Host community similarity and geography shape the diversity and distribution of haemosporidian parasites in Amazonian birds

Identifying the mechanisms driving the distribution and diversity of parasitic organisms and characterizing the structure of parasite assemblages are critical to understanding host–parasite evolution, community dynamics, and disease transmission risk. Haemosporidian parasites of the genera Plasmodium and Haemoproteus are a diverse and cosmopolitan group of bird pathogens. Despite their global distribution, the ecological and historical factors shaping the diversity and distribution of these protozoan parasites across avian communities and geographic regions remain unclear. Here we used a region of the mitochondrial cytochrome b gene to characterize the diversity, biogeographical patterns, and phylogenetic relationships of Plasmodium and Haemoproteus infecting Amazonian birds. Specifically, we asked whether, and how, host community similarity and geography (latitude and area of endemism) structure parasite assemblages across 15 avian communities in the Amazon Basin. We identified 265 lineages of haemosporidians recovered from 2661 sampled birds from 330 species. Infection prevalence varied widely among host species, avian communities, areas of endemism, and latitude. Composition analysis demonstrated that both malarial parasites and host communities differed across areas of endemism and as a function of latitude. Thus, areas with similar avian community composition were similar in their parasite communities. Our analyses, within a regional biogeographic context, imply that host switching is the main event promoting diversification in malarial parasites. Although dispersal of haemosporidian parasites was constrained across six areas of endemism, these pathogens are not dispersal‐limited among communities within the same area of endemism. Our findings indicate that the distribution of malarial parasites in Amazonian birds is largely dependent on local ecological conditions and host evolutionary relationships.     

Coloniality and migration are related to selection on MHC genes in birds

The major histocompatibility complex (MHC) plays a key role in pathogen recognition as a part of the vertebrate adaptive immune system. The great diversity of MHC genes in natural populations is maintained by different forms of balancing selection and its strength should correlate with the diversity of pathogens to which a population is exposed and the rate of exposure. Despite this prediction, little is known about how life‐history characteristics affect selection at the MHC. Here, we examined whether the strength of balancing selection on MHC class II genes in birds (as measured with nonsynonymous nucleotide substitutions, dN) was related to their social or migratory behavior, two life‐history characteristics correlated with pathogen exposure. Our comparative analysis indicated that the rate of nonsynonymous substitutions was higher in colonial and migratory species than solitary and resident species, suggesting that the strength of balancing selection increases with coloniality and migratory status. These patterns could be attributed to: (1) elevated transmission rates of pathogens in species that breed in dense aggregations, or (2) exposure to a more diverse fauna of pathogens and parasites in migratory species. Our study suggests that differences in social structure and basic ecological traits influence MHC diversity in natural vertebrate populations.     

Impact of forest size on parasite biodiversity: implications for conservation of hosts and parasites

Studies of biodiversity traditionally focus on charismatic megafauna. By comparison, little is known about parasite biodiversity. Recent studies suggest that co-extinction of host specific parasites with their hosts should be common and that parasites may even go extinct before their hosts. The few studies examining the relationship between parasite diversity and habitat quality have focused on parasites that require intermediate hosts and pathogens that require vectors to complete their life-cycles. Declines in parasite and pathogen richness in these systems could be due to the decline of any of the definitive hosts, intermediate hosts, or vectors. Here we focus on avian ectoparasites, primarily lice, which are host specific parasites with simple, direct, life-cycles. By focusing on these parasites we gain a clearer understanding of how parasites are linked to their hosts and their hosts’ environment. We compare parasite richness on birds from fragmented forests in southern China. We show that parasite richness correlates with forest size, even among birds that are locally common. The absence of some ectoparasite genera in small forests suggests that parasites can go locally extinct even if their hosts persist. Our data suggest that the conservation of parasite biodiversity may require preservation of habitat fragments that are sufficiently large to maintain parasite populations, not just their host populations.     

