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.     

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.     

SEXUALLY TRANSMITTED DISEASE AND PARASITE-MEDIATED SEXUAL SELECTION

Few studies have investigated the consequences of parasite-mediated sexual selection on the parasites involved. In some cases parasite-mediated sexual selection could lead to increased virulence, but I develop a simple model that shows that, if a parasite is sexually transmitted (i.e., is a sexually transmitted disease, or STD) and if mating success of the host is adversely affected by the parasite, then less virulent STDs will be selected for because transmission of the STD depends on the mating success of the host. This selection for reduced virulence could have important consequences for the role of STDs in sexual selection.     

Maximized virulence in a sterilizing pathogen: the anther-smut fungus and its co-evolved hosts

Host sterilization is a common feature of sexually transmitted diseases (STDs). Because host reproductive failure may free up resources for pathogen reproduction and transmission, theory predicts that selection on sterilizing pathogens will favour maximum virulence (i.e. complete sterilization). We examined patterns of infection in sexually transmitted anther-smut fungi (Microbotryum) on four of their host species in the Caryophyllaceae. Using controlled fungal matings and experimental inoculations, we compared disease expression in inoculations ranging from host-specific pathogens to hybrids and cross-species treatments. Our data support the existence of host-specific sibling species within the genus Microbotryum based on a low infection rate from cross-inoculations and reduced fitness for hybrid pathogens. These patterns of host specificity and reproductive isolation, however, were not absolute. We did observe some successful cross-species and hybrid infections, but the expression of disease was frequently incomplete, including only partial host sterilization and the failed dehiscence of pathogen spores. The prevalence of these maladapted disease phenotypes may greatly inhibit the emergence of novel host pathogen combinations. Infections by hybrid pathogen genotypes were intermediate, in terms of both infection rate and the normality of disease symptoms, between host-specific and cross-inoculated pathogens. In addition, the frequency with which hybrid and cross-inoculated anther-smut pathogens were able to infect but not sterilize new hosts supports the prediction that sterilizing STDs are under selection to maximize virulence in natural populations.     

A proposed feedback loop of sexually transmitted diseases and sexual behavior: the Red Queen's Dilemma

(Micro)organisms, such as bacteria, which cause sexually transmitted diseases (STDs) in humans are presented with an interesting ecological challenge. These microorganisms need humans to have sexual contact with each other in order for the microorganisms to spread to other hosts as well as to have subsequent generations of descendants. However, diseases tend to lower the sex drive and to render the host less sexually attractive. It is argued that, over time, selective advantages sculpted organisms which cause STDs to be minimally symptomatic and to indirectly increase the number of sexual partners of the host. Neisseria gonorrhoeae which cause the STD gonorrhea are used as a prototype for these putative sexual dynamics. As a counter to the (micro)organisms' biological adaptations, human cultural innovations emerged and became integrated into the various traditions of social structures.     

Frequency-dependent incidence in models of sexually transmitted diseases: portrayal of pair-based transmission and effects of illness on contact behaviour

We explore the transmission process for sexually transmitted diseases (STDs). We derive the classical frequency-dependent incidence mechanistically from a pair-formation model, using an approximation that applies to populations with rapid pairing dynamics (such as core groups or non-pair-bonding animals). This mechanistic derivation provides a framework to assess how accurately frequency-dependent incidence portrays the pair-based transmission known to underlie STD dynamics. This accuracy depends strongly on the disease being studied: frequency-dependent formulations are more suitable for chronic less-transmissible infections than for transient highly transmissible infections. Our results thus support earlier proposals to divide STDs into these two functional classes, and we suggest guidelines to help assess under what conditions each class can be appropriately modelled using frequency-dependent incidence. We then extend the derivation to include situations where infected individuals exhibit altered pairing behaviour. For four cases of increasing behavioural complexity, analytic expressions are presented for the generalized frequency-dependent incidence rate, basic reproductive number (R0) and steady-state prevalence (i infinity) of an epidemic. The expression for R0 is identical for all cases, giving refined insights into determinants of invasibility of STDs. Potentially significant effects of infection-induced changes in contact behaviour are illustrated by simulating epidemics of bacterial and viral STDs. We discuss the application of our results to STDs (in humans and animals) and other infectious diseases.     

