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Reconciling genetic expectations from host specificity with historical population dynamics in an avian brood parasite, Horsfield's Bronze-Cuckoo Chalcites basalis of Australia.

Mitochondrial DNA (mtDNA) is being used increasingly to explore the evolution of host specificity in avian brood parasites. A stable coevolutionary equilibrium between multiple phylogenetically unrelated hosts and a brood parasitic species predicts that mtDNA diversity in the parasite should be relatively deep and phylogenetically structured. Also, the different intraspecific clades resulting from parasitism to multiple sympatric hosts should themselves occur sympatrically. However, mtDNA diversity in brood parasites is as susceptible to effects of historical population dynamics as in any species. We demonstrate the relevance of these dynamics to the use of mtDNA in understanding coevolution between an Australian brood-parasite, Horsfield's Bronze-Cuckoo Chalcites basalis and its hosts, Malurus fairy-wrens and Acanthiza thornbills. Previous ecological and behavioural analyses argue that Malurus- and Acanthiza-specific host races exist in C. basalis. Yet mtDNA diversity in C. basalis is low and phylogenetically unstructured (mean sequence divergence 0.15 +/- 0.07%, range 0.00%-0.31%) and tests of mtDNA neutrality and range expansion vs. population stability (Tajima's D, Fu & Li's F* and D*, Fu's F(S), mismatch analyses) all indicate that C. basalis has expanded its range very recently, probably within the last few tens of thousands of years following climatic amelioration after a peak of aridity in the late Pleistocene. The low mtDNA diversity and its lack of phylogenetic structure in C. basalis deny the existence of evolutionarily long-term stable host races in C. basalis but not the possibility of recently evolved ones. They highlight the need for renewed behavioural and ecological study of the relationship between C. basalis and its hosts. Our findings illustrate the need to understand the evolutionary context in which a brood parasite and its hosts have evolved if mtDNA data are to be used in testing hypotheses concerning the origin and maintenance of host specificity. They also add to the growing body of work illustrating the use of mismatch analyses and Fu's F(S) in detecting range expansions.

Animals↗

Antigenic diversity of Plasmodium falciparum and antibody-mediated parasite neutralization.

The malaria parasite Plasmodium falciparum, causing the most severe form of the disease in humans, is characterized by a broad antigenic diversity between different strains and isolates of the parasite. The antigenic diversity reflects on the one hand polymorphisms in allelic gene products and, on the other hand, antigenic variation as a result of expression of alternative genes in multigene families. Using selected polymorphic regions in two merozoite surface antigens, a method for genotyping P. falciparum parasites has been developed. This has resulted in new information on the clonal multiplicity and dynamics of parasite populations. Observations from in vivo and in vitro studies have identified many potential parasite-neutralizing immune responses and several of the target antigens are being explored as vaccine candidates. Studies of antibody-mediated neutralization of parasites in P. falciparum in vitro cultures, with or without leukocytes as effector cells, have been instrumental in identifying potential target antigens for protective immunity and for elucidation of the effects of immune pressure on the dynamics of parasite populations and their antigenic plasticity.

Adult↗

Two species of feminizing microsporidian parasite coexist in populations of Gammarus duebeni.

The amphipod crustacean Gammarus duebeni hosts two species of vertically transmitted microsporidian parasites, Nosema granulosis and Microsporidium sp. A. Here it is demonstrated that these co-occurring parasite species both cause infected females to produce female-biased broods. A survey of European G. duebeni populations demonstrates that these two parasites co-occur in six of 10 populations. These findings contrast with the theoretical prediction that two vertically transmitted feminizing parasites should not coexist in a panmictic population of susceptible hosts at equilibrium. Possible explanations for the co-occurrence of the two feminizing microsporidia in G. duebeni include the recent invasion of a new parasite, horizontal transmission of one or both parasites and the spread of alleles for resistance to the dominant parasite in host populations.

Amphipoda↗

Parasite load in guinea pig foetus with real time PCR after maternofoetal transmission of Toxoplasma gondii.

