Are plant pathogen populations adapted for encounter with their host? A case study of phenological synchrony between oak and an obligate fungal parasite along an altitudinal gradient

Biotrophic fungal pathogens are expected to have adapted to their host plants for phenological synchrony, to optimize the possibility of contacts leading to infections. We investigated the patterns and causes of variation in phenological synchrony in the oak‐powdery mildew pathosystem, a major disease in natural ecosystems. The study was carried out along an altitudinal gradient, representing a wide temperature range, in mature oak stands. Both sporulation (pathogen infective stage) and oak flushing (host susceptible stage) were delayed with increasing elevation, but with a significantly different sensitivity for the two species. This resulted in a variable host–pathogen synchrony along the gradient. A common garden experiment did not give evidence of among‐population genetic differentiation (past adaptation) for fungal phenology. This could be explained by the high phenotypic variation in phenology within host populations, precluding selection on fungal phenology at the population scale, but possibly favouring adaptation at the within‐population scale. Phenotypic plasticity was the major cause of the observed variation in the phenology of the fungal populations.     

Do different parasite species interact in their effects on host fitness? A case study on parasites of the amphipod Paracalliope fluviatilis

There is a gap in our understanding of the relative and interactive effects of different parasite species on the same host population. Here we examine the effects of the acanthocephalan Acanthocephalus galaxii, an unidentified cyclophyllidean cestode, and the trematodes Coitocaecum parvum and Microphallus sp. on several fitness components of the amphipod Paracalliope fluviatilis, using a combination of infection surveys and both survival and behavioural trials. In addition to significant relationships between specific parasites and measures of amphipod survival, maturity, mating success and behaviour, interactions between parasite species with respect to amphipod photophilia were also significant. While infection by either A. galaxii or C. parvum was associated with increased photophilia, such increases were negated by co-infection with Microphallus sp. We hypothesize that this is due to the more subtle manipulative effect of A. galaxii and C. parvum being impaired by Microphallus sp. We conclude that the low frequency at which such double infections occur in our sampled population means that such interactions are unlikely to be important beyond the scale of the host individual. Whether or not this is generally true, implying that parasitological models and theory based on single parasite species studies do generally hold, requires cross-species meta-analytical studies.     

Is an elongated stylohyoid process prevalent in the elderly? A radiographic study in a Brazilian population

Background: Elongation and calcification of the stylohyoid ligament complex may be correlated with Eagle's syndrome. The styloid complex pathogenesis is still being debated. Objective: The aim of this study was to investigate the prevalence of stylohyoid ligament complex elongation in panoramic radiographs of 2252 patients in a Brazilian adult, partially edentulous population, of both sexes. Methods: The radiographs, taken in the Semiology Department at the Dental School in Brazil, were randomly selected from January 1997 to December 2000. The stylohyoid ligament complexes were measured from the cranial base up to the osseous tip of each process. Mineralisation of the complex of more than 25 mm in length on the radiograph was considered to be abnormal. The same operator made all the measurements. The lengths of the areas of mineralisation were recorded, and whether the condition was bilateral was noted. Results: This abnormality was present in both sexes. A calcified complex was found in 451 of the 2252 patients. The majority of these calcified complexes (n = 248; 54.9%) were bilateral. Three hundred and fifty‐six (39.5%) of them were longer than 25 mm (and so were abnormal), and the length varied from 26.1 to 65 mm. (average length = 27.8 mm). Forty (4.4%) of the abnormalities were longer than 50 mm, and of these 36 (90%) were in the 40–59 year age group. The mean length of a mineralised stylohyoid ligament complex in patients in the 60–79 year age group was 32.75 mm. Conclusion: The results suggested that an anatomical variant of the stylohyoid ligament complex was more frequently found in the elderly female population, although this abnormality was present in both sexes. There was a greater tendency for the abnormality to be present in patients between 60 and 79 years of age.     

Corticosterone levels in host and parasite nestlings: Is brood parasitism a hormonal stressor?

