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.     

Are sexes equally parasitized in damselflies and dragonflies?

Parasitism plays an essential part in ecology and evolution of host species and understanding the reasons for differential parasitism within and among hosts species is therefore important. Among the very important factors potentially affecting parasitism is the gender of the host. Here, we studied whether either females or males are more likely to harbour parasites among Odonatan insects, by relying on an extensive literature review and new field data. We collected data on numerous dragonfly and damselfly species and their ectoparasites (water mites) and endoparasites (gregarines) to examine the generality of similarities and differences in prevalence, intensity and maximum number of parasites of male and female hosts. We found three main results. Firstly, most of the odonate host species showed no differences between sexes in either gregarine or water mite prevalence and intensity. The only exception was female damselflies’ higher gregarine prevalence and intensity compared to conspecific males. These inequalities in gregarine parasitism may be due to behavioral and physiological differences between conspecific males and females. In comparison, there were no differences in dragonflies between sexes in water mite or gregarine prevalence and intensity. Secondly, damselflies had higher prevalence and intensity levels of both gregarine and water mite parasites compared to dragonflies. Finally, we found a strong species level pattern between female and male parasitism: a certain level of gregarine or water mite parasitism in one sex was matched with a similar parasitism level for the other. This indicates similar exposure and susceptibility to parasites on both sexes. Even though significant differences of parasite levels between the sexes were observed within certain host species, our results strongly suggest that on a general level a more parasitized sex does not exist in the order, Odonata.     

The Sicker Sex: Understanding Male Biases in Parasitic Infection,Resource Allocation and Fitness

The “sicker sex” idea summarizes our knowledge of sex biases in parasite burden and immune ability whereby males fare worse than females. The theoretical basis of this is that because males invest more on mating effort than females, the former pay the costs by having a weaker immune system and thus being more susceptible to parasites. Females, conversely, have a greater parental investment. Here we tested the following: a) whether both sexes differ in their ability to defend against parasites using a natural host-parasite system; b) the differences in resource allocation conflict between mating effort and parental investment traits between sexes; and, c) effect of parasitism on survival for both sexes. We used a number of insect damselfly species as study subjects. For (a), we quantified gregarine and mite parasites, and experimentally manipulated gregarine levels in both sexes during adult ontogeny. For (b), first, we manipulated food during adult ontogeny and recorded thoracic fat gain (a proxy of mating effort) and abdominal weight (a proxy of parental investment) in both sexes. Secondly for (b), we manipulated food and gregarine levels in both sexes when adults were about to become sexually mature, and recorded gregarine number. For (c), we infected male and female adults of different ages and measured their survival. Males consistently showed more parasites than females apparently due to an increased resource allocation to fat production in males. Conversely, females invested more on abdominal weight. These differences were independent of how much food/infecting parasites were provided. The cost of this was that males had more parasites and reduced survival than females. Our results provide a resource allocation mechanism for understanding sexual differences in parasite defense as well as survival consequences for each sex.     

The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis

We investigated the role of host sex in parasite transmission and questioned: ‘Is host sex important in influencing the dynamics of infection in free living animal populations?’ We experimentally reduced the helminth community of either males or females in a yellow‐necked mice (Apodemus flavicollis) population using an anthelmintic, in replicated trapping areas, and subsequently monitored the prevalence and intensity of macroparasites in the untreated sex. We focussed on the dominant parasite Heligmosomoides polygyrus and found that reducing parasites in males caused a consistent reduction of parasitic intensity in females, estimated through faecal egg counts, but the removal of parasites in females had no significant influence on the parasites in males. This finding suggests that males are responsible for driving the parasite infection in the host population and females may play a relatively trivial role. The possible mechanisms promoting such patterns are discussed.     

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.     

Effect of sexual segregation on host-parasite interaction: Model simulation for abomasal parasite dynamics in alpine ibex (Capraibex)

We investigated whether sexual segregation might affect parasite transmission and host dynamics, hypothesising that if males are the more heavily infected sex and more responsible for the transmission of parasite infections, female avoidance of males and the space they occupy could reduce infection rates. A mathematical model, simulating the interaction between abomasal parasites and a hypothetical alpine ibex (Capraibex) host population composed of its two sexes, was developed to predict the effect of different degrees of sexual segregation on parasite intensity and on host abundance. The results showed that when females tended to be segregated from males, and males were distributed randomly across space, the impact of parasites was the lowest, resulting in the highest host abundance, with each sex having the lowest parasite intensity. The predicted condition that minimises the impact of parasites in our model was the one closest to that observed in nature where females actively seek out the more segregated sites while males are less selective in their ranging behaviour. The overlapping of field observation with the predicted optimal strategy lends support to our idea that there might be a connection between parasite transmission and sexual segregation. Our simulations provide the biological boundaries of host-parasite interaction needed to determine a parasite-mediated effect on sexual segregation and a formalised null hypothesis against which to test future field experiments.     

