Abstract
Whether, when, and how genetic diversity buffers individuals and populations against infectious disease risk is a critical and open question for understanding wildlife disease and zoonotic disease risk. Several, but not all, studies have found negative relationships between infection and heterozygosity in wildlife. Since they can host multiple zoonotic infections, we sampled a population of wild deer mice (Peromyscus maniculatus), sequenced their genomes, and examined their fecal samples for coccidia and nematode eggs. We analyzed coccidia infection status, abundance, and coinfection status in relation to per-locus and per-individual measures of heterozygosity, as well as identified SNPs associated with infection status. Since heterozygosity might affect host condition, and condition is known to affect immunity, it was included as a co-variate in the per-individual analyses and as response variable in relation to heterozygosity. Not only did coccidia-infected individuals have lower levels of genome-wide per-locus diversity across all metrics, but we found an inverse relationship between genomic diversity and severity of coccidia infection. We also found weaker evidence that coinfected individuals had lower levels of private allelic variation than all other groups. In the per-individual analyses, relationships between heterozygosity and infection were marginal but followed the same negative trends. Condition was negatively correlated with infection, but was not associated with heterozygosity, suggesting that effects of heterozygosity on infection were not mediated by host condition in this system. Association tests identified multiple loci involved in the inflammatory response, with a particular role for NF-κB signaling, supporting previous work on the genetic basis of coccidia resistance. Taken together, we find that increased genome-wide neutral diversity, the presence of specific genetic variants, and improved condition positively impact infection status. Our results underscore the importance of considering host genomic variation as a buffer against infection, especially in systems that can harbor zoonotic diseases.
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Data availability
The infection and SNP data generated during this study are available on Dryad (https://doi.org/10.5061/dryad.k0p2ngfb4).
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Acknowledgements
This work was performed at the Claremont Colleges' Robert J. Bernard Biological Field Station. We thank Finley Melnikoff for assistance with the field sampling and fecal egg counts. Erin Alexander, Tamara Mehta, Moira McCarthy, and Binita Pandya also assisted with fecal egg counts. Emma Garval helped with preliminary mixed modeling analyses. Funding was provided by the W.M. Keck Science Department.
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S.A. Budischak and F. Finseth developed the project and wrote the manuscript. S.A. Budischak carried out the field sampling, parasite counts, and performed analyses. F. Finseth prepared the samples for sequencing, performed the bioinformatics, and analyzed the data. S. Halvorsen analyzed the data and provided feedback on the manuscript.
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Budischak, S.A., Halvorsen, S. & Finseth, F. Genomic heterozygosity is associated with parasite abundance, but the effects are not mediated by host condition. Evol Ecol 37, 75–96 (2023). https://doi.org/10.1007/s10682-022-10175-8
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DOI: https://doi.org/10.1007/s10682-022-10175-8