with increasing body mass in male than female individuals (M. glareolus, G. andersoni, M. natalensis), whereas the opposite pattern was found in M. arvalis. Our findings suggest that sex and body mass are common determinants of parasite infestation in mammalian hosts, but neither of them follows universal rules. This implies that the effect of host individual characteristics on mechanisms responsible for flea acquisition may be manifested differently in different host species.
A new species of the genus Oxynema Linstow 1899, is described from the African sciurids Xerus erythropus and Heliosciurus gambianus. Oxynema xerusi n. sp. is characterized by the lack of cervical and caudal alae and by having unequal spicules. It differs from the closest species, Oxynema linstowi Deshmukh, 1987 and Oxynema bioccai Campana-Rouget, 1956, by the number, shape, and distribution of the caudal papillae, the length of the spicules, and the ratio of spicule length to body length.
The phylogeny of monogeneans of the genus Thaparocleidus that parasitize the gills of Pangasiidae in Borneo and Sumatra was inferred from molecular data to investigate parasite speciation. The phylogeny of the Pangasiidae was also reconstructed in order to investigate host-parasite coevolutionary history. The monophyly of Thaparocleidus parasitizing Pangasiidae was confirmed. Low intraspecies molecular variability was observed in three Thaparocleidus species collected from geographically distant localities. However, a high intraspecies molecular variability was observed in two Thaparocleidus species suggesting that these species represent a complex of species highly similar in morphology. Distance-based and tree-based methods revealed a significant global fit between parasite and host phylogenies. Parasite duplication (i.e., intrahost speciation) was recognized as the most common event in Thaparocleidus, while the numbers of cospeciation and host switches were lower and similar to each other. When collapsing nodes correspond to duplication cases, our results suggest host switches in the Thaparocleidus-Pangasiidae system precluding congruence between host and parasite trees. We found that the morphometric variability of the parasite attachment organ is not linked to phylogeny, suggesting that the attachment organ is under adaptive constraint. We showed that haptor morphometry is linked to host specificity, whereby nonspecific parasites display higher morphometric variability than specialists.
Predicting habitats prone to favor disease transmission is challenging due to confounding information on habitats, reservoirs, and diseases. Comparative analysis, which aims at investigating ecological and evolutionary patterns among species, is a tool that may help. The emergence of zoonotic pathogens is a major health concern and is closely linked to habitat modifications by human activities. Risk assessment requires a better knowledge of the interactions between hosts, parasites, and the landscape.
Field parasitological studies consistently demonstrate the reality of polyparasitism in natural systems. However, only recently, studies from ecological and evolutionary fields have emphasised a broad spectrum of potential multiple infections-related impacts. The main goal of our review is to reunify the different approaches on the impacts of polyparasitism, not only from laboratory or human medical studies but also from field or theoretical studies. We put forward that ecological and epidemiological determinants to explain the level of polyparasitism, which regularly affects not only host body condition, survival or reproduction but also host metabolism, genetics or immune investment. Despite inherent limitations of all these studies, multiple infections should be considered more systematically in wildlife to better appreciate the importance of parasite diversity in wildlife, cumulative effects of parasitism on the ecology and evolution of their hosts.
Parasite diversity is hypothesized to act on host life-history traits through investment in immunity. In order to incorporate the diversity of the parasite community that an individual host or a host species may face, two indices can be used: Taxonomic Species Richness and Taxonomic Entropy, where the taxonomic information is incorporated with the taxonomic weight. We tested whether these indices correlate with several morphological traits potentially implicated in immune defence and in reproduction, using data on gastrointestinal helminths and their rodent hosts sampled in Southeast Asia. We found no relationship between parasite diversity indices and either spleen mass or testes size at the intraspecific level, i.e. at the level of individuals. At the interspecific level, we found no relationship between the parasite diversity indices and testes size. However, we found that female spleen mass is significantly influenced by the specific species richness of parasites, whereas male spleen mass is influenced by individual mean parasite diversity indices. We concluded that female spleen mass may have evolved in response to gastrointestinal helminth pressure acting at species levels, while in males, the individual spleen mass could be constrained by other factors, such as the blood storage function of the spleen.