Weak relationships of parasite infection with sexual and life‐history traits in wild‐caught Texas field crickets (Gryllus texensis)

1. Sex differences in immune investment and infection rate are predicted due to the divergent life histories of males and females, where females invest more toward immunity due to the fitness consequences of a reduced lifespan and males allocate less toward immunity due to increased resource investment in traits critical to sexual selection. Consequently, males are expected to fight infection less adeptly, resulting in higher parasite loads relative to females across all taxa.
2. Wild animals rarely face a single parasite within their given environment, yet nearly all studies on sex‐biased infection rates have focused on a single host–parasite relationship. Here, we investigate how simultaneous natural infections of ecto‐ and endosymbionts (i.e. both parasitic and phoretic taxa) correlate with sex biases in host immune response and reproductive investment in a field‐caught cricket, Gryllus texensis.
3. Our comprehensive analysis found no significant sex differences in two measures of immune response (melanization and nodulation), and found no strong evidence of a sex bias in the prevalence or intensity of parasitism by the three most common parasites infecting wild G. texensis field crickets (Eutrombidiidae, gregarines, and nematodes).
4. Two traits related to female fitness, egg number and egg size, showed no relation to parasitic infection; however, males having wider heads and poorer body condition were significantly more infected by eutrombidiid mites, gregarines, and nematodes.
5. Despite frequent predictions of male‐biased parasitism in the literature, our results concur with many other studies indicating that the divergent life histories of males and females alone are not sufficient to explain natural infection rates in wild insects.

     

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.     

Ecological causes of sex-biased parasitism in threespine stickleback

Males and females can differ in levels of parasitism and such differences may be mediated by the costs of sexual selection or by ecological differences between the genders. In threespine stickleback, Gasterosteus aculeatus , males exhibit paternal care and territorial nest defence and the costs of reproduction may be particularly high for males relative to females. We monitored levels of parasitism for 15 years in a population of stickleback infected by four different parasite species. Consistent with general predictions, overall parasite prevalence (total parasitism) was greater in males than in females. However, this excess did not occur for each species of parasite. Males had higher prevalence of a cestode Cyathocephalus truncatus and a trematode Bunodera sp. relative to females, while females had higher prevalence of a cestode Schistocephalus solidus and nematodes. This suggested ecological sources to differences in parasitism rather than reproductive costs and therefore we examined diet of unparasitized stickleback, predicting that differences in dietary niche would influence relative parasitism. This was partially confirmed and showed that female stomach contents had increased frequency of pelagic items, the major habitat for the primary host of S. solidus whereas males exhibited increased frequency of benthic items, the dominant habitat of C. truncatus and Bunodera. Temporal shifts in the extent and direction of differential parasitism among years between the sexes were associated with temporal shifts in dietary differences. Our results, combined with those in the literature, suggest that ecological differences between genders could be a more important component to patterns of parasitic infection in natural populations than currently appreciated.     

Influence of host weight, sex and reproductive status on helminth parasites of the wild rabbit, Oryctolagus cuniculus, in Navarra, Spain.

A study was carried out in Navarra (northern Spain) on the influence of the weight, sex and reproductive status (lactant, pregnant or lactant + pregnant females and testicular weight for males) of the wild rabbit (Oryctolagus cuniculus) on two cestodes species: Andrya cuniculi and Mosgovoyia ctenoides and four intestinal nematodes: Graphidium strigosum, Trichostrongylus retortaeformis, Nematodiroides zembrae and Dermatoxys hispaniensis. A significantly higher prevalence of A. cuniculi was detected in lactant + pregnant females compared with non-breeding females. Trichostrongylus retortaeformis and N. zembrae showed a significantly higher mean intensity in lactant and lactant + pregnant females than in non-reproductive females. Trichostrongylus retortaeformis presented a higher mean intensity in females than in males, and the mean intensity of the same parasite species was significantly lower in active and inactive males compared with lactant and lactant + pregnant females. There were no significant differences between sexes in the prevalence of helminth parasites. No significant correlation was detected between host weight and the intensity (of infection) of helminths studied. No significant differences in the prevalence and mean intensity of the two cestode species were observed in the three weight categories studied (kittens, juveniles and adults). The prevalence of G. strigosum and mean intensity of T. retortaeformis were significantly higher in older heavier animals than in juveniles.     

Sexual effects on parasite infection

Males and females differ physiologically, but they also do different things. Thus, we when we note sex differences in average rates of parasite prevalence, incidence or intensity of infection, or in clinical outcome, we may attribute such differences either to the different physiology, or to different activities, or to some combination of differences between the sexes. Hence the subject of this month's debate-to explore the question of ‘why do certain males or females have higher or lower incidence or prevalence or severity of parasitic infection?’ Don Bundy opens with a discussion of the epidemiological patterns, while Jim Alexander and Bill Stimson explore some of the physiological effects of sex and sex hormones on the host's immune response to infection.     

THE GENOMIC ARCHITECTURE OF SEXUAL DIMORPHISM IN THE DIOECIOUS PLANT SILENE LATIFOLIA

Evaluating the genetic architecture of sexual dimorphism can aid our understanding of the extent to which shared genetic control of trait variation versus sex‐specific control