Phylogenetic systematics and evolution of primate-derived Pneumocystis based on mitochondrial or nuclear DNA sequence comparison

Previous studies have demonstrated that the agent of Pneumocystis pneumonia (PcP), Pneumocystis carinii, is actually a complex of eukaryotic organisms, and cophylogeny could explain the distribution of the hosts and parasites. In the present work, we tested the hypothesis of cophylogeny between the primate-derived Pneumocystis group and their hosts. Specific strains isolated from 20 primate species, including humans, were used to produce a phylogeny of the parasites. Aligned sequences corresponding to DNA sequences of three genes (DHPS, mtSSU-rRNA, and mtLSU-rRNA) were separately analyzed and then combined in a single data set. The resulting parasite phylogeny was compared with different controversial phylogenies for the hosts. This comparison demonstrated that, depending upon which topology is accepted for the hosts, at least 61% and perhaps 77% of the homologous nodes of the respective cladograms of the hosts and parasites may be interpreted as resulting from codivergence events. This finding and the high specificity of these parasites suggests that cophylogeny may be considered the dominant pattern of evolution for Pneumocystis organisms, representing a new example of parallel evolution between primates and their specific parasites. Because the phylogeny of Pneumocystis followed very closely the differentiation of their hosts at the species level, the study of the parasites could provide valuable information on the phylogeny of their hosts. We used this information to explore controversial hypotheses of the phylogeny of the Platyrrhini by comparison with the phylogeny of their specific Pneumocystis parasites. If these organisms were closely associated as lung parasites with primates through the ages, the hypothesis of the Pneumocystis spp. being new pathogenic agents could be refuted. However, these organisms are opportunistic symbionts, becoming pathogenic whenever the immunological defences of their hosts decline. This study also provides support for the hypothesis that the different Pneumocystis species are genetically independent organisms, helping to clarify their taxonomic status.     

War and peace: social interactions in infections

One of the most striking facts about parasites and microbial pathogens that has emerged in the fields of social evolution and disease ecology in the past few decades is that these simple organisms have complex social lives, indulging in a variety of cooperative, communicative and coordinated behaviours. These organisms have provided elegant experimental tests of the importance of relatedness, kin discrimination, cooperation and competition, in driving the evolution of social strategies. Here, we briefly review the social behaviours of parasites and microbial pathogens, including their contributions to virulence, and outline how inclusive fitness theory has helped to explain their evolution. We then take a mechanistically inspired ‘bottom-up’ approach, discussing how key aspects of the ways in which parasites and pathogens exploit hosts, namely public goods, mobile elements, phenotypic plasticity, spatial structure and multi-species interactions, contribute to the emergent properties of virulence and transmission. We argue that unravelling the complexities of within-host ecology is interesting in its own right, and also needs to be better incorporated into theoretical evolution studies if social behaviours are to be understood and used to control the spread and severity of infectious diseases.     

Ecological impacts of parasitic chytrids,syndiniales and perkinsids on populations of marine photosynthetic dinoflagellates

Parasitism is a widespread interaction that plays significant roles in ecosystem balance and evolution. Historically the biology of zoosporic parasites is often a neglected field when studying aquatic ecological dynamics, especially in marine ecosystems. In the marine environment, dinoflagellates represent a significantly large component of primary production, and may be infected by a variety of fungal and fungus-like parasites including chytrids, syndiniales, and perkinsids as well as other microorganisms. The relationship between these organisms and their dinoflagellate hosts constitutes a highly significant pathosystem given the increasing importance of aquaculture. Because of their small size and lack of morphological characteristics these organisms are difficult to identify. This review compares the taxonomy, life cycle, host range, infection strategies, and ecological roles of species of Parvilucifera, Amoebophrya and Dinomyces which are parasites of dinoflagellates. Most of these species have only been described recently. Implications for environmental management are discussed.     

How parasite interaction strategies alter virulence evolution in multi‐parasite communities

The majority of organisms host multiple parasite species, each of which can interact with hosts and competitors through a diverse range of direct and indirect mechanisms. These within‐host interactions can directly alter the mortality rate of coinfected hosts and alter the evolution of virulence (parasite‐induced host mortality). Yet we still know little about how within‐host interactions affect the evolution of parasite virulence in multi‐parasite communities. Here, we modeled the virulence evolution of two coinfecting parasites in a host population in which parasites interacted through cross immunity, immune suppression, immunopathology, or spite. We show (1) that these within‐host interactions have different effects on virulence evolution when all parasites interact with each other in the same way versus when coinfecting parasites have unique interaction strategies, (2) that these interactions cause the evolution of lower virulence in some hosts, and higher virulence in other hosts, depending on the hosts infection status, and (3) that for cross immunity and spite, whether parasites increase or decrease the evolutionarily stable virulence in coinfected hosts depended on interaction strength. These results improve our understanding of virulence evolution in complex parasite communities, and show that virulence evolution must be understood at the community scale.     

