Parasite Fitness Traits Under Environmental Variation: Disentangling the Roles of a Chytrid’s Immediate Host and External Environment

Parasite environments are heterogeneous at different levels. The first level of variability is the host itself. The second level represents the external environment for the hosts, to which parasites may be exposed during part of their life cycle. Both levels are expected to affect parasite fitness traits. We disentangle the main and interaction effects of variation in the immediate host environment, here the diatom Asterionella formosa (variables host cell volume and host condition through herbicide pre-exposure) and variation in the external environment (variables host density and acute herbicide exposure) on three fitness traits (infection success, development time and reproductive output) of a chytrid parasite. Herbicide exposure only decreased infection success in a low host density environment. This result reinforces the hypothesis that chytrid zoospores use photosynthesis-dependent chemical cues to locate its host. At high host densities, chemotaxis becomes less relevant due to increasing chance contact rates between host and parasite, thereby following the mass-action principle in epidemiology. Theoretical support for this finding is provided by an agent-based simulation model. The immediate host environment (cell volume) substantially affected parasite reproductive output and also interacted with the external herbicide exposed environment. On the contrary, changes in the immediate host environment through herbicide pre-exposure did not increase infection success, though it had subtle effects on zoospore development time and reproductive output. This study shows that both immediate host and external environment as well as their interaction have significant effects on parasite fitness. Disentangling these effects improves our understanding of the processes underlying parasite spread and disease dynamics.     

The costs of evolving resistance in heterogeneous parasite environments

The evolution of host resistance to parasites, shaped by associated fitness costs, is crucial for epidemiology and maintenance of genetic diversity. Selection imposed by multiple parasites could be a particularly strong constraint, as hosts either accumulate costs of multiple specific resistances or evolve a more costly general resistance mechanism. We used experimental evolution to test how parasite heterogeneity influences the evolution of host resistance. We show that bacterial host populations evolved specific resistance to local bacteriophage parasites, regardless of whether they were in single or multiple-phage environments, and that hosts evolving with multiple phages were no more resistant to novel phages than those evolving with single phages. However, hosts from multiple-phage environments paid a higher cost, in terms of population growth in the absence of phage, for their evolved specific resistances than those from single-phage environments. Given that in nature host populations face selection pressures from multiple parasite strains and species, our results suggest that costs may be even more critical in shaping the evolution of resistance than previously thought. Furthermore, our results highlight that a better understanding of resistance costs under combined control strategies could lead to a more 'evolution-resistant' treatment of disease.     

Unique physiology of host–parasite interactions in microsporidia infections

Microsporidia are intracellular parasites of all major animal lineages and have a described diversity of over 1200 species and an actual diversity that is estimated to be much higher. They are important pathogens of mammals, and are now one of the most common infections among immunocompromised humans. Although related to fungi, microsporidia are atypical in genomic biology, cell structure and infection mechanism. Host cell infection involves the rapid expulsion of a polar tube from a dormant spore to pierce the host cell membrane and allow the direct transfer of the spore contents into the host cell cytoplasm. This intimate relationship between parasite and host is unique. It allows the microsporidia to be highly exploitative of the host cell environment and cause such diverse effects as the induction of hypertrophied cells to harbour prolific spore development, host sex ratio distortion and host cell organelle and microtubule reorganization. Genome sequencing has revealed that microsporidia have achieved this high level of parasite sophistication with radically reduced proteomes and with many typical eukaryotic pathways pared-down to what appear to be minimal functional units. These traits make microsporidia intriguing model systems for understanding the extremes of reductive parasite evolution and host cell manipulation.     

