Abstract
BackgroundSusceptibility 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.ResultsUsing 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.ConclusionsOur 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.
Highlights
Susceptibility to parasite infection affects fitness-related processes, such as mate choice and survival, yet its genetic regulation remains poorly understood
Animals showed no signs of clinical significance during the period of the study that could be linked to acute parasite infections
We suggest that the -485C/T single nucleotide polymorphisms (SNPs) detected in redfronted lemurs affects IL4 gene transcription in a similar way: decreased IL4 mRNA and decreased IL-4 protein levels in the rare genotype (T/T) individuals could contribute to higher nematode infection intensities as IL-4 is known to play an important role in enteropathic expulsion of nematode worms and increases mucosal permeability after infections [31,32,33,34]
Summary
Susceptibility to parasite infection affects fitness-related processes, such as mate choice and survival, yet its genetic regulation remains poorly understood. Evidence mainly from human diseases is accumulating that single nucleotide polymorphisms (SNPs) in the promoter region of the interleukin 4 gene (IL4) affect its transcription, resulting in altered IL-4 protein levels and, in either higher or lower IgE titres [21,22,23,24] In this way, IL4 SNPs can effectively influence the intensity of various infections [22,25,26,27,28,29,30], including enteric pathogens [31,32,33,34]. Despite its key role in the regulation of parasite infections and resulting evolutionary significance of IL4 polymorphisms [19], empirical evidence of the importance of IL4 on the intensity of parasite infections in natural population is lacking
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