Mating Competition,Promiscuity, and Life History Traits as Predictors of Sexually Transmitted Disease Risk in Primates

Competition among males influences the distribution of copulations and should therefore influence the spread of sexually transmitted diseases (STDs). We developed a model to investigate STDs in the mating and social systems found in primates, and we tested predictions using comparative methods. In the model, groups were distributed on a square lattice in which males or females disperse and males undergo characteristic dominance trajectories at maturity (challenge vs. queuing). We investigated the impact of mating rate, mating skew, migration rate of males or females, and group size on disease spread and prevalence. The model generated several predictions: 1) STD prevalence is higher in females than males; 2) STD risk increases with copulation rate; 3) high skew is negatively associated with STD risk; 4) STD risk is higher for all individuals when females disperse and 5) when mortality rates are lower; and 6) reproductive skew and later age of male dominance (queuing) produce more strongly female-biased STD prevalence. In comparative tests, we quantified STD risk as prevalence and richness of sexually transmitted organisms at the host species level. We found positive associations between host longevity and higher STD richness, and only (nonsignificant) weak trends for females to have higher STD prevalence. Mating skew showed a weakly positive association with STD richness, contrary to predictions of our model but consistent with predictions from a previous model. In some tests, we also found that female dispersal resulted in greater STD infection risk. Collectively, these results demonstrate that mating competition and demography influence patterns of STD infection, with mortality rates having the strongest effects in comparative tests.     

Constraints on parasite fecundity and transmission in an insect-STD system

Parasites that are sexually transmitted (causing sexually transmitted diseases, or STDs) can have important effects on host population dynamics, but we know almost nothing for such parasites about constraints on fecundity and transmission. In this study, we have examined the effect of two potentially important constraints in one of the few empirically well-studied animal-STD systems, the ladybird, Adalia bipunctata , and its sexually transmitted mite, Coccipolipus hippodamiae . Using a factorial design, we manipulated: (i) within-host competition, by varying infection intensity; and (ii) host condition, by introducing dietary stress. Infection with C . hippodamiae significantly reduced ladybird survival whether or not diet was restricted, and restricting diet led to reduced survival regardless of infection status. Increased infection intensity and reduced host condition (dietary stress) both independently constrained per capita rates of parasite egg production and the development of infective larvae. Furthermore, when host condition was compromised, significantly fewer larvae were transmitted per adult mite during copulation. The effect of infection intensity on per mite transmission was more complex: there was no significant effect when hosts were fed normally, but when the ladybirds were nutritionally stressed higher infection intensity was associated with a slight increase in the numbers that were transmitted (despite the fact that mite fecundity was reduced under these conditions). These results indicate that host condition and within-host competition may both play an important role in shaping the epidemiology of the A . bipunctata – C . hippodamiae system, by influencing the parasite's basic reproductive ratio (R₀) and the rate of epidemic spread. Our data also extend general insights into STD ecology, by highlighting the importance of constraints on disease dynamics that are likely to be widespread.     

Sexually transmitted diseases in polygynous mating systems: prevalence and impact on reproductive success

Studies of disease in relation to animal mating systems have focused on sexual selection and the evolution of sexual reproduction. Relatively little work has examined other aspects of ecological and evolutionary relationships between host social and sexual behaviour, and dynamics and prevalence of infectious diseases; this is particularly evident with respect to sexually transmitted diseases (STDs). Here, we use a simulation approach to investigate rates of STD spread in host mating systems ranging from permanent monogamy to serial polygyny or polyandry and complete promiscuity. The model assumes that one sex (female) is differentially attracted to the other, such that groups of varying size are formed within which mating and disease transmission occur. The results show that equilibrium disease levels are generally higher in females than males and are a function of variance in male mating success and the likelihood of a female switching groups between mating seasons. Moreover, initial rates of disease spread (determining whether an STD establishes in a population) depend on patterns of host movement between groups, variance in male mating success and host life history (e.g. mortality rates). Male reproductive success can be reduced substantially by a sterilizing STD and this reduction is greater in males that are more 'attractive' to females. In contrast, females that associate with more attractive males have lower absolute fitness than females associating with less attractive males. Thus, the potential for STDs to act as a constraint on directional selection processes leading to polygyny (or polyandry) is likely to depend on the details of mate choice and group dynamics.     

