Exploitation or cooperation? Evolution of a host (ciliate)-benefiting alga in a long-term experimental microcosm culture

Controversy persists as to whether the acquisition of beneficial metabolic functions via endosymbiosis can occur suddenly on an evolutionary time scale. In this study, an early stage of endosymbiotic associations, which evolved from previously unassociated auto (photo)- and heterotrophic unicellular organisms was analyzed using an experimental ecosystem model, called CET microcosm. This ecosystem model was composed of a green alga (Micractinium sp.; formerly described as Chlorella vulgaris), a bacterium (Escherichia coli), and a ciliate (Tetrahymena thermophila). Our previous study using a CET microcosm that was cultured 3–5 years revealed that fitness of the ciliate increased by harboring algal cells within its own cells. This fact suggested three possibilities: (i) the ciliate evolved the ability to exploit intracellular algal cells (“exploiter ciliate hypothesis”), (ii) the alga evolved the ability to benefit the host ciliate by providing photosynthates (“cooperator alga hypothesis”), and (iii) a combination of (i) and (ii). To test these hypotheses, two-by-two co-cultures were conducted between the ancestral or derived ciliate and the ancestral or derived alga. The experimental results demonstrated that a cooperative alga evolved in the microcosm, although the possibility remains that an exploitative genotype of the ciliate might also exist in the population as a polymorphism. Remarkably, an algal isolate prolonged the longevity of not only the isolated ciliate, but also the ancestral ciliate. This result suggests that once a cooperative algal genotype evolves in a local population, it can then be transmitted to other individuals of the prospective host species and spread rapidly beyond the local range due to its positive effect on the host fitness. Such transmission suggests the possibility of a sudden acquisition of beneficial autotrophic function by the pre-associated host.     

Coevolution of dispersal in a parasitoid–host system

Interspecific interactions and the evolution of dispersal are both of interest when considering the potential impact of habitat fragmentation on community ecology, but the interaction between these processes is not well studied. We address this by considering the coevolution of dispersal strategies in a host–parasitoid system. An individual-based host–parasitoid metapopulation model was constructed for a patchy environment, allowing for evolution in dispersal rates of both species. Highly rarefied environments with few suitable patches selected against dispersal in both species, as did relatively static environments. Provided that parasitoids persist, all the variables studied led to stable equilibria in dispersal rates for both species. There was a tendency toward higher dispersal rates in parasitoids because of the asymmetric relationships of the two species to the patches: vacant patches are most valuable for hosts, but unsuitable for parasitoids, which require an established host population to reproduce. High host dispersal rate was favoured by high host population growth rate, and in the parasitoid by high growth rates in both species. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

A host–microparasite model with a resistant host

The theory of heterozygote advantage is often used to explain the genetic variation found in natural populations. If a large population randomly mates and the various genotypes have the same growth and death rates, the evolution of the genotypes follows Hardy–Weinberg proportions and polymorphism results. When other environmental stresses, like predators, prey and diseases, are present, polymorphism may or may not occur depending on how the various genotypes are affected by the stress. In this paper, we use a basic host–microparasite model to demonstrate that polymorphism can occur even if one genotype suffers a higher death rate than the others in the absence of the parasite if the heterozygote has resistance or immunity to the parasite.     

Immunocytochemical localization of host (Apis mellifera) proteins in growing oocytes of a hemophagous mite (Varroa jacobsoni) by the unlabeled antibody—enzyme (PAP) method

The mite, Varroa jacobsoni is a hemophagous ectoparasite of honeybees (Apis spec.). Host hemolymph proteins are resorbed by Varroa without digestive degradation. By immunocytochemical methods, these foreign proteins can be localized in growing Varroa oocytes; they are assimilated into the eggs.     

Community-wide patterns of parasitism of a host “generalist” brood-parasitic cowbird

