Sex‐biased transmission of a complex life‐cycle parasite: why males matter

Male‐bias in parasite infection exists in a variety of host–parasite systems, but the epidemiological importance of males and, specifically, whether males are responsible for producing a disproportionate amount of onward transmission events (male‐biased transmission) has seldom been tested. The primary goal of our study was to experimentally test for male‐biased transmission in a system with no sex‐biased prevalence. We performed a longitudinal field experiment and continuously removed intestinal nematode parasites from either male or female white‐footed mice and recorded the subsequent transmission among the untreated sex. We predicted males are responsible for the majority of transmission and female mice would have lower infection prevalence under the male‐anthelmintic treatment than controls and that male mice would experience little or no change in infection prevalence under female‐anthelmintic treatment compared to controls. Our second goal was to evaluate physiological hypotheses relating to the mechanisms that could generate the observed transmission pattern. To that end, we examined a cross‐sectional sample of hosts to explicitly test for differences in parasite intensity, parasite egg shedding rate and reproductive output per parasite between male and female hosts. Removing parasites from male mice resulted in lower infection rates among female mice but, in contrast, there was no effect of female‐deworming on infection rates among male mice; providing evidence that males provide disproportionately greater numbers of transmission events than females. We found no difference in prevalence, intensity, or fecundity of parasites between sexes in the cross‐sectional sample of mice and rejected the mechanistic hypotheses. Without male‐biased prevalence, intensity, or parasite fecundity, we concluded that male‐biased transmission is unlikely to be created via physiological differences and the parsimonious explanation is that male behavior spreads infective stages in a more successful manner. We demonstrate that transmission heterogeneities can exist in the absence of individual heterogeneities in infection.     

Maternal antibodies contribute to sex-based difference in hantavirus transmission dynamics

Individuals often differ in their ability to transmit disease and identifying key individuals for transmission is a major issue in epidemiology. Male hosts are often thought to be more important than females for parasite transmission and persistence. However, the role of infectious females, particularly the transient immunity provided to offspring through maternal antibodies (MatAbs), has been neglected in discussions about sex-biased infection transmission. We examined the effect of host sex upon infection dynamics of zoonotic Puumala hantavirus (PUUV) in semi-natural, experimental populations of bank vole (Myodes glareolus). Populations were founded with either females or males that were infected with PUUV, whereas the other sex was immunized against PUUV infection. The likelihood of the next generation being infected was lower when the infected founders were females, underlying the putative importance of adult males in PUUV transmission and persistence in host populations. However, we show that this effect probably results from transient immunity that infected females provide to their offspring, rather than any sex-biased transmission efficiency per se. Our study proposes a potential contrasting nature of female and male hosts in the transmission dynamics of hantaviruses.     

Sex‐dependent infection causes nonadditive effects on kissing bug fecundity

The influence of parasites on host reproduction has been widely studied in natural and experimental conditions. Most studies, however, have evaluated the parasite impact on female hosts only, neglecting the contribution of males for host reproduction. This omission is unfortunate as sex‐dependent infection may have important implications for host–parasite associations. Here, we evaluate for the first time the independent and nonindependent effects of gender infection on host reproductive success using the kissing bug Mepraia spinolai and the protozoan Trypanosoma cruzi as model system. We set up four crossing treatments including the following: (1) both genders infected, (2) both genders uninfected, (3) males infected—females uninfected, and (4) males uninfected—females infected, using fecundity measures as response variables. Interactive effects of infection between sexes were prevalent. Uninfected females produced more and heavier eggs when crossed with uninfected than infected males. Uninfected males, in turn, sired more eggs and nymphs when crossed with uninfected than infected females. Unexpectedly, infected males sired more nymphs when crossed with infected than uninfected females. These results can be explained by the effect of parasitism on host body size. As infection reduced size in both genders, infection on one sex only creates body size mismatches and mating constraints that are not present in pairs with the same infection status. Our results indicate the fitness impact of parasitism was contingent on the infection status of genders and mediated by body size. As the fecundity impact of parasitism cannot be estimated independently for each gender, inferences based only on female host infection run the risk of providing biased estimates of parasite‐mediated impact on host reproduction.     

Sex differences in parasitic infections among arthropod hosts: is there a male bias?

