Immunological Change in a Parasite-Impoverished Environment: Divergent Signals from Four Island Taxa

Dramatic declines of native Hawaiian avifauna due to the human-mediated emergence of avian malaria and pox prompted an examination of whether island taxa share a common altered immunological signature, potentially driven by reduced genetic diversity and reduced exposure to parasites. We tested this hypothesis by characterizing parasite prevalence, genetic diversity and three measures of immune response in two recently-introduced species (Neochmia temporalis and Zosterops lateralis) and two island endemics (Acrocephalus aequinoctialis and A. rimitarae) and then comparing the results to those observed in closely-related mainland counterparts. The prevalence of blood parasites was significantly lower in 3 of 4 island taxa, due in part to the absence of certain parasite lineages represented in mainland populations. Indices of genetic diversity were unchanged in the island population of N. temporalis; however, allelic richness was significantly lower in the island population of Z. lateralis while both allelic richness and heterozygosity were significantly reduced in the two island-endemic species examined. Although parasite prevalence and genetic diversity generally conformed to expectations for an island system, we did not find evidence for a pattern of uniformly altered immune responses in island taxa, even amongst endemic taxa with the longest residence times. The island population of Z. lateralis exhibited a significantly reduced inflammatory cell-mediated response while levels of natural antibodies remained unchanged for this and the other recently introduced island taxon. In contrast, the island endemic A. rimitarae exhibited a significantly increased inflammatory response as well as higher levels of natural antibodies and complement. These measures were unchanged or lower in A. aequinoctialis. We suggest that small differences in the pathogenic landscape and the stochastic history of mutation and genetic drift are likely to be important in shaping the unique immunological profiles of small isolated populations. Consequently, predicting the impact of introduced disease on the many other endemic faunas of the remote Pacific will remain a challenge

Leprosy and tuberculosis concomitant infection: a poorly understood, age-old relationship

Historically, archaeological evidence, post-mortem findings and retro- spective analysis of leprosy institutions’ data demonstrates a high observed incidence of concomitant infection with leprosy and tuberculosis (TB). However, reports of concomitant infection in the modern literature remain scarce, with estimates of annual new case detection rates of concomitant infection at approximately 0·02 cases per 100,000 population. Whilst the mechanism for this apparent decline in concomitant infections remains unclear, further research on this topic has remained relatively neglected. Modelling of the interaction of the two organisms has suggested that the apparent decline in observations of concomitant infection may be due to the protective effects of cross immunity, whilst more recently others have questioned whether it is a more harmful relationship, predisposing towards increased host mortality. We review recent evidence, comparing it to previously held understanding on the epidemiological relationship and our own experience of concomitant infection. From this discussion, we highlight several under-investigated areas, which may lead to improvements in the future delivery of leprosy management and services, as well as enhance understanding in other fields of infection management. These include, a) highlighting the need for greater understanding of host immunogenetics involved in concomitant infection, b) whether prolonged courses of high dose steroids pre-dispose to TB infection? and, c) whether there is a risk of rifampicin resistance developing in leprosy patients treated in the face of undiagnosed TB and other infections? Longitudinal work is still required to characterise these temporal relationships further and add to the current paucity of literature on this subject matter

