Parasites as predators: unifying natural enemy ecology

Parasitism and predation have long been considered analogous interactions. Yet by and large, ecologists continue to study parasite-host and predator-prey ecology separately. Here we discuss strengths and shortcomings of the parasite-as-predator analogy and its potential to provide new insights into both fields. Developments in predator-prey ecology, such as temporal risk allocation and associational resistance, can drive new hypotheses for parasite-host systems. Concepts developed in parasite-host ecology, such as threshold host densities and phylodynamics, might provide new ideas for predator-prey ecology. Topics such as trait-mediated indirect effects and enemy-mediated facilitation provide opportunities for the two fields to work together. We suggest that greater unification of predator-prey and parasite-host ecology would foster advances in both fields.     

Summary and perspective on evolutionary ecology of fishes

This special issue of Evolutionary Ecology provides ten papers that have been presented at a conference on Evolutionary Ecology of Fishes in 2009. In addition to briefly summarizing the main content of the papers which is related to adaptive radiations, processes of ecological divergence, and fisheries-induced evolution, we review and synthesize in short the recent advance in studies on evolutionary ecology of fishes. We conclude that fishes are excellent model systems to study evolutionary ecology of animals, and suggest three promising new research avenues; (1) the contribution of behavioural processes to evolution, in particular the consideration of animal personalities and predator–prey interactions, (2) metabolic physiology and parasite-host interactions as new niche dimensions to be considered for adaptive diversification, and (3) the opportunities for mechanistic understanding of adaptation and speciation emerging from new genetic tools.     

The importance of clutch characteristics and learning for antiparasite adaptations in hosts of avian brood parasites

There is considerable variation in rejection rates of parasitic eggs among hosts of avian brood parasites. In this article, we develop a model that can be used to predict host egg rejection behavior in brood parasite-host systems in general, by considering both intra- and interclutch variation in host egg appearance; clutch characteristics that may be important in calculating the fitness of individuals adopting rejecter or acceptor strategies. In addition, we consider the importance of learning the appearance of own eggs during the first breeding attempt and host probability of survival between breeding seasons on evolution of rejection behavior. Based on this model we can predict at which level of parasitism fitness of rejecter individuals is higher than that of acceptor individuals and vice versa. The model analyses show that variation in egg appearance can be a key factor for the evolution of host defense against parasitism. In more detail, analyses show that we should expect to find a prolonged learning period only in hosts that have a high intraclutch variation in egg appearance, because such hosts may potentially experience high costs in terms of recognition errors. Furthermore, learning is in general more adaptive in parasite-host systems in which hosts do have some reproductive success even when parasitized, and when parasitism rates are moderate. By including variables that have not been considered in previous models, our model represents a useful tool in investigations of host rejection behavior in various host-parasite systems.     

Cuckoos, cowbirds and hosts: adaptations, trade-offs and constraints

The interactions between brood parasitic birds and their host species provide one of the best model systems for coevolution. Despite being intensively studied, the parasite-host system provides ample opportunities to test new predictions from both coevolutionary theory as well as life-history theory in general. I identify four main areas that might be especially fruitful: cuckoo female gentes as alternative reproductive strategies, non-random and nonlinear risks of brood parasitism for host individuals, host parental quality and targeted brood parasitism, and differences and similarities between predation risk and parasitism risk. Rather than being a rare and intriguing system to study coevolutionary processes, I believe that avian brood parasites and their hosts are much more important as extreme cases in the evolution of life-history strategies. They provide unique examples of trade-offs and situations where constraints are either completely removed or particularly severe.     

Organization of ETRAMPs and EXP-1 at the parasite-host cell interface of malaria parasites

The parasite-host cell interface is a key compartment of vacuolated intracellular pathogens but little is known about its molecular composition and architecture. We used in vivo cross-linking to analyse the parasite-host cell interface of asexual stages of the most virulent human malaria parasite Plasmodium falciparum. We show that the integral membrane protein members of the early transcribed membrane protein (ETRAMP) family and exported protein 1 (EXP-1), which are components of the parasite-host cell interface, form complexes of oligomeric arrays in this compartment. The most notable feature is that each ETRAMP member and EXP-1 define separate arrays, demonstrating that the protein distribution in this membrane is non-random. Each of three recombinant ETRAMPs readily oligomerized in bacterial membranes, confirming that these arrays can form independently of other Plasmodium proteins. We propose that the malaria parasite-host cell interface contains patches of integral membrane proteins forming a mosaic of different microdomains in this membrane.     