Abundance-occupancy and abundance-variance relationships are two of the most general macroecological patterns capturing essential fundamentals of the structuring of species distributions and are widely documented for free-living animal and plant species populations at different spatial scales. However, empirical data for parasites have been gathered using appropriate sampling designs only recently. We performed analyses across species of the variation in infection parameters and patterns of aggregation of the most widespread parasites in the marine sparid fish Boops boops across seven localities of two marine biogeographical regions, the North East Atlantic and the Mediterranean. We used a large dataset of multiple population samples replicated over time for 20 parasite species and carried out assessments both intraspecifically and interspecifically, across taxonomic and ecological groupings. This taxonomically diverse complex of species representing five major metazoan higher taxa with differing transmission ecologies allowed us to assess the effect of taxonomic and ecological determinants on the abundance-occupancy and abundance-variance relationships in the model marine host-parasite system. The results revealed that: (i) a power function, relating spatial variance to mean abundance, represents a suitable model for the spatial distribution of the species; (ii) prevalence, abundance and the degree of spatial heterogeneity are true species characteristics and differ consistently between higher level taxonomic groupings; (iii) infection parameters and abundance-variance relationship are dependent on host specificity and regional distribution patterns of the parasites; and (iv) the observed infection parameters agree well with predictions from the epidemiological negative binomial abundance-occupancy model built on parameters of Taylors power law both within and across species.
Orientia tsutsugamushi, an obligate intracellular bacterium closely related to the genus Rickettsia, is the causative agent of scrub typhus, a major cause of febrile illness in rural areas of Asia-Pacific region. Scrub typhus is transmitted by the bite of infected mites of the genus Leptotrombidium. The region of the 56-kDa TSA gene spanning from variable domain I (VDI) to variable domain IV (VDIV) was sequenced and used for genotyping 77 O. tsutsugamushi samples from human patients confirmed with scrub typhus from 2001 to 2003 and 2009 to 2010 in different regions of Thailand. These sequences were also compared to previously published 56-kDa TSA sequences. Only 4 genotypes out of 8 previously reported in Thailand were identified, i.e. Karp, JG-v, TA763 and Kato, respectively. Two strains were not associated with known genotypes but were closely related to Taiwanese strains. The Karp genotype was confirmed as the predominant clade. The JG-v and TA763 genotypes, in contrast to other studies, also were found. The genotype TA716 was not found, except for one strain previously described.
The basic function of the immune system is to protect an organism against infection in order to minimize the fitness costs of being infected. According to life-history theory, energy resources are in a trade-off between the costly demands of immunity and other physiological demands. Concerning fish, both physiology and immunity are influenced by seasonal changes (i.e. temporal variation) associated to the changes of abiotic factors (such as primarily water temperature) and interactions with pathogens and parasites. In this study, we investigated the potential associations between the physiology and immunocompetence of common carp (Cyprinus carpio) collected during five different periods of a given year. Our sampling included the periods with temporal variability and thus, it presented a different level in exposure to parasites. We analyzed which of two factors, seasonality or parasitism, had the strongest impact on changes in fish physiology and immunity.
We discuss geographical distribution and phylogeny of Dactylogyridea (Monogenea) parasitizing Cichlidae to elucidate their hosts history. Although mesoparasitic Monogenea (Enterogyrus spp.) show typical vicariant distribution, ectoparasitic representatives from different continents are not considered sister taxa, hence their distribution cannot result from vicariance alone. Because of the close host-parasite relationship, this might indicate that present-day cichlid distribution may also reflect dispersal through coastal or brackish waters. Loss of ectoparasites during transoceanic migration, followed by lateral transfer from other fish families might explain extant host-parasite associations. Because of its mesoparasitic nature, hence not subject to salinity variations of the hosts environment, Enterogyrus could have survived marine migrations, intolerable for ectoparasites. Host-switches and salinity transitions may be invoked to explain the pattern revealed by a preliminary morphological phylogeny of monogenean genera from Cichlidae and other selected Monogenea genera, rendering the parasite distribution explicable under both vicariance and dispersal. Testable hypotheses are put forward in this parasitological approach to cichlid biogeography. Along with more comprehensive in-depth morphological phylogeny, comparison with molecular data, clarifying dactylogyridean evolution on different continents and from various fish families, and providing temporal information on host-parasite history, are needed to discriminate between the possible scenarios.