Coinfecting parasites can modify fluctuating selection dynamics in host–parasite coevolution

Genetically specific interactions between hosts and parasites can lead to coevolutionary fluctuations in their genotype frequencies over time. Such fluctuating selection dynamics are, however, expected to occur only under specific circumstances (e.g., high fitness costs of infection to the hosts). The outcomes of host–parasite interactions are typically affected by environmental/ecological factors, which could modify coevolutionary dynamics. For instance, individual hosts are often infected with more than one parasite species and interactions between them can alter host and parasite performance. We examined the potential effects of coinfections by genetically specific (i.e., coevolving) and nonspecific (i.e., generalist) parasite species on fluctuating selection dynamics using numerical simulations. We modeled coevolution (a) when hosts are exposed to a single parasite species that must genetically match the host to infect, (b) when hosts are also exposed to a generalist parasite that increases fitness costs to the hosts, and (c) when coinfecting parasites compete for the shared host resources. Our results show that coinfections can enhance fluctuating selection dynamics when they increase fitness costs to the hosts. Under resource competition, coinfections can either enhance or suppress fluctuating selection dynamics, depending on the characteristics (i.e., fecundity, fitness costs induced to the hosts) of the interacting parasites.     

Intracellular parasitism: cell biological adaptations of parasitic protozoa to a life inside cells

Several protozoan parasites evade the host's immune defence because most of their development takes place inside specific host cells. Only a few of these protozoa live within the host cell cytosol. Most parasites are sequestered within membrane-bound compartments, collectively called ‘vacuoles’. Recent advances in the cell biology of intracellular parasites have revealed fundamental differences in the strategies whereby such organisms gain entry into their respective host cells. These differences have important implications for host-parasite interaction and for nutrient acquisition by the parasite. Leishmania spp. take advantage of the phagocytic properties of their host cells and presumably contribute little to the uptake process. In contrast, apicomplexan parasites have developed highly specialised organelles, called micronemes and rhoptries, to actively invade a variety of nucleated cells and, in the case of Plasmodium falciparum, human erythrocytes. Following invasion, parasites use a multitude of strategies to protect themselves from the defence mechanisms of the parasitized cells. In addition, they induce novel pathways within the infected cell that allow a most efficient nutrient acquisition both from the host cell cytoplasm and from the extracellular environment. Parasite-induced changes of host cells are most apparent in erythrocytes infected with Plasmodium spp. Mammalian erythrocytes are deficient in de novo protein and lipid biosynthesis and, consequently, pathways which allow the transport of macromolecules and small solutes are established by metabolic activities of the parasite. Research into the cell biology of intracellular parasitism has identified fascinating phenomena some of which we are beginning to understand at a molecular level. They are fascinating because they allow insights into a very intimate interaction between two eukaryotic cells of entirely different phylogenetic origins.     

Coexistence of three microsporidia parasites in populations of the freshwater amphipod Gammarus roeseli: evidence for vertical transmission and positive effect on reproduction

We investigated the prevalence, transmission mode and fitness effects of infections by obligatory intracellular, microsporidian parasites in the freshwater amphipod Gammarus roeseli. We found three different microsporidia species in this host, all using transovarial (vertical) transmission. All three coexist at different prevalences in two host populations, but bi-infected individuals were rarely found, suggesting no (or very little) horizontal transmission. It is predicted that vertically-transmitted parasites may exhibit sex-specific virulence in their hosts, or they may have either positive or neutral effects on host fitness. All three species differed in their transmission efficiency and infection intensity and our data suggest that these microsporidia exert sex-specific virulence by feminising male hosts. The patterns of infection we found exhibit convergent evolution with those of another amphipod host, Gammarus duebeni. Interestingly, we found that infected females breed earlier in the reproductive season than uninfected females. This is the first study, to our knowledge, to report a positive effect of microsporidian infection on female host reproduction.     

Consequences of host adaptation for performance of vesicular stomatitis virus in novel thermal environments

Although it is widely assumed that the selective advantage of niche specialization drives species biodiversity, some theory suggests that generalists are favored over specialists when environments change unexpectedly. But this idea is rarely tested empirically, and its relevance is unknown for microparasites such as RNA viruses. Due to their small genome sizes pleiotropy is not uncommon in RNA viruses. Therefore, the genetic architectures underlying generalist traits may be indirectly molded by selection to better prepare generalist organisms for growth in new environments. Previously, vesicular stomatitis viruses were evolved to specialize on a single host, or to generalize on multiple hosts. Here we test whether virus generalists arising in the context of host adaptation also perform differently than specialists when viruses grow at novel temperatures. We compared thermal reaction norms of performance, within and among groups of viral specialists and generalists. Results showed that host adaptation was consequential for some fitness traits at novel temperatures due to modification of pleiotropic viral genes. Contrary to theoretical predictions, host generalists were selectively disadvantaged at extreme cool and warm environments. Multi-host adaptation may compromise the evolved thermostability of viral proteins, creating a cost of host generalization when viruses replicate at extreme temperatures.     