Biology of Cryptosporidium from marsupial hosts

The majority of biological data on Cryptosporidium has been collected from humans and domestic animal hosts which creates a bias in knowledge on the biodiversity and evolution of this parasite genus. Further to understanding Cryptosporidium biology are studies encompassing broad hosts that represent diverse taxa sampled across wide geographic ranges. Marsupials represent a group of wildlife hosts from which limited information on Cryptosporidium is available. As marsupial hosts are an ancient mammalian lineage they represent an important group for studying parasite evolution. This review summarises information of the biology, epidemiology and evolution of Cryptosporidium in marsupial hosts, and discusses the importance of further understanding interactions in this parasite-host system.     

Enterobius vermicularis: ancient DNA from North and South American human coprolites

A molecular paleoparasitological diagnostic approach was developed for Enterobius vermicularis. Ancient DNA was extracted from 27 coprolites from archaeological sites in Chile and USA. Enzymatic amplification of human mtDNA sequences confirmed the human origin. We designed primers specific to the E. vermicularis 5S ribosomal RNA spacer region and they allowed reproducible polymerase chain reaction identification of ancient material. We suggested that the paleoparasitological microscopic identification could accompany molecular diagnosis, which also opens the possibility of sequence analysis to understand parasite-host evolution.     

Description of Hygrobates aloisii sp. nov. from Hong Kong, a new species of Hygrobates (Lurchibates) subgen. nov. (Acari, Hydrachnidia, Hygrobatidae), with data on the parasite-host relationship to the Hong Kong Newt Paramesotriton hongkongensis (Amphibia, Caudata, Salamandridae)

Adults and deutonymphs of a new water mite species of the genus Hygrobates Koch, 1837 (Acari, Hydrachnidia, Hygrobatidae) were found to parasitize the Hong Kong Newt, Paramesotriton hongkongensis Myers and Leviton, 1962 (Amphibia, Caudata, Salamandridae), endemic to Hong Kong and coastal areas of Guangdong Province: Hygrobates aloisii sp. nov. Males and females, as well as deutonymphs and larvae are described. A new subgenus - Lurchibates subgen. nov. - is defined to accommodate the species of the Hygrobates salamandrarum-group. The parasite-host association, infestation rate, attachment sites and the impact of mite infestation on the newts behaviour and body condition are investigated. These ecological aspects of the parasite-host association between freshwater mites and newts are examined for the first time in detail in their natural habitat.     

Relative helminth size in crustacean hosts: in vivo determination, and effects of host gender and within-host competition in a copepod infected by a cestode

Crustaceans are important hosts for a number of helminth parasites, and they are increasingly used as models for studying the physiology, ecology and evolution of parasite-host interactions. In ecological studies, this interaction is commonly described only in terms of prevalence and number of larvae per infected host. However, the volume of helminth parasites can vary greatly, and this variation can potentially give important insights into the nature of a parasite-host relationship. It may influence and be influenced, for example, by within-host competition, host size, growth, and life history. Here we present a simple method that allows rapid approximation of the absolute and relative volumes of cestode larvae within copepod hosts of various developmental stages (nauplii, copepodites and adults). The measurements are taken in vivo without much disturbance of the animals, i.e. the technique allows study of growth and development of the parasites in relation to that of their hosts. The principles of this technique can be adopted to other helminth parasites and other crustacean hosts. Using this method in the copepod Macrocyclops albidus infected with the cestode Schistocephalus solidus, we found that the relative parasite size (= `parasite index') ranged from 0.5% to 6.5% of host size 14 days after infection. It was greater in male than in female hosts. With increasing number of parasites per host, the total parasite volume increased while the mean volume of the individual parasites decreased. The magnitude of the observed parasite indices, the large variation that was found within a sample of 46 infected adult copepods, and the observed correlates suggest that this new index can indeed be an important measure of parasite success and its pathogenecity.     