We studied the co-occurrence of flea species in infracommunities of 16 rodents from four regions (South Africa, Tanzania, central Europe and western Siberia) using null models, and predicted that flea co-occurrences will be expressed more strongly in male than in female hosts. We examined patterns of co-occurrence (measured as the C score) in infracommunities of fleas that are parasitic on male and female hosts by comparing co-occurrence frequencies with those expected by chance. When a significant degree of nonrandomness in flea co-occurrences was detected, it indicated aggregative infracommunity structure. In Tanzanian rodents, no significant flea co-occurrences were detected in either male or female hosts. In a South African rodent, significant flea co-occurrences were not detected in males, but were found in females in some localities. In Palaearctic rodents, significant nonrandomness was detected either equally for males and females or more frequently in males than in females. Meta-analyses demonstrated that the frequency of the detection of nonrandomness in flea co-occurrences was significantly higher in male than in female hosts. The values of the standardized effect size (SES) for the C score differed significantly among host species, but not between host genders. When the Palaearctic hosts were analyzed separately, the effects of both host gender and species appeared to be significant, with the SES values for the C score in males being smaller than those in females. The strength of the gender difference in the manifestation of flea community structure increased with increasing gender difference in flea species richness, and with decreasing gender difference in flea prevalence for the Palaearctic hosts. We conclude that male hosts are the main drivers of flea infracommunity structure. However, the manifestation of gender bias in flea community structure varies among host species, and is likely determined by the pattern of species-specific spatial behavior.
We used data on fleas and gamasid mites parasitic on 8 species of small mammals to test whether (a) species composition of ectoparasite infracommunities may be used to predict host habitat occupancy and (b) the accuracy of this prediction differs between ectoparasite taxa, host genders and seasons.
Assessment of the relative impact of diseases and pathogens is important for agencies and other organizations charged with providing disease surveillance, management and control. It also helps funders of disease-related research to identify the most important areas for investment. Decisions as to which pathogens or diseases to target are often made using complex risk assessment approaches; however, these usually involve evaluating a large number of hazards as it is rarely feasible to conduct an in-depth appraisal of each. Here we propose the use of the H-index (or Hirsch index) as an alternative rapid, repeatable and objective means of assessing pathogen impact. H-index scores for 1,414 human pathogens were obtained from the Institute for Scientific Informations Web of Science (WOS) in July/August 2010. Scores were compared for zoonotic/non-zoonotic, and emerging/non-emerging pathogens, and across taxonomic groups. H-indices for a subset of pathogens were compared with Disability Adjusted Life Year (DALY) estimates for the diseases they cause. H-indices ranged from 0 to 456, with a median of 11. Emerging pathogens had higher H-indices than non-emerging pathogens. Zoonotic pathogens tended to have higher H-indices than human-only pathogens, although the opposite was observed for viruses. There was a significant correlation between the DALY of a disease and the H-index of the pathogen(s) that cause it. Therefore, scientific interest, as measured by the H-index, appears to be a reflection of the true impact of pathogens. The H-index method can be utilized to set up an objective, repeatable and readily automated system for assessing pathogen or disease impact.
Trypanosoma lewisi is a mild or non-pathogenic parasite of the sub-genus Herpetosoma transmitted by fleas to rats. In a previous study we described pan-trypanosome specific primers TRYP1 which amplify the ITS1 of ribosomal DNA by hybridizing in highly conserved regions of 18S and 5.8S genes. These primers proved to be useful for detecting T. lewisi DNA in laboratory rats, but a recent large scale survey in wild rodents demonstrated a lack of specificity. In the present study, we designed and evaluated mono-specific primers LEW1S and LEW1R, for the detection and identification of T. lewisi by a single-step PCR. These primers were designed inside the highly variable region of the ITS1 sequence of T. lewisi ribosomal DNA. The product size of 220 bp is specific to T. lewisi. The sensitivity limit was estimated between 0.055 and 0.55 pg of DNA per reaction, equivalent to 1-10 organisms per reaction. All the PCR products obtained from 6 different T. lewisi isolates were more than 98% similar with each other and similar to the sequences of T. lewisi already published in Genbank. All DNA of 7 T. lewisi stocks from China gave the specific 220 bp product. We showed that LEW1S and LEW1R primers enabled sensitive detection and identification of T. lewisi infection in laboratory and wild rats. This assay is recommended for monitoring T. lewisi infections in rat colonies or for studying infections in the wild fauna. An absence of cross reaction with human DNA means that these primers can be used to investigate atypical trypanosome infections in humans. Given the risk of T. lewisi infection in human, we believe that these primers will be beneficial for public health diagnosis and rodents investigation programmes.