RNA granules present only in extracellular toxoplasma gondii increase parasite viability

Toxoplasma gondii is an obligate intracellular parasite. When searching for a new cell to invade, the parasites have to confront the stress of being exposed to the extracellular environment. The mechanisms by which T. gondii survives outside the host cells are poorly understood. In this work we show that extracellular parasites form mRNA aggregates with characteristics of stress granules. Intracellular tachyzoites or bradyzoites do not form mRNA granules. We tested different stimuli that trigger granule formation in vitro and discovered that a buffer that mimics the host cell cytosol ionic composition (high potassium) strongly induces granule formation, suggesting that the granules arise when the parasites come in contact with the host cell cytosol during egress. We examined the importance of granule formation for parasite viability and show that the parasite populations that are able to form granules have a growth advantage, increased invasion, and decreased apoptosis in the extracellular environment. Overall, granule formation improves the fitness of extracellular parasites and increases the efficiency of the lytic cycle.     

Plasmodium berghei: Osmotic fragility of malaria parasites and mouse host erythrocytes

The osmotic properties of intraerythrocytic and ultrasonically liberated malaria parasites (Plasmodium berghei) were analyzed and compared with those of mouse host erythrocytes utilizing a multiple tube fragility test. Cells were incubated in phosphate buffered saline solutions of varying osmolalities ranging from 20–4000 mOsm. Changes in cell ultrastructure and parasite infectivity were used as indicators of osmotic damage. Intraerythrocytic and host cell-free plasmodia showed similar patterns of cell alteration and changes in infectivity following osmotic stress. The various developmental forms within each of the preparations responded somewhat differently to hypo-osmotic stress, however. The majority of merozoites seemed to be more sensitive than many trophozoites, schizonts, and segmenters. Small trophozoites were, on the average, more resistant than other developmental forms. Incubation of parasite populations in hypotonic salt solutions with osmolalities slightly greater than the infectivity threshold of 100 mOsm lysed the majority of the merozoites, whereas many small trophozoites were still intact. While normal erythrocytes were more resistant to hypo-osmotic stress than were either intracellular or free parasites, the majority of parasitized erythrocytes was less resistant than normal erythrocytes. The predominant alteration induced by hyperosmotic stress appears in the parasite's nuclear region with myelination of the nuclear membranes and chromatin clumping. The infectivity threshold in the hypertonic range was found to be approximately 2500 mOsm. Results indicate that these obligate intracellular parasites have a wide range of osmotic sensitivities and that they are capable of existing for short periods in various osmotic environments ranging from 100–2500 mOsm without complete loss of infectivity. This suggests that these parasites have osmotic regulatory capabilities at least comparable to those of host cells.     

Positive genetic correlation between female preference and offspring fitness

In many species, females display preferences for extreme male signal traits, but it has not been determined if such preferences evolve as a consequence of females gaining genetic benefits from exercising choice. If females prefer extreme male traits because they indicate male genetic quality that will enhance the fitness of offspring, a genetic correlation will evolve between female preference genes and genes that confer offspring fitness. We show that females of Drosophila serrata prefer extreme male cuticular hydrocarbon (CHC) blends, and that this preference affects offspring fitness. Female preference is positively genetically correlated with offspring fitness, indicating that females have gained genetic benefits from their choice of males. Despite male CHCs experiencing strong sexual selection, the genes underlying attractive CHCs also conferred lower offspring fitness, suggesting a balance between sexual selection and natural selection may have been reached in this population.     