Molecular strategies to study Plasmodium-mosquito interactions

It is widely known that malaria kills millions of people every year. Less well recognized is the fact that the situation is steadily deteriorating for a lack of effective means to counter the disease. An essential first step towards the development of new approaches to fight malaria is a thorough understanding of the mechanisms that direct parasite growth and differentiation, including parasite-host interactions. This article reviews recent achievements and introduces some promising new technologies and approaches for studying host-parasite interactions.     

A mathematical model for the evolutions of anthelmintic resistance in a direct life cycle nematode parasite

Some of the elements required of a mathematical model for the evolution of anthelmintic resistance in strongylid nematodes are described. The model comprises a series of coupled first order differential equations and assumes the parasite has a direct life cycle with overlapping generations. The parasite-host system involved only a single host. In all the cases considered, drug resistance was assumed to be determined by two alleles at a single autosomal locus. The pretreatment allelic frequencies were maintained by heterozygote advantage involving the mortality of the free-living stages of the parasite. The model suggests that alternating anthelmintic with different modes of action may be a less effective resistance management strategy than administering the same drugs simultaneously.     

primetv: a viewer for reconciled trees

Background  

Evolutionary processes, such as gene family evolution or parasite-host co-speciation, can often be viewed as a tree evolving inside another tree. Relating two given trees under such a constraint is known as reconciling them. Adequate software tools for generating illustrations of tree reconciliations are instrumental for presenting and communicating results and ideas regarding these phenomena. Available visualization tools have been limited to illustrations of the most parsimonious reconciliation. However, there exists a plethora of biologically relevant non-parsimonious reconciliations. Illustrations of these general reconciliations may not be achieved without manual editing.     

Different infective forms trigger distinct immune response in experimental Chagas disease

Although metacyclic and blood trypomastigotes are completely functional in relation to parasite-host interaction and/or target cell invasion, they differ in the molecules present on the surface. Thus, aspects related to the variability that the forms of T. cruzi interacts with host cells may lead to fundamental implications on the immune response against this parasite and, consequently, the clinical evolution of Chagas disease. We have shown that BT infected mice presented higher levels of parasitemia during all the acute phase of infection. Moreover, the infection with either MT or BT forms resulted in increased levels of total leukocytes, monocytes and lymphocytes, specifically later for MT and earlier for BT. The infection with BT forms presented earlier production of proinflammatory cytokine TNF-α and later of IFN-γ by both T cells subpopulations. This event was accompanied by an early cardiac inflammation with an exacerbation of this process at the end of the acute phase. On the other hand, infection with MT forms result in an early production of IFN-γ, with subsequent control in the production of this cytokine by IL-10, which provided to these animals an immunomodulatory profile in the end of the acute phase. These results are in agreement with what was found for cardiac inflammation where animals infected with MT forms showed intense cardiac inflammation later at infection, with a decrease in the same at the end of this phase. In summary, our findings emphasize the importance of taking into account the inoculums source of T. cruzi, since vectorial or transfusional routes of T. cruzi infection may trigger distinct parasite-host interactions during the acute phase that may influence relevant biological aspects of chronic Chagas disease.     

Avian vision and the evolution of egg color mimicry in the common cuckoo

Coevolutionary arms races are a potent force in evolution, and brood parasite-host dynamics provide classical examples. Different host-races of the common cuckoo, Cuculus canorus, lay eggs in the nests of other species, leaving all parental care to hosts. Cuckoo eggs often (but not always) appear to match remarkably the color and pattern of host eggs, thus reducing detection by hosts. However, most studies of egg mimicry focus on human assessments or reflectance spectra, which fail to account for avian vision. Here, we use discrimination and tetrachromatic color space modeling of bird vision to quantify egg background and spot color mimicry in the common cuckoo and 11 of its principal hosts, and we relate this to egg rejection by different hosts. Egg background color and luminance are strongly mimicked by most cuckoo host-races, and mimicry is better when hosts show strong rejection. We introduce a novel measure of color mimicry-"color overlap"-and show that cuckoo and host background colors increasingly overlap in avian color space as hosts exhibit stronger rejection. Finally, cuckoos with better background color mimicry also have better pattern mimicry. Our findings reveal new information about egg mimicry that would be impossible to derive by the human eye.     

