Brood parasitism causes female‐biased host nestling mortality regardless of parasite species

Inequality in male and female numbers may affect population dynamics and extinction probabilities and so has significant conservation implications. We previously demonstrated that Brown‐headed Cowbird Molothrus ater brood parasitism of Song Sparrows Melospiza melodia results in a 50% reduction in the proportion of female host offspring by day 6 post‐hatch and at fledging, which modelling demonstrated is as significant as nest predation in affecting demography. Many avian brood parasites possess special adaptations to parasitize specific hosts so this sex‐ratio effect could be specific to the interaction between these two species. Alternatively, perturbations associated with brood parasitism per se (e.g. the addition of an extra, larger, unrelated nestling), rather than a Cowbird nestling specifically, may be responsible. We experimentally eliminated the effects of Cowbird‐specific traits by parasitizing nests with a conspecific nestling rather than a Cowbird, while otherwise emulating the circumstances of Cowbird parasitism by adding an extra, larger (2‐day‐older), unrelated Song Sparrow nestling to Song Sparrow nests. Our parasitism treatment led to few host offspring deaths and no evidence of male‐biased sex ratios by day 6 post‐hatch. However, after day 6, female nestling mortality rates increased significantly in experimentally parasitized nests, resulting in a 60% reduction in the proportion of females fledging. Cowbird‐specific traits are thus not necessary to cause female‐biased host nestling mortality and far more general features associated with Cowbird parasitism instead appear responsible. Our results suggest, however, that Cowbird‐specific traits may help accelerate the pace of female host deaths. The conservation implications of our results could be wide reaching. Cowbirds are unrelated to all their hosts, are larger than the great majority, and a Cowbird nestling's presence can mean there is an extra mouth to feed. Thus, sex‐biased mortality in parasitized nests could be occurring across a range of host species.     

On the importance of risky behavior in the transmission of sexually transmitted diseases

We consider a population with two types of individuals: those who engage in risky sexual behavior (the core) and those who do not (the majority). We are interested in the situation where the majority would not be able to sustain an epidemic without the presence of a core. We show that even if the core is randomly spread out in the general population and is very infectious there will be no epidemic if the proportion of individuals in the core is below a certain threshold (that depends on the infection rates). Risky behavior does put the whole population at risk but only if the behavior is widespread enough. This gives support to the idea of concentrating resources to fight sexually transmitted diseases on the core group in order to lower the proportion of individuals in the core. We show our results for two models: one with total mixing and the other with limited mixing.     

The ghosts of parasitism past: lingering frontline anti-brood parasite defenses in a former host

Coevolutionary arms races between brood parasites and hosts provide tractable systems for understanding antagonistic coevolution in nature; however, little is known about the fate of frontline antiparasite defenses when the host “wins” the coevolutionary arms race. By recreating bygone species interactions, using artificial parasitism experiments, lingering defensive behaviors that evolved in the context of parasitism can be understood and may even be used to identify the unknown agent of parasitism past. Here we present the first study of this type by evaluating lingering “frontline” nest defenses that have evolved to prevent egg laying in a former brood parasite host. The Australian reed warbler Acrocephalus australis is currently not parasitized but is known to exhibit fine-tuned egg discrimination—a defensive behavior indicative of a past brood parasite–host arms race and common in closely related parasitized species. Here, using 3D-printed models of adult brood parasites, we examined whether the Australian reed warbler also exhibits frontline defenses to adult brood parasites, and whether we could use these defenses to identify the warbler’s “ghost of parasitism past.” Our findings provide evidence that the Australian reed warbler readily engages in frontline defenses that are considered adaptive specifically in the context of brood parasitism. However, individuals were unable to discriminate between adults of different brood parasite species at their nest. Overall, our results demonstrate that despite a relaxation in selection, defenses against brood parasitism can be maintained across multiple stages of the host’s nesting cycle, and further suggest that, in accordance with previous findings, that learning may be important for fine-tuning frontline defense.     