Parasite chicks from non-evictor species usually try to monopolize host parental care, thereby increasing considerably the level of food competition in the nest. Here, we propose that brood parasitism is an important stressor for host and parasite nestlings and explore this hypothesis in the non-evictor great spotted cuckoo (Clamator glandarius) and its main hosts, the same-sized black-billed magpie (Pica pica) and the larger carrion crow (Corvus corone). We experimentally created 3-nestling broods of different brood compositions (only cuckoo chicks, only host chicks, or cuckoo and host chicks together) and measured baseline corticosterone levels of nestlings along their developmental period (early, middle and late). We found that brood parasitism increased corticosterone levels in magpie nestlings in the mid and late nestling period compared to those raised in unparasitized nests. Interestingly, carrion crow nestlings from parasitized nests only increased their corticosterone levels in the mid nestling period, when the competition for food with the cuckoo nestling was highest. Our results suggest that brood parasitism could be a potential physiological stressor for host nestlings, especially during the developmental stages where food requirements are highest. Conversely, cuckoo nestlings could be physiologically adapted to high competition levels since they did not show significant differences in corticosterone levels in relation to brood composition.     

Apicomplexan AMA1 in host cell invasion: a model at the junction?

Host cell invasion by the malaria parasite is a crucial step in its life cycle. In this issue of Cell Host & Microbe, Giovannini et al. (2011) raise questions about the validity of a widely accepted model of the tight junction, a ring-like structure through which the invading parasite passes.     

Is dimethylsulfoniopropionate (DMSP) produced by the symbionts or the host in an anemone–zooxanthella symbiosis?

Many groups of tropical cnidarians including scleractinian corals, octocorals, corallimorphs, and anemones contain the tertiary sulfonium compound dimethylsulfoniopropionate (DMSP). It is not known if the compound is synthesized by the animals, their microalgal symbionts, or derived through their diet. We determined the source of the DMSP in several species of tropical and temperate anemones using three approaches: (1) conducting comparative measurements of DMSP in aposymbiotic and zooxanthellate anemones of three species that harbor zooxanthellae, and similar measurements in one species that can harbor both zooxanthellae and zoochlorellae, (2) manipulating the presence or absence of zooxanthellae by inoculating juvenile aposymbiotic anemones (Aiptasia pallida) with their symbiont, Symbiodinium bermudense, and (3) manipulating the numbers of S. bermudense by growing aposymbiotic and zooxanthellate A. pallida in the light and the dark. DMSP was present in zooxanthellate anemones in concentrations of 3.4–15 μmol g⁻¹ fresh mass (FM). In aposymbiotic Aiptasia spp. and Anthopleura elegantissima that lacked large numbers of zooxanthellae, concentrations ranged from being undetectable to 0.43 μmol g⁻¹ FM. When aposymbiotic A. pallida were inoculated with zooxanthellae, concentrations of DMSP were an average of 4.24 μmol g⁻¹ FM after 5 weeks; DMSP was undetectable in uninoculated control animals. Aposymbiotic anemones maintained in the light or the dark for 6 weeks contained no DMSP or zooxanthellae. Zooxanthellate anemones in the light contained five times as many zooxanthellae and approximately 7.5 times as much DMSP as zooxanthellate anemones maintained in the dark. Taken together, these data show that the zooxanthellae are the sole source of DMSP in A. pallida. The trends in DMSP concentrations in other species of zooxanthellate anemones suggest that this phenomenon is not limited to A. pallida but may be more generally true for other anemones or even other cnidarians hosting species of Symbiodinium. Communicated by Biology Editor Dr. Michael Lesser     

Life history interactions with environmental conditions in a host–parasite relationship and the parasite's mode of transmission

The microsporidian parasite Edhazardia aedis is capable of vertical or horizontal transmission among individuals of its host, the mosquito Aedes aegypti, and either mode of transmission may follow the other. We show that following the horizontal infection of host larvae, the parasite's subsequent mode of transmission largely depends on host life history traits and their responses to different environmental conditions. In two experiments the intensity of larval exposure to infection and the amount of food available to them were simultaneously manipulated. One experiment followed the dynamics of host development and the parasite's production of spores while the other estimated the outcome of their relationship. Host life history traits varied widely across treatment conditions while those of the parasite did not. Of particular importance was the host's larval growth rate. Horizontal rather than vertical transmission by the parasite was more likely as low food and high dose conditions favoured slower larval growth rates. This pattern of transmission behaviour with host growth rate can be considered in terms of reproductive value: the potential vertical transmission success that female mosquitoes offer the parasite decreases as larval growth rates slow and makes them more attractive to exploitation for horizontal transmission (requiring host mortality). However, the lack of variation in the parasite's life history traits gave rise in some conditions to low estimates for both its vertical and horizontal transmission success. We suggest that the unresponsive behaviour of the parasite's life history traits reflects a bet-hedging strategy to reduce variance in its overall transmission success in the unpredictable environmental conditions and host larval growth rates that this parasite encounters in nature.     

