BIODIVERSITY RESEARCH: Parasites of exotic species in invaded areas: does lower diversity mean lower epizootic impact?

Aim Exotic species may serve as vectors for the introduction of parasites from their native range and may also become infected by parasites already present in invaded areas, but the total number of parasites infecting such exotic species in their invaded areas is typically less than that in their native range. We tested whether the diversity of parasites associated with exotic species in the native and invaded areas is related to the epizootic impact these parasites cause. Location Global. Methods We examined the diversity and epizootic impact of 384 parasite taxa associated with 22 exotic freshwater invertebrate species. The epizootic impact of each parasite was rated based on whether it had been documented to cause a major pathological impact on a large proportion of an infected host population (other than the invader under consideration). Results The total number of parasites associated with an exotic host in its native range was about twice that of all parasites associated with it in its entire invaded range. This was mainly because of the loss in the invaded areas of low impact parasites, whereas the average number of high impact parasites per host in these areas did not differ statistically from that in the native range. Main conclusions Our study suggests similar levels of adverse impact of parasites of exotic species in both their native and invaded areas. In addition to the introduction of highly pathogenic exotic parasites, other mechanisms that may be involved include (1) acquisition by the invaders of new high impact parasites in the invaded ranges, (2) high abundance of the invaders in their new ranges and (3) susceptibility of novel hosts to exotic parasites because of the ‘naive host syndrome’.     

The changing ecology of primate parasites: Insights from wild‐captive comparisons

Host movements, including migrations or range expansions, are known to influence parasite communities. Transitions to captivity—a rarely studied yet widespread human‐driven host movement—can also change parasite communities, in some cases leading to pathogen spillover among wildlife species, or between wildlife and human hosts. We compared parasite species richness between wild and captive populations of 22 primate species, including macro‐ (helminths and arthropods) and micro‐parasites (viruses, protozoa, bacteria, and fungi). We predicted that captive primates would have only a subset of their native parasite community, and would possess fewer parasites with complex life cycles requiring intermediate hosts or vectors. We further predicted that captive primates would have parasites transmitted by close contact and environmentally—including those shared with humans and other animals, such as commensals and pests. We found that the composition of primate parasite communities shifted in captive populations, especially because of turnover (parasites detected in captivity but not reported in the wild), but with some evidence of nestedness (holdovers from the wild). Because of the high degree of turnover, we found no significant difference in overall parasite richness between captive and wild primates. Vector‐borne parasites were less likely to be found in captivity, whereas parasites transmitted through either close or non‐close contact, including through fecal‐oral transmission, were more likely to be newly detected in captivity. These findings identify parasites that require monitoring in captivity and raise concerns about the introduction of novel parasites to potentially susceptible wildlife populations during reintroduction programs.     

Trematode parasites infect or die in snail hosts

The Red Queen hypothesis is based on the assumption that parasites must genetically match their hosts to infect them successfully. If the parasites fail, they are assumed to be killed by the host's immune system. Here, we tested this using sympatric (mostly susceptible) and allopatric (mostly resistant) populations of a freshwater snail and its trematode parasite. We determined whether parasites which do not infect are either killed or passed through the host's digestive tract and remain infectious. Our results show that parasites do not get a second chance: they either infect or are killed by the host. The results suggest strong selection against parasites that are not adapted to local host genotypes.     

A Late Campanian sphenodontid (Reptilia, Diapsida) from northern Patagonia

The fossil record of sphenodontids in the Southern Hemisphere is much longer than in Laurasia, where they became extinct after Early Cretaceous times. Recent works demonstrated the persistence of at least eilenodontine sphenodontids until the ‘mid’-Cretaceous of Patagonia. Focused examination of the Los Alamitos Formation collections provided remains of Late Campanian sphenodontids. Although the phylogenetic position of these remains is still uncertain, they belong to a new, unrecorded species of sphenodontid perhaps related to opisthodontians or primitive, toothed sapheosaurs. To cite this article: S. Apesteguía, C. R. Palevol 4 (2005).     