The effect of aggregative overwintering on an insect sexually transmitted parasite system

In contrast to the extensively studied sexually transmitted diseases (STDs) of humans, little is known of the ecology or evolutionary biology of sexually transmitted parasites in natural systems. This study of a sexually transmitted parasite on an insect host augments our understanding of both the parasite's population dynamics and virulence effects. The impact of overwintering was assessed on the prevalence of the parasitic mite Coccipolipus hippodamiae on the two-spot ladybird, Adalia bipunctata. First, the effect of infection on host survival was examined during the stressful overwintering period. Box experiments in the field revealed that the infected ladybirds, especially males, are less likely to survive overwintering. The study provides the first evidence that the parasite harms males and suggests revisions of theories on the adaptive virulence of sexually transmitted parasites. It also indicates the importance of using a range of experimental conditions because virulence can be dependent on host condition and sex. Box experiments were also used to examine whether transmission of the parasite occurs within overwintering aggregations. These revealed that substantial transmission does not occur in aggregations and that transmission is predominantly sexual. Overall, the virulence effects and the lack of transmission mean that the overwintering period acts to diminish parasite prevalence and will retard the spring epidemic associated with host reproductive activity.     

Galectin-1 on cervical epithelial cells is a receptor for the sexually transmitted human parasite Trichomonas vaginalis

The extracellular protozoan parasite Trichomonas vaginalis causes the most prevalent non-viral sexually transmitted human infection, yet the pathogenesis of infection is poorly understood, and host cell receptors have not been described. The surface of T. vaginalis is covered with a glycoconjugate called lipophosphoglycan (LPG), which plays a role in the adherence and cytotoxicity of parasites to human cells. T. vaginalis LPG contains high amounts of galactose, making this polysaccharide a candidate for recognition by the galactose-binding galectin family of lectins. Here we show that galectin-1 (gal-1) is expressed by human cervical epithelial cells and binds T. vaginalis LPG. Gal-1 binds to parasites in a carbohydrate-dependent manner that is inhibited in the presence of T. vaginalis LPG. Addition of purified gal-1 to cervical epithelial cells also enhances parasite binding, while a decrease in gal-1 expression by small interfering RNA (siRNA) transfection decreases parasite binding. In contrast, the related galectin-7 (gal-7) does not bind T. vaginalis in a carbohydrate-dependent manner, and is unable to mediate attachment of parasites to host cells. Our data are consistent with the presence of multiple host cell receptors for T. vaginalis of which gal-1 is the first to be identified and highlight the importance of glycoconjugates in host-pathogen interactions.     

The role of host phenology in determining the incidence of an insect sexually transmitted infection

Changes in the timing of life history events within the year alter the degree to which the activity patterns of different species coincide, making the dynamics of interspecific interactions sensitive to the phenology of the interacting parties. For parasites, the availability of suitable hosts to infect represents a crucial determinant of dynamics, and changes in the host (and parasite) phenology may thus alter disease epidemiology and the conditions for disease maintenance. We tested the hypothesis that the incidence of a sexually transmitted mite infection, Coccipolipus hippodamiae, in Adalia bipunctata ladybird beetles in Sweden was determined by host phenology, namely presence/absence of sexual contact between cohorts of the host. We observed that the pattern of mite presence/absence across Swedish A. bipunctata populations was highly reproducible between years, implying a persistent biological/ecological basis underlying the incidence. Further, ladybirds from populations where the mite was absent were able to acquire mites during copulation, develop a mite infection, and transmit infection onward, indicating an ecological (rather than biological) driver of mite incidence. Observations of ladybird phenology in natural populations provided evidence of sexual contact between overwintered and new cohort adults in populations where the mite was present. In contrast, new cohort ladybirds in the two northern Swedish populations where the mite was not present had not had sexual contact with the overwintered generation, creating a ‘hard stop’ to mite transmission. We conclude that variation in host phenology may be an important driver of the incidence of sexually transmitted infections (STIs) by determining the presence/absence of sexual contact between generations. More generally, we hypothesize that sensitivity to variation in host phenology will be highest for parasites like STIs that infect one host species, one host life stage and are directly transmitted on contact between host individuals.     