The brown-headed cowbird (Molothrusater) is a generalist obligate brood parasite. Despite intensive study and growing concern over the negative impact of cowbird parasitism on populations of many hosts, very little is known about the factors influencing community-wide patterns of cowbird parasitism. Using systematic nest searches, nest parasitism was studied over two breeding seasons at a study site in northeastern Illinois encompassing grassland, forest-edge, and forest habitat, supporting a diverse avian community. Parasitism was observed for 18 out of 34 altricial bird species found nesting at the study site. A total of 299 cowbird eggs and nestlings were found in 191 of a total of 593 nests. Analyses revealed several ecological and behavioral factors associated with frequency of parasitism and the resulting distribution of cowbird eggs. Much higher frequencies of parasitism were found in edge and forest habitats than in grassland. Within the edge habitat, open nests were parasitized significantly more often than cavity nests. Among open nests in the edge habitat, the two largest species were never parasitized. Host behavior, particularly egg-ejection behavior, was associated with a reduced observed frequency of parasitism, but at least three species known to eject cowbird eggs were sometimes parasitized. For six common hosts capable of rearing cowbirds, we found no correlation between level of parasitism and host nest-survivorship, suggesting that fine-grained assessments of host quality by female cowbirds do not influence patterns of parasitism among acceptable host species, or that differences in host quality are not great and/or predictable enough for such fine-grained assessments. Our results suggest that when a variety of possible nests are available, the level of parasitism on a particular species is a balance between a␣cowbird's preference for a particular species and the effectiveness of host species' defenses. A conceptual model was developed that incorporates the observed correlation of cowbird eggs or nestlings with habitat, nest-type, host species' body mass, and host behavioral defenses. Additional community-wide studies of cowbird parasitism will test if this model is applicable to other avian communities. Received: 20 December 1996 / Accepted: 17 May 1997     

Dermatophyte–host relationship of a murine model of experimental invasive dermatophytosis

Recognizing the invasive potential of the dermatophytes and understanding the mechanisms involved in this process will help with disease diagnosis and with developing an appropriate treatment plan. In this report, we present the histopathological, microbiological and immunological features of a model of invasive dermatophytosis that is induced by subcutaneous infection of Trichophyton mentagrophytes in healthy adult Swiss mice. Using this model, we observed that the fungus rapidly spreads to the popliteal lymph nodes, spleen, liver and kidneys. Similar to the human disease, the lymph nodes were the most severely affected sites. The fungal infection evoked acute inflammation followed by a granulomatous reaction in the mice, which is similar to what is observed in patients. The mice were able to mount a Th1-polarized immune response and displayed IL-10-mediated immune regulation. We believe that the model described here will provide valuable information regarding the dermatophyte–host relationship and will yield new perspective for a better understanding of the immunological and pathological aspects of invasive dermatophytosis.     

Do distances among host patches and host density affect the distribution of a specialist parasitoid?

The effect of spatial habitat structure and patchiness may differ among species within a multi-trophic system. Theoretical models predict that species at higher trophic levels are more negatively affected by fragmentation than are their hosts or preys. The absence or presence of the higher trophic level, in turn, can affect the population dynamics of lower levels and even the stability of the trophic system as a whole. The present study examines different effects of spatial habitat structure with two field experiments, using as model system the parasitoid Cotesia popularis which is a specialist larval parasitoid of the herbivore Tyria jacobaeae. One experiment examines the colonisation rate of the parasitoid and the percentage parasitism at distances occurring on a natural scale; the other experiment examines the dispersal rate and the percentage parasitism in relation to the density of the herbivore and its host plant. C. popularis was able to reach artificial host populations at distances up to the largest distance created (at least 80 m from the nearest source population). Also, the percentage parasitism did not differ among the distances. The density experiment showed that the total number of herbivores parasitised was higher in patches with a high density of hosts, regardless of the density of the host plant. The percentage parasitism, however, was not related to the density of the host. The density of the host plant did have a (marginally) significant effect on the percentage parasitism, probably indicating that the parasitoid uses the host plant of the herbivore as a cue to find the herbivore itself. In conclusion, the parasitoid was not affected by the spatial habitat structure on spatial scales that are typical of local patches.     

Manipulation of host behaviour by parasites: a weakening paradigm?

New scientific paradigms often generate an early wave of enthusiasm among researchers and a barrage of studies seeking to validate or refute the newly proposed idea. All else being equal, the strength and direction of the empirical evidence being published should not change over time, allowing one to assess the generality of the paradigm based on the gradual accumulation of evidence. Here, I examine the relationship between the magnitude of published quantitative estimates of parasite-induced changes in host behaviour and year of publication from the time the adaptive host manipulation hypothesis was first proposed. Two independent data sets were used, both originally gathered for other purposes. First, across 137 comparisons between the behaviour of infected and uninfected hosts, the estimated relative influence of parasites correlated negatively with year of publication. This effect was contingent upon the transmission mode of the parasites studied. The negative relationship was very strong among studies of parasites which benefit from host manipulation (transmission to the next host occurs by predation on an infected intermediate host), i.e. among studies which were explicit tests of the adaptive manipulation hypothesis. There was no correlation with year of publication among studies on other types of parasites which do not seem to receive benefits from host manipulation. Second, among 14 estimates of the relative, parasite-mediated increase in transmission rate (i.e. increases in predation rates by definitive hosts on intermediate hosts), the estimated influence of parasites again correlated negatively with year of publication. These results have several possible explanations, but tend to suggest biases with regard to what results are published through time as accepted paradigms changed.     