Parasite local maladaptation in the Canarian lizard Gallotia galloti (Reptilia: Lacertidae) parasitized by haemogregarian blood parasite

Biologists commonly assume that parasites are locally adapted since they have shorter generation times and higher fecundity than their hosts, and therefore evolve faster in the arms race against the host's defences. As a result, parasites should be better able to infect hosts within their local population than hosts from other allopatric populations. However, recent mathematical modelling has demonstrated that when hosts have higher migration rates than parasites, hosts may diversify their genes faster than parasites and thus parasites may become locally maladapted. This new model was tested on the Canarian endemic lizard and its blood parasite (haemogregarine genus). In this host–parasite system, hosts migrate more than parasites since lizard offspring typically disperse from their natal site soon after hatching and without any contact with their parents who are potential carriers of the intermediate vector of the blood parasite (a mite). Results of cross-infection among three lizard populations showed that parasites were better at infecting individuals from allopatric populations than individuals from their sympatric population. This suggests that, in this host–parasite system, the parasites are locally maladapted to their host.     

THE EFFECT OF ELEVATED MUTATION RATES ON THE EVOLUTION OF COOPERATION AND VIRULENCE OF PSEUDOMONAS AERUGINOSA

Within-host competition between parasite genotypes can play an important role in the evolution of parasite virulence. For example, competition can increase virulence by imposing selection for parasites that replicate at a faster absolute rate within the host, but may also decrease virulence by selecting for faster relative growth rates through social exploitation of conspecifics. For many parasites, both outcomes are possible. We investigated how competition affected the evolution of virulence of the opportunistic pathogen Pseudomonas aeruginosa in caterpillar hosts, over the course of an approximately 60 generation selection experiment. We initiated infections with clonal populations of either wild-type bacteria or an isogenic mutant with an approximately 100-fold higher mutation rate, resulting in low and high between-genotype competition, respectively. We observed the evolution of increased virulence, growth rate, and public goods cheating (exploitation of extracellular iron scavenging siderophores produced by ancestral populations) in mutator but not wild-type, populations. We conclude increases in absolute within-host growth rates appear to be more important than social cheating in driving virulence evolution in this experimental context.     

Parasites, sex, and clonal diversity in natural snail populations

Under the Red Queen hypothesis, host-parasite coevolution selects against common host genotypes. Although this mechanism might underlie the persistence of sexual reproduction, it might also maintain high clonal diversity. Alternatively, clonal diversity might be maintained by multiple origins of parthenogens from conspecific sexuals, a feature in many animal groups. Herein, we addressed the maintenance of overall genetic diversity by coevolving parasites, as predicted by the Red Queen hypothesis. We specifically examined the contribution of parasites to host clonal diversity and the frequency of sexually reproducing individuals in natural stream populations of Potamopyrgus antipodarum snails. We also tested the alternative hypothesis that clonal diversity is maintained by the input of clones by mutation from sympatric sexuals. Clonal diversity and the frequency of sexual individuals were both positively related to infection frequency. Surprisingly, although clones are derived by mutation from sexual snails, parasites explained more of the genotypic variation among parthenogenetic subpopulations. Our findings thus highlight the importance of parasites as drivers of clonal diversity, as well as sex.     

Babesia rodhaini: A study of the effects of immune serum

The effect of passively administered immune serum against B. rodhaini has been studied quantitatively. The curve relating the proportion of parasites surviving, to the dose of serum, is sigmoid with a steep middle region. Parasites are killed at a rate proportional to the dose of serum in the early stages of infection, but after about 24 h a residual population of parasites multiplies at a rate only slightly less than that of normal parasites in normal hosts. The slight reduction is attributed to a residual effect of immune serum, and to the induction of an active immune response inadequate to prevent continuing multiplication of parasites.

The relationship between log₁₀ (parasite dose) and ST₅₀ for groups of mice is used to measure the dose of infective parasites.     