Relative importance of host environment,transmission potential and host phylogeny to the structure of parasite metacommunities

Identification of mechanisms that shape parasite community and metacommunity structures have important implications to host health, disease transmission, and the understanding of community assembly in general. Using a long‐term dataset on parasites from desert rodents, we examined the relative contributions of host traits that represent important aspects of parasite environment, transmission probability between host species, and host phylogeny to the structure of a parasite metacommunity as well as for taxonomically restricted parasite metacommunities (coccidians, ectoparasites and helminths). This was done using a combination of metacommunity analysis and variance partitioning based on canonical correspondence analysis. Coccidian and ectoparasite metacommunities did not exhibit coherent structure. In contrast, helminths and the full parasite metacommunity had Clementsian and quasi‐Clementsian structure, respectively, indicating that parasite species distributions for these metacommunities were compartmentalized along a dominant gradient. Variance decomposition indicated that characteristics associated with the host environment consistently explained more variation than did host traits associated with transmission opportunities or host phylogeny, indicating that the host environment is primary in shaping parasite species distributions among host species. Moreover, the importance of different types of host traits in structuring parasite metacommunities was consistent among taxonomic groups (i.e. full metacommunity, coccidians, and helminths) despite manifest differences in emergent structures (i.e. Clementsian, quasi‐Clementsian, and random) that arose in response to variation in host environment.     

Temporal patterns of host availability, brown-headed cowbird brood parasitism, and parasite egg mass

I studied relationships between temporal patterns of host availability, brood parasitism, and egg mass for the parasitic brown-headed cowbird (Molothrus ater). At a study site consisting largely of edge habitat in north-eastern Illinois, I found 834 bird nests from 27 species. A total of 407 cowbird eggs and nestlings were found in these nests over three laying seasons. Nearly all (n= 379; 93%) were found in the nests of seven host species. For these species and all taken together, weekly nest availability generally decreased whereas parasitism frequency generally increased throughout the cowbird laying season, but the proportions of nests parasitized and the mean number of cowbird eggs in them did not. Additionally, no correlation was found between the proportions of nests parasitized and nest availability. Cowbird egg mass generally increased throughout the laying season, indicating that foraging conditions improved and that, early in the laying season, egg mass and quality may be less important than quantity. Consistently high weekly levels of parasitism indicate that cowbird reproduction was less limited by resources needed for egg production and more by the availability of suitable host nests. Fluctuating weekly host availabilities suggest that previously established, constant rates of cowbird egg laying would produce an excess of eggs during periods of low host availability. Further, the low frequency of parasitism (1%) of nests in stages too advanced for successful parasitism, and of abandoned nests, is consistent with the hypothesis that cowbirds' consistently high rate of egg production helps assure an egg is available when an appropriate nest is found. Frequently, nests were parasitized multiple times, raising the possibility that cowbirds were interfering with their own reproduction. A diverse host community increases the possibility that a decline of any one host species is unlikely to affect cowbird reproduction significantly. Received 11 July 1997 / Accepted: 31 March 1998     

Evolution of sexually transmitted and sexually transmissible human herpesviruses

Herpesviruses occur in an impressively wide range of animals and are associated with various diseases. The numerous routes taken during hundreds of millions of years of evolution have contributed to their striking adaptability and success as pathogens. Herpesviruses share a distinct virion structure and are classified taxonomically into a single order, the Herpesvirales, which is divided into three families. The phylogenetic relationships among members of the most populous family, the Herpesviridae, which includes all nine human herpesviruses, are generally similar to those among their hosts, supporting the view that there has been a large degree of coevolution between virus and host. Three human herpesviruses (human cytomegalovirus, Kaposi's sarcoma-associated herpesvirus, and herpes simplex virus type 1) are classed as agents capable of sexually transmissible infection (StxI), and one (herpes simplex virus type 2) as an agent capable of sexually transmitted infection (STI). The evolutionary characteristics of these viruses are described.     

Extensive genetic diversity, unique population structure and evidence of genetic exchange in the sexually transmitted parasite Trichomonas vaginalis

Background

Trichomonas vaginalis is the causative agent of human trichomoniasis, the most common non-viral sexually transmitted infection world-wide. Despite its prevalence, little is known about the genetic diversity and population structure of this haploid parasite due to the lack of appropriate tools. The development of a panel of microsatellite makers and SNPs from mining the parasite''s genome sequence has paved the way to a global analysis of the genetic structure of the pathogen and association with clinical phenotypes.