Gimme shelter – the relative sensitivity of parasitic nematodes with direct and indirect life cycles to climate change

Climate change is expected to alter the dynamics of host–parasite systems globally. One key element in developing predictive models for these impacts is the life cycle of the parasite. It is, for example, commonly assumed that parasites with an indirect life cycle would be more sensitive to changing environmental conditions than parasites with a direct life cycle due to the greater chance that at least one of their obligate host species will go extinct. Here, we challenge this notion by contrasting parasitic nematodes with a direct life cycle against those with an indirect life cycle. Specifically, we suggest that behavioral thermoregulation by the intermediate host may buffer the larvae of indirectly transmitted parasites against temperature extremes, and hence climate warming. We term this the ‘shelter effect’. Formalizing each life cycle in a comprehensive model reveals a fitness advantage for the direct life cycle over the indirect life cycle at low temperatures, but the shelter effect reverses this advantage at high temperatures. When examined for seasonal environments, the models suggest that climate warming may in some regions create a temporal niche in mid‐summer that excludes parasites with a direct life cycle, but allows parasites with an indirect life cycle to persist. These patterns are amplified if parasite larvae are able to manipulate their intermediate host to increase ingestion probability by definite hosts. Furthermore, our results suggest that exploiting the benefits of host sheltering may have aided the evolution of indirect life cycles. Our modeling framework utilizes the Metabolic Theory of Ecology to synthesize the complexities of host behavioral thermoregulation and its impacts on various temperature‐dependent parasite life history components in a single measure of fitness, R₀. It allows quantitative predictions of climate change impacts, and is easily generalized to many host–parasite systems.     

Fitness Factors in Vibrios: a Mini-review

Vibrios are Gram-negative curved bacilli that occur naturally in marine, estuarine, and freshwater systems. Some species include human and animal pathogens, and some vibrios are necessary for natural systems, including the carbon cycle and osmoregulation. Countless in vivo and in vitro studies have examined the interactions between vibrios and their environment, including molecules, cells, whole animals, and abiotic substrates. Many studies have characterized virulence factors, attachment factors, regulatory factors, and antimicrobial resistance factors, and most of these factors impact the organism's fitness regardless of its external environment. This review aims to identify common attributes among factors that increase fitness in various environments, regardless of whether the environment is an oyster, a rabbit, a flask of immortalized mammalian cells, or a planktonic chitin particle. This review aims to summarize findings published thus far to encapsulate some of the basic similarities among the many vibrio fitness factors and how they frame our understanding of vibrio ecology. Factors representing these similarities include hemolysins, capsular polysaccharides, flagella, proteases, attachment factors, type III secretion systems, chitin binding proteins, iron acquisition systems, and colonization factors.     

A GCN2-like eukaryotic initiation factor 2 kinase increases the viability of extracellular Toxoplasma gondii parasites

Toxoplasmosis is a significant opportunistic infection caused by the protozoan parasite Toxoplasma gondii, an obligate intracellular pathogen that relies on host cell nutrients for parasite proliferation. Toxoplasma parasites divide until they rupture the host cell, at which point the extracellular parasites must survive until they find a new host cell. Recent studies have indicated that phosphorylation of Toxoplasma eukaryotic translation initiation factor 2-alpha (TgIF2α) plays a key role in promoting parasite viability during times of extracellular stress. Here we report the cloning and characterization of a TgIF2α kinase designated TgIF2K-D that is related to GCN2, a eukaryotic initiation factor 2α (eIF2α) kinase known to respond to nutrient starvation in other organisms. TgIF2K-D is present in the cytosol of both intra- and extracellular Toxoplasma parasites and facilitates translational control through TgIF2α phosphorylation in extracellular parasites. We generated a TgIF2K-D knockout parasite and demonstrated that loss of this eIF2α kinase leads to a significant fitness defect that stems from an inability of the parasite to adequately adapt to the environment outside host cells. This phenotype is consistent with that reported for our nonphosphorylatable TgIF2α mutant (S71A substitution), establishing that TgIF2K-D is the primary eIF2α kinase responsible for promoting extracellular viability of Toxoplasma. These studies suggest that eIF2α phosphorylation and translational control are an important mechanism by which vulnerable extracellular parasites protect themselves while searching for a new host cell. Additionally, TgIF2α is phosphorylated when intracellular parasites are deprived of nutrients, but this can occur independently of TgIF2K-D, indicating that this activity can be mediated by a different TgIF2K.     