Latitudinal gradients of parasite species richness in primates

Infectious disease risk is thought to increase in the tropics, but little is known about latitudinal gradients of parasite diversity. We used a comparative data set encompassing 330 parasite species reported from 119 primate hosts to examine latitudinal gradients in the diversity of micro and macroparasites per primate host species. Analyses conducted with and without controlling for host phylogeny showed that parasite species richness increased closer to the equator for protozoan parasites, but not for viruses or helminths. Relative to other major parasite groups, protozoa reported from wild primates were transmitted disproportionately by arthropod vectors. Within the protozoa, our results revealed that vector‐borne parasites showed a highly significant latitudinal gradient in species richness. This higher diversity of vector‐borne protozoa near the tropics could be influenced by a greater abundance or diversity of biting arthropods in the tropics, or by climatic effects on vector behaviour and parasite development. Many vector‐borne diseases, such as leishmaniasis, trypanosomiasis, and malaria pose risks to both humans and wildlife, and nearly one‐third of the protozoan parasites from free‐living primates in our data set have been reported to infect humans. Because the geographical distribution and prevalence of many vector‐borne parasites are expected to increase because of global warming, these results are important for predicting future parasite‐mediated threats to biodiversity and human health.     

The roles of intramembrane proteases in protozoan parasites

Intramembrane proteolysis is widely conserved throughout different forms of life, with three major types of proteases being known for their ability to cleave peptide bonds directly within the transmembrane domains of their substrates. Although intramembrane proteases have been extensively studied in humans and model organisms, they have only more recently been investigated in protozoan parasites, where they turn out to play important and sometimes unexpected roles. Signal peptide peptidases are involved in endoplasmic reticulum (ER) quality control and signal peptide degradation from exported proteins. Recent studies suggest that repurposing inhibitors developed for blocking presenilins may be useful for inhibiting the growth of Plasmodium, and possibly other protozoan parasites, by blocking signal peptide peptidases. Rhomboid proteases, originally described in the fly, are also widespread in parasites, and are especially expanded in apicomplexans. Their study in parasites has revealed novel roles that expand our understanding of how these proteases function. Within this diverse group of parasites, rhomboid proteases contribute to processing of adhesins involved in attachment, invasion, intracellular replication, phagocytosis, and immune evasion, placing them at the vertex of host–parasite interactions. This article is part of a Special Issue entitled: Intramembrane Proteases.     

EFFECTS OF EPISTASIS ON INFECTIVITY RANGE DURING HOST‐PARASITE COEVOLUTION

Understanding how parasites adapt to changes in host resistance is crucial to evolutionary epidemiology. Experimental studies have demonstrated that parasites are more capable of adapting to gradual, rather than sudden changes in host phenotype, as the latter may require multiple mutations that are unlikely to arise simultaneously. A key, but as yet unexplored factor is precisely how interactions between mutations (epistasis) affect parasite evolution. Here, we investigate this phenomenon in the context of infectivity range, where parasites may experience selection to infect broader sets of genotypes. When epistasis is strongly positive, we find that parasites are unlikely to evolve broader infectivity ranges if hosts exhibit sudden, rather than gradual changes in phenotype, in close agreement with empirical observations. This is due to a low probability of fixing multiple mutations that individually confer no immediate advantage. When epistasis is weaker, parasites are more likely to evolve broader infectivity ranges if hosts make sudden changes in phenotype, which can be explained by a balance between mutation supply and selection. Thus, we demonstrate that both the rate of phenotypic change in hosts and the form of epistasis between mutations in parasites are crucial in shaping the evolution of infectivity range.     

Parasites in food webs: the ultimate missing links

Parasitism is the most common consumer strategy among organisms, yet only recently has there been a call for the inclusion of infectious disease agents in food webs. The value of this effort hinges on whether parasites affect food‐web properties. Increasing evidence suggests that parasites have the potential to uniquely alter food‐web topology in terms of chain length, connectance and robustness. In addition, parasites might affect food‐web stability, interaction strength and energy flow. Food‐web structure also affects infectious disease dynamics because parasites depend on the ecological networks in which they live. Empirically, incorporating parasites into food webs is straightforward. We may start with existing food webs and add parasites as nodes, or we may try to build food webs around systems for which we already have a good understanding of infectious processes. In the future, perhaps researchers will add parasites while they construct food webs. Less clear is how food‐web theory can accommodate parasites. This is a deep and central problem in theoretical biology and applied mathematics. For instance, is representing parasites with complex life cycles as a single node equivalent to representing other species with ontogenetic niche shifts as a single node? Can parasitism fit into fundamental frameworks such as the niche model? Can we integrate infectious disease models into the emerging field of dynamic food‐web modelling? Future progress will benefit from interdisciplinary collaborations between ecologists and infectious disease biologists.     

