Prior exposure to pathogens augments host heterogeneity in susceptibility and has key epidemiological consequences.

Pathogen epidemics are key threats to human and wildlife health. Across systems, host protection from pathogens following initial exposure is often incomplete, resulting in recurrent epidemics through partially-immune hosts. Variation in population-level protection has important consequences for epidemic dynamics, but how acquired protection influences inter-individual heterogeneity in susceptibility and its epidemiological consequences remains understudied. We experimentally investigated whether prior exposure (none, low-dose, or high-dose) to a bacterial pathogen alters host heterogeneity in susceptibility among songbirds. Hosts with no prior pathogen exposure had little variation in protection, but heterogeneity in susceptibility was significantly augmented by prior pathogen exposure, with the highest variability detected in hosts given high-dose prior exposure. An epidemiological model parameterized with experimental data found that heterogeneity in susceptibility from prior exposure more than halved epidemic sizes compared with a homogeneous population with identical mean protection. However, because infection-induced mortality was also greatly reduced in hosts with prior pathogen exposure, reductions in epidemic size were smaller than expected in hosts with prior exposure. These results highlight the importance of variable protection from prior exposure and/or vaccination in driving population-level heterogeneity and epidemiological dynamics.

Mercury concentrations in Seaside Sparrows and Marsh Rice Rats differ across the Mississippi River Estuary.

Mercury (Hg) concentrations and their associated toxicological effects in terrestrial ecosystems of the Gulf of Mexico are largely unknown. Compounding this uncertainty, a large input of organic matter from the 2010 Deepwater Horizon oil spill may have altered Hg cycling and bioaccumulation dynamics. To test this idea, we quantified blood concentrations of total mercury (THg) in Seaside Sparrows (Ammospiza maritima) and Marsh Rice Rats (Oryzomys palustris) in marshes west and east of the Mississippi River in 2015 and 2016. We also tested for a difference in THg concentrations between oiled and non-oiled sites. To address the potential confounding effect of diet variation on Hg transfer, we used stable nitrogen (δ15N) and carbon (δ13C) isotope values as proxies of trophic position and the source of primary production, respectively. Our results revealed that five to six years after the spill, THg concentrations were not higher in sites oiled by the spill compared to non-oiled sites. In both species, THg was higher at sites east of the Mississippi River compared to control and oiled sites, located west. In Seaside Sparrows but not in Marsh Rice Rats, THg increased with δ15N values, suggesting Hg trophic biomagnification. Overall, even in sites with the most elevated THg, concentrations were generally low. In Seaside Sparrows, THg concentrations were also lower than previously reported in this and other closely related passerines, with only 7% of tested birds exceeding the lowest observed effect concentration associated with toxic effects across bird species (0.2 µg/g ww). The factors associated with geographic heterogeneity in Hg exposure remain uncertain. Clarification could inform risk assessment and future restoration and management actions in a region facing vast anthropogenic changes.

Prior exposure to pathogens augments host heterogeneity in susceptibility and has key epidemiological consequences.

Pathogen epidemics are key threats to human and wildlife health. Across systems, host protection from pathogens following initial exposure is often incomplete, resulting in recurrent epidemics through partially-immune hosts. Variation in population-level protection has important consequences for epidemic dynamics, but how acquired protection influences inter-individual heterogeneity in susceptibility and its epidemiological consequences remains understudied. We experimentally investigated whether prior exposure (none, low-dose, or high-dose) to a bacterial pathogen alters host heterogeneity in susceptibility among songbirds. Hosts with no prior pathogen exposure had little variation in protection, but heterogeneity in susceptibility was significantly augmented by prior pathogen exposure, with the highest variability detected in hosts given high-dose prior exposure. An epidemiological model parameterized with experimental data found that heterogeneity in susceptibility from prior exposure more than halved epidemic sizes compared with a homogeneous population with identical mean protection. However, because infection-induced mortality was also greatly reduced in hosts with prior pathogen exposure, reductions in epidemic size were smaller than expected in hosts with prior exposure. These results highlight the importance of variable protection from prior exposure and/or vaccination in driving population-level heterogeneity and epidemiological dynamics.

Genetic variants associated with hantavirus infection in a reservoir host are related to regulation of inflammation and immune surveillance.

The immunogenetics of wildlife populations influence the epidemiology and evolutionary dynamic of the host-pathogen system. Profiling immune gene diversity present in wildlife may be especially important for those species that, while not at risk of disease or extinction themselves, are host to diseases that are a threat to humans, other wildlife, or livestock. Hantaviruses (genus: Orthohantavirus) are globally distributed zoonotic RNA viruses with pathogenic strains carried by a diverse group of rodent hosts. The marsh rice rat (Oryzomys palustris) is the reservoir host of Orthohantavirus bayoui, a hantavirus that causes fatal cases of hantavirus cardiopulmonary syndrome in humans. We performed a genome wide association study (GWAS) using the rice rat "immunome" (i.e., all exons related to the immune response) to identify genetic variants associated with infection status in wild-caught rice rats naturally infected with their endemic strain of hantavirus. First, we created an annotated reference genome using 10× Chromium Linked Reads sequencing technology. This reference genome was used to create custom baits which were then used to target enrich prepared rice rat libraries (n = 128) and isolate their immunomes prior to sequencing. Top SNPs in the association test were present in four genes (Socs5, Eprs, Mrc1, and Il1f8) which have not been previously implicated in hantavirus infections. However, these genes correspond with other loci or pathways with established importance in hantavirus susceptibility or infection tolerance in reservoir hosts: the JAK/STAT, MHC, and NFκB. These results serve as informative markers for future exploration and highlight the importance of immune pathways that repeatedly emerge across hantavirus systems. Our work aids in creating cross-species comparisons for better understanding mechanisms of genetic susceptibility and host-pathogen coevolution in hantavirus systems.