Host sexual dimorphism and parasite adaptation

In species with separate sexes, parasite prevalence and disease expression is often different between males and females. This effect has mainly been attributed to sex differences in host traits, such as immune response. Here, we make the case for how properties of the parasites themselves can also matter. Specifically, we suggest that differences between host sexes in many different traits, such as morphology and hormone levels, can impose selection on parasites. This selection can eventually lead to parasite adaptations specific to the host sex more commonly encountered, or to differential expression of parasite traits depending on which host sex they find themselves in. Parasites adapted to the sex of the host in this way can contribute to differences between males and females in disease prevalence and expression. Considering those possibilities can help shed light on host-parasite interactions, and impact epidemiological and medical science.     

Infrapopulation sizes of co-occurring trematodes in the snail Ilyanassa obsoleta

This study addresses the infrapopulation sizes of 2 larval trematode species Himasthla quissetensis and Zoogonus rubellus as they co-occur within their estuarine snail host Ilyanassa obsoleta. Rediae of H. quissetensis and sporocysts of Z rubellus were counted in snails singly infected with each parasite and in snails infected with both. Comparisons of the counts indicate that infrapopulations of H. quissetensis were unaffected by co-occurrence with Z rubellus. However, Z. rubellus infrapopulations were reduced when co-occurring with H. quissetensis. It is proposed that this situation does not result from an interspecific interaction between parasite species. Although this double infection is relatively frequent in certain snail populations, it is contended that these trematode species do not co-occur often enough to evolve responses to one another. However, the host environment must be encountered in each life cycle, and both trematode species must be adapted to use it. On this basis, whatever happens when these 2 species occupy the same host is based on adaptations of the parasites to the host. It is proposed that these parasites are adapted to self-limit their infrapopulations in the snail host. They can, thus, preserve and use the host for many years and thereby enhance total cercarial transmission (fitness). Infrapopulation sizes would be determined by host resource levels, which, among other factors, would be influenced by the presence of multiple parasite species. In single infections, by far the most common situation, host resource levels would be set by the nutritional status or age (size) of the host (or both). The reduced infrapopulation sizes of Z rubellus on co-occurrence suggest that this trematode is more sensitive to host resource levels than is H. quissetensis.     

Host specificity of microbiome assembly and its fitness effects in phytoplankton

Insights into symbiosis between eukaryotic hosts and their microbiomes have shifted paradigms on what determines host fitness, ecology, and behavior. Questions remain regarding the roles of host versus environment in shaping microbiomes, and how microbiome composition affects host fitness. Using a model system in ecology, phytoplankton, we tested whether microbiomes are host-specific, confer fitness benefits that are host-specific, and remain conserved in time in their composition and fitness effects. We used an experimental approach in which hosts were cleaned of bacteria and then exposed to bacterial communities from natural environments to permit recruitment of microbiomes. We found that phytoplankton microbiomes consisted of a subset of taxa recruited from these natural environments. Microbiome recruitment was host-specific, with host species explaining more variation in microbiome composition than environment. While microbiome composition shifted and then stabilized over time, host specificity remained for dozens of generations. Microbiomes increased host fitness, but these fitness effects were host-specific for only two of the five species. The shifts in microbiome composition over time amplified fitness benefits to the hosts. Overall, this work solidifies the importance of host factors in shaping microbiomes and elucidates the temporal dynamics of microbiome compositional and fitness effects.Subject terms: Microbial ecology, Freshwater ecology     

The evolutionary transition to coloniality promotes higher blood parasitism in birds

Parasitism has been argued as one of the major costs of breeding sociality in birds. However, there is no clear evidence for an increased parasite pressure associated with the evolutionary transition from solitary to colonial breeding. I used the pairwise comparative method to test whether colonial bird species incur in a greater risk of infection and if they must to face with a greater diversity of blood parasites (Haematozoa), by comparing pairs of congeners that included one solitary and one colonial breeding species. The richness, both in terms of number of species and number of genera, as well as the prevalence of blood parasites resulted higher in colonial species than in their solitary breeding sisters, while controlling for differences in research effort and other potentially confounding effects. These results point towards higher transmission rates of blood parasites among colonial hosts. Given the detrimental effects of blood parasites on their host fitness, the higher risk of infection and the exposition to a more diverse parasite fauna may have imposed an important cost associated to the evolution of avian coloniality. This may help to explain why colonial species have larger immune system organs, as well as to explore differences in other host life history traits potentially shaped by blood parasites.     