A higher susceptibility to diseases or parasites in males than females may be an ultimate consequence of the different reproductive strategies favored by selection in the two sexes. At the proximate level, the immunosuppressant effects of testosterone in vertebrates provide a mechanism that can cause male biases in parasite infections. Invertebrates, however, lack testosterone and other steroid hormones. We used a meta-analysis of published results to investigate whether sex biases in parasite infections were generally observed among arthropod hosts despite the absence of the immune-endocrine coupling provided by testosterone. Overall, male and female arthropods did not differ in prevalence or intensity of parasite infections. This is based on an analysis of sex differences corrected for sample size and, when possible, variability in the original data. Sex biases in parasite infection were not more likely to be observed in certain host or parasite taxa, and were not more pronounced in experimental studies than in surveys of naturally infected hosts. Our results suggest that because of the absence of endocrine-immune interactions in arthropods, males are not generally more prone to parasite infections than females despite the greater intensity of sexual selection acting on males.     

Male hosts are responsible for the transmission of a trophically transmitted parasite, Pterygodermatites peromysci, to the intermediate host in the absence of sex-biased infection

Field studies have identified that male-biased infection can lead to increased rates of transmission, so we examined the relative importance of host sex on the transmission of a trophically transmitted parasite (Pterygodermatites peromysci) where there is no sex-biased infection. We experimentally reduced infection levels in either male or female white-footed mice (Peromyscus leucopus) on independent trapping grids with an anthelmintic and recorded subsequent infection levels in the intermediate host, the camel cricket (Ceuthophilus pallidipes). We found that anthelmintic treatment significantly reduced the prevalence of infection among crickets in both treatment groups compared with the control, and at a rate proportional to the number of mice de-wormed, indicating prevalence was not affected by the sex of the shedding definitive host. In contrast, parasite abundance in crickets was higher on the grids where females were treated compared with the grids where males were treated. These findings indicate that male hosts contribute disproportionately more infective stages to the environment and may therefore be responsible for the majority of parasite transmission even when there is no discernable sex-biased infection. We also investigated whether variation in nematode length between male and female hosts could account for this male-biased infectivity, but found no evidence to support that hypothesis.     

HOW CAN SEX RATIO DISTORTERS REACH EXTREME PREVALENCES? MALE‐KILLING WOLBACHIA ARE NOT SUPPRESSED AND HAVE NEAR‐PERFECT VERTICAL TRANSMISSION EFFICIENCY IN ACRAEA ENCEDON

Abstract.— Maternally transmitted bacteria that kill male hosts early in their development are found in many insects. These parasites typically infect 1–30% of wild females, but in a few species of insects, prevalences exceed 95%. We investigated one such case in the butterfly Acraea encedon , which is infected with a male-killing Wolbachia bacterium. We measured three key parameters that affect the prevalence of the parasite: transmission efficiency, rate of survival of infected males, and the direct cost of infection. We observed that all wild females transmit the bacterium to all their offspring and that all infected males die in wild populations. We were unable to detect any physiological cost to infection in lab culture. These observations explain the high prevalence of the A. encedon male killer, as theory predicts that under these conditions the parasite will spread to fixation. This will occur provided the death of males provides some benefit to the surviving infected females. The problem therefore becomes why the bacterium has not reached fixation and driven the butterfly extinct due to the shortage of males. We therefore investigated whether males choose to mate with uninfected rather than infected females, as this would prevent the bacterium from reaching fixation. We tested this hypothesis in the "lekking swarms" of virgin females found in the most female-biased populations, and were unable to detect any evidence of mate choice. In conclusion, this male killer has spread to high prevalence because it has a high transmission efficiency and low cost, but the factors maintaining uninfected females in the population remain unknown.     

Water-seeking behavior in insects harboring hairworms: should the host collaborate?