Do climatic conditions affect host and parasite phenotypes differentially? A case study of magpies and great spotted cuckoos

Climatic conditions, through their effects on resource availability, may affect important life history strategies and trade-offs in animals, as well as their interactions with other organisms such as parasites. This impact may depend on species-specific pathways of development that differ even among species with similar resource requirements (e.g., avian brood parasites and their hosts). Here we explore the degree of covariation between environmental-climatic conditions and nestling phenotypes (i.e., tarsus length, body mass, immune response to phytohemagglutinin injection) and ectoparasite loads of great spotted cuckoos (Clamator glandarius) and those of their magpie (Pica pica) hosts, both within and among 11 study years (1997–2011). Our main results were that (1) nestling phenotypes differed among years, but differently for great spotted cuckoos and magpies; (2) nestling phenotypes showed significant among-year covariation with breeding climatic conditions (temperature and precipitation); and (3) these associations differed for cuckoos and magpies for some phenotypic traits. As the average temperature at the beginning of the breeding season (April) increased, body mass and tarsus length increased only for cuckoos, but not for magpie hosts, while immune response decreased in both species. Finally, (4) the strength of the within-year relationships between the probability of ectoparasitism by Carnus hemapterus flies and laying date (used as an estimate of the within-year variation in climatic conditions) was negatively affected by the annual accumulated precipitation in April. These results strongly suggest that variation in climatic conditions would result in asymmetric effects on different species with respect to the probability of ectoparasitism, immunity and body size. Such asymmetric effects may affect animal interactions in general and those of brood parasites and their hosts in particular.     

Is the switch to an ectomycorrhizal state an evolutionary key innovation in mushroom‐forming fungi? A case study in the Tricholomatineae (Agaricales)

Although fungi are one of the most diverse groups of organisms, little is known about the processes that shape their high taxonomic diversity. This study focuses on evolution of ectomycorrhizal (ECM) mushroom‐forming fungi, symbiotic associates of many trees and shrubs, in the suborder Tricholomatineae of the Agaricales. We used the BiSSE model and BAMM to test the hypothesis that the ECM habit represents an evolutionary key innovation that allowed the colonization of new niches followed by an increase in diversification rate. Ancestral state reconstruction (ASR) supports the ancestor of the Tricholomatineae as non‐ECM. We detected two diversification rate increases in the genus Tricholoma and the Rhodopolioid clade of the genus Entoloma. However, no increases in diversification were detected in the four other ECM clades of Tricholomatineae. We suggest that diversification of Tricholoma was not only due to the evolution of the ECM lifestyle, but also to the expansion and dominance of its main hosts and ability to associate with a variety of hosts. Diversification in the Rhodopolioid clade could be due to the unique combination of spore morphology and ECM habit. The spore morphology may represent an exaptation that aided spore dispersal and colonization. This is the first study to investigate rate shifts across a phylogeny that contains both non‐ECM and ECM lineages.     

Is inorganic nutrient enrichment a driving force for the formation of red tides?: A case study of the dinoflagellate Scrippsiella trochoidea in an embayment