In order to evaluate the circulation of hantaviruses present in southeast Asia, a large scale survey of small mammal species was carried out at seven main sites in the region (Cambodia, Lao Peoples Democratic Republic, and Thailand). Small scale opportunistic trapping was also performed at an eighth site (Cambodia). Using a standard IFA test, IgG antibodies reacting to Hantaan virus antigens were detected at six sites. Antibody prevalence at each site varied from 0 to 5.6% with antibodies detected in several rodent species (Bandicota indica, B. savilei, Maxomys surifer, Mus caroli, M. cookii, Rattus exulans, R. nitidius, R. norvegicus, and R. tanezumi). When site seroprevalence was compared with site species richness, seropositive animals were found more frequently at sites with lower species richness. In order to confirm which hantavirus species were present, a subset of samples was also subjected to RT-PCR. Hantaviral RNA was detected at a single site from each country. Sequencing confirmed the presence of two hantavirus species, Thailand and Seoul viruses, including one sample (from Lao PDR) representing a highly divergent strain of Seoul virus. This is the first molecular evidence of hantavirus in Lao PDR and the first reported L segment sequence data for Thailand virus.
It is widely assumed that the likelihood of invasion decreases with increased species richness in the recipient community. However, the invasion paradox supports a negative and a positive relationship between native biodiversity and the success of an invader. Here, we show that for a host-parasite system (Anguilla anguilla as host and Anguillicoloides crassus as parasitic invader), invasion increases with native micro- and macroparasitic species richness. In fact, about 30% of the A. crassus intensity in eels could be explained by the number of both micro- and macroparasite species. This pattern could be due to the fact that A. crassus exploits a niche (the swim bladder) that is unoccupied by native parasite species and by the Th1/Th2 trade-off between native microparasites and the invader. We conclude that the host-parasite system resistance to invasion may depend on both niche availability and the Th1/Th2 trade-off. As well, we encourage researchers to incorporate native parasite richness as a risk factor in epidemiological models of A. crassus.
Domestic and wild rodents known as the most abundant and diversified order of mammals have a key role in the ecological food chain and also in the transmission of parasites and pathogens to other animals. While foraging on the ground, they can get infected by Toxoplasma gondii, a protozoan parasite, which is the causative agent of toxoplasmosis. Therefore, they serve as intermediate hosts of T. gondii and can transmit it to their predators. To assess their role in the maintenance of T. gondii lifecycle in Thailand, we sampled rodents in a range of biotopes representative of the high biodiversity and conducted a serological survey with latex agglutination test to detect anti-T. gondii antibodies. Overall, 21 of 461 (4.6%) rodents had diagnostically significant antibody titers (cutoff, 1:64). Every species with at least 37 individuals captured tested positive, confirming the wide range of potential mammalian hosts of toxoplasmosis. None of the ecological traits (sex, maturity, morphology, season, or habitat) was found significant to predict the susceptibility to T. gondii both univariately and in a multivariate analysis. However, high prevalences were reported in either forested or anthropized areas. This survey constitutes the first confirmed serological investigation of T. gondii in rodents in Thailand. The rarity of both domestic and wild felids in Thailand emphasizes the importance of rodents in maintaining T. gondii, and questions the involvement of other carnivores in the life cycle.
Orientia tsutsugamushi, the causative agent of scrub typhus in South East Asia and Pacific, is an obligate intracellular bacterium closely related to the Rickettsia. The pathogen is transmitted to humans through the bites of infected larvae of trombiculid mites of the genus Leptotrombidium in which is maintained trough vertical transmission mechanism. The infection in rodents has been described in over 20 species. Scrub typhus is commonly confused with other tropical fevers and late diagnosis and treatment can lead to severe organ failures and a strain-dependent mortality rate of up to 50%. A MLST scheme associating seven core function genes: adk, lepB, lipA, lipB, secY, sodB and sucA was developed and validated on seven Cambodian strains detected in patients and two complete reference genomes from Korea and Japan. Sequence data were analyzed both with respect to sequence type (ST) diversity and DNA polymorphism. Differing trends were revealed. DNA polymorphism and phylogeny of individual gene loci indicated a significant level of recombination and genetic diversity. However, the ST distribution is clearly clonal and the clinical situation can be summarized by the formula: one patient, one strain, one ST. This contradiction is only apparent and is most likely the consequence of the unique life cycle of O. tsutsugamushi. The quasi exclusive vertical transmission mode in mites generates repeated bottlenecks and small-size populations and strongly limits genetic diversity. O. tsutsugamushi has developed specific mechanisms for generating genetic diversity which include recombination, duplication and conjugation. Recombination and other mechanisms for increasing genetic diversity are likely to occur in rodents which can act as maintenance hosts, although occurrence in mites cannot be excluded. Consequences for the epidemiology of scrub typhus are discussed.