Comparative Immune Function in Wild Birds

Over the last several decades, interest in quantifying immune function in comparative studies of wild animals has grown appreciably. Now, the field of ecological immunology is undergoing a transition, and ¿second generation¿ studies are being designed and carried out. With a greater appreciation of the complexity of immune systems, these second generation studies are commonly distinguished from their antecedents by making comparisons using multiple assays and including multiple species. I worked to advance this transition by developing novel approaches to comparative immunology, exploring the interrelationships among indices of immune function, and applying multiple indices to a question of comparative avian evolution. First, I worked to develop individual methodologies that would be broadly applicable given the numerous limitations of field-based immunology. I present methodological details on two assays¿a hemolysis-hemagglutination assay and a bacteria killing assay, and I report on intra- and inter-specific comparisons using both. Relatedly, using ten species of waterfowl, I examine how these and other indices correlate at both the individual and species levels. Next, with an interest in developing a better understanding of the evolutionary forces molding immune function, I set out to broadly compare immune function in 15 phylogenetically matched pairs of bird populations from North America and from the islands of Hawaii, Bermuda, and the Gal¿pagos. If immune defenses were costly, populations from relatively disease-free, oceanic islands are expected to exhibit attenuated immune function in response to reduced pathogen and parasite pressure. In fact, many island animals exhibit this postulated ¿island syndrome,¿ one facet of which is increased susceptibility to disease. After employing three protocols to measure eight indices of immune function, I found no support for my hypothesis. Rather than evidence of depauperate parasite communities and inherent costs of immune defenses selecting for reduced immune function, I found that several indices were elevated in island birds. I suggest that life on islands is accompanied by an apparent reorganization of the relative importance of various immune components. Finally, in collaborative efforts with investigators here and at other institutions, I apply the hemolysis-hemagglutination assay to address a variety of questions across three diverse avian study systems

Regulation of Global Gene Expression in Human Loa loa Infection Is a Function of Chronicity

Infection with the filarial parasite Loa loa causes a parasite-specific downregulation of T cell responses. However, differences exist (clinical and immunologic) between patients born and living in filarial endemic regions (endemics) and those who become infected during travel or short-term residency (expatriates). T cell responses are more depressed in endemics while expatriates have more clinical “allergic-type” symptoms. In this study, we showed that these differences reflect transcriptional differences within the T cell compartment. Using microarrays, we examined global gene expression in both CD4+ and CD8+ T cells of microfilaremic endemic and expatriate patients and found differences not only ex vivo, but also to parasite and, for CD8+ cells, to nonparasite antigens. Functional analysis showed that endemic patients expressed genes linked to inflammatory disease and caspase associated cell death at homeostasis while expatriates tended to have a more activation-induced gene profile at homeostasis and a CD4+ inflammatory response to parasite antigen. Patient groups were similar in their CD4+ response to nonparasite antigen but strongly differed in their CD8+ responses, demonstrating the potential global ramifications of chronic, longstanding infection. Our study describes potential transcriptional mechanisms for the variability seen in patients with different levels of exposure to and chronicity of filarial infection

Global Effect of Climate Change on Seasonal Cycles, Vector Population and Rising Challenges of Communicable Diseases: A Review

This article explains ongoing changes in global climate and their effect on the resurgence of vector and pathogen populations in various parts of the world. Today, major prevailing changes are the elevation of global temperature and accidental torrent rains, floods, droughts, and loss of productivity and food commodities. Due to the increase in water surface area and the longer presence of flood water, the breeding of insect vectors becomes very high; it is responsible for the emergence and re-emergence of so many communicable diseases. Due to the development of resistance to chemicals in insect pests, and pathogens and lack of control measures, communicable zoonotic diseases are remerging with high infectivity and mortality. This condition is becoming more alarming as the climate is favoring pathogen-host interactions and vector populations. Rapid changes seen in meteorology are promoting an unmanageable array of vector-borne infectious diseases, such as malaria, Japanese encephalitis, filarial, dengue, and leishmaniasis. Similarly, due to unhygienic conditions, poor sanitation, and infected ground and surface water outbreak of enteric infections such as cholera, vibriosis, and rotavirus is seen on the rise. In addition, parasitic infection ascariasis, fasciolosis, schistosomiasis, and dysentery cases are increasing. Today climate change is a major issue and challenge that needs timely quick solutions. Climate change is imposing non-adaptive forced human migration territorial conflicts, decreasing ecosystem productivity, disease outbreaks, and impelling unequal resource utilization. Rapid climate changes, parasites, pathogens, and vector populations are on the rise, which is making great threats to global health and the environment. This article highlighted the necessity to develop new strategies and control measures to cut down rising vector and pathogen populations in endemic areas. For finding quick solutions educational awareness, technology up-gradation, new vaccines, and safety measures have to be adopted to break the cycle of dreadful communicable diseases shortly

