Altitudinal Effects on Innate Immune Response of a Subterranean Rodent.

Immune defense is costly to maintain and deploy, and the optimal investment into immune defense depends on risk of infection. Altitude is a natural environmental factor that is predicted to affect parasite abundance, with lower parasite abundance predicted at higher altitudes due to stronger environmental stressors, which reduce parasite transmission. Using high and low altitude populations of the Turkish blind mole-rat (TBMR) Nannospalax xanthodon, we tested for effects of altitude on constitutive innate immune defense. Field studies were performed with 32 wild animals in 2017 and 2018 from two low- and one high-altitude localities in the Central Taurus Mountains, at respective altitudes of 1010 m, 1115 m, and 2900 m above sea level. We first compared innate standing immune defense as measured by the bacteria-killing ability of blood serum. We then measured corticosterone stress hormone levels, as stressful conditions may affect immune response. Finally, we compared prevalence and intensity of gastrointestinal parasites of field-captured TBMR. We found that the bacteria-killing ability of serum is greater in the mole-rat samples from high altitude. There was no significant difference in stress (corticosterone) levels between altitude categories. Coccidian prevalence and abundance were significantly higher in 2017 than 2018 samples, but there was no significant difference in prevalence, abundance, or intensity between altitudes, or between sexes. Small sample sizes may have reduced power to detect true differences; nevertheless, this study provides support that greater standing innate immunity in high altitude animals may reflect greater investment into constitutive defense.

Genomics of host-pathogen interactions: challenges and opportunities across ecological and spatiotemporal scales.

Evolutionary genomics has recently entered a new era in the study of host-pathogen interactions. A variety of novel genomic techniques has transformed the identification, detection and classification of both hosts and pathogens, allowing a greater resolution that helps decipher their underlying dynamics and provides novel insights into their environmental context. Nevertheless, many challenges to a general understanding of host-pathogen interactions remain, in particular in the synthesis and integration of concepts and findings across a variety of systems and different spatiotemporal and ecological scales. In this perspective we aim to highlight some of the commonalities and complexities across diverse studies of host-pathogen interactions, with a focus on ecological, spatiotemporal variation, and the choice of genomic methods used. We performed a quantitative review of recent literature to investigate links, patterns and potential tradeoffs between the complexity of genomic, ecological and spatiotemporal scales undertaken in individual host-pathogen studies. We found that the majority of studies used whole genome resolution to address their research objectives across a broad range of ecological scales, especially when focusing on the pathogen side of the interaction. Nevertheless, genomic studies conducted in a complex spatiotemporal context are currently rare in the literature. Because processes of host-pathogen interactions can be understood at multiple scales, from molecular-, cellular-, and physiological-scales to the levels of populations and ecosystems, we conclude that a major obstacle for synthesis across diverse host-pathogen systems is that data are collected on widely diverging scales with different degrees of resolution. This disparity not only hampers effective infrastructural organization of the data but also data granularity and accessibility. Comprehensive metadata deposited in association with genomic data in easily accessible databases will allow greater inference across systems in the future, especially when combined with open data standards and practices. The standardization and comparability of such data will facilitate early detection of emerging infectious diseases as well as studies of the impact of anthropogenic stressors, such as climate change, on disease dynamics in humans and wildlife.

Host-pathogen evolutionary signatures reveal dynamics and future invasions of vampire bat rabies.

Anticipating how epidemics will spread across landscapes requires understanding host dispersal events that are notoriously difficult to measure. Here, we contrast host and virus genetic signatures to resolve the spatiotemporal dynamics underlying geographic expansions of vampire bat rabies virus (VBRV) in Peru. Phylogenetic analysis revealed recent viral spread between populations that, according to extreme geographic structure in maternally inherited host mitochondrial DNA, appeared completely isolated. In contrast, greater population connectivity in biparentally inherited nuclear microsatellites explained the historical limits of invasions, suggesting that dispersing male bats spread VBRV between genetically isolated female populations. Host nuclear DNA further indicated unanticipated gene flow through the Andes mountains connecting the VBRV-free Pacific coast to the VBRV-endemic Amazon rainforest. By combining Bayesian phylogeography with landscape resistance models, we projected invasion routes through northern Peru that were validated by real-time livestock rabies mortality data. The first outbreaks of VBRV on the Pacific coast of South America could occur by June 2020, which would have serious implications for agriculture, wildlife conservation, and human health. Our results show that combining host and pathogen genetic data can identify sex biases in pathogen spatial spread, which may be a widespread but underappreciated phenomenon, and demonstrate that genetic forecasting can aid preparedness for impending viral invasions.

Duplication and population dynamics shape historic patterns of selection and genetic variation at the major histocompatibility complex in rodents.

Genetic variation at the major histocompatibility complex (MHC) is vitally important for wildlife populations to respond to pathogen threats. As natural populations can fluctuate greatly in size, a key issue concerns how population cycles and bottlenecks that could reduce genetic diversity will influence MHC genes. Using 454 sequencing, we characterized genetic diversity at the DRB Class II locus in montane voles (Microtus montanus), a North American rodent that regularly undergoes high-amplitude fluctuations in population size. We tested for evidence of historic balancing selection, recombination, and gene duplication to identify mechanisms maintaining allelic diversity. Counter to our expectations, we found strong evidence of purifying selection acting on the DRB locus in montane voles. We speculate that the interplay between population fluctuations and gene duplication might be responsible for the weak evidence of historic balancing selection and strong evidence of purifying selection detected. To further explore this idea, we conducted a phylogenetically controlled comparative analysis across 16 rodent species with varying demographic histories and MHC duplication events (based on the maximum number of alleles detected per individual). On the basis of phylogenetic generalized linear model-averaging, we found evidence that the estimated number of duplicated loci was positively related to allelic diversity and, surprisingly, to the strength of purifying selection at the DRB locus. Our analyses also revealed that species that had undergone population bottlenecks had lower allelic richness than stable species. This study highlights the need to consider demographic history and genetic structure alongside patterns of natural selection to understand resulting patterns of genetic variation at the MHC.