Rodents are recognized as hosts for at least 60 zoonotic diseases and may represent a serious threat for human health. In the context of global environmental changes and increasing mobility of humans and animals, contacts between pathogens and potential animal hosts and vectors are modified, amplifying the risk of disease emergence. An accurate identification of each rodent at a specific level is needed in order to understand their implications in the transmission of diseases. Among the Muridae, the Rattini tribe encompasses 167 species inhabiting South East Asia, a hotspot of both biodiversity and emerging and re-emerging diseases. The region faces growing economical development that affects habitats, biodiversity and health. Rat species have been demonstrated as significant hosts of pathogens but are still difficult to recognize at a specific level using morphological criteria. DNA-barcoding methods appear as accurate tools for rat species identification but their use is hampered by the need of reliable identification of reference specimens. In this study, we explore and highlight the limits of the current taxonomy of the Rattini tribe.
Disruptive selection mediated by predation on aquatic immature stages has been proposed as a major force driving ecological divergence and fostering speciation between the M and S molecular forms of the African malaria mosquito, Anopheles gambiae. In the dry savannahs of West Africa where both molecular forms co-occur, the S form thrives in temporary pools filled with rainwater, whereas the M form preferentially breeds in permanent freshwater habitats where predator pressure is higher. Here, we explored the proximal mechanisms by which predation may contribute to habitat segregation between molecular forms using progeny of female mosquitoes captured in Burkina Faso. We show that the S form suffers higher predation rates than the M form when simultaneously exposed to the widespread predator, Anisops jaczewskii in an experimental arena. Furthermore, behavioral plasticity induced by exposure to the predator was observed in the M form, but not in the S form, and may partially explain its habitat use and ecological divergence from the S form. We discuss the role of adaptive phenotypic plasticity in allowing successful colonization of a new ecological niche by the M form and highlight further research areas that need to be addressed for a better understanding of the ultimate mechanisms underlying ecological speciation in this pest of major medical importance.
Cowdriosis or heartwater is a major tick-borne disease on ruminants in Africa and the Caribbean. The causative agent is Ehrlichia ruminantium, an intracellular bacterium. Development of vaccines against heartwater has been hampered the limited efficiency of vaccine in the field, thought to be a consequence of the high genetic diversity of strains circulating in a same area. A sampling scheme was set to collect ticks over 2 years in a delimited area and well identified flock. Prevalence was low at about 3%. A set of 37 strains was considered for MLST analysis along with two reference strains, i.e. ERGA and ERWO, for which full-length genome was available, using a previously described scheme based on the genes gltA, groEL, lepA, lipA, lipB, secY, sodB and sucA. Two populations were identified both with limited genetic variability but with differing evolutionary patterns. Population 1 is in genomic stasis, in agreement with the paradigm for intracellular bacteria. The two reference strains, one from the Caribbean separated from West African strains three centuries ago and another one isolated in South Africa, belong to Population 1. Population 2 is on expansion following a recent clonal emergence from Population 1. The founder strain was identified as strain 395. Strain 623 displays a particularly high rate of mutations in groEL. Owing to the chaperone function of GroEL, this might indicate another clonal emergence under way. This work brings further insight in the genomic plasticity of E. ruminantium and its impact on vaccine strategy.
The effect of habitat anthropization is investigated using a comparative analysis based on a literature survey of the gastrointestinal helminths of murid rodents described in Southeast Asia (SEA). The literature survey gave 30 references on helminth diversity concerning 20 murid rodent species. The diversity of helminths was high with a total of 13 species of cestodes, 15 species of trematodes, 29 species of nematodes and one species of acanthocephalans. The highest helminth species richness was found in Rattus tanezumi, Rattus norvegicus and Rattus argentiventer, all these species were found in more human-dominated habitats (agricultural areas or human settlements). Helminth species richness was positively linked across rodent species to the level of the anthropization of the host environment from forests, agricultural areas to human settlements.