We explored the idea that hosts infected with manipulative parasitesmight mitigate the costs of infection by collaborating withthe parasite rather than resisting it. Nematomorphs are usuallyconsidered to be manipulative parasites of arthropods becausethey cause hosts to seek an aquatic environment, which is neededby the adult parasite. We placed infected cricket hosts in situationsof forced noncompliance and compared some fitness parameters(life expectancy, gonad development, and reproductive behaviors)in noncompliant hosts and hosts allowed to express parasite-inducedbehavior. Compared to uninfected controls, reduced survivalwas observed in both males and females from the two categoriesof infected hosts, collaborative or not. A substantial proportionof collaborative females produced eggs or had developed ovarieswhile such phenomena were never observed among noncollaborativeones. Collaborative females retained a nymphal phenotype, butadult males nevertheless courted and produced spermatophoresto such females. However, collaborative females had difficultiesmounting males, taking spermatophores and/or ovipositing. Incontrast to females, all males were entirely castrated by theparasite regardless of their behavior, collaborative or not.Thus, bringing the parasite into water does not effectivelymitigate the costs of infection for the host.     

Lack of preference for infective faeces in Hymenolepis diminuta-infected beetles (Tenebrio molitor)

The beetle-tapeworm life cycle provides a convenient system to study how host behaviour influences the probability of re-infection because initial and secondary infections can be tracked. The beetle, Tenebrio molitor, is infected with the tapeworm Hymenolepis diminuta when it ingests rat faeces containing tapeworm eggs, which upon hatching undergo five morphologically distinct stages while developing inside the beetle. In a series of preference trials, both individual and groups of previously infected beetles were exposed to baits of infective (faeces with eggs) and uninfective faeces. Beetles did not differ in the amount of time spent or in the number of occurrences at each bait type, suggesting that infected beetles show no preference for infective faeces. This may be a host adaptation to avoid further infection, parasite manipulation to avoid competition for host resources, or both. Further, once infected, beetles are no more or no less likely to become re-infected than uninfected beetles. An analysis of the mean and variance of infection suggests that some individuals are highly susceptible to and some are highly resistant to infection, with males being more variable than females. This could explain the higher load of cysticercoids observed in males.     

Parasitized female mice display reduced aversive responses to the odours of infected males.

The present study showed that parasites influence both the responses of uninfected females to males and the responses of female hosts to infected males. In female laboratory mice one of the consequences of exposure to the olfactory cues associated with an infected male was a reduction of the reactivity to a thermal surface, i.e. pain inhibition or analgaesia. Uninfected oestrous and non-oestrous female mice displayed marked analgaesic responses after exposure to the odours of males infected with either the enteric single-host nematode parasite, Heligmosomoides polygyrus, or the protozoan parasite, Eimeria vermiformis. The uninfected oestrous females distinguished between infected and physically stressed males, displaying a greater analgaesic response to the odours of infected males. These analgaesic responses and their anxiety/ fearfulness-associated behavioural correlates could elicit either a reduced interest in, or avoidance of, parasitized males by females. Oestrous female mice infected with H. polygyrus displayed a reduced analgaesic response to the odours of the infected males and differentially responded to the odours of males infected with either the same (H. polygyrus) or a different parasite (E. vermiformis). An exposure time of 1 min elicited minimal responses to the odours of males infected with the same parasite, H. polygyrus, and an attenuated, though significant, non-opioid peptide-mediated analgaesic response to males infected with E. vermiformis. An exposure time of 30 min elicited similar markedly reduced endogenous opioid peptide-mediated analgaesic responses to the odours of both of the categories of infected males. The responses to the odours of a stressed male were, however, unaffected by the parasitic infection. The reduced analgaesic responses of the parasitized females to the odours of infected males may involve either enhanced odour familiarity and responses to group odour templates and/or neuromodulatory shifts resulting in reduced fearfulness and potentially greater interest in the infected males.     

Male-biased sex-ratio distortion caused by Octosporea bayeri, a vertically and horizontally-transmitted parasite of Daphnia magna

Female-biased sex-ratio distortion is often observed in hosts infected with vertically-transmitted microsporidian parasites. This bias is assumed to benefit the spread of the parasite, because male offspring usually do not transmit the parasite further. The present study reports on sex-ratio distortion in a host-parasite system with both horizontal and vertical parasite transmission: the microsporidium Octosporea bayeri and its host, the planktonic cladoceran Daphnia magna. In laboratory and field experiments, we found an overall higher proportion of male offspring in infected than in uninfected hosts. In young males, there was no parasite effect on sperm production, but, later in life, infected males produced significantly less sperm than uninfected controls. This shows that infected males are fertile. As males are unlikely to transmit the parasite vertically, an increase in male production could be advantageous to the host during phases of sexual reproduction, because infected mothers may obtain uninfected grandchildren through their sons. Life-table experiments showed that, overall, sons harboured more parasite spores than their sisters, although they reached a smaller body size and died earlier. Male production may thus be beneficial for the parasite when horizontal transmission has a large pay-off as males may contribute more effectively to parasite spread than females.     

