ABSTRACT
MHC genes are extraordinarily polymorphic in most taxa. Host-pathogen coevolution driven by negative frequency-dependent selection (NFDS) is one of the main hypotheses for the maintenance of such immunogenetic variation. Here, we test a critical but rarely tested assumption of this hypothesis-that MHC alleles affect resistance/susceptibility to a pathogen in a strain-specific way, that is, there is a host genotype-by-pathogen genotype interaction. In a field study of bank voles naturally infected with the tick-transmitted bacterium Borrelia afzelii, we tested for MHC class II (DQB) genotype-by-B. afzelii strain interactions for infection prevalence between 10 DQB alleles and seven strains. One allele (DQB*37) showed an interaction, such that voles carrying DQB*37 had higher prevalence of two strains and lower prevalence of one strain than individuals without the allele. These findings were corroborated by analyses of strain composition of infections, which revealed an effect of DQB*37 in the form of lower ß diversity among infections in voles carrying the allele. Taken together, these results provide rare support at the molecular genetic level for a key assumption of models of antagonistic coevolution through NFDS.
Subject(s)
Borrelia , Animals , Arvicolinae/genetics , Genotype , Prevalence , RodentiaABSTRACT
Infection tolerance is the ability of a host to limit the health effects of a given parasite load. A few recent studies have demonstrated genetic variation for tolerance, but little is known about how environmental factors affect tolerance. Here, we used the intestinal nematode Heligmosomoides polygyrus in laboratory mice to test for effects of protein malnutrition on tolerance. We performed an experiment where two different mouse strains (CBA and BALB/c) were fed either adequate-protein food or low-protein food, and trickle-infected with different doses of H. polygyrus larvae during four weeks. We found that protein malnutrition decreases tolerance measured as intestinal barrier function, but only in one of the strains (BALB/c); that is, there was a host genotype-by-environment interaction for tolerance. We conclude that nutritional status can affect tolerance and that sensitivity of tolerance to malnutrition may differ between host genotypes.
Subject(s)
Intestinal Diseases, Parasitic/parasitology , Nematospiroides dubius/physiology , Protein Deficiency/parasitology , Strongylida Infections/parasitology , Animals , Dietary Proteins , Disease Resistance/genetics , Genetic Variation , Host-Parasite Interactions , Immune Tolerance , Intestinal Diseases, Parasitic/immunology , Intestinal Mucosa/immunology , Intestinal Mucosa/parasitology , Mice, Inbred BALB C , Mice, Inbred CBA , Protein Deficiency/immunology , Strongylida Infections/immunologyABSTRACT
Host specificity is a fundamental property of parasites. Whereas most studies focus on measures of specificity on host range, only few studies have considered quantitative aspects such as infection intensity or prevalence. The relative importance of these quantitative aspects is still unclear, mainly because of methodological constraints, yet central to a precise assessment of host specificity. Here, we assessed simultaneously two quantitative measures of host specificity of Heligmosomoides glareoli and Heligmosomoides polygyrus polygyrus infections in sympatric rodent hosts. We used standard morphological techniques as well as real-time quantitative PCR and sequencing of the rDNA ITS2 fragment to analyse parasite infection via faecal sample remains. Although both parasite species are thought to be strictly species-specific, we found morphologically and molecularly validated co- and cross-infections. We also detected contrasting patterns within and between host species with regard to specificity for prevalence and intensity of infection. H. glareoli intensities were twofold higher in bank voles than in yellow-necked mice, but prevalence did not differ significantly between species (33 vs. 18%). We found the opposite pattern in H. polygyrus infections with similar intensity levels between host species but significantly higher prevalence in mouse hosts (56 vs. 10%). Detection rates were higher with molecular tools than morphological methods. Our results emphasize the necessity to consider quantitative aspects of specificity for a full view of a parasites' capacity to replicate and transmit in hosts and present a worked example of how modern molecular tools help to advance our understanding of selective forces in host-parasite ecology and evolution.
Subject(s)
Arvicolinae/parasitology , Heligmosomatoidea/physiology , Host Specificity , Murinae/parasitology , Rodent Diseases/parasitology , Strongylida Infections/veterinary , Animals , DNA, Helminth/genetics , DNA, Ribosomal Spacer/genetics , Female , Heligmosomatoidea/genetics , Heligmosomatoidea/isolation & purification , Male , Nematospiroides dubius/genetics , Nematospiroides dubius/isolation & purification , Nematospiroides dubius/physiology , Prevalence , Real-Time Polymerase Chain Reaction/veterinary , Rodent Diseases/epidemiology , Species Specificity , Strongylida Infections/epidemiology , Strongylida Infections/parasitology , SympatryABSTRACT
BACKGROUND: Susceptibility to parasite infection affects fitness-related processes, such as mate choice and survival, yet its genetic regulation remains poorly understood. Interleukin-4 (IL4) plays a central role in the humoral immune defence against nematode parasite infections, inducing IgE switch and regulation of worm expulsion from the intestines. The evolutionary and functional significance of single nucleotide polymorphisms (SNPs) in IL4-genes is known, yet empirical information on the effect of IL4 SNPs on gastro-intestinal infections is lacking. Using samples from a population of wild red-fronted lemurs (Eulemur fulvus rufus, Primates: Lemuridae), from western Madagascar, we explored the association of IL4-gene promoter polymorphisms with nematode infections and investigated a possible functional role of the IL4 polymorphism on male reproductive success. RESULTS: Using sequence analyses of lemur DNA we detected a new SNP in the IL4 gene promoter area. Carriers of the genotype T/T showed higher nematode infection intensities than individuals of genotypes C/T and C/C. Genetic population analyses using data from more than 10 years, suggested higher reproductive success of T/T males than expected. CONCLUSIONS: Our results suggest a regulatory effect of an IL4 gene promoter polymorphism on the intensity of parasite infections in a natural population of red-fronted lemurs, with a seemingly disadvantageous genotype represented in low frequencies. Long-term population analyses, however, point in the direction of a negative frequency-dependent association, giving a fitness advantage to the rare genotype. Due to low frequencies of the genotype in question conclusive evidence of a functional role of IL4 polymorphism cannot be drawn here; still, we suggest the use of IL4 polymorphism as a new molecular tool for quick assessment of individual genetic constitution with regard to nematode infection intensities, contributing to a better understanding of the actual components of the immune response that mediate protection against gastro-intestinal parasites.