Methodology/Principal Findings

Here we utilize a panel of T. vaginalis-specific genetic markers to genotype 235 isolates from Mexico, Chile, India, Australia, Papua New Guinea, Italy, Africa and the United States, including 19 clinical isolates recently collected from 270 women attending New York City sexually transmitted disease clinics. Using population genetic analysis, we show that T. vaginalis is a genetically diverse parasite with a unique population structure consisting of two types present in equal proportions world-wide. Parasites belonging to the two types (type 1 and type 2) differ significantly in the rate at which they harbor the T. vaginalis virus, a dsRNA virus implicated in parasite pathogenesis, and in their sensitivity to the widely-used drug, metronidazole. We also uncover evidence of genetic exchange, indicating a sexual life-cycle of the parasite despite an absence of morphologically-distinct sexual stages.

Conclusions/Significance

Our study represents the first robust and comprehensive evaluation of global T. vaginalis genetic diversity and population structure. Our identification of a unique two-type structure, and the clinically relevant phenotypes associated with them, provides a new dimension for understanding T. vaginalis pathogenesis. In addition, our demonstration of the possibility of genetic exchange in the parasite has important implications for genetic research and control of the disease.     

Effects of brood parasitism on host reproductive success: evidence from larval interactions among dung beetles

This paper investigates the effect of brood parasitism in a dung beetle assemblage in an arid region of Spain. The study was conducted during the spring season (March-May 1994-1998) using mesh cylinders buried into the ground, filled with sand and with sheep dung on top. We quantified the proportion of nests containing larvae of parasitic beetles and their effect on host larvae survival. Experiments on the effect of parasitic larvae on host-larvae survival were conducted by placing scarab brood masses (raised from captive scarabs in the laboratory) in containers with and without aphodiid larvae. During the spring, dung desiccation is rapid, preventing aphodiids nesting in the dung, and forcing these species to adopt brood parasitism as a nesting strategy. Parasitic aphodiids were found in 12-47% of scarab nests of three species. The incidence of brood parasitization was positively related with the number of brood masses contained in the nests, being also higher in the most abundant species. Field data and experiments showed that brood parasites significantly reduced host larvae survival from 74.8% in non-parasitized nests to 8.8% in parasitized nests. Because different rates of nest parasitization and mortality were caused by parasites, brood parasitism had a differential effect on different host species. Thus, brood parasitism constitutes an important mortality factor reducing the reproductive success of the host species and potentially affecting the beetle abundance in the area.     

Condition-dependent virulence in a horizontally and vertically transmitted bacterial parasite

Virulence is a key component of parasite fitness. Its expression and selective value may not only depend on the features of the parasite's life cycle, but also on host genotype or environmental conditions. Using the freshwater ciliate Paramecium caudatum and its endonuclear bacterial parasite Holospora undulata , we measured variation in virulence (reduction in host division and survival), parasite load and fidelity of vertical transmission for (i) different stages of infection (associated with different opportunities for vertical and horizontal transmission), (ii) different host clones, and (iii) two food conditions. Later stages of infection dedicated to horizontal transmission were more virulent than earlier stages which rely on vertical transmission only. Besides, investment in horizontal transmission decreased the efficacy of vertical transmission, indicating a tradeoff between the two pathways. This may explain the phenotypic plasticity of transmission mode of this parasite. To some extent, virulence, parasite load and transmission fidelity varied with host clone identity and food treatment (higher virulence at low food). These results suggest that virulence is not a constant property of the parasite, and that a single (and simple) relationship between virulence and transmission does not exist.     