On the specificity of avian blood parasites: revealing specific and generalist relationships between haemosporidians and biting midges

The study of host-parasite relationships involving vector-borne parasites requires understanding interactions between parasites and vectors. The capacity of haemosporidians to infect insects has clear evolutionary consequences for the transmission of diseases. Here, we investigated (i) the associations between blood parasites, biting midges and birds and (ii) the potential specificity between biting midge and haemosporidian haplotypes. A total of 629 parous biting midges Culicoides and 224 wild birds (belonging to seven species) from a locality of central Spain were individually examined for the presence of Haemoproteus and Plasmodium parasites by sequencing a fragment of cytochrome B. Biting midges were identified morphologically and characterized on the basis of a fragment of the cytochrome c oxidase (COI) gene. Overall, 12 Haemoproteus and three Plasmodium haplotypes were isolated and sequenced. Among them, 10 haplotypes were exclusively isolated from biting midges, three haplotypes only from birds and two haplotypes from both biting midges and birds. Biting midge haplotypes showed both specific and generalist relationships with Haemoproteus haplotypes but only generalist relationships with Plasmodium haplotypes. Several C. festivipennis and C. kibunesis haplotypes established significant coevolutionary links with Haemoproteus haplotypes. These results shed light on the specificity of interactions between vectors and blood parasites.     

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.     

The social parasite wasp Polistes atrimandibularis does not form host races

Parasites that exploit the parental behaviour of several host species may be selected to form distinct host-specific genetic lineages. This process is well documented in bird brood parasites, but not in insect social parasites. Polistes atrimandibularis is the only paper-wasp social parasite known to exploit four host species. It does not form genetically distinct host races according to analyses based on microsatellite loci. Also, there were no size-matching between parasites and host species. Instead, P. atrimandibularis queens seemed to be successful as parasites in this population only when they originated from nests of P. dominulus, the largest species. The other host species are a sink for P. atrimandibularis since adult females emerging from those nests appear too small to usurp colonies themselves. Traits that may help P. atrimandibularis infiltrate multiple species may include its nonaggressive usurpation tactics and its ability to acquire host cuticular hydrocarbon recognition labels.     

The tau mutation in the Syrian hamster differentially reprograms the circadian clock in the SCN and peripheral tissues

The hypothalamic suprachiasmatic nuclei (SCN), the principal circadian oscillator in mammals, are synchronized to the solar day by the light-dark cycle, and in turn, they coordinate circadian oscillations in peripheral tissues. The tau mutation in the Syrian hamster is caused by a point mutation leading to a deficiency in the ability of Casein Kinase 1epsilon to phosphorylate its targets, including circadian PER proteins. How this accelerates circadian period in neural tissues is not known, nor is its impact on peripheral circadian oscillators established. We show that this mutation has no effect on per mRNA expression nor the nuclear accumulation of PER proteins in the SCN. It does, however, accelerate the clearance of PER proteins from the nucleus to an extent sufficient to explain the shortened circadian period of behavioral rhythms. The mutation also has novel, unanticipated consequences for circadian timing in the periphery, including tissue-specific phase advances and/or reduced amplitude of circadian gene expression. The results suggest that the tau mutation accelerates a specific phase, during mid-late subjective night of the SCN circadian feedback loop, rather than cause a global compression of the entire cycle. This reprogrammed output from the clock is associated with peripheral desynchrony, which in turn could account for impaired growth and metabolic efficiency of the mutant.     

Effectively vertical transmission of a Drosophila‐parasitic nematode: mechanism and consequences

1. Long‐term control of insects by parasites is possible only if the parasite populations persist. Because parasite transmission rate depends on host density, parasite populations may go extinct during periods of low host density. Vertical transmission of parasites, however, is independent of host density and may therefore provide a demographic bridge through times when their insect hosts are rare. 2. The nematode Howardula aoronymphium, which parasitises mycophagous species of Drosophila, can experience both horizontal and effectively vertical transmission, relative rates of which depend, in theory at least, on the density of hosts at breeding sites. 3. A nine‐generation experiment was carried out in which nematodes were transmitted either exclusively vertically or primarily horizontally. This experiment revealed that these parasites can persist and exhibit positive population growth even when there is only vertical transmission. 4. Assays at the end of the experiment revealed that the vertically transmitted nematodes had suffered no inbreeding depression and that they were similar to the horizontally transmitted nematodes in terms of virulence, infectivity, within‐host growth rate, and fecundity. Thus, vertical transmission of H. aoronymphium did not appear to compromise the ability of these parasites to control Drosophila populations.     