ABSTRACT
Parasites and infectious diseases represent ecological forces shaping animal social evolution. Although empirical studies supporting this link abound in various vertebrate orders, both the study of the dynamics and impact of parasite infections and infectious diseases in strepsirrhine primates have received little empirical attention. We conducted a longitudinal parasitological study on four groups of wild red-fronted lemurs (Eulemur fulvus rufus) at Kirindy Forest, Madagascar, during two field seasons in consecutive years to investigate i) the degree of gastrointestinal parasite infection on population and individual levels and ii) factors potentially determining individual infection risk. Using a comprehensive dataset with multiple individually assignable parasite samples as well as information on age, sex, group size, social rank, and endocrine status (fecal androgen and glucocorticoid), we examined parasite infection patterns and host traits that may affect individual infection risk. In addition, we examined whether parasite infection affects mating and reproductive success. Our results indicated high variability in parasite infection on individual and population levels. Time of year and group size was important determinants of variability in parasite infection. Variation in hormone levels was also associated with parasite species richness and parasite infection intensity. Differences in parasite infection between years indicate a potential immune-enhancing function of steroid hormones on nematode infections, which has not been reported before from other vertebrates studied under natural conditions. Male mating and reproductive success were not correlated to any measure of parasite infection, which suggests a nonfunctional role of the parasites we examined in primate sexual selection.
Subject(s)
Host-Parasite Interactions , Intestinal Diseases, Parasitic/parasitology , Intestinal Diseases, Parasitic/veterinary , Lemur/parasitology , Age Factors , Analysis of Variance , Animals , Feces/chemistry , Feces/parasitology , Female , Hormones/analysis , Linear Models , Longitudinal Studies , Madagascar , Male , Sex Factors , Sexual Behavior, Animal , Social Dominance , Spatial BehaviorABSTRACT
Although parasites are important regulatory factors in animal populations, basic knowledge on their fauna in many vertebrate taxa is lacking. In particular, parasite infections of primate species have gained little attention. Here, I present data on the gastro-intestinal fauna of a population of wild red-fronted lemurs ( Eulemur fulvus rufus; Primates: Lemuriformes) monitored over a total of 8 mo during 2 consecutive field seasons in 2006 and 2007 in Kirindy Forest, western Madagascar. Using fecal samples for parasite analyses, I identified 10 parasite species, including 6 nematodes (Lemuricola vauceli, Trichuris sp., 2 species of Callistoura, 1 trichostrongylid, and 1 strongyloid), 1 anoplocephalid cestode, a dicrocoeliid trematode, as well as 2 protozoans (Entamoeba sp. and Balantidium coli). The population in Kirindy Forest had the highest prevalence and number of parasite species ever recorded for species of lemurs. Additionally, prevalence of some parasite species differed between the social groups studied. These findings lead to 2 conclusions. First, it is important to extend a parasitological study to several social groups of a host population, since groups may differ in parasite fauna as a result of minor microclimatic or habitat parameters, and, second, short-term assessments of lemur health might underestimate the real parasite burden.
Subject(s)
Gastrointestinal Diseases/veterinary , Helminthiasis, Animal/parasitology , Lemur/parasitology , Primate Diseases/parasitology , Protozoan Infections, Animal/parasitology , Animals , Feces/parasitology , Female , Gastrointestinal Diseases/epidemiology , Gastrointestinal Diseases/parasitology , Helminthiasis, Animal/epidemiology , Linear Models , Madagascar/epidemiology , Male , Prevalence , Primate Diseases/epidemiology , Protozoan Infections, Animal/epidemiology , SeasonsABSTRACT
Researchers studying individual variation in conspicuous skin coloration in primates have suggested that color indicates male quality. Although primate fur color can also be flamboyant, the potential condition dependence and thus signaling function of fur remains poorly studied. We studied sources of variation in sexually dichromatic facial hair coloration in red-fronted lemurs (Eulemur fulvus rufus). We collected data on 13 adult males in Kirindy Forest, Madagascar, during two study periods in 2006 and 2007, to determine whether variation in facial hair coloration correlates with male age, rank, androgen status, and reproductive success. We quantified facial hair coloration via standardized digital photographs of each male, assessed androgen status using fecal hormone measurements, and obtained data on reproductive success through genetic paternity analyses. Male facial hair coloration showed high individual variation, and baseline coloration was related to individual androgen status but not to any other parameter tested. Color did not reflect rapid androgen changes during the mating season. However, pronounced long-term changes in androgen levels between years were accompanied by changes in facial hair coloration. Our data suggest that facial hair coloration in red-fronted lemur males is under proximate control of androgens and may provide some information about male quality, but it does not correlate with dominance rank or male reproductive success.