Characteristics of acquired resistance of lambs to mature ticks Hyalomma asiaticum asiaticum (experimental studies)]

A new method was employed for studies of parasite-host relationships between ixodid ticks and their hosts. It has been established that ixodid ticks are able to desensibilize the reactive sensibility of the host and to satiate themselves without unhibiting the latter. Every day and long parasitism of the ticks on cattle (in nature) and increasing doses of secretion of the ticks' saliva (sensibilizer) lead apparently to the weakening of the host's organism (desensitization). However, under laboratory conditions in hosts a resistence to bites of ixodid ticks can appear.     

Diversification and host switching in avian malaria parasites

The switching of parasitic organisms to novel hosts, in which they may cause the emergence of new diseases, is of great concern to human health and the management of wild and domesticated populations of animals. We used a phylogenetic approach to develop a better statistical assessment of host switching in a large sample of vector-borne malaria parasites of birds (Plasmodium and Haemoproteus) over their history of parasite-host relations. Even with sparse sampling, the number of parasite lineages was almost equal to the number of avian hosts. We found that strongly supported sister lineages of parasites, averaging 1.2% sequence divergence, exhibited highly significant host and geographical fidelity. Event-based matching of host and parasite phylogenetic trees revealed significant cospeciation. However, the accumulated effects of host switching and long distance dispersal cause these signals to disappear before 4% sequence divergence is achieved. Mitochondrial DNA nucleotide substitution appears to occur about three times faster in hosts than in parasites, contrary to findings on other parasite-host systems. Using this mutual calibration, the phylogenies of the parasites and their hosts appear to be similar in age, suggesting that avian malaria parasites diversified along with their modern avian hosts. Although host switching has been a prominent feature over the evolutionary history of avian malaria parasites, it is infrequent and unpredictable on time scales germane to public health and wildlife management.     

Complete chaos in a simple epidemiological model

A first-order difference equation which constitutes a simple model for a lethal parasite-host interaction is studied. Completing a study initiated by May and Anderson, the dynamics are shown to be completely chaotic.     

Interactions of the malaria parasite and its mammalian host

A hallmark of Plasmodium development inside its mammalian victim is the remarkable restriction to the host species. Adaptation to an intracellular life style in specific target cells is determined by multiple parasite-host interactions. The first line of crosstalk occurs during intradermal sporozoite injection by an Anopheles mosquito. The following expansion in the liver is highly efficient and leads to successful establishment of the parasite population. During the periodic waves of fevers and chills the parasite destroys and re-infects red blood cells. Recent advances in experimental genetics and imaging techniques begin to expose the complex interactions at the changing parasite-host interfaces. Understanding the cellular and molecular mechanisms of target cell recognition, nutrient acquisition, and hijacking of cellular and immune functions may ultimately explain the elaborate biology of a medically important single cell eukaryote.     

Modes of evolution in a parasite-host interaction: dis-entangling factors determining the evolution of regulated fimbriation in E. coli

Escherichia coli expresses type-I fimbriae; these are protrusions from the outer cell wall and have been identified as a virulence factor. They are also expressed by commensal strains of E. coli although (at any one time) only by a small proportion of the population. The orthodox interpretation of this is that fimbriation is regulated so as (i) to trigger a host-based release of nutrients in the form of inflammation signals by slightly activating host defenses and (ii) while avoiding a full scale inflammatory response. This article presents a number of computer simulations of the evolution of fimbriae to scrutinize the evolutionary plausibility of this orthodox view. It turns out that these simulations suggest a revised interpretation of the fimbriae mediated parasite-host interaction. Rather than being a passive victim the host is actively providing a niche that evolutionary favors less virulent parasites. The article closes with a number of testable predictions of this model.