Parasite loads of different tissues were assessed in guinea pig foetus after maternal infection. Twelve female guinea pigs were infected with 100 cysts of the 76 K strain of Toxoplasma gondii by the oral route. Inoculation was performed 20 +/- 5 days (G20) or 40 +/- 5 days (G40) after the beginning of gestation. Gestational age was determined by progesterone assay. Maternal and foetal organ samples were taken 60 days after the beginning of gestation. Parasite loads (from placenta, amniotic fluid (AF), cord blood (CB), foetal brain, liver, lung and spleen) were assessed by a real-time PCR quantification using fluorescence resonance energy transfer (FRET) hybridization probes on the Light Cycler. Congenital transmission was proven by the presence of parasites in blood or tissue samples of the foetus in 84.6% (11/13) and 100% (16/16) of cases after inoculation on G20 and G40, respectively. The quantitative analysis of our results after inoculation at G20 and G40 has allowed us to determinate the positive parasitic loads as a function of the origin of the sample and the period of inoculation. The parasite loads expressed as log (parasite/g) were low in AF and CB samples: 1.49 +/- 0.50 and 1.05 +/- 0.10 at G20 and 1.21 +/- 0.36 and 1.20 +/- 0.42 at G40 respectively. In contrast the placenta and the different foetal tissues had higher parasite burdens: 2.89 +/- 0.54 to 5.30 +/- 0.51 at G20 and 2.81 +/- 0.71 to 3.65 +/- 0.59 at G40. All the placentae were positive for parasites even in the two cases with no proven transmission. Real time quantitative PCR using the hybridization probe was a very sensitive and reproducible technique to study the kinetics of congenital toxoplasmosis in the guinea pig model wich is close to that of humans.

Amniotic Fluid↗

Rheumatic manifestations of parasitic diseases.

OBJECTIVES: To consolidate the spectrum and frequency of parasite-related rheumatic syndromes, which have largely been regarded as exceedingly rare by the general medicine, infectious disease, and rheumatology literature. METHODS: A MEDLINE search was performed for articles on rheumatic syndromes related to parasitic infections published from 1966 through December 2000. Identified articles included clinical and epidemiologic studies describing cases of rheumatic syndromes associated with verified parasitic infection. RESULTS: Rheumatologic syndromes, including inflammatory arthritis, inflammatory myositis, and vasculitis, have been described among multiple different parasite infections of all parasitic divisions, including Protozoa, Nematoda, and Platyhelminthes. Individual parasitic divisions are often associated with particular rheumatic syndromes, such as reactive arthritis and spondyloarthropathy, inflammatory or infectious myositis, and reactive or parainfectious vasculitis. CONCLUSIONS AND RELEVANCE: Parasitic infection may underlie the clinical presentation of some rheumatic conditions. Given the continued and growing number of patients at risk for parasitosis by virtue of their country of origin, travel habits, and an immunocompromised state, potential parasitosis must be considered in patients undergoing evaluation for rheumatic complaints.

Cestode Infections↗

Progress in parasitic plant biology: host selection and nutrient transfer.

Host range varies widely among species of parasitic plants. Parasitic plants realize host selection through induction by chemical molecular signals, including germination stimulants and haustoria-inducing factors (HIFs). Research on parasitic plant biology has provided information on germination, haustorium induction, invasion, and haustorial structures and functions. To date, some molecular mechanisms have been suggested to explain how germination stimulants work, involving a chemical change caused by addition of a nucleophilic protein receptor, and direct or indirect stimulation of ethylene generation. Haustorium initiation is induced by HIFs that are generated by HIF-releasing enzymes from the parasite or triggered by redox cycling between electrochemical states of the inducers. Haustorium attachment is non-specific, however, the attachment to a host is facilitated by mucilaginous substances produced by haustorial hairs. Following the attachment, the intrusive cells of parasites penetrate host cells or push their way through the host epidermis and cortex between host cells, and some types of cell wall-degrading enzymes may assist in the penetration process. After the establishment of host-parasite associations, parasitic plants develop special morphological structures (haustoria) and physiological characteristics, such as high transpiration rates, high leaf conductance, and low water potentials in hemiparasites, for nutrient transfer and resource acquisition from their hosts. Therefore, they negatively affect the growth and development and even cause death of their hosts.

Biological Transport↗

When do parasites fail to speciate in response to host speciation?

Cospeciation generally increases the similarity between host and parasite phylogenies. Incongruence between host and parasite phylogenies has previously been explained in terms of host switching, sorting, and duplication events. Here, we describe an additional process, failure of the parasite to speciate in response to host speciation, that may be important in some host-parasite systems. Failure to speciate is likely to occur when gene flow among parasite populations is much higher than that of their hosts. We reconstructed trees from mitochondrial and nuclear DNA sequences for pigeons and doves (Aves: Columbiformes) and their feather lice in the genus Columbicola (Insecta: Phthiraptera). Although comparisons of the trees from each group revealed a significant amount of cospeciation, there was also a significant degree of incongruence. Cophylogenetic analyses generally indicated that host switching may be an important process in the history of this host-parasite association. Using terminal sister taxon comparisons, we also identified three apparent cases where the host has speciated but the associated parasite has not. In two of these cases of failure to speciate, these comparisons involve allopatric sister taxa of hosts whose lice also occur on hosts sympatric with both of the allopatric sisters. These additional hosts for generalist lice may promote gene flow with lice on the allopatric sister species. Relative rate comparisons for the mitochondrial cytochrome oxidase I gene indicate that molecular substitution occurs about 11 times faster in lice than in their avian hosts.