Host sex and ectoparasites choice: preference for, and higher survival on female hosts

1. Sex differences in levels of parasite infection are a common rule in a wide range of mammals, with males usually more susceptible than females. Sex-specific exposure to parasites, e.g. mediated through distinct modes of social aggregation between and within genders, as well as negative relationships between androgen levels and immune defences are thought to play a major role in this pattern. 2. Reproductive female bats live in close association within clusters at maternity roosts, whereas nonbreeding females and males generally occupy solitary roosts. Bats represent therefore an ideal model to study the consequences of sex-specific social and spatial aggregation on parasites' infection strategies. 3. We first compared prevalence and parasite intensities in a host-parasite system comprising closely related species of ectoparasitic mites (Spinturnix spp.) and their hosts, five European bat species. We then compared the level of parasitism between juvenile males and females in mixed colonies of greater and lesser mouse-eared bats Myotis myotis and M. blythii. Prevalence was higher in adult females than in adult males stemming from colonial aggregations in all five studied species. Parasite intensity was significantly higher in females in three of the five species studied. No difference in prevalence and mite numbers was found between male and female juveniles in colonial roosts. 4. To assess whether observed sex-biased parasitism results from differences in host exposure only, or, alternatively, from an active, selected choice made by the parasite, we performed lab experiments on short-term preferences and long-term survival of parasites on male and female Myotis daubentoni. When confronted with adult males and females, parasites preferentially selected female hosts, whereas no choice differences were observed between adult females and subadult males. Finally, we found significantly higher parasite survival on adult females compared with adult males. 5. Our study shows that social and spatial aggregation favours sex-biased parasitism that could be a mere consequence of an active and adaptive parasite choice for the more profitable host.     

Trypanosomatid parasites infecting managed honeybees and wild solitary bees

The parasite Crithidia mellificae (Kinetoplastea: Trypanosomatidae) infects honeybees, Apis mellifera. No pathogenic effects have been found in individual hosts, despite positive correlations between infections and colony mortalities. The solitary bee Osmia cornuta might constitute a host, but controlled infections are lacking to date. Here, we challenged male and female O. cornuta and honeybee workers in laboratory cages with C. mellificae. No parasite cells were found in any control. Parasite numbers increased 6.6 fold in honeybees between days 6 and 19 p.i. and significantly reduced survival. In O. cornuta, C. mellificae numbers increased 2–3.6 fold within cages and significantly reduced survival of males, but not females. The proportion of infected hosts increased in O. cornuta cages with faeces, but not in honeybee cages without faeces, suggesting faecal – oral transmission. The data show that O. cornuta is a host of C. mellificae and suggest that males are more susceptible. The higher mortality of infected honeybees proposes a mechanism for correlations between C. mellificae infections and colony mortalities.     

Reduced blood parasite prevalence with age in the Seychelles Warbler: selective mortality or suppression of infection?

Avian malaria can affect survival and reproduction of their hosts. Two patterns commonly observed in birds are that females have a higher prevalence of malaria than do males and that prevalence decreases with age. The mechanisms behind these patterns remain unclear. However, most studies on blood parasite infections are based on cross-sectional analyses of prevalence, ignoring malaria related mortality and individual changes in infection. Here, we analyse both within-individual changes in malaria prevalence and long-term survival consequences of infection in the Seychelles Warbler (Acrocephalus sechellensis). Adults were less likely to be infected than juveniles but, contrary to broad patterns previously reported in birds, females were less likely to be infected than males. We show by screening individual birds in two subsequent years that the decline with age is a result both of individual suppression of infection and selective mortality. Birds that were infected early in life had a lower survival rate compared to uninfected birds, but among those that survived to be screened twice the proportion of infected birds had also decreased. Uninfected birds did not become infected later in life. Males were found to be more infected than females in this species possibly because, unlike most birds, males are the dispersing sex and the cost of dispersal may have to be traded against immunity. Infected males took longer to suppress their infection than did females. We conclude that these infections are indeed costly, and that age-related patterns in blood parasite prevalence are influenced both by suppression and selective mortality.     