The role of seabirds of the Iles Eparses as reservoirs and disseminators of parasites and pathogens

The role of birds as reservoirs and disseminators of parasites and pathogens has received much attention over the past several years due to their high vagility. Seabirds are particularly interesting hosts in this respect. In addition to incredible long-distance movements during migration, foraging and prospecting, these birds are long-lived, site faithful and breed in dense aggregations in specific colony locations. These different characteristics can favor both the local maintenance and large-scale dissemination of parasites and pathogens. The Iles Eparses provide breeding and feeding grounds for more than 3 million breeding pairs of seabirds including at least 13 species. Breeding colonies on these islands are relatively undisturbed by human activities and represent natural metapopulations in which seabird population dynamics, movement and dispersal can be studied in relation to that of circulating parasites and pathogens. In this review, we summarize previous knowledge and recently-acquired data on the parasites and pathogens found in association with seabirds of the Iles Eparses. These studies have revealed the presence of a rich diversity of infectious agents (viruses, bacteria and parasites) carried by the birds and/or their local ectoparasites (ticks and louse flies). Many of these agents are widespread and found in other ecosystems confirming a role for seabirds in their large scale dissemination and maintenance. The heterogeneous distribution of parasites and infectious agents among islands and seabird species suggests that relatively independent metacommunities of interacting species may exist within the western Indian Ocean. In this context, we discuss how the patterns and determinants of seabird movements may alter parasite and pathogen circulation. We conclude by outlining key aspects for future research given the baseline data now available and current concerns in eco-epidemiology and biodiversity conservation.     

Parasite Replication and the Evolutionary Epidemiology of Parasite Virulence

Parasite virulence evolution is shaped by both within-host and population-level processes yet the link between these differing scales of infection is often neglected. Population structure and heterogeneity in both parasites and hosts will affect how hosts are exploited by pathogens and the intensity of infection. Here, it is shown how the degree of relatedness among parasites together with epidemiological parameters such as pathogen yield and longevity influence the evolution of virulence. Furthermore, the role of kin competition and the degree of cheating within highly structured parasite populations also influences parasite fitness and infectivity patterns. Understanding how the effects of within-host processes scale up to affect the epidemiology has importance for understanding host-pathogen interactions.     

Blood parasites of birds on the White Sea-Baltic migration route. 4. The ecological aspect

The effect of some ecological factors on the infection of birds with blood Protozoa was studied. Most favourable conditions for circulation of Haemoproteidae on the Kurish Spit were recorded in July. The possibility of the infection of young small passerine birds from the first broods with Haemoproteidae is most high first of all at the expense of their longer stay in the nesting territory in the period of the active transport of parasites. The presence of Leucocytozoidae in Kurish populations is explained mainly by the distribution of birds. The registration of Leucocytozoidae from birds on the Kurish Spit in spring and autumn is the result of the flight of extensively infected northern populations. It is noted that a constant change in the populational composition of the ornithofauna during seasonal migrations should be taken into account when studying the parasites of wild birds. Otherwise the characteristic features of the circulation of parasites in the region in question can be distorted as a result of the overlap of data on the infection of birds of different populations. The dependence of the infection on sex and size of birds--hosts and the role of the nesting period in the distribution of some Haemosporidia are analysed.     

Molecular Detection of Hematozoa Infections in Tundra Swans Relative to Migration Patterns and Ecological Conditions at Breeding Grounds

Tundra swans (Cygnus columbianus) are broadly distributed in North America, use a wide variety of habitats, and exhibit diverse migration strategies. We investigated patterns of hematozoa infection in three populations of tundra swans that breed in Alaska using satellite tracking to infer host movement and molecular techniques to assess the prevalence and genetic diversity of parasites. We evaluated whether migratory patterns and environmental conditions at breeding areas explain the prevalence of blood parasites in migratory birds by contrasting the fit of competing models formulated in an occupancy modeling framework and calculating the detection probability of the top model using Akaike Information Criterion (AIC). We described genetic diversity of blood parasites in each population of swans by calculating the number of unique parasite haplotypes observed. Blood parasite infection was significantly different between populations of Alaska tundra swans, with the highest estimated prevalence occurring among birds occupying breeding areas with lower mean daily wind speeds and higher daily summer temperatures. Models including covariates of wind speed and temperature during summer months at breeding grounds better predicted hematozoa prevalence than those that included annual migration distance or duration. Genetic diversity of blood parasites in populations of tundra swans appeared to be relative to hematozoa prevalence. Our results suggest ecological conditions at breeding grounds may explain differences of hematozoa infection among populations of tundra swans that breed in Alaska.     