Species richness of parasite assemblages varies among host species. Earlier studies that searched for host-related determinants of parasite diversity mainly considered host traits that affect the probability of host encounter with parasites, whereas host traits related to defensibility against parasites have rarely been investigated. From the latter perspective, evolutionary investment in "expensive" tissue or organs (like testes or brain) may trade off against energetically costly anti-parasitic defences. If so, richer parasite assemblages are expected in hosts with larger testes and brains. We studied the relationships between testes and brain size and diversity of parasites (fleas, gamasid mites and helminths) in 55 rodent species using a comparative approach and application of two methods, namely the method of independent contrasts and generalized least-squares (GLS) analysis. Both phylogenetically correct methods produced similar results for flea and helminth species richness. Testes size positively correlated with flea and helminth species richness but not gamasid mite species richness. No correlation between brain size and species richness of any parasite group was found by the method of independent contrasts. However, GLS analysis indicated negative correlation between brain size and mite species richness. Our results cast doubt on the validity of the expensive tissue hypothesis, but suggest instead that larger testes are associated with higher parasite diversity via their effect on mobility and/or testosterone-mediated immunosuppression.
This work reports for the first time the presence of two Pneumocystis species in wild Rattus norvegicus specimens from Thailand. Pneumocystis DNA was detected in 57.7% (15/26) wild rats without apparent association with typical pneumocystosis. Pneumocystis carinii was found alone in five rats (19.2%), Pneumocystis wakefieldiae was detected alone in six rats (23.1%), and two rats were infected by both species (7.7%). In addition, a new P. wakefieldiae variant sequence has been identified in three wild R. norvegicus specimens caught in the same geographical area. The high frequency of Pneumocystis in wild rats documented in this study and the apparent scarcity of severe pneumocystosis were consistent with an efficient circulation of rat Pneumocystis species in ecosystems.
Animals often suffer from multiple parasite attacks in natural conditions (i.e., polyparasitism). The community of these parasites, which simultaneously or sequentially infest given host species, has rarely been investigated as a parasitic pressure per se. From this perspective, and despite the impressive number of immunoecological or comparative studies, the impacts of polyparasitism on immune responses are far from being appreciated. Focusing on helminths across a wide range of mammalian species and using a phylogenetic comparative method, we show, for the first time, that an increase in the number of helminth parasite species is positively correlated with an increase in basal immune investment (estimated by the counts of white blood cells) across mammal species. After discussing inherent limits of this comparative approach, we put this result in the evolutionary perspective of multiple parasitic infestations.
Heartwater, caused by the intracellular bacterium Ehrlichia ruminantium, is a major tick-borne disease of livestock in Africa also introduced in the Caribbean. The main problem encountered with the control of this disease is the lack of efficient vaccine in the field. This is thought to be related to the high genetic diversity of strains circulating in a same area. A set of eight circulating strains was isolated from a herd of cows in a small locality in Burkina-Faso and analyzed along with two reference strains, i.e. ERGA and ERWO, for which full-length genome was available. A MLST analysis was developed based on the genes gltA, groEL, lepA, lipA, lipB, secY, sodB and sucA. Phylogeny analysis was conducted both on concatenated MLST loci and on each individual locus. This showed differing phylogenies for each individual target gene. Most of the recorded polymorphism was borne by three strains: 331, 469 and 623. The neutrality hypothesis could not be rejected. Recombination and linkage disequilibrium were shown to have occurred. A core of seven strains displayed little polymorphism and signs of most likely ancient recombination events. The two reference strains, one from the Caribbean separated from west African strains three centuries ago and another one isolated in South Africa, were very closely related to the core strains whereas the three differing strains displayed recombination and most of the parcimony informative sites. These data suggest that some strains are in genomic stasis, as expected for intracellular parasites, while others emerge in the same area with DNA polymorphism. This work also shows that the MLST scheme developed can discriminate between these two kinds of strains.
Parasite diversity among and within host species is not solely the result of random processes; rather, it depends on a suite of physiological or ecological host traits as well as environmental factors. Because most macroparasites exhibit life cycles that include infective stages off the definitive host and that rely on host movements for dissemination, parasite acquisition by a host depends largely on hosts being present in a given area where and when infective stages are present. Consequently, host ranging pattern may have a major influence on parasite diversity. Larger home range size is hypothesized to be associated with higher parasite species richness because hosts living in large home ranges should encounter a greater diversity of habitats and other host individuals, which in turn may favor infection by a great diversity of parasite species. By focusing on helminths in wild mammals, we show that an increase in home range area does not lead to an increase in parasite diversity in ungulates and, moreover, that it is associated with a decrease in parasite species richness in carnivores and in glires (rodents and lagomorphs). We also show that home range size is negatively correlated with host density in mammals after correcting both variables for host body mass. We discuss these results from an epidemiological perspective.