Diversity matters: how bees benefit from different resin sources

Biodiverse environments provide a variety of resources that can be exploited by consumers. While many studies revealed a positive correlation between biodiversity and consumer biomass and richness, only few studies have investigated how resource diversity affects single consumers. To better understand whether a single consumer species benefits from diverse resources, we tested how the protective function of a defensive plant resource (i.e. resin exploited by social bees) varied among different sources and target organisms (predators, parasites and pathogens). To assess synergistic effects, resins from different plant genera were tested separately and in combination. We found that resin diversity is beneficial for bees, with its functional properties depending on the target organisms, type and composition of resin. Different resins showed different effects, and mixtures were more effective than some of the single resins (functional complementarity). We conclude that resins of different plant species target different organisms and act synergistically where combined. Bees that rely on resin for protection benefit more when they have access to diverse resin sources. Loss of biodiversity may in turn destabilize consumer populations due to restricted access to a variety of resources.     

Evolution of pathogens in a man-made world.

Human activities have resulted in substantial, large-scale environmental modifications, especially in the past century. Ecologists and evolutionary biologists are increasingly coming to realize that parasites and pathogens, like free-living organisms, evolve as the consequence of these anthropogenic changes. Although this area now commands the attention of a variety of researchers, a broad predictive framework is lacking, mainly because the links between human activities, the environment and parasite evolution are complex. From empirical and theoretical examples chosen in the literature, we give an overview of the ways in which humans can directly or indirectly influence the evolution of different traits in parasites (e.g. specificity, virulence, polymorphism). We discuss the role of direct and indirect factors as diverse as habitat fragmentation, pollution, biodiversity loss, climate change, introduction of species, use of vaccines and antibiotics, ageing of the population, etc. We also present challenging questions for further research. Understanding the links between anthropogenic changes and parasite evolution needs to become a cornerstone of public health planning, economic development and conservation biology.     

Complex interactions among a nematode parasite (Daubaylia potomaca), a commensalistic annelid (Chaetogaster limnaei limnaei), and trematode parasites in a snail host (Helisoma anceps)

Many biotic interactions can affect the prevalence and intensity of parasite infections in aquatic snails. Historically, these studies have centered on interactions between trematode parasites or between trematodes and other organisms. The present investigation focuses on the nematode parasite Daubaylia potomaca and its interactions with a commensal, Chaetogaster limnaei limnaei , and a variety of trematode species. It was found that the presence of C. l. limnaei indirectly increased the mean intensity of D. potomaca infections, apparently by acting as a restraint for various trematode parasites, particularly the rediae of Echinostoma sp. In turn, Echinostoma sp. rediae adversely affected the mean intensity of D. potomaca by their consumption of both juvenile and adult nematodes present in tissues of the snail. These organisms not only belong to 3 different phyla but occupy distinct trophic levels as well. The complex interactions among these 3 organisms in the snail host provide an excellent example of biotic interactions influencing the infection dynamics of parasites in aquatic snails.     

The evolution of host protection by vertically transmitted parasites

Hosts are often infected by a variety of different parasites, leading to competition for hosts and coevolution between parasite species. There is increasing evidence that some vertically transmitted parasitic symbionts may protect their hosts from further infection and that this protection may be an important reason for their persistence in nature. Here, we examine theoretically when protection is likely to evolve and its selective effects on other parasites. Our key result is that protection is most likely to evolve in response to horizontally transmitted parasites that cause a significant reduction in host fecundity. The preponderance of sterilizing horizontally transmitted parasites found in arthropods may therefore explain the evolution of protection seen by their symbionts. We also find that protection is more likely to evolve in response to highly transmissible parasites that cause intermediate, rather than high, virulence (increased death rate when infected). Furthermore, intermediate levels of protection select for faster, more virulent horizontally transmitted parasites, suggesting that protective symbionts may lead to the evolution of more virulent parasites in nature. When we allow for coevolution between the symbiont and the parasite, more protection is likely to evolve in the vertically transmitted symbionts of longer lived hosts. Therefore, if protection is found to be common in nature, it has the potential to be a major selective force on host–parasite interactions.     

Experimental coevolution leads to a decrease in parasite-induced host mortality

Host-parasite coevolution can lead to a variety of outcomes, but whereas experimental studies on clonal populations have taken prominence over the last years, experimental studies on obligately out-crossing organisms are virtually absent so far. Therefore, we set up a coevolution experiment using four genetically distinct lines of Tribolium castaneum and its natural obligately killing microsporidian parasite, Nosema whitei. After 13 generations of experimental coevolution, we employed a time-shift experiment infecting hosts from the current generation with parasites from nine different time points in coevolutionary history. Although initially parasite-induced mortality showed synchronized fluctuations across lines, a general decrease over time was observed, potentially reflecting evolution towards optimal levels of virulence or a failure to adapt to coevolving sexual hosts.     