Emerging Infectious Disease: Host and Parasite Perspectives

Avian malaria and related haematozoa are nearly ubiquitous parasites that can impose fitness costs of variable severity and may, in some cases, cause substantial mortality in their host populations. One example of the latter, the emergence of avian malaria in the endemic avifauna of Hawaii, has become a model for understanding the consequences of human-mediated disease introduction. The drastic declines of native Hawaiian birds due to avian malaria provided the impetus for examining more closely several aspects of host-parasite interactions in this system. Host-specificity is an important character determining the extent to which a parasite may emerge. Traditional parasite classification, however, has used host information as a character in taxonomical identification, potentially obscuring the true host range of many parasites. To improve upon previous methods, I first developed molecular tools to identify parasites infecting a particular host. I then used these molecular techniques to characterize host-specificity of parasites in the genera Plasmodium and Haemoproteus. I show that parasites in the genus Plasmodium exhibit low specificity and are therefore most likely to emerge in new hosts in the future. Subsequently, I characterized the global distribution of the single lineage of P. relictum that has emerged in Hawaii. I demonstrate that this parasite has a broad host distribution worldwide, that it is likely of Old World origin and that it has been introduced to numerous islands around the world, where it may have been overlooked as a cause of decline in native birds. I also demonstrate that morphological classification of P. relictum does not capture differences among groups of parasites that appear to be reproductively isolated based on molecular evidence. Finally, I examined whether reduced immunological capacity, which has been proposed to explain the susceptibility of Hawaiian endemics, is a general feature of an "island syndrome" in isolated avifauna of the remote Pacific. I show that, over multiple time scales, changes in immune response are not uniform and that observed changes probably reflect differences in genetic diversity, parasite exposure and life history that are unique to each species

Toll-like receptor variation in the bottlenecked population of the endangered Seychelles warbler

In small populations, drift results in a loss of genetic variation, which reduces adaptive evolutionary potential. Furthermore, the probability of consanguineous mating increases which may result in inbreeding depression. Under certain circumstances, balancing selection can counteract drift and maintain variation at key loci. Identifying such loci is important from a conservation perspective and may provide insight into how different evolutionary forces interact in small populations. Toll-like receptor (TLR) genes play a pivotal role in vertebrate innate immune defence by recognizing invading pathogens. We characterize TLR variation in the Seychelles warbler (SW) Acrocephalus sechellensis, an endangered passerine that recently suffered a population bottleneck. Five of seven TLR loci were polymorphic, with one locus (TLR15) containing four functional variants and showing an excess of heterozygotes. Haplotype-level tests failed to detect selection at these loci, but site-specific tests detected signatures of positive selection within TLR3 and TLR15. After characterizing variation (excluding TLR15) in 5–6 other Acrocephalus species, we found that TLR variation was positively correlated with population size across species and followed the pattern observed at neutral microsatellite loci. The depauperate TLR variation observed suggests that even at important immunity-related loci, balancing selection may only attenuate the overriding effects of drift. However, in the SW, TLR15 appears to be an outlier and warrants further investigation. The low levels of TLR variation may be disadvantageous for the long-term viability of the SW and conservatio

Lichen Conservation in Eastern North America: Population Genomics, Climate Change, and Translocations