A comparison of diversity estimators applied to a database of host–parasite associations

Understanding the drivers of biodiversity is important for forecasting changes in the distribution of life on earth. However, most studies of biodiversity are limited by uneven sampling effort, with some regions or taxa better sampled than others. Numerous methods have been developed to account for differences in sampling effort, but most methods were developed for systematic surveys in which all study units are sampled using the same design and assemblages are sampled randomly. Databases compiled from multiple sources, such as from the literature, often violate these assumptions because they are composed of studies that vary widely in their goals and methods. Here, we compared the performance of several popular methods for estimating parasite diversity based on a large and widely used parasite database, the Global Mammal Parasite Database (GMPD). We created artificial datasets of host–parasite interactions based on the structure of the GMPD, then used these datasets to evaluate which methods best control for differential sampling effort. We evaluated the precision and bias of seven methods, including species accumulation and nonparametric diversity estimators, compared to analyzing the raw data without controlling for sampling variation. We find that nonparametric estimators, and particularly the Chao2 and second-order jackknife estimators, perform better than other methods. However, these estimators still perform poorly relative to systematic sampling, and effect sizes should be interpreted with caution because they tend to be lower than actual effect sizes. Overall, these estimators are more effective in comparative studies than for producing true estimates of diversity. We make recommendations for future sampling strategies and statistical methods that would improve estimates of global parasite diversity.     

Laboratory host range testing of Lilioceris sp. near impressa (Coleoptera: Chrysomelidae) – a potential biological control agent of air potato,Dioscorea bulbifera (Dioscoreaceae)

Air potato, Dioscorea bulbifera, is an invasive, herbaceous, climbing vine, which dominates invaded native vegetation in Florida. The fortuitous discovery of Lilioceris sp. near impressa defoliating D. bulbifera vines and feeding on the bulbils (aerial tubers) in the Katmandu Valley of Nepal initiated a project to assess the potential of this leaf beetle for biological control of air potato in Florida. Quarantine host specificity tests were conducted on 41 plant species in 24 families and 13 orders, with 26 species outside of the Dioscoreaceae and 15 species within the Dioscoreaceae. Adults test fed (nibbled) on 4/12 of tested Dioscorea species, but no larval feeding or development occurred on any plant other than the target, D. bulbifera. The larvae feed gregariously and quickly skeletonize offered leaves of air potato. Air potato bulbils that received any feeding damage to the primary meristematic region did not sprout. The ability of the beetle larvae and adults to feed on the bulbils is important because in Florida, the plant rarely flowers or produces fruit, so these aerial tubers are the primary means of persistence and spread. The adults can live for several months without food. This extremely specialized herbivore from part of the weed's native range appears to have great promise as a biological control of air potato.     

Identification of “nodule-specific” host proteins (nodulins) involved in the development of Rhizobium-Legume symbiosis

Infection of legume roots with Rhizobium species results in the development of a root nodule structure in which the bacteria form an intracellular symbiosis with the plant. We report here that the infection of soybean (Glycine max L.) roots with Rhizobium japonicum results in the synthesis by the plant of at least 18–20 polypeptides other than leghemoglobin during the development of root nodules. Identification of these “nodule-specific” host polypeptides (referred to as nodulins) was accomplished by two-dimensional gel analysis of the immunoprecipitates formed by a “nodule-specific” antiserum with in vitro translation products of root-nodule polysomes that are free of bacteroidal contaminations. Nodulins account for 7–11% of the total ³⁵S-methionine-labeled protein synthesized in the host cell cytoplasm, and the majority of them are of 12,000–20,000 molecular weight. These proteins are absent from the uninfected roots, bacteroids and free-living Rhizobium, and appear to be coded for by the plant genes that may be obligatory for the development of symbiosis in the legume root nodules. Analysis of nodulins in ineffective (unable to fix nitrogen) nodules developed due to Rhizobium strains SM5 and 61A24 showed that their synthesis is reduced and their expression differentially influenced by mutations in rhizobia. Two polypeptides of bacterial origin were also found to be cross-reactive with the “nodule-specific” antiserum, suggesting that they are secreted by Rhizobium into the host cell cytoplasm during symbiotic nitrogen fixation.     

Will reduced host connectivity curb the spread of a devastating epidemic?