Metallothionein protein evolution: a miniassay

Metallothionein (MT) evolution is one of the most obscure yet fascinating aspects of the study of these atypical metal-binding peptides. The different members of the extremely heterogeneous MT protein superfamily probably evolved through a web of duplication, functional differentiation, and/or convergence events leading to the current scenario, which is particularly hard to interpret in terms of molecular evolution. Difficulties in drawing straight evolutionary relationships are reflected in the lack of definite MT classification criteria. Presently, MTs are categorized either according to a pure taxonomic clustering or depending on their metal binding preferences and specificities. Extremely well documented MT revisions were recently published. But beyond classic approaches, this review of MT protein evolution will bring together new aspects that have seldom been discussed before. Hence, the emergence of life on our planet, since metal ion utilization is accepted to be at the root of the emergence of living organisms, and global trends that underlie structural and functional MT diversification, will be presented. Major efforts are currently being devoted to identifying rules for function-constrained MT evolution that may be applied to different groups of organisms.     

Host life span and the evolution of resistance characteristics

There is a wide variety of resistance mechanisms that hosts may evolve in response to their parasites. These can be functionally classified as avoidance (lower probability of becoming infected), recovery (faster rate of clearance), tolerance (reduced death rate when infected), or acquired immunity. It is commonly thought that longer lived organisms should invest more in costly resistance. We show that due to epidemiological feedbacks the situation is often more complex. Using evolutionary theory we examine how the optimal investment in costly resistance varies with life span in a broad range of scenarios. In the absence of acquired immunity, longer lived populations do generally invest more in resistance. If hosts have acquired immunity, the optimal resistance may either increase or decrease with increasing life span. In addition, there may be evolutionary bistability with high and low investments in avoidance or tolerance. The optimal investment in the duration of acquired immunity always increases with life span, and due to bistability, shorter lived hosts may commonly not evolve any immunity. In contrast, the optimal investment in the probability of acquiring immunity initially increases and then decreases with life span. Our results have important implications for the evolution of invertebrate and vertebrate immunity, and for the evolution of acquired immunity itself.     

Do parasites express receptors for host lipoproteins?

Although cholesterol is the predominant sterol in parasite tissue, many parasites are unable to synthesize cholesterol or longchain fatty acids, de novo, and must therefore obtain these components from the host. Of particular interest are the plasma lipoproteins, a rich and abundant source of cholesterol, and other lipids that could be used by parasites inhabiting the vascular system of their host or with access to plasma proteins at extravascular sites. It is not inconceivable that parasites may have evolved a variety of receptors for lipoproteins by convergent evolution. Here, Mark Rogers discusses evidence for the presence of lipoprotein receptors in protozoan and metazoan parasites of mammals.     

Fish introduction and parasites in marine ecosystems: a need for information

Invasive species provide unique and useful systems by which to examine various ecological and evolutionary issues, both in terms of the effects on native environments and the subsequent evolutionary impacts. While biological invasions are an increasing agent of change in aquatic systems, alien species also act as vectors for new parasites and diseases. To date, colonizations by hosts and parasites have not been treated and reviewed together, although both are usually interwoven in various ways and may have unpredictable negative consequences. Fish are widely introduced worldwide and are convenient organisms to study parasites and diseases. We report a global overview of fish invasions with associated parasitological data. Data available on marine and freshwater are in sharp contrast. While parasites and diseases of inland freshwater fish, ornamental, reared and anadromous fish species are well documented, leading to the emergence of several evolutionary hypotheses in freshwater ecosystems during the last decade, the transfer of such organisms are virtually unexplored in marine ecosystems. The paucity of information available on the parasites of introduced marine fish reflects the paucity of information currently available on parasites of non-indigenous species in marine ecosystems. However, such information is crucial as it can allow estimations of the extent to which freshwater epidemiology/evolution can be directly transferred to marine systems, providing guidelines for adapting freshwater control to the marine environment.     