Infection increases the value of nuptial gifts, and hence male reproductive success, in the Hymenolepis diminuta-Tenebrio molitor association

During copulation, male insects pass accessory gland components to the female with the spermatophore. These gifts can affect female reproductive behaviour, ovulation and oviposition. Here, we show that female mealworm beetles, Tenebrio molitor, mated with males infected with metacestodes of the rat tapeworm, Hymenolepis diminuta, produced significantly more offspring than those mated with uninfected males. There is a significant positive relationship between parasite intensity in the male and reproductive output in the female. Infection results in a significant increase in bean-shaped accessory gland (BAG) size. We suggest that infected males pass superior nuptial gifts to females and discuss the confounding effects of infection in male and female beetles upon overall fitness costs of infection for the host and the likelihood that the parasite is manipulating host investment in reproduction.     

A cost of Wolbachia-induced sex reversal and female-biased sex ratios: decrease in female fertility after sperm depletion in a terrestrial isopod

A number of parasites are vertically transmitted to new host generations via female eggs. In such cases, host reproduction is an intimate component of parasite fitness and no cost of the infection on host reproduction is expected to evolve. A number of these parasites distort host sex ratios towards females, thereby increasing either parasite fitness or the proportion of the host that transmit the parasite. In terrestrial isopods (woodlice), Wolbachia bacteria are responsible for sex reversion and female-biased sex ratios, changing genetic males into functional neo-females. Although sex ratio distortion is a powerful means for parasites to increase in frequency in host populations, it also has potential consequences on host biology, which may, in turn, have consequences for parasite prevalence. We used the woodlouse Armadillidium vulgare to test whether the interaction between Wolbachia infection and the resulting excess of females would limit female fertility through the reduction in sperm number that they receive from males. We showed that multiple male mating induces sperm depletion, and that this sperm depletion affects fertility only in infected females. This decrease in fertility, associated with male mate choice, may limit the spread of Wolbachia infections in host populations.     

Transmission pattern and intraspecific competition as determinants of population structure in pinworms (Oxyurida: Nematoda).

The transmission pattern of Zonothrix columbianus (Nematoda: Oxyurida) in its host Tropisternus columbianus (Coleoptera: Hydrophilidae), an aquatic beetle, was studied to determine whether parasites were dispersed with their hosts and to examine the possible role of intraspecific competition in limiting population size. Beetles were sampled at regular intervals from fall 1986 through fall 1989 and examined for worms. Worms, absent in larval stages of the host, were uncommon in newly metamorphosed beetles and therefore probably do not infect adult stages until after they have dispersed; worms are not dispersed with the host. Prevalence reached its lowest points in spring and fall when newly metamorphosed beetles were most common, but it was near 100% for most of the year. Worms were uniformly distributed in the host population. Many hosts had exactly 1 male and 1 female worm; the high prevalence suggests that this infrahost population results from interference competition between males on the one hand and females on the other. Only 3 of 285 beetles contained more than 1 male. Females shared the host with members of the same sex more commonly than males, but females from hosts harboring more than 1 female had significantly fewer eggs than lone females in hosts. Numbers of adult stages of beetles were estimated during spring, summer, and fall of 1989 and were lower in early spring and late fall. Because worms do not disperse with hosts, the panmictic unit could be estimated from the number of infected beetles; this probably was about 50 individuals during the winter bottleneck.     

Impact of a novel species of Nosema on the southwestern corn borer (Lepidoptera: Crambidae)

A study was undertaken to elucidate the impact of an undescribed Nosema sp. on the southwestern corn borer (SWCB; Diatraea grandiosella Dyar). The Nosema sp. (isolate 506) included in the study was isolated from an overwintering SWCB larva in Mississippi. It was highly infectious per os, with a median infective dose of 2.0 x 10(3) spores per larva. Even at the highest dosage tested (10(7) spores per larva), minimal mortality (< or = 3%) was observed in infected larvae, pupae, and adults reared in the laboratory on an artificial diet. However, infected pupae (0- and 7-d-old) were smaller, and the time to adult eclosion from pupation was slightly increased. Furthermore, the number of eggs produced by infected SWCB female moths substantially decreased (32%), and this effect was most pronounced on day 2, when the greatest number of eggs were oviposited by infected and noninfected moths. For eggs produced by infected females mated with infected males, hatch was slightly decreased by 16 and 15% for eggs laid on days 2 and 3, respectively. In addition, egg hatch was reduced in eggs oviposited by noninfected females mated with infected males on day 3. A low prevalence of infection (< 6%) was observed in the F1 generation originating from infected females mating with noninfected males, from noninfected females mating with infected males, and from infected females mating with infected males. Nosema 506 spores were observed in the proximity of reproductive tissues of infected female and male moths. Spores also were detected on the chorion surface and within eggs laid by infected females. Furthermore, 1-11% of larvae hatching from surface-sterilized eggs were infected by Nosema 506 indicating a transovarial mechanism of transmission.     