Lack of parasite-mediated sexual selection in a ladybird/sexually transmitted disease system

Despite the clear potential of sexually transmitted diseases (STDs) to affect host mating behaviour via both host and parasite evolution, there have been few explicit tests of the relationships between STDs and sexual behaviour in animals. We investigated the effect of infection on host sexual behaviour within an invertebrate system. Coccipolipus hippodamiae is a sexually transmitted ectoparasite of Adalia bipunctata, the two-spot ladybird. The parasite feeds on host haemolymph, develops rapidly, and is deleterious to A. bipunctata hosts of both sexes. We examined whether infection affected mating success, and whether males or females showed any preferences with respect to infection status. We observed field mating rates of infected and uninfected ladybirds and carried out controlled laboratory experiments. We did not detect any negative effects of parasite infection on host mating vigour, nor any evidence for the existence of a host mating preference based on infection status. In addition, there was no evidence of parasite-induced changes in behaviour, such as increased promiscuity, which would increase transmission opportunities for the parasite. In summary, contrary to a body of speculation, there was no evidence of any connection between infection and mating rate, in either sex. We discuss possible explanations for these findings.     

Modeling AIDS as a function of other sexually transmitted disease.

The spread of AIDS, as with any sexually transmitted disease, will depend on the pattern of sexual activity. Both the proportion of the population who have high partner exchange rates and the extent to which that proportion interacts with the remainder of the population are likely to be important determinants of the AIDS epidemic. However, it does not seem likely that surveys could obtain sufficiently reliable information of this nature for use in an accurate model of the AIDS epidemic. On the other hand, such information is implicitly contained in the epidemiology of other sexually transmitted diseases (STDs). Therefore a method is suggested of calculating the parameters of a model of the AIDS epidemic by comparing it with the epidemiology of another STD. The result is a model that predicts the likelihood of infection by the AIDS virus as a function of time and an individual's history of STD. It is suggested that further work along these lines may lead to a quantitative approach to assessing the importance of various STDs as cofactors in the spread of AIDS.     

The spatial distribution of plant populations, disease dynamics and evolution of resistance

Empirical studies of the interaction between the anther smut fungus Microbotryum violaceum and its host plant Lychnis alpina were combined with modelling approaches to investigate how variation in the spatial distribution of host populations influences disease dynamics and variation in resistance. Patterns of disease incidence and prevalence were surveyed in three contrasting systems of natural L . alpina populations where there is substantial variation in spatial structure, ranging from large continuous populations through to small isolated patches. Disease incidence (fraction of populations where disease was present) was highest in the continuous situation, and lowest in the most isolated populations. The reverse was true for prevalence (fraction of individuals diseased). To better understand the long-term ecological and evolutionary consequences of differences in among population spatial structure, we developed a two-dimensional spatially explicit simulation model in which host-population spacing was modelled by varying the percentage of sites suitable for the host. The general patterns of disease incidence and prevalence generated in the simulations corresponded well with the patterns observed in natural populations of L. alpina and M. violaceum ; i.e. the fraction of sites with disease increased while the average disease prevalence in diseased populations decreased when host populations became more connected. One likely explanation for the differences in disease incidence and prevalence seen in natural populations is that the evolution of host resistance varies as a function of the degree of fragmentation. This is supported by simulation results that were qualitatively similar to the survey data when resistance was allowed to vary, but not when hosts were assumed to be uniformly susceptible. In the former, the frequency of resistance increased markedly as host populations became more connected.     

Transcontinental migratory connectivity predicts parasite prevalence in breeding populations of the European barn swallow

Parasites exert a major impact on the eco‐evolutionary dynamics of their hosts and the associated biotic environment. Migration constitutes an effective means for long‐distance invasions of vector‐borne parasites and promotes their rapid spread. Yet, ecological and spatial information on population‐specific host–parasite connectivity is essentially lacking. Here, we address this question in a system consisting of a transcontinental migrant species, the European barn swallow (Hirundo rustica) which serves as a vector for avian endoparasites in the genera Plasmodium, Haemoproteus and Leucocytozoon. Using feather stable isotope ratios as geographically informative markers, we first assessed migratory connectivity in the host: Northern European breeding populations predominantly overwintered in dry, savannah‐like habitats in Southern Africa, whereas Southern European populations were associated with wetland habitats in Western Central Africa. Wintering areas of swallows breeding in Central Europe indicated a migratory divide with both migratory programmes occurring within the same breeding population. Subsequent genetic screens of parasites in the breeding populations revealed a link between the host's migratory programme and its parasitic repertoire: controlling for effects of local breeding location, prevalence of Africa‐transmitted Plasmodium lineages was significantly higher in individuals overwintering in the moist habitats of Western Central Africa, even among sympatrically breeding individuals with different overwintering locations. For the rarer Haemoproteus parasites, prevalence was best explained by breeding location alone, whereas no clear pattern emerged for the least abundant parasite Leucocytozoon. These results have implications for our understanding of spatio‐temporal host–parasite dynamics in migratory species and the spread of avian borne diseases.     

