Unraveling the Effects of Selection and Demography on Immune Gene Variation in Free-Ranging Plains Zebra (Equus quagga) Populations

Pauline L Kamath,Wayne M Getz

doi:10.1371/journal.pone.0050971

Pauline L Kamath, Wayne M Getz

Open Access

https://doi.org/10.1371/journal.pone.0050971

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Abstract

Demography, migration and natural selection are predominant processes affecting the distribution of genetic variation among natural populations. Many studies use neutral genetic markers to make inferences about population history. However, the investigation of functional coding loci, which directly reflect fitness, is critical to our understanding of species' ecology and evolution. Immune genes, such as those of the Major Histocompatibility Complex (MHC), play an important role in pathogen recognition and provide a potent model system for studying selection. We contrasted diversity patterns of neutral data with MHC loci, ELA-DRA and -DQA, in two southern African plains zebra (Equus quagga) populations: Etosha National Park, Namibia, and Kruger National Park, South Africa. Results from neutrality tests, along with observations of elevated diversity and low differentiation across populations, supported previous genus-level evidence for balancing selection at these loci. Despite being low, MHC divergence across populations was significant and may be attributed to drift effects typical of geographically separated populations experiencing little to no gene flow, or alternatively to shifting allele frequency distributions driven by spatially variable and fluctuating pathogen communities. At the DRA, zebra exhibited geographic differentiation concordant with microsatellites and reduced levels of diversity in Etosha due to highly skewed allele frequencies that could not be explained by demography, suggestive of spatially heterogeneous selection and local adaptation. This study highlights the complexity in which selection affects immune gene diversity and warrants the need for further research on the ecological mechanisms shaping patterns of adaptive variation among natural populations.

Highlights

Spatiotemporal fluctuations in pathogens generate complex patterns in the distribution of gene variation among host populations
We examined the distribution of genetic variation in the ELA- differentiation at ELA loci across populations (DRA) and DQA peptide binding regions (PBRs) within zebra populations differing in parasite richness and severity (Table 1) to shed light on how selection may affect Major Histocompatibility Complex (MHC) gene variation
Total genotyping error varied by locus and mean error rate was estimated to be 0.3% and 2.5% in blood and fecal samples genotyped, respectively

Summary

Introduction

Spatiotemporal fluctuations in pathogens generate complex patterns in the distribution of gene variation among host populations. Neutral genetic data is informative for studying demography [3], for example, to examine relatedness, mating behavior, dispersal patterns, changes in population size, population genetic structure and speciation [4,5,6]. It is functional gene variation, that reflects natural selection, fitness and the potential to adapt to changing environments, making it of critical importance to the study of evolution, ecology and conservation [7,8]. Contrasting patterns of diversity at neutral and immune response loci can be informative for understanding how hosts adapt to pathogens, by illuminating the relative effects of selection versus demography on gene variation and population dynamics [9,10,11,12,13,14]

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