Animals↗

Nest predation and the evolution of conspecific brood parasitism: from risk spreading to risk assessment.

Conspecific brood parasitism (CBP) is a taxonomically widespread reproductive tactic. One of the earliest hypotheses put forward to explain the evolution of CBP was "risk spreading"; that is, by laying eggs in more than one nest, parasites may increase the likelihood that at least one offspring will survive to independence. However, the risk spreading hypothesis, based on the assumptions of random nest predation and random selection of target nests by parasites, was theoretically refuted soon after its appearance. New results from the common goldeneye (Bucephala clangula) have revealed that nests are not predated at random and that parasites preferentially lay in safe nests. By taking into account these findings and by modifying accordingly the basic assumptions of the earlier model that refuted the risk spreading hypothesis, we built a model to address the role of nest predation in the evolution of CBP. Model simulations revealed that the selective advantage of parasitic laying, related to nest predation, is much higher than previously thought. Furthermore, the invasion probability of parasitic tactic when initially rare was reasonably high within our model framework. We show that the use of risk assessing, instead of random risk spreading, makes parasitic laying evolutionarily advantageous.

Animals↗

Computational aspects of host-parasite phylogenies.

Computational aspects of host-parasite phylogenies form part of a set of general associations between areas and organisms, hosts and parasites, and species and genes. The problem is not new and the commonalities of exploring vicariance biogeography (organisms tracking areas) and host-parasite co-speciation (parasites tracking hosts) have been recognised for some time. Methods for comparing host-parasite phylogenies are now well established and fall within two basic categories defined in terms of the way the data are interpreted in relation to the comparison of host-parasite phylogenies, so-called a posteriori, eg Brooks' Parsimony Analysis (BPA), or a priori, eg reconciled trees and other model-based methods, as implemented in the program TreeMap; the relative merits of the two philosophies inherent in these two approaches remain hotly debated. This paper reviews the computational methods currently available to analyse host-parasite relationships.

Algorithms↗

Parasitism of Aedes aegypti and Ae. albopictus (Diptera: Culicidae) by Ascogregarina spp. (Apicomplexa: Lecudinidae) in Florida.

Aedes aegypti (L.) and Ae. albopictus (Skuse) from 40 sites in 17 counties of Florida were surveyed for gregarine parasites during the spring and autumn of 1993 and in July 1994. Larvae collected from containers (mainly tires) were dissected to determine the number of gregarine trophozoites present. Ascogregarina spp. were found at 70% of the sites and occurred as frequently in Ae. aegypti populations as in Ae. albopictus. Within sites, parasite distributions were highly variable and aggregated in host populations. Parasite loads ranged from 1 to 486 trophozoites per host. Mean parasite load was significantly higher in Ae. aegypti larvae (52.5 per host) than in Ae. albopictus (33.5 per host). Parasite prevalence was significantly higher in Ae. aegypti populations that were not sympatric with Ae. albopictus compared with allopatric Ae. albopictus or sympatric populations of either species. In sympatric populations, Ae. aegypti tended to have equal or higher parasite prevalence than the cohabiting Ae. albopictus. Ascogregarina taiwanensis (Lien & Levine) prevalence in Ae. albopictus was significantly higher in areas where these hosts have been present for at least 3 yr. These data contribute to the hypothesis that parasite-mediated competition may be a factor in the apparent displacement of Ae. aegypti by Ae. albopictus in Florida.

Aedes↗

Zinc deficiency impairs immune responses against parasitic nematode infections at intestinal and systemic sites.