Sexually transmitted diseases among prostitutes in Fukuoka, Japan

The prevalence of sexually transmitted diseases (STDs) among prostitutes was investigated at a genitourinary hospital in Fukuoka, Japan, in 1985 and 1986. The most common STD was Chlamydia trachomatis infection, followed by gonorrhea and condyloma acuminatum. Candidiasis, trichomoniasis and genital herpes were relatively uncommon. The rate of prostitutes who had STD but had no subjective symptoms were 42.9% in 1985 and 30.9% in 1986. The rate of prostitutes having mixed STD infection was 35.8% among the summed 162 STD-contracted prostitutes.     

Wildlife disease prevalence in human‐modified landscapes

Human‐induced landscape change associated with habitat loss and fragmentation places wildlife populations at risk. One issue in these landscapes is a change in the prevalence of disease which may result in increased mortality and reduced fecundity. Our understanding of the influence of habitat loss and fragmentation on the prevalence of wildlife diseases is still in its infancy. What is evident is that changes in disease prevalence as a result of human‐induced landscape modification are highly variable. The importance of infectious diseases for the conservation of wildlife will increase as the amount and quality of suitable habitat decreases due to human land‐use pressures. We review the experimental and observational literature of the influence of human‐induced landscape change on wildlife disease prevalence, and discuss disease transmission types and host responses as mechanisms that are likely to determine the extent of change in disease prevalence. It is likely that transmission dynamics will be the key process in determining a pathogen's impact on a host population, while the host response may ultimately determine the extent of disease prevalence. Finally, we conceptualize mechanisms and identify future research directions to increase our understanding of the relationship between human‐modified landscapes and wildlife disease prevalence. This review highlights that there are rarely consistent relationships between wildlife diseases and human‐modified landscapes. In addition, variation is evident between transmission types and landscape types, with the greatest positive influence on disease prevalence being in urban landscapes and directly transmitted disease systems. While we have a limited understanding of the potential influence of habitat loss and fragmentation on wildlife disease, there are a number of important areas to address in future research, particularly to account for the variability in increased and decreased disease prevalence. Previous studies have been based on a one‐dimensional comparison between unmodified and modified sites. What is lacking are spatially and temporally explicit quantitative approaches which are required to enable an understanding of the range of key causal mechanisms and the reasons for variability. This is particularly important for replicated studies across different host‐pathogen systems. Furthermore, there are few studies that have attempted to separate the independent effects of habitat loss and fragmentation on wildlife disease, which are the major determinants of wildlife population dynamics in human‐modified landscapes. There is an urgent need to understand better the potential causal links between the processes of human‐induced landscape change and the associated influences of habitat fragmentation, matrix hostility and loss of connectivity on an animal's physiological stress, immune response and disease susceptibility. This review identified no study that had assessed the influence of human‐induced landscape change on the prevalence of a wildlife sexually transmitted disease. A better understanding of the various mechanisms linking human‐induced landscape change and the prevalence of wildlife disease will lead to more successful conservation management outcomes.     

Seroprevalence of anti-human parvovirus B19 antibodies in patients attending a centre for sexually transmitted diseases.

The aim of this study was to establish the serological prevalence of anti-human Parvovirus B19 (HP-B19) antibodies in a group of 321 patients attending a Centre for Sexually Transmitted Diseases (STDs) and epidemiologically examine whether this virus may also be sexually transmitted. For this purpose, the serum prevalence of anti-HP-B19 evaluated in STD patients (39%) was compared with that of 164 healthy blood donors (10%, p < 0.001), using commercially available ELISA methods detecting the anti-VP1 reactivity of the sera. The same STD patients were also analyzed for serum reactivities against 4 STD-causing microorganisms, namely T. pallidum (TPHA), HBV (HBcAb), HCV (HCV-Ab) and HIV (HIV-Ab), to observe possible associations with the serum anti-HP-B19 reactivity. These tests were also carried out with commercially available kits. The results suggest that the serum anti-HP-B19 antibody prevalence in patients with STDs is increased, also independently of their intravenous drug addition and varies with the reactivity pattern determined. In addition, as expected for a STD, the anti-HP-B19 prevalence is increased in homobisexual patients compared with heterosexuals.     