Living off a fish: a trade-off between parasites and the immune system

Research in fish immune system and parasite invasion mechanisms has advanced the knowledge of the mechanisms whereby parasites evade or cope with fish immune response. The main mechanisms of immune evasion employed by fish parasites are reviewed and considered under ten headings. 1) Parasite isolation: parasites develop in immuno-privileged host tissues, such as brain, gonads, or eyes, where host barriers prevent or limit the immune response. 2) Host isolation: the host cellular immune response isolates and encapsulates the parasites in a dormant stage without killing them. 3) Intracellular disguise: typical of intracellular microsporidians, coccidians and some myxosporeans. 4) Parasite migration, behavioural and environmental strategies: parasites migrate to host sites the immune response has not yet reached or where it is not strong enough to kill them, or they accommodate their life cycles to the season or the age in which the host immune system is down-regulated. 5) Antigen-based strategies such as mimicry or masking, variation and sharing of parasite antigens. 6) Anti-immune mechanisms: these allow parasites to resist innate humoral factors, to neutralize host antibodies or to scavenge reactive oxygen species within macrophages. 7) Immunodepression: parasites either suppress the fish immune systems by reducing the proliferative capacity of lymphocytes or the phagocytic activity of macrophages, or they induce apoptosis of host leucocytes. 8) Immunomodulation: parasites secrete or excrete substances which modulate the secretion of host immune factors, such as cytokines, to their own benefit. 9) Fast development: parasites proliferate faster than the ability of the host to mount a defence response. 10) Exploitation of the host immune reaction. Knowledge of the evasion strategies adopted by parasites will help us to understand host-parasite interactions and may therefore help in the discovery of novel immunotherapeutic agents or targeted vaccines, and permit the selection of host-resistant strains.     

Intracellular survival of apicomplexan parasites and host cell modification

The intracellular stages of apicomplexan parasites are known to extensively modify their host cells to ensure their own survival. Recently, considerable progress has been made in understanding the molecular details of these parasite-dependent effects for Plasmodium-, Toxoplasma- and Theileria-infected cells. We have begun to understand how Plasmodium liver stage parasites protect their host hepatocytes from apoptosis during parasite development and how they induce an ordered cell death at the end of the liver stage. Toxoplasma parasites are also known to regulate host cell survival pathways and it has been convincingly demonstrated that they block host cell major histocompatibility complex (MHC)-dependent antigen presentation of parasite epitopes to avoid cell-mediated immune responses. Theileria parasites are the masters of host cell modulation because their presence immortalises the infected cell. It is now accepted that multiple pathways are activated to induce Theileria-dependent host cell transformation. Although it is now known that similar host cell pathways are affected by the different parasites, the outcome for the infected cell varies considerably. Improved imaging techniques and new methods to control expression of parasite and host cell proteins will help us to analyse the molecular details of parasite-dependent host cell modifications.     

南极鱼类后生动物寄生虫研究进展: 线虫、绦虫与桡足类

极端的环境造就了南极独特的生物群体, 其中鱼类是南大洋生态系统中最具多样性的脊椎动物, 也是许多寄生虫的中间或终末宿主。南极鱼类寄生虫种类丰富, 是南大洋海洋生物多样性的重要组成部分。探究南极鱼类及其寄生虫的营养关系可为阐释南极海洋生态系统功能及其变动提供重要的生态数据。虽然关于南极鱼类寄生虫的研究已有一百多年的历史, 但这些研究主要集中在寄生虫的种类鉴定、区系调查和组织病理等方面。由于南极鱼类寄生虫研究跨度时间长、地域范围广, 相关研究较为零散。文章综述了南极鱼类寄生线虫、绦虫以及桡足类的种类组成、宿主范围和地理分布等方面的研究, 并对今后开展南极鱼类寄生虫研究工作提出了展望。