Stable isotope analyses identify trophic niche partitioning between sympatric terrestrial vertebrates in coastal saltmarshes with differing oiling histories.

Bioindicator species are commonly used as proxies to help identify the ecological effects of oil spills and other stressors. However, the utility of taxa as bioindicators is dependent on understanding their trophic niche and life history characteristics, as these factors mediate their ecological responses. Seaside sparrows (Ammospiza maritima) and marsh rice rats (Oryzomys palustris) are two ubiquitous terrestrial vertebrates that are thought to be bioindicators of oil spills in saltmarsh ecosystems. To improve the utility of these omnivorous taxa as bioindicators, we used carbon and nitrogen stable isotope analysis to quantify their trophic niches at saltmarshes in coastal Louisiana with differing oiling histories. We found that rats generally had lower trophic positions and incorporated more aquatic prey relative to seaside sparrows. The range of resources used (i.e.,trophic niche width) varied based on oiling history. Seaside sparrows had wider trophic niches than marsh rice rats at unoiled sites, but not at oiled sites. Trophic niche widths of conspecifics were less consistent at oiled sites, although marsh rice rats at oiled sites had wider trophic niches than rats at unoiled sites. These results suggest that past oiling histories may have imparted subtle, yet differing effects on the foraging ecology of these two co-occurring species. However, the temporal lag between initial oiling and our study makes identifying the ultimate drivers of differences between oiled and unoiled sites challenging. Even so, our findings provide a baseline quantification of the trophic niches of sympatric seaside sparrows and marsh rice rats that will aid in the use of these species as indicators of oiling and other environmental stressors in saltmarsh ecosystems.

Polycyclic aromatic hydrocarbon exposure in seaside sparrows (Ammodramus maritimus) following the 2010 Deepwater Horizon oil spill.

The seaside sparrow (Ammodramus maritimus) is an abundant and permanent resident of coastal salt marshes impacted by the 2010 BP Deepwater Horizon oil spill. Such terrestrial species are often overlooked in the aftermath of marine spills, despite the potential for long-term oil exposure. We sampled the livers of seaside sparrows residing in oiled and unoiled sites from 2011 to 2014 and quantified expression of cytochrome p450 1A (CYP1A), a gene involved in the metabolism of polycyclic aromatic hydrocarbons (PAHs). In August 2011, CYP1A expression was markedly higher in birds from an oiled site compared to an unoiled site, but differences had disappeared by June 2012. In June 2013, CYP1A expression was elevated compared to 2012 levels on all sites, including those collected from sites that had not been directly oiled during the spill. This rise in CYP1A expression was possibly due to Hurricane Isaac, which made landfall near our sites between the 2012 and 2013 sampling periods. CYP1A expression was significantly attenuated again in June 2014. We also collected sediment samples from the same marshes for a total concentration analysis of PAHs. The PAH concentrations in sediment samples exhibited a similar pattern to the CYP1A data, supporting the link between marsh PAHs and bird CYP1A expression. These results indicate that contamination from marine oil spills can immediately extend to terrestrial ecosystems, and that storms, weather, or other factors may influence subsequent spatial and temporal oil exposure for several additional years.

Human disturbance causes the formation of a hybrid swarm between two naturally sympatric fish species.

Most evidence for hybrid swarm formation stemming from anthropogenic habitat disturbance comes from the breakdown of reproductive isolation between incipient species, or introgression between allopatric species following secondary contact. Human impacts on hybridization between divergent species that naturally occur in sympatry have received considerably less attention. Theory predicts that reinforcement should act to preserve reproductive isolation under such circumstances, potentially making reproductive barriers resistant to human habitat alteration. Using 15 microsatellites, we examined hybridization between sympatric populations of alewife (Alosa pseudoharengus) and blueback herring (A. aestivalis) to test whether the frequency of hybridization and pattern of introgression have been impacted by the construction of a dam that isolated formerly anadromous populations of both species in a landlocked freshwater reservoir. The frequency of hybridization and pattern of introgression differed markedly between anadromous and landlocked populations. The rangewide frequency of hybridization among anadromous populations was generally 0-8%, whereas all landlocked individuals were hybrids. Although neutral introgression was observed among anadromous hybrids, directional introgression leading to increased prevalence of alewife genotypes was detected among landlocked hybrids. We demonstrate that habitat alteration can lead to hybrid swarm formation between divergent species that naturally occur sympatrically, and provide empirical evidence that reinforcement does not always sustain reproductive isolation under such circumstances.