The epidemiology of H5N1 HPAI is still unclear despite the efforts of the research community. Studies bringing new insights add more variability in the host-pathogen system and uncertainty in the prediction of local risks. Global analyses of the pathways of wild birds in parallel with virus outbreaks have brought limited conclusions once the raw information was extracted from relevant maps. In this article, we propose an integration of epidemiology, evolutionary biology and community ecology on a local level in a research framework. This multidisciplinary approach aims at understanding the pathogen transmission processes at the interface between different bird groups whether wild or domesticated. We believe that this ecological data brought together with the epidemiological and molecular data is a key element to explore the mechanism of the AIV ecology in their hosts.
Black rats are major invasive vertebrate pests with severe ecological, economic and health impacts. Remarkably, their evolutionary history has received little attention, and there is no firm agreement on how many species should be recognized within the black rat complex. This species complex is native to India and Southeast Asia. According to current taxonomic classification, there are three taxa living in sympatry in several parts of Thailand, Cambodia and Lao Peoples Democratic Republic, where this study was conducted: two accepted species (Rattus tanezumi, Rattus sakeratensis) and an additional mitochondrial lineage of unclear taxonomic status referred to here as Rattus R3. We used extensive sampling, morphological data and diverse genetic markers differing in rates of evolution and parental inheritance (two mitochondrial DNA genes, one nuclear gene and eight microsatellite loci) to assess the reproductive isolation of these three taxa. Two close Asian relatives, Rattus argentiventer and Rattus exulans, were also included in the genetic analyses. Genetic analyses revealed discordance between the mitochondrial and nuclear data. Mitochondrial phylogeny studies identified three reciprocally monophyletic clades in the black rat complex. However, studies of the phylogeny of the nuclear exon interphotoreceptor retinoid-binding protein gene and clustering and assignation analyses with eight microsatellites failed to separate R. tanezumi and R3. Morphometric analyses were consistent with nuclear data. The incongruence between mitochondrial and nuclear (and morphological) data rendered R. tanezumi/R3 paraphyletic for mitochondrial lineages with respect to R. sakeratensis. Various evolutionary processes, such as shared ancestral polymorphism and incomplete lineage sorting or hybridization with massive mitochondrial introgression between species, may account for this unusual genetic pattern in mammals.
The presence of gastrointestinal helminths (GI helminths) was investigated among 725 murid rodents, trapped in various habitats of Nan, Loei and Buri Ram Provinces, Thailand. The study revealed 17 species of rodents infected with 21 species or taxonomic groups of parasites (3 trematodes, 3 cestodes, 14 nematodes and 1 acanthocephalan). The overall prevalence of infection was 57.7% (418/725). Of the gastrointestinal (GI) helminths, the dominant parasitic group was members of the family Trichostrongylidae (24.3%), followed by the cestodes Raillietina sp (17.1%) and Hymenolepis diminuta (8.6%) and the nematode Syphacia muris (8.6%). The GI helminthic infection rates were highest in Mus caroli (81.8%), Mus cervicolor (76.5%), Leopoldamys edwardsi (75.0%), Bandicota indica (71.5%) and Bandicota savilei (71.4%). Highest rodent species richness (RSR) and helminth species richness (HSR) rates were found in Loei, followed by Nan and Buri Ram. The helminth prevalence rate was higher in rodents from Nan, followed by rodents from Loei and Buri Ram. Rodents from irrigated fields had the highest infection rates followed by rodents from upland or dry agricultural areas, forests and domestic habitats. Raillietina sp, Rodentolepis nana (syn. Hymenolepis nana), Hymenolepis diminuta, Moniliformis moniliformis and Cyclodontostomum purvisi, considered zoonotic parasites, were mainly found in rodents from domestic habitats and lowland irrigated fields.
Among 1,341 blood samples from rodents that were trapped in Southeast Asia between 2008 and 2010, we found a prevalence of Bartonella infection ranging from 9.6 to 11.9%. Bartonella species identified (143 isolates) included B. elizabethae, B. coopersplainsensis, B. phoceensis, B. queenslandensis, B. rattimassiliensis, B. tribocorum, and three new putative Bartonella species.
Comparative analysis, which aims at investigating ecological and evolutionary patterns among species, may help at targeting reservoirs of zoonotic diseases particularly in countries presenting high biodiversity. Here, we developed a simple method to target rodent reservoirs using published studies screening microparasite infections.