The coevolutionary dynamics of obligate ant social parasite systems--between prudence and antagonism

In this synthesis we apply coevolutionary models to the interactions between socially parasitic ants and their hosts. Obligate social parasite systems are ideal models for coevolution, because the close phylogenetic relationship between these parasites and their hosts results in similar evolutionary potentials, thus making mutual adaptations in a stepwise fashion especially likely to occur. The evolutionary dynamics of host-parasite interactions are influenced by a number of parameters, for example the parasite's transmission mode and rate, the genetic structure of host and parasite populations, the antagonists' migration rates, and the degree of mutual specialisation. For the three types of obligate ant social parasites, queen-tolerant and queen-intolerant inquilines and slavemakers, several of these parameters, and thus the evolutionary trajectory, are likely to differ. Because of the fundamental differences in lifestyle between these social parasite systems, coevolution should further select for different traits in the parasites and their hosts. Queen-tolerant inquilines are true parasites that exert a low selection pressure on their host, because of their rarity and the fact that they do not conduct slave raids to replenish their labour force. Due to their high degree of specialisation and the potential for vertical transmission, coevolutionary theory would predict interactions between these workerless parasites and their hosts to become even more benign over time. Queen-intolerant inquilines that kill the host queen during colony take-over are best described as parasitoids, and their reproductive success is limited by the existing worker force of the invaded host nest. These parasites should therefore evolve strategies to best exploit this fixed resource. Slavemaking ants, by contrast, act as parasites only during colony foundation, while their frequent slave raids follow a predator prey dynamic. They often exploit a number of host species at a given site, and theory predicts that their associations are best described in terms of a highly antagonistic coevolutionary arms race.     

Parasites of native and exotic freshwater fishes in south‐western Australia

In this study, 1429 fishes of 18 different species (12 native and six exotic) were sampled from 29 localities to compare the levels of parasitism between native and exotic fish species and to examine the relationship between environmental degradation and parasite diversity. Forty‐four putative species of parasites were found and most of these appear to be native parasites, which have not previously been described. Two parasite species, Lernaea cyprinacea and Ligula intestinalis, are probably introduced. Both were found on or in a range of native fish species, where they may cause severe disease. Levels of parasitism and parasite diversity were significantly greater in native fishes than in exotic species, and this may contribute to an enhanced demographic performance and competitive ability in invading exotics. Levels of parasitism and parasite diversity in native fishes were negatively related to habitat disturbance, in particular to a suite of factors that indicate increased human use of the river and surrounding environment. This was due principally to the absence in more disturbed habitats of a number of species of endoparasites with complex life cycles, involving transmission between different host species.     

Avian host composition,local speciation and dispersal drive the regional assembly of avian malaria parasites in South American birds

Identifying the ecological factors that shape parasite distributions remains a central goal in disease ecology. These factors include dispersal capability, environmental filters and geographic distance. Using 520 haemosporidian parasite genetic lineages recovered from 7,534 birds sampled across tropical and temperate South America, we tested (a) the latitudinal diversity gradient hypothesis and (b) the distance–decay relationship (decreasing proportion of shared species between communities with increasing geographic distance) for this host–parasite system. We then inferred the biogeographic processes influencing the diversity and distributions of this cosmopolitan group of parasites across South America. We found support for a latitudinal gradient in diversity for avian haemosporidian parasites, potentially mediated through higher avian host diversity towards the equator. Parasite similarity was correlated with climate similarity, geographic distance and host composition. Local diversification in Amazonian lineages followed by dispersal was the most frequent biogeographic events reconstructed for haemosporidian parasites. Combining macroecological patterns and biogeographic processes, our study reveals that haemosporidian parasites are capable of circumventing geographic barriers and dispersing across biomes, although constrained by environmental filtering. The contemporary diversity and distributions of haemosporidian parasites are mainly driven by historical (speciation) and ecological (dispersal) processes, whereas the parasite community assembly is largely governed by host composition and to a lesser extent by environmental conditions.