The influence of host plant species on parasitism of pollen beetles (Meligethes spp.) by Phradis morionellus

We investigated the response of the specialist insect predator Oligota kashmirica benefica (Coleoptera: Staphylinidae) to volatiles from lima bean leaves infested with the spider mite Tetranychus urticae (Acari: Tetranychidae), both in a Y-tube olfactometer and in a field in Kyoto, Japan. Adult male and female predators were significantly more attracted to T. urticae-infested leaves than to clean air. Adult male and female predators were not more attracted to uninfested leaves, artificially damaged leaves, or the spider mites and their visible products when compared to clean air. In a field trap experiment, 12 adult predators were caught in three traps containing T. urticae-infested lima bean plants over 13 days, whereas no adult predators were trapped in three traps containing uninfested lima bean plants during the same period. These results showed that O. kashmirica benefica adults responded to herbivore-induced plant volatiles from T. urticae-infested lima bean leaves under both laboratory and field conditions.     

Male circumcision and sexually transmitted infections in Botswana

This study set out to investigate the influence of male circumcision and other factors on sexually transmitted infections in Botswana. A syndromic approach, which diagnoses a sexually transmitted infection based on the presence of urethral discharge or genital ulcers rather than on laboratory tests, was used. The data were from the 2001 Botswana AIDS Impact Survey where a nationally representative, randomly selected sample of men and women aged 10-64 years were interviewed in both urban and rural areas. The sample selected for this study consisted of 216,480 men aged 15-64 years who had ever had sexual intercourse. The logistic regression technique was executed to examine the association between male circumcision and self-reported urethral discharge or genital ulcers, while controlling for all other independent variables in the analysis. The main finding of this study was that among men who are circumcised, the odds for self-reported urethral discharge or genital ulcers are significantly lower than for those men who are not circumcised in both urban and rural Botswana. The analysis also showed that the odds in favour of self-reported urethral discharge or genital ulcers, for men who drink alcohol, are twice as large as those for men who do not drink alcohol, controlling for all other independent variables in the analysis. Religion and ethnicity also came through as factors exerting a protective influence against self-reported symptoms of sexually transmitted infections. The conclusion is that while male circumcision appears to be significantly associated with the risk for self-reported urethral discharge or genital ulcers, it is man's behaviour, irrespective of ethnicity or religious dictates, that continues to play a vital role in protection against self-reported symptoms of sexually transmitted infections in Botswana.     

Monogamous networks and the spread of sexually transmitted diseases

Patterns of sexual mixing and heterogeneity in the number of sexual partners can have a huge effect on the spread of a sexually transmitted disease (STD). The sexual mixing network identifies all partnerships within a population over a given period and is a powerful tool in the study of such infections. Previous models assumed all links within the network to be concurrent active partnerships. We present a novel modelling approach in which we adapt the notion of a sexual contact network to a monogamous population by allowing the nature of the links to change. We use the underlying network to represent potential sexual partnerships, only some of which are active at any one time. Thus serial monogamy can be modelled while maintaining the patterns of mixing displayed by the population.     

Molecular parasitism in the Escherichia coli-Bdellovibrio bacteriovorus system: translocation of the matrix protein from the host to the parasite outer membrane

During the intracellular maturation in Escherichia coli of the parasite Bdellovibrio bacteriovorus the outer membrane, major protein I of E. coli (i.e., the matrix protein) becomes associated with the outer membrane of the emerging parasite cells. The binding properties of this protein with the outer membrane of the host and of the parasite are identical. An analogous phenomenon also occurs during Bdellovibrio parasitism on Klebsiella pneumoniae and on Salmonella typhimurium. Possible roles for this scavenging action of Bdellovibrio, and similar phenomena in other parasitic systems, are discussed.     

The evolution of risky behaviour in the presence of a sexually transmitted disease

Sexually transmitted diseases (STDs) are widespread in nature, often sterilizing their hosts or causing other pathogenic effects. Despite this, there is a widespread occurrence of behaviours that are likely to increase the risk to an individual of contracting an STD. Here, we examine the evolution of behaviours such as promiscuity or mate choice that increase the risk of contracting an STD, but also provide a fitness benefit. As might be expected, the balance between risk and fitness benefit defines the optimal strategy, but this relationship is not straightforward. In particular, we often predict the coexistence of highly risky and highly risk-averse individuals. Surprisingly, very safe strategists that only suffer a small cost will tend to coexist with highly risky strategists rather than outcompete them as might have been expected. Rather than selecting for monogamy or for reduced mate choice, therefore, the presence of an STD may often lead to variability in either promiscuity or mate choice.