The effect of combat exposure on sexually transmitted diseases

Traumatic exposures can affect beliefs and behaviors related to the spread of sexually transmitted diseases (STDs), a persistent public health problem. I leverage a natural experiment created by variation in US military deployment location assignments to estimate how combat exposure changes a surviving deployed male veteran’s probability of acquiring a sexually transmitted disease. I analyze longitudinal data from 1994 to 2008 on 485 deployed veterans with information theoretic methods to reduce the sensitivity of estimates to small samples, an infrequently observed outcome, and highly correlated covariates. For veterans assigned to a combat zone, I estimate combat exposure results in a 5.4 percentage point increase in the probability of acquiring an STD. Additional estimations provide evidence suggesting risky behaviors involving substance use or multiple sexual partners may serve as pathways from combat exposure to STDs. My results are relevant to discussions regarding STD screening and care needs for trauma exposed individuals.     

Effect of Ascaridia compar infection on rock partridge population dynamics: empirical and theoretical investigations

Helminth parasites have the potential to significantly affect the dynamics of their hosts. As a consequence, they can dramatically threaten the persistence of endangered species, such as rock partridge Alectoris graeca saxatilis, found in the Province of Trento (northern Italy). The aim of this work was to understand the effect of helminth parasites on rock partridge fitness, and the subsequent potential effects on host population dynamics. In particular, we investigated the hypothesis that infections from Ascaridia compar induce rock partridge population cycles observed in Trentino. In order to support this hypothesis, we compared the predictions obtained from a host–parasite interaction model including variable parasite aggregation with multi‐annual empirical data of A. compar infection in natural host populations. We estimated host demographic parameters using rock partridge census data from Trentino, and the parasitological parameters from a series of experimental infections in a captive rock partridge population. The host–parasite model predicted higher A. compar abundance in rock partridge populations exhibiting cyclic dynamics compared to non‐cyclic ones. In addition, for cyclic host populations, the model predicted an increase in mean parasite burden with the length of cycle period. Model predictions were well‐supported by field data: significant differences in parasite infection between cyclic and non‐cyclic populations and among cyclic populations with different oscillation periods were observed. On the basis of these results, we conclude that helminth parasites can not be ruled out as drivers of rock partridge population dynamics in Trentino and must be considered when planning conservation strategies of this threatened species.     

Apparent seasonality of parasite dynamics: analysis of cyclic prevalence patterns

Seasonal disease dynamics are common in nature, but their causes are often unknown. Our case study provides insight into the cyclic prevalence pattern of the horizontally and vertically transmitted microsporidium Octosporea bayeri in its Daphnia magna host. Data from several populations over a four year period revealed a regular prevalence increase during summer and a decrease over winter when hosts underwent diapause. Prevalence also decreased after summer diapause indicating that the decline is causally linked to diapause rather than to winter conditions. Experiments showed that host diapause itself can explain a certain proportion of the decline. The decline further depends on the environmental conditions during diapause: infected resting eggs suffered from higher mortality under experimental winter than under experimental summer diapause conditions. Investigating the mechanisms of prevalence increase after diapause, the parasite was found to survive winter outside its host, enabling horizontal infection of susceptible hosts in the following growing season. Allowing for horizontal transmission in experimental host populations resulted in a steep prevalence increase, while excluding it led to a pronounced decline. Thus, the apparent seasonality in O. bayeri prevalence is characterized by a decline during host diapause followed by horizontal spread of the parasite during the host's asexual growth phase.     

Conquering sexually transmitted diseases

Sexually transmitted diseases (STDs) are a major public-health problem and also a significant financial burden on the economy. Past and ongoing attempts to create vaccines against sexually transmitted pathogens have met with varying success. This article highlights some of the public-health and social problems that are associated with STDs and the technical and ethical challenges in treating them, and raises several questions that need to be addressed if STDs are to be conquered.