The white‐nose syndrome (WNS), caused by the fungal pathogen Pseudogymnoascus destructans, is threatening the cave‐dwelling bat fauna of North America by killing individuals by the thousands in hibernacula each winter since its appearance in New York State less than ten years ago. Epidemiological models predict that WNS will reach the western coast of the USA by 2035, potentially eliminating most populations of susceptible bat species in its path (Frick et al. 2015; O'Regan et al. 2015). These models were built and validated using distributional data from the early years of the epidemic, which spread throughout eastern North America following a route driven by cave density and winter severity (Maher et al. 2012). In this issue of Molecular Ecology, Wilder et al. (2015) refine these findings by showing that connectivity among host populations, as assessed by population genetic markers, is crucial in determining the spread of the pathogen. Because host connectivity is much reduced in the hitherto disease free western half of North America, Wilder et al. make the reassuring prediction that the disease will spread more slowly west of the Great Plains.     

Is palatability of a root-hemiparasitic plant influenced by its host species?

Palatability of parasitic plants may be influenced by their host species, because the parasites take up nutrients and secondary compounds from the hosts. If parasitic plants acquired the full spectrum of secondary compounds from their host, one would expect a correlation between host and parasite palatability. We examined the palatability of leaves of the root-hemiparasite Melampyrum arvense grown with different host plants and the palatability of these host plants for two generalist herbivores, the caterpillar of Spodoptera littoralis and the slug Arion lusitanicus. We used 19 species of host plants from 11 families that are known to contain a wide spectrum of anti-herbivore compounds. Growth of M. arvense was strongly influenced by the host species. The palatability of the individual host species for the two herbivores differed strongly. Both A. lusitanicus and S. littoralis discriminated also between hemiparasites grown with different host plants. There was no correlation between the palatability of a host species and that of the parasites grown on that host, i.e., hemiparasites grown on palatable host species were not more palatable than those grown on unpalatable hosts. We suggest an interacting pattern of specific effects of chemical anti-herbivore defences and indirect effects of the hosts on herbivores through effects on growth and tissue quality of the parasites.     

Parasitized snails take the heat: a case of host manipulation?

Infection-induced changes in a host’s thermal physiology can represent (1) a generalized host response to infection, (2) a pathological side-effect of infection, or (3), provided the parasite’s development is temperature-dependent, a subtle case of host manipulation. This study investigates parasite-induced changes in the thermal biology of a first intermediate host infected by two castrating trematodes (genera Maritrema and Philophthalmus) using laboratory experiments and field surveys. The heat tolerance and temperatures selected by the snail, Zeacumantus subcarinatus, displayed alterations upon infection that differed between the two trematodes. Upon heating, snails infected by Maritrema sustained activity for longer durations than uninfected snails, followed by a more rapid recovery, and selected higher temperatures in a thermal gradient. These snails were also relatively abundant in high shore localities in the summer only, corresponding with seasonal elevated microhabitat temperatures. By contrast, Philophthalmus-infected snails fell rapidly into a coma upon heating and did not display altered thermal preferences. The respective heat tolerance of each trematode corresponded with the thermal responses induced in the snail: Maritrema survived exposure to 40°C, while Philophthalmus was less heat tolerant. Although both trematodes infect the same tissues, Philophthalmus leads to a reduction in the host’s thermal tolerance, a response consistent with a pathological side effect. By contrast, Maritrema induces heat tolerance in the snail and withstood exposure to high heat. As the developmental rate and infectivity of Maritrema increase with temperature up to 25°C, one adaptive explanation for our findings is that Maritrema manipulates the snail’s thermal responses to exploit warm microhabitats.     

Cytolethal distending toxin (CDT): a bacterial weapon to control host cell proliferation?

Cytolethal distending toxins (CDT) constitute a family of genetically related bacterial protein toxins able to stop the proliferation of numerous cell lines. This effect is due to their ability to trigger in target cells a signaling pathway that normally prevents the transition between the G2 and the M phase of the cell cycle. Produced by several unrelated Gram-negative mucosa-associated bacterial species, CDTs are determined by a cluster of three adjacent genes (cdtA, cdtB, cdtC) encoding proteins whose respective role is not yet fully elucidated. The CDT-B protein presents sequence homology to several mammalian and bacterial phosphodiesterases, such as DNase I. The putative nuclease activity of CDT-B, together with the activation by CDT of a G2 cell cycle checkpoint, strongly suggests that CDT induces an as yet uncharacterized DNA alteration. However, the effective entry of CDT into cells and subsequent translocation into the nucleus have not yet been demonstrated by direct methods. The relationship between the potential DNA-damaging properties of this original family of toxins and their role as putative virulence factors is discussed.