Phylogeography of parasites and microbes is a recent field. Phylogeographic studies have been performed mostly to test three major hypotheses that are not mutually exclusive on the origins and distributions of human parasites and microbes: (1) the "out of Africa" pattern where parasites are supposed to have followed the dispersal and expansion of modern humans in and out of Africa, (2) the "domestication" pattern where parasites were captured in the domestication centres and dispersed through them and (3) the "globalization" pattern, in relation to historical and more recent trade routes. With some exceptions, such studies of human protozoans, helminths and ectoparasites are quite limited. The conclusion emphasizes the need to acquire more phylogeographic data in non-Occidental countries, and particularly in Asia where all the animal domestications took place.
Although competitive speciation is more and more regarded as a plausible mechanism for sympatric speciation of non-parasite species, virtually no empirical or theoretical study has considered this evolutionary process to explain intra-host diversification of parasites. We expanded the theory of competitive speciation to parasite species looking at the effect of macro-parasite life history on the conditions for sympatric speciation under the so-called pleiotropic scenario. We included within-host competition in the classical Anderson and May framework assuming that individuals exploit within-host resources according to a quantitative trait. We derived the invasion fitness function of mutants considering different distributions of individuals among hosts. Although the mutant fitness depends on parameters describing the key features of macro-parasite life history, and on the relative distributions of mutant and residents in hosts, the conditions for competitive speciation of macro-parasites are exactly the same as those previously established for free-living species. As an interesting by-product, within-host competitive speciation is expected not to depend on the aggregation level of the parasites. This theoretical pattern is confirmed by comparing the speciation rate of weakly and strongly aggregated monogenean parasites.
We investigated infection of rodents and shrews by Leptospira spp. in two localities of Cambodia (Veal Renh, Kaev Seima) and in four types of habitat (forests, non-flooded lands, lowland rain-fed paddy fields, houses) during the wet and the dry seasons. Habitat preference was common, and rodent and shrew species were found only in houses or in rain-fed paddy fields or in forests. Among 649 small mammals trapped belonging to 12 rodent species and 1 shrew species, 71 of 642 animals tested were carriers of Leptospira according to the 16S ribosomal RNA marker used. Rodent infection was higher in low-slope locations, corresponding to rain-fed paddy fields, especially in the rainy season and in Kaev Seima. Rodents (Rattus exulans) and shrews (Suncus murinus) inhabiting households showed significantly low levels of infections, whereas rodents living in and near to forests (shrubby wasteland, orchards) showed high levels of infection.
A large number (828) of rodents belonging to nine genera (Bandicota, Berylmys, Chiropodomys, Hapalomys, Leopoldamys, Maxomys, Mus, Niviventer and Rattus) were trapped in four Thai provinces between 2008 and 2010. A new species of Protospirura (Nematoda: Spiruridae) was identified and described. Protospirura siamensis n. sp. was found in 10 rodent species from the four Thai provinces surveyed. The new species can be distinguished from known species of the genus by the arrangement of the papillae on the male and the morphology and length of the spicules. This is the first species of Protospirura to be described from South-East Asia.
Predation of aquatic immature stages has been identified as a major evolutionary force driving habitat segregation and niche partitioning in the malaria mosquito Anopheles gambiae sensu stricto in the humid savannahs of Burkina Faso, West Africa. Here, we explored behavioural responses to the presence of a predator in wild populations of the M and S molecular forms of An. gambiae that typically breed in permanent (e.g., rice field paddies) and temporary (e.g., road ruts) water collections.
Sex-biased parasitism is rarely investigated in relation to host tolerance and resistance, which are two defense strategies hosts can adopt when challenged by parasites. Health or fitness deteriorations in less tolerant individuals with increasing parasite burden would be faster than those in more tolerant ones. Hence, the body condition and reproductive potential of an infected individual host can be considered proxies for tolerance to parasitism. We studied Mediterranean populations of the wood mouse (Apodemus sylvaticus) and its helminth parasites. We assessed their resistance using the phytohemagglutinin test and spleen size, and their tolerance using body condition in males and females and testes mass in males. In order to avoid spurious correlations, we took into account the phylogeographic structure of the Mediterranean wood mouse populations. We used a mixed model adapted from the animal model used in quantitative genetics. While helminth infection did not differ between the two sexes, females and males differed in their measured defenses. Females seem to invest more in immune defense with increasing risk of parasite diversity, but also appear to be potentially more tolerant of parasitic diversity. These results suggest the existence of sexual differences in resistance and tolerance, and that measurements of parasitic loads alone could be insufficient to detect any underlying sexual differences in the two strategies that have evolved in response to multiple parasitic attacks.
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