Red tides (high biomass phytoplankton blooms) have frequently occurred in Hong Kong waters, but most red tides occurred in waters which are not very eutrophic. For example, Port Shelter, a semi-enclosed bay in the northeast of Hong Kong, is one of hot spots for red tides. Concentrations of ambient inorganic nutrients (e.g. N, P), are not high enough to form the high biomass of chlorophyll a (chl a) in a red tide when chl a is converted to its particulate organic nutrient (N) (which should equal the inorganic nutrient, N). When a red tide of the dinoflagellate Scrippsiella trochoidea occurred in the bay, we found that the red tide patch along the shore had a high cell density of 15,000 cells ml⁻¹, and high chl a (56 μg l⁻¹), and pH reached 8.6 at the surface (8.2 at the bottom), indicating active photosynthesis in situ. Ambient inorganic nutrients (NO₃, PO₄, SiO₄, and NH₄) were all low in the waters and deep waters surrounding the red tide patch, suggesting that the nutrients were not high enough to support the high chl a >50 μg l⁻¹ in the red tide. Nutrient addition experiments showed that the addition of all of the inorganic nutrients to a non-red-tide water sample containing low concentrations of Scrippsiella trochoidea did not produce cell density of Scrippsiella trochoidea as high as in the red tide patch, suggesting that nutrients were not an initializing factor for this red tide. During the incubation of the red tide water sample without any nutrient addition, the phytoplankton biomass decreased gradually over 9 days. However, with a N addition, the phytoplankton biomass increased steadily until day 7, which suggested that nitrogen addition was able to sustain the high biomass of the red tide for a week with and without nutrients. In contrast, the red tide in the bay disappeared on the sampling day when the wind direction changed. These results indicated that initiation, maintenance and disappearance of the dinoflagellate Scrippsiella trochoidea red tide in the bay were not directly driven by changes in nutrients. Therefore, how nutrients are linked to the formation of red tides in coastal waters need to be further examined, particularly in relation to dissolved organic nutrients.     

Is there a relationship between dietary MSG obesity in animals or humans?

The sodium salt of glutamate (monosodium glutamate; MSG) imparts a savory/meaty taste to foods, and has been used as a flavoring agent for millennia. Past research on MSG/glutamate has evaluated its physiologic, metabolic and behavioral actions, and its safety. Ingested MSG has been found to be safe, and to produce no remarkable effects, except on taste. However, some recent epidemiologic and animal studies have associated MSG use with obesity and aberrations in fat metabolism. Reported effects are usually attributed to direct actions of ingested MSG in brain. As these observations conflict with past MSG research findings, a symposium was convened at the 13th International Congress on Amino Acids, Peptides and Proteins to discuss them. The principal conclusions were: (1) the proposed link between MSG intake and weight gain is likely explained by co-varying environmental factors (e.g., diet, physical activity) linked to the “nutrition transition” in developing Asian countries. (2) Controlled intervention studies adding MSG to the diet of animals and humans show no effect on body weight. (3) Hypotheses positing dietary MSG effects on body weight involve results from rodent MSG injection studies that link MSG to actions in brain not applicable to MSG ingestion studies. The fundamental reason is that glutamate is metabolically compartmentalized in the body, and generally does not passively cross biologic membranes. Hence, almost no ingested glutamate/MSG passes from gut into blood, and essentially none transits placenta from maternal to fetal circulation, or crosses the blood–brain barrier. Dietary MSG, therefore, does not gain access to brain. Overall, it appears that normal dietary MSG use is unlikely to influence energy intake, body weight or fat metabolism.     

Does superparasitism improve host suitability for parasitoid development? A case study in the Microplitis rufiventris-Spodoptera littoralis system

Superparasitism refers to the oviposition behavior of parasitoid females who lay their eggs in an already parasitized host. Recent studies have shown that allocation of additional eggs to an already parasitized host may be beneficial under certain conditions. In the present work, mortality of Microplitis rufiventris wasps was significantly influenced by both host instar of Spodoptera littoralis larvae at parasitism and level of parasitism. In single parasitization, all host instars (first through sixth) were not equally suitable. Percentage of emergence success of wasp larvae was very high in parasitized first through third (highly suitable hosts), fell to 60% in the fourth instar (moderate suitable) and sharply decreased in the penultimate (5th) instars (marginally suitable). Singly parasitized sixth (last) instar hosts produced no wasp larvae (entirely unsuitable), pupated and eclosed to apparently normal adult moths. The scenario was different under superparasitism, whereas supernumerary individuals in the highly suitable hosts were almost always killed as first instars, superparasitization in unsuitable hosts (4th through 6th) had significant increase in number of emergence success of wasp larvae. Also, significantly greater number of parasitoid larvae successfully developed in unsuitable hosts containing three wasp eggs than counterparts containing two wasp eggs. Moreover, the development of surplus wasp larvae was siblicidal in earlier instars and nonsiblicidal gregarious one in the penultimate and last “sixth” instars. It is suggested that the optimal way for M. rufiventris to deal with high quality hosts (early instars) is to lay a single egg, while the optimal way to deal with low quality hosts (late instars) might be to superparasitize these hosts.     