Research on the complex interactions among host nutritional status, parasitic infection and immune responsiveness has focused on the detrimental consequences of parasitic infections on host nutritional status and on mechanisms by which malnutrition impairs immunocompetence. Curiously, relatively few studies have examined the effects of malnutrition on the immune response in the parasite-infected host, and even fewer have considered the events occurring at the intestinal level, where absorption of nutrients occurs, intestinal parasites reside, and the gastrointestinal-associated lymphoid tissues play a role in directing both the local and the more systemic immune responses. Our work using a zinc-deficient nematode-infected mouse model reveals that parasites are better able to survive in the zinc-deficient hosts than in well-nourished hosts; that the production of interleukin-4 in the spleen of zinc-deficient mice is depressed, leading to depressed levels of IgE, IgG(1) and eosinophils; and that the function of T cells and antigen-presenting cells is impaired by zinc deficiency as well as by energy restriction. Given the paramount role of the gastrointestinal-associated lymphoid tissues in inducing and regulating immune responses to intestinal parasites and in orchestrating responses in the spleen and peripheral circulation, we conclude that zinc deficiency (in association with energy restriction) exerts profound effects on the gut mucosal immune system, leading to changes in systemically disseminated immune responses and, importantly, to prolonged parasite survival.

Animals↗

Incidence of intestinal parasitic disease in an acquired immunodeficiency syndrome day-care center.

In June, 1986, the Bronx Municipal Hospital Center opened an acquired immunodeficiency syndrome day-care center to provide a quality educational experience for children infected with the human immunodeficiency virus. A major concern was the possibility of increasing secondary infections among these immunocompromised children by placing them in a group environment. One particular worry was intestinal parasitic disease, a serious public health problem in day-care centers throughout the United States. To minimize the risk of parasitic infections, scrupulous hygienic and monitoring procedures were instituted at the acquired immunodeficiency syndrome day-care center. This study reports the incidence of intestinal parasitic disease at the acquired immunodeficiency syndrome day-care center during its first 40 months of operation, encompassing 669 child-months of enrollment, with 131 stool specimens examined for ova and parasites. There were 2 cases of parasitic infection: Entamoeba histolytica in an asymptomatic 6-year-old and Giardia intestinalis in a 7-year-old with diarrhea. In neither case was there any secondary spread. None of the 15 children in diapers had a positive specimen, and we found no Cryptosporidium. Our experience suggests that with appropriate precautions human immunodeficiency virus-infected children can participate in a group day-care program without excessive risk for parasitic disease. Strict adherence to hygienic procedures may also decrease the risk of intestinal parasitic disease among healthy children attending day-care centers.

Acquired Immunodeficiency Syndrome↗

Defending against parasites: fungus-growing ants combine specialized behaviours and microbial symbionts to protect their fungus gardens.

Parasites influence host biology and population structure, and thus shape the evolution of their hosts. Parasites often accelerate the evolution of host defences, including direct defences such as evasion and sanitation and indirect defences such as the management of beneficial microbes that aid in the suppression or removal of pathogens. Fungus-growing ants are doubly burdened by parasites, needing to protect their crops as well as themselves from infection. We show that parasite removal from fungus gardens is more complex than previously realized. In response to infection of their fungal gardens by a specialized virulent parasite, ants gather and compress parasitic spores and hyphae in their infrabuccal pockets, then deposit the resulting pellet in piles near their gardens. We reveal that the ants' infrabuccal pocket functions as a specialized sterilization device, killing spores of the garden parasite Escovopsis. This is apparently achieved through a symbiotic association with actinomycetous bacteria in the infrabuccal pocket that produce antibiotics which inhibit Escovopsis. The use of the infrabuccal pocket as a receptacle to sequester Escovopsis, and as a location for antibiotic administration by the ants' bacterial mutualist, illustrates how the combination of behaviour and microbial symbionts can be a successful defence strategy for hosts.

Actinobacteria↗

Costs to host defence and the persistence of parasitic cuckoos.

Raising genetically unrelated young is maladaptive, yet brood parasitism is widespread in birds. In several systems, hosts can evolve near-perfect defences against the parasite (discrimination and rejection of unlike eggs), making it difficult to understand how the parasite continues to exist. This study demonstrates costs to host defences (e.g. rejection of one's own eggs) such that once the parasite goes extinct on a particular host species, defence mechanisms are selectively disadvantageous. The consequent loss of host defences, and potential for re-exploitation of the host by the parasite, can explain the continued persistence of avian brood parasites. The results provide one general explanation for coexistence of parasites and their hosts.

Adaptation, Physiological↗

Parasite infection rather than tactile stimulation is the proximate cause of cleaning behaviour in reef fish.