General Rules for Optimal Codon Choice

Different synonymous codons are favored by natural selection for translation efficiency and accuracy in different organisms. The rules governing the identities of favored codons in different organisms remain obscure. In fact, it is not known whether such rules exist or whether favored codons are chosen randomly in evolution in a process akin to a series of frozen accidents. Here, we study this question by identifying for the first time the favored codons in 675 bacteria, 52 archea, and 10 fungi. We use a number of tests to show that the identified codons are indeed likely to be favored and find that across all studied organisms the identity of favored codons tracks the GC content of the genomes. Once the effect of the genomic GC content on selectively favored codon choice is taken into account, additional universal amino acid specific rules governing the identity of favored codons become apparent. Our results provide for the first time a clear set of rules governing the evolution of selectively favored codon usage. Based on these results, we describe a putative scenario for how evolutionary shifts in the identity of selectively favored codons can occur without even temporary weakening of natural selection for codon bias.     

Myrmica ants host highly diverse parasitic communities: from social parasites to microbes

Myrmica ants have been model species for studies in a variety of disciplines, including insect physiology, chemical communication, ant social dynamics, ant population, community ecology, and ant interactions with other organisms. Species belonging to the genus Myrmica can be found in virtually every habitat within the temperate regions of the northern hemisphere and their biology and systematics have been thoroughly studied. These ants serve as hosts to highly diverse parasitic organisms from socially parasitic butterfly caterpillars to microbes, and many Myrmica species even evolved into parasitizing species of their own genus. These parasites have various impacts both on the individuals and on the social structure of their hosts, ranging from morphological malformations to reduction in colony fitness. A comprehensive review of the parasitic organisms supported by Myrmica and the effects of these organisms on individuals and on whole ant colonies has not yet been compiled. Here, we provide a review of the interactions of these organisms with Myrmica ants by discussing host and parasite functional, behavioral or physiological adaptations. In addition, for all “symbiont groups” of Myrmica ants described in this paper, we examine the present limitations of the knowledge at present of their impact on individuals and host colony fitness. In conclusion, we argue that Myrmica ants serve as remarkable resource for the evolution of a wide variety of associated organisms.     

Parasites of the superorganism: are they indicators of ecosystem health?

The concept of ecosystem health is derived from analogies with human health, which subsequently leads to the implication that the ecosystem has organismal properties, a 'superorganism' in the Clementsian sense. Its application and usefulness has been the subject of a contentious debate; yet, the term 'ecosystem health' has captured the public's imagination and woven its way into the current lexicon, even incorporated into public policy. However, the application of parasites as bioindicators of ecosystem health poses a curious conundrum. Perceptions of parasites range from mild distaste to sheer disgust among the general public, the media, environmental managers and non-parasitologists in the scientific community. Nevertheless, the biological nature of parasitism incorporates natural characteristics that are informative and useful for environmental management. The helminths in particular have evolved elegant means to ensure their transmission, often relying on complex life cycle interactions that include a variety of invertebrate and vertebrate hosts. The assemblage of these diverse parasites within a host organism potentially reflect that host's trophic position within the food web as well as the presence in the ecosystem of any other organisms that participate in the various parasite life cycles. Perturbations in ecosystem structure and function that affect food web topology will also impact upon parasite transmission, thus affecting parasite species abundance and composition. As such, parasite populations and communities are useful indicators of environmental stress, food web structure and biodiversity. In addition, there may be useful other means to utilise parasitic organisms based on their biology and life histories such as suites or guilds that may be effective bioindicators of particular forms of environmental degradation. The challenge for parasitology is to convince resource managers and fellow scientists that parasites are a natural part of all ecosystems, each species being a potentially useful information unit, and that healthy ecosystems have healthy parasites.     

Transmission stages of Plasmodium: does the parasite use the one same signal, provided both by the host and the vector, for gametocytogenesis and sporozoite maturation?

Among the microorganisms that strictly depend upon other organisms (hosts or vectors) for achieving their life cycle, protozoan and metazoan parasites have been often primarily distinguished through the major pathogenic processes they could induce. A variety of different mechanisms linked to parasitism can indeed systemically (e.g. Plasmodium falciparum) or locally (e.g. Toxoplasma gondii) induce important alterations of tissue homeostasis. But more than obvious pathogenicity, it is the capacity to be transmitted that is essential for parasite survival and there is increasing evidence that certain parasites can achieve their life cycle to the point of transmission in the absence of clinically detectable processes. For this, constitutive microenvironments of the host or vector can be exploited. Moreover, parasites are sometimes able to highjack effectors of the host's immune response towards conditioning the microenvironments which are permissive to differentiation of transmissible developmental stages. Based on a few examples taken from studies on the transmission stages of Leishmania, Toxoplasma and Plasmodium, we have here attempted to formulate a few hypothesis on the biology of the transmission stages of P. falciparum, i.e. on gametocytogenesis and sporozoite maturation. As discussants, we may have been somewhat dwarfed by issues evoked by the organizers of this meeting in the title of the session, i.e. 'Vector-parasite-man interactions'!... In reaction, we may have taken refuge in somewhat over-selective comments, biased by the objects of our personal research....