Avian research in the Caribbean: past contributions and current priorities

ABSTRACT The islands of the Caribbean contain habitat of critical importance to a large number of endemic and resident birds, as well as many overwintering Neotropical migrants, and they rank as a globally outstanding conservation priority ecoregion and biodiversity hotspot. Considerable research from the region has focused on the ecology of permanent resident species, and these studies have had particular significance for threatened species management, especially parrot biology and conservation, but also for tropical community ecology in general. Work by ornithologists in the Caribbean has been instrumental in improving our understanding of the ecology of overwintering Neotropical migrants and in developing long‐term monitoring programs. Although Caribbean‐based studies of birds have resulted in significant contributions in many important areas of ecological research, there is a great need for additional research. Especially needed are studies with application to the management of resident species, and studies of how bird populations may be affected by pathogens, parasites, plants, and other types of biotic interactions. Studies focusing on how bird species and populations are affected by global climate change, and cumulative, landscape‐level changes in land use are also needed. Along with additional research, scientists have an important role to play in building capacity to prepare the next generation of biologists in the region who will need to address mounting challenges related to biodiversity protection. As with many conservation efforts, funding is a critical need for almost all organizations and agencies involved in research, conservation action, and capacity building in the West Indies.     

Leukocyte counts in different populations of Antarctic <Emphasis Type="Italic">Pygoscelid</Emphasis> penguins along the Antarctic Peninsula

The Antarctic Peninsula is one of the areas where the climate is changing at the fastest pace, having several effects on the populations of pygoscelid penguins. Few studies have analysed the variation in immune parameters of antarctic birds in a geographical context; thus, analyses of geographical differences in the immune components of wild pygoscelid penguins are still scarce. Leukocyte counts in birds provide information on their immunity and physiological stress. The objective of this study was to analyse the leukocyte counts in penguins of the genus Pygoscelis (gentoo, Adélie and chinstrap penguins), covering sites along the South Shetland Islands and some islands on the west coast of the Antarctic Peninsula. Our results revealed differences in the number of heterophils and eosinophils and in the heterophil/lymphocyte ratio in the northeastern populations of gentoo and Adélie penguins as compared to the rest of the colonies studied. The results contribute to better understanding of the variations in physiological parameters of penguins related to a geographical context.     

Diversification by host switching and dispersal shaped the diversity and distribution of avian malaria parasites in Amazonia

Understanding how pathogens and parasites diversify through time and space is fundamental to predicting emerging infectious diseases. Here, we use biogeographic, coevolutionary and phylogenetic analyses to describe the origin, diversity, and distribution of avian malaria parasites in the most diverse avifauna on Earth. We first performed phylogenetic analyses using the mitochondrial cytochrome b (cyt b) gene to determine relationships among parasite lineages. Then, we estimated divergence times and reconstructed ancestral areas to uncover how landscape evolution has shaped the diversification of Parahaemoproteus and Plasmodium in Amazonia. Finally, we assessed the coevolutionary patterns of diversification in this host–parasite system to determine how coevolution may have influenced the contemporary diversity of avian malaria parasites and their distribution among Amazonian birds. Biogeographic analysis of 324 haemosporidian parasite lineages recovered from 4178 individual birds provided strong evidence that these parasites readily disperse across major Amazonian rivers and this has occurred with increasing frequency over the last five million years. We also recovered many duplication events within areas of endemism in Amazonia. Cophylogenetic analyses of these blood parasites and their avian hosts support a diversification history dominated by host switching. The ability of avian malaria parasites to disperse geographically and shift among avian hosts has played a major role in their radiation and has shaped the current distribution and diversity of these parasites across Amazonia.     

Parasites contribute to ecologically dependent postmating isolation in the adaptive radiation of three-spined stickleback

Spatial variation in parasitic infections is common, and has the potential to drive population divergence and the reproductive isolation of hosts. However, despite support from theory and model laboratory systems, little strong evidence has been forthcoming from the wild. Here, we show that parasites are likely to cause reproductive isolation in the adaptive radiation of three-spined stickleback. Adjacent wild populations on the Scottish island of North Uist differ greatly and consistently in the occurrence of different parasites that have substantial effects on fitness. Laboratory-reared fish are more resistant to experimental infection by parasite species from their own population. Furthermore, hybrid backcrosses between the host populations are more resistant to parasites from the parental population to which they are more closely related. These patterns provide strong evidence that parasites can cause ecological speciation, by contributing to selection against migrants and ecologically dependent postmating isolation.     