Is Toxoplasma egress the first step in invasion?

The protozoan parasite Toxoplasma gondii maintains an intracellular lifestyle that requires careful timing and coordination when exiting one cell (egress) and entering another (invasion). Here it is argued that T. gondii uses similar molecular mechanisms for egress and invasion, based on common morphology, dependence on motility, and regulation by a calcium-dependent signal transduction pathway. In our view, this strategy is highly advantageous because it allows the parasite to egress rapidly from one cell and immediately invade an adjacent cell, thereby minimizing exposure to the extracellular environment where it could be destroyed by host immune mediators.     

Differential virulence in a multiple‐host parasite of bumble bees: resolving the paradox of parasite survival?

Parasite virulence determines both the impact that parasites have on their hosts and parasite fitness. While most studies of virulence have involved single-species host–parasite interactions, the majority of parasites are likely to use multiple concurrent host species. Our understanding of how this impacts on parasite epidemiology and virulence is limited. Using the bumble bee Bombus lucorum , which exists in sympatry with B. terrestris in multi-species assemblages, and their generalist micosporidian parasite Nosema bombi , we tested whether the apparent paradox of parasite maintenance due to parasite virulence in a single host, B. terrestris , could be resolved through understanding the parasite's virulence in this sympatric host species. Nosema bombi significantly impacted colony growth, individual longevity, and individual development in B. lucorum . However, these effects were different both qualitatively and quantitatively to the parasite's impact in B. terrestris . Infected colonies of B. lucorum successfully produced both male and female reproductives, and infected female reproductives were capable of successful mating. Variation in life-history across host species may explain differences in the virulence, or impact of the parasite in B. terrestris and B. lucorum , with species with shorter life-cycles being more likely to transfer the parasite from one annual generation to the next. These results suggest that to understand the virulence and epidemiology of multi-host parasites we need to examine their ecological interactions across their various host species.     

Is urbanization scrambling the genetic structure of human populations? A case study

Recent population expansion and increased migration linked to urbanization are assumed to be eroding the genetic structure of human populations. We investigated change in population structure over three generations by analysing both demographic and mitochondrial DNA (mtDNA) data from a random sample of 2351 men from 22 Iranian populations. Potential changes in genetic diversity (theta) and genetic distance (F(ST)) over the last three generations were analysed by assigning mtDNA sequences to populations based on the individual's place of birth or that of their mother or grandmother. Despite the fact that several areas included cities of over one million inhabitants, we detected no change in genetic diversity, and only a small decrease in population structure, except in the capital city (Tehran), which was characterized by massive immigration, increased theta and a large decrease in F(ST) over time. Our results suggest that recent erosion of human population structure might not be as important as previously thought, except in some large conurbations, and this clearly has important implications for future sampling strategies.     

Is polyploidy a persevering accident or an adaptive evolutionary pattern? The case of the brine shrimp Artemia

Asexual organisms are confronted with substantial drawbacks, both immediate and delayed, threatening their evolutionary persistence. Yet, genetic associations with asexuality may refresh the gene pool promoting adaptation of clonal lineages; polyploidy is one of them. Parthenogenesis itself and/or polyploidy are responsible for the maintenance and spread of clones in Artemia, a sexual-asexual genus of halophilic anostracans. We applied flow cytometry, microsatellite genotyping, and mtDNA sequencing to 23 asexual populations. Artemia parthenogens have evolved multiple times either through hybridization or spontaneously. Nine out of 23 populations contained clones of mixed ploidy (2n, 3n, 4n). Most clones were diploid (20/31) while two and nine clones were triploid and tetraploid, respectively. Apomictic triploids and tetraploids formed two distinct groups of low genetic diversity compared with the more divergent automictic diploids. Polyploidy is also polyphyletic in Artemia, with triploids and tetraploids having independent origins from different sexual ancestors. We discern a pattern of geographical parthenogenesis with all clonal groups being more widespread than their closest sexuals. In favour of a specialist model, asexual diploids are restricted to single locations and are strikingly segregated from generalist triploids and tetraploids occupying a variety of sites. This is a rare pattern of mixed life-history strategies within an asexual complex.