Conservation biology is a scientific discipline that draws on methods from diverse fields to address specific conservation concerns and inform conservation actions. This field is overwhelmingly focused on charismatic animals and vascular plants, often ignoring other diverse and ecologically important groups. This trend is slowly changing in some ways; for example, increasing number of fungal species are being added to the IUCN Red-List. However, a strong taxonomic bias still exists. Here I contribute four research chapters to further the conservation of lichens, one group of frequently overlooked organisms. I address specific conservation concerns in eastern North America using modern methods. The results of these studies provide insight into lichen conservation in each situation, implications for the broader ecosystems within the study regions, and advancement of methods for the study of lichen conservation and biology. The first research chapter (Chapter 2) is a population genomics study based on whole genome shotgun sequencing of Cetradonia linearis, an endangered, lichenized fungus. These data were used to 1) assemble and annotate a reference genome, 2) characterize the mating system, 3) test for isolation by distance (IBD) and isolation by environment (IBE), and 4) investigate the biogeographic history of the species. Approximately 70% of the genome (19.5 Mb) was assembled. Using this assembly, only a single mating type was located, suggesting the species could be unisexual. There was strong evidence for both low rates of recombination and for Isolation by Distance, but no evidence for Isolation by Environment. The hypothesis that C. linearis had a larger range during the last glacial maximum, especially in the southern portion of its current extent, was supported by Hindcast species distribution models and the spatial distribution of genetic diversity. Given the findings here, it is recommended that C. linearis remain protected by the U.S. Endangered Species Act and listed as Vulnerable on the International Union for the Conservation of Nature Red-List. The third chapter is an estimation of the impacts of climate change on high-elevation, endemic lichens in the southern Appalachians, a global diversity hotspot for many groups, including lichens. Extensive field surveys in the high elevations of the region were carried out to accurately document the current distributions of eight narrowly endemic species. These data were compared with herbarium records, and species distribution modeling was used to predict how much climatically suitable area will remain within, and north of, the current range of the target species at multiple time points and climate change scenarios. Fieldwork showed that target species ranged from extremely rare to locally abundant and models predicted average losses of suitable area within the current distribution of species ranging from 93.8 to 99.7%. The results indicate that climate change poses a significant threat to high-elevation lichens, and illustrates the application of current modeling techniques for rare, montane species. In the fourth chapter, a dataset of \u3e13,000 occurrence records for lichens in the Mid-Atlantic Coastal Plain (MACP) of eastern North America was used to model distributions of 193 species. The resulting models were used to quantify the amount of each species’ distribution that is occupied by unsuitable land use types, along with the potential area that will be lost to sea-level rise (SLR). These analyses showed that species have likely already lost an average of 32% of their distributional area to development and agriculture, and are predicted to lose an average of 12.4 and 33.7% of their distributional area with one foot (~0.3 m) and six feet (~1.8 m) of SLR, respectively. Functional and taxonomic groups were compared to identify specific effects of SLR. Species reproducing with symbiotic propagules were found to have significantly larger distributions than species that reproduce sexually with fungal spores alone, and the sexually reproducing species were predicted to lose greater distributional area to SLR. Cladonia species occupy significantly less area in the MACP than Parmotrema species and were predicted to lose more of their distributions to SLR. Patterns of total species diversity showed that the area with the highest diversity is the Dare Peninsula in North Carolina, which was also predicted to lose the most land area to SLR. The workflow established here is flexible and applicable to estimating SLR impacts worldwide and can provide essential insights for local conservation planning. The fifth chapter describes the results of three experiments conducted to test new and established methods for lichen transplantation. First, small fragments of Graphis sterlingiana, Hypotrachyna virginica, and Lepraria lanata were placed on medical gauze attached to each of the species’ most common substrate to test the feasibility of transplanting narrowly endemic species. Second, burlap, cheesecloth, medical gauze, and a plastic air filter were directly compared for their use as artificial transplant substrates with Lepraria finkii as the test lichen. Third, transplants of Usnea angulata were established to test its amenability to transplantation via hanging fragments on monofilament. The first two experiments were established on Roan Mountain, North Carolina and the third experiment at Highlands Biological Station, North Carolina. In the first two experiments medical gauze did not withstand local weather conditions and nearly all pieces fell from the trees within 6 months. The plastic air filter and burlap performed best as artificial substrates for transplants, with a 100% and 80% success rate, respectively. Cheesecloth remained attached to the trees, but only 20% of lichen fragments remained attached to the substrate after one year. In the third experiment U. angulata grew 3.5 ± 1.4 cm in 5 months, exceeding previously reported growth rates for this species. These results advance methods for conservation-focused lichen transplants, and expand established methods to a new region and new species