Cleaning behaviour is a popular example of non-kin cooperation. However, quantitative support for this is generally sparse and the alternative, that cleaners are parasitic, has also been proposed. Although the behaviour involves some of the most complex and highly developed interspecific communication signals known, the proximate causal factors for why clients seek cleaners are controversial. However, this information is essential to understanding the evolution of cleaning. I tested whether clients seek cleaners in response to parasite infection or whether clients seek cleaners for tactile stimulation regardless of parasite load. Parasite loads on client fish were manipulated and clients exposed to cleaner fish and control fish behind glass. I found that parasitized client fish spent more time than unparasitized fish next to a cleaner fish. In addition, parasitized clients spent more time next to cleaners than next to control fish, whereas unparasitized fish were not attracted to cleaners. This study shows, I believe for the first time, which is somewhat surprising, that parasite infection alone causes clients to seek cleaning by cleaners and provides insight into how this behaviour evolved.

Animals↗

Genetic and environmental determinants of malaria parasite virulence in mosquitoes.

Models of malaria epidemiology and evolution are frequently based on the assumption that vector-parasitic associations are benign. Implicit in this assumption is the supposition that all Plasmodium parasites have an equal and neutral effect on vector survival, and thus that there is no parasite genetic variation for vector virulence. While some data support the assumption of avirulence, there has been no examination of the impact of parasite genetic diversity. We conducted a laboratory study with the rodent malaria parasite, Plasmodium chabaudi and the vector, Anopheles stephensi, to determine whether mosquito mortality varied with parasite genotype (CR and ER clones), infection diversity (single versus mixed genotype) and nutrient availability. Vector mortality varied significantly between parasite genotypes, but the rank order of virulence depended on environmental conditions. In standard conditions, mixed genotype infections were the most virulent but when glucose water was limited, mortality was highest in mosquitoes infected with CR. These genotype-by-environment interactions were repeatable across two experiments and could not be explained by variation in anaemia, gametocytaemia, blood meal size, mosquito body size, infection rate or oocyst burden. Variation in the genetic and environmental determinants of virulence may explain conflicting accounts of Plasmodium pathogenicity to mosquitoes in the malaria literature.

Animals↗

Marine dinoflagellates show induced life-history shifts to escape parasite infection in response to water-borne signals.

Many dinoflagellate species form dormant resting cysts as a part of their life cycle, and in some freshwater species, hatching of these cysts can be delayed by the presence of water-borne signals from grazing zooplankton. Some marine dinoflagellates can form temporary cysts, which may function to resist unfavourable short-term environmental conditions. We investigated whether the marine dinoflagellate Alexandrium ostenfeldii is able to induce an increased resistance to the parasitic flagellate Parvilucifera infectans by forming temporary cysts. We performed several laboratory experiments where dinoflagellates were exposed either to direct contact with parasites or to filtered water from cultures of parasite-infected conspecifics (parasite-derived signals). Infection by P. infectans is lethal to motile A. ostenfeldii cells, but temporary cysts were more resistant to parasite infection. Furthermore, A. ostenfeldii induced a shift in life-history stage (from motile cells to temporary cysts) when exposed to parasite-derived water-borne signals. The response was relaxed within a couple of hours, indicating that A. ostenfeldii may use this behaviour as a short-term escape mechanism to avoid parasite infection. The results suggest that intraspecies chemical communication evoked by biotic interactions can be an important mechanism controlling life-history shifts in marine dinoflagellates, which may have implications for the development of toxic algal blooms.

Adaptation, Physiological↗

Outcrossing increases infection success and competitive ability: experimental evidence from a hermaphrodite parasite.

The maintenance of two genetically distinct reproductive modes such as outcrossing and selfing within a population of animals or plants is still a matter of considerable debate. Hermaphroditic parasites often reproduce either alone by selfing or in pairs by outcrossing. They can be used as a model to study potential benefits of outcrossing. Any advantage from outcrossing may be important, especially in host-parasite coevolution, but has not, to our knowledge, been studied yet in any parasite species. We studied the potential effect of outcrossing in a tapeworm, Schistocephalus solidus, on both infection success and growth in its first intermediate host, the copepod Macrocyclops albidus. Tapeworms that had been obtained from natural populations of three-spined sticklebacks (Gasterosteus aculeatus) were allowed to reproduce either alone or in pairs, in an in vitro system that replaced the final host's gut. This resulted in either selfed or outcrossed offspring, respectively. In one part of the experiment, copepods were exposed to either selfed or outcrossed parasites, in a second part to both types simultaneously, in order to study the effect of competition between them. To discriminate parasites of either origin within the same host, a novel method for fluorescent vital labeling was used. We show here for the first time that outcrossed parasites had a higher infection success and faster development in the host. This advantage of outcrossing became apparent only in the competitive situation, in which superior abilities of parasites to extract limiting resources from the host become crucial.

Animals↗