Host age,sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques

Parasites are characteristically aggregated within hosts, but identifying the mechanisms underlying such aggregation can be difficult in wildlife populations. We examined the influence of host age and sex over an annual cycle on the eggs per gram of feces (EPG) of nematode parasites infecting wild Japanese macaques (Macaca fuscata yakui) on Yakushima Island. Five species of nematode were recorded from 434 fecal samples collected from an age-structured group of 50 individually recognizable macaques. All parasites exhibited aggregated EPG distributions. The age–infection profiles of all three directly transmitted species (Oesophagostomum aculeatum, Strongyloides fuelleborni, and Trichuris trichiura) exhibited convex curves, but concavity better characterized the age–infection curves of the two trophically transmitted species (Streptopharagus pigmentatus and Gongylonema pulchrum). There was a male bias in EPG and prevalence of infection with directly transmitted species, except in the prevalence of O. aculeatum, and no sex bias in the other parasites. Infection with O. aculeatum showed a female bias in prevalence among young adults, and additional interactions with sex and seasonality show higher EPG values in males during the mating season (fall) but in females during the birth season (spring). These patterns suggest that an immunosuppressive role by reproductive hormones may be regulating direct, but not indirect, life-cycle parasites. Exposure at an early age may trigger an immune response that affects all nematodes, but trophically transmitted species appear to accumulate thereafter. Although it is difficult to discern clear mechanistic explanations for parasite distributions in wildlife populations, it is critical to begin examining these patterns in host species that are increasingly endangered by anthropogenic threats.     

Different transmission strategies of a parasite in male and female hosts

We investigated whether a parasite with two routes of transmission responds to the different transmission opportunities offered by male and female hosts by using different transmission strategies in the two sexes. The parasite Ascogregarina culicis, which infects the mosquito Aedes aegypti, can be transmitted as its host’s pupa transforms into an adult or when a female lays its eggs. As the latter transmission route is missing in males, we expected, and found, that the parasite releases a greater proportion of its infectious forms during emergence when it is within a male than when it infects a female. The transmission route, which influences the parasite’s dispersal and the evolution of its virulence, was also affected by the dose of infection and the parasite’s previous transmission route. Our results emphasize the complexity underlying the development of parasites and show their ability to tune their strategy to their environment.     

Strength in numbers: high parasite burdens increase transmission of a protozoan parasite of monarch butterflies (<Emphasis Type="Italic">Danaus plexippus</Emphasis>)

Parasites often produce large numbers of offspring within their hosts. High parasite burdens are thought to be important for parasite transmission, but can also lower host fitness. We studied the protozoan Ophryocystis elektroscirrha, a common parasite of monarch butterflies (Danaus plexippus), to quantify the benefits of high parasite burdens for parasite transmission. This parasite is transmitted vertically when females scatter spores onto eggs and host plant leaves during oviposition; spores can also be transmitted between mating adults. Monarch larvae were experimentally infected and emerging adult females were mated and monitored in individual outdoor field cages. We provided females with fresh host plant material daily and quantified their lifespan and lifetime fecundity. Parasite transmission was measured by counting the numbers of parasite spores transferred to eggs and host plant leaves. We also quantified spores transferred from infected females to their mating partners. Infected monarchs had shorter lifespans and lower lifetime fecundity than uninfected monarchs. Among infected females, those with higher parasite loads transmitted more parasite spores to their eggs and to host plant leaves. There was also a trend for females with greater parasite loads to transmit more spores to their mating partners. These results demonstrate that high parasite loads on infected butterflies confer a strong fitness advantage to the parasite by increasing between-host transmission.