Introduction. Antarctic ecology: from genes to ecosystems. Part 2. Evolution, diversity and functional ecology

The Antarctic biota has evolved over the last 100 million years in increasingly isolated and cold conditions. As a result, Antarctic species, from micro-organisms to vertebrates, have adapted to life at extremely low temperatures, including changes in the genome, physiology and ecological traits such as life history. Coupled with cycles of glaciation that have promoted speciation in the Antarctic, this has led to a unique biota in terms of biogeography, patterns of species distribution and endemism. Specialization in the Antarctic biota has led to trade-offs in many ecologically important functions and Antarctic species may have a limited capacity to adapt to present climate change. These include the direct effects of changes in environmental parameters and indirect effects of increased competition and predation resulting from altered life histories of Antarctic species and the impacts of invasive species. Ultimately, climate change may alter the responses of Antarctic ecosystems to harvesting from humans. The unique adaptations of Antarctic species mean that they provide unique models of molecular evolution in natural populations. The simplicity of Antarctic communities, especially from terrestrial systems, makes them ideal to investigate the ecological implications of climate change, which are difficult to identify in more complex systems.     

Investigation of blood parasites of pygoscelid penguins at the King George and Elephant Islands, South Shetlands Archipelago, Antarctica

Parasites may adversely affect the breeding success and survival of penguins, potentially hampering the viability of their populations. We examined 161 pygoscelid penguins (3 Pygoscelis adeliae, 98 Pygoscelis antarcticus, and 60 Pygoscelis papua) at the South Shetlands Archipelago during the 2010–2011 summer; blood smears were examined for 64 penguins (2 P. adeliae, 18 P. antarcticus, and 44 P. papua), and a PCR test targeting Haemoproteus sp. and Plasmodium sp. was applied for 37 penguins (2 P. adeliae, 17 P. antarcticus, 19 P. papua). No blood parasites were observed, and all PCR tests were negative, leukocyte profiles were similar to those reported in other studies for wild pygoscelid penguins, and all penguins were in good body condition and had no external signs of disease. One specimen of chewing lice (Austrogoniodes sp.) was recorded in one P. antarcticus at King George Island. Ticks (Ixodes uriae) were not observed on the penguins, but were found on the ground near P. antarcticus nests at King George Island. The absence of avian blood parasites in Antarctic penguins is thought to result from the absence of competent invertebrate hosts in the climatic conditions. Predicted climate changes may redefine the geographic distribution of vector-borne pathogens, and therefore, the occurrence of blood parasites and their invertebrate hosts should be monitored regularly in Antarctic birds, particularly in the northernmost Antarctic Peninsula.     

Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts

Spatial variation in parasitism is commonly observed in intermediate host populations. However, the factors that determine the causes of this variation remain unclear. Increasing evidence has suggested that spatial heterogeneity in parasitism among intermediate hosts may result from variation in recruitment processes initiated by definitive hosts. I studied the perching and habitat use patterns of wading birds, the definitive hosts in this system, and its consequences for the recruitment of parasites in snail intermediate hosts. Populations of the mangrove snail, Cerithidea scalariformis, collected from mangrove swamps on the east coast of central Florida are parasitized by a diverse community of trematode parasites. These parasites are transmitted from wading birds, which frequently perch on dead mangrove trees. I tested the hypothesis that mangrove perches act as transmission foci for trematode infections of C. scalariformis and that the spatial variation of parasitism frequently observed in this system is likely to emanate from the distribution of wading birds. On this fine spatial scale, definitive host behaviors, responding to a habitat variable, influenced the distribution, abundance and species composition of parasite recruitment to snails. This causal chain of events is supported by regressions between perch density, bird abundance, bird dropping density and ultimately parasite prevalence in snails. Variation between prevalence of parasites in free-ranging snails versus caged snails shows that while avian definitive hosts initiate spatial patterns of parasitism in snails through their perching behaviors, these patterns may be modified by the movement of snail hosts. Snail movement could disperse their associated parasite populations within the marsh, which may potentially homogenize or further increase parasite patchiness initiated by definitive hosts.     

Parasites, disease and the structure of ecological communities

Pathogens and parasites are fascinating to epidemiologists and ecologists alike; as well as causing disease in individual species, they can perturb the normal functioning of a community and thus give insights into the way that the community 'functions' Several recent studies on diseases in animal populations have confirmed the importance of pathogens and parasites as components of ecological systems, while also revealing the underlying structure of complex multispecies communities.     

Pathogens and the structure of plant communities

There is increasing interest in the direct and indirect effects of pathogens and parasites on the structure of plant communities. The direct influence of pathogens is seen in cases where pathogens reduce the populations of adult and seedling plants or prevent the recruitment of seeds. Indirect effects occur when epidemic outbreaks or endemic parasites of herbivores lead to reductions in grazing pressure, which temporarily allow plants to escape from the detrimental effects of their herbivores. In both cases, the presence of pathogens can lead to changes in the relative abundance of the species in a plant community, which are discernible for many years after the initial disease outbreak has passed.     

Mechanisms of disease-induced extinction

Parasites are important determinants of ecological dynamics. Despite the widespread perception that parasites (in the broad sense, including microbial pathogens) threaten species with extinction, the simplest deterministic models of parasite dynamics (i.e. of specialist parasites with density‐dependent transmission) predict that parasites will always go extinct before their hosts. We review the primary theoretical mechanisms that allow disease‐induced extinction and compare them with the empirical literature on parasitic threats to populations to assess the importance of different mechanisms in threatening natural populations. Small pre‐epidemic population size and the presence of reservoirs are the most commonly cited factors for disease‐induced extinction in empirical studies.     

Life cycles shape parasite evolution: comparative population genetics of salmon trematodes

Little is known about what controls effective sizes and migration rates among parasite populations. Such data are important given the medical, veterinary, and economic (e.g., fisheries) impacts of many parasites. The autogenic-allogenic hypothesis, which describes ecological patterns of parasite distribution, provided the foundation on which we studied the effects of life cycles on the distribution of genetic variation within and among parasite populations. The hypothesis states that parasites cycling only in freshwater hosts (autogenic life cycle) will be more limited in their dispersal ability among aquatic habitats than parasites cycling through freshwater and terrestrial hosts (allogenic life cycle). By extending this hypothesis to the level of intraspecific genetic variation, we examined the effects of host dispersal on parasite gene flow. Our a priori prediction was that for a given geographic range, autogenic parasites would have lower gene flow among subpopulations. We compared intraspecific mitochondrial DNA variation for three described species of trematodes that infect salmonid fishes. As predicted, autogenic species had much more highly structured populations and much lower gene flow among subpopulations than an allogenic species sampled from the same locations. In addition, a cryptic species was identified for one of the autogenic trematodes. These results show how variation in life cycles can shape parasite evolution by predisposing them to vastly different genetic structures. Thus, we propose that knowledge of parasite life cycles will help predict important evolutionary processes such as speciation, coevolution, and the spread of drug resistance.     

Ecology of marine parasites

Important ecological aspects of marine parasites are discussed. Whereas effects of parasites on host individuals sometimes leading to death are known from many groups of parasites, effects on host populations have been studied much less. Mass mortalities have been observed mainly among hosts occurring in abnormally dense populations or after introduction of parasites by man. As a result of large-scale human activities, it becomes more and more difficult to observe effects of parasites on host populations under natural conditions. Particular emphasis is laid on ecological characteristics of parasites, such as host range and specificity, microhabitats, macrohabitats, food, life span, aggregated distribution, numbers and kinds of parasites, pathogenicity and mechanisms of reproduction and infection and on how such characteristics are affected by environment and hosts. It is stressed that host specificity indices which take frequency and/or intensity of infection into account, are a better measure of restriction of parasites to certain hosts than host range which simply is the number of host species found to be infected.     

Host resistance and coevolution in spatially structured populations

Natural, agricultural and human populations are structured, with a proportion of interactions occurring locally or within social groups rather than at random. This within-population spatial and social structure is important to the evolution of parasites but little attention has been paid to how spatial structure affects the evolution of host resistance, and as a consequence the coevolutionary outcome. We examine the evolution of resistance across a range of mixing patterns using an approximate mathematical model and stochastic simulations. As reproduction becomes increasingly local, hosts are always selected to increase resistance. More localized transmission also selects for higher resistance, but only if reproduction is also predominantly local. If the hosts disperse, lower resistance evolves as transmission becomes more local. These effects can be understood as a combination of genetic (kin) and ecological structuring on individual fitness. When hosts and parasites coevolve, local interactions select for hosts with high defence and parasites with low transmissibility and virulence. Crucially, this means that more population mixing may lead to the evolution of both fast-transmitting highly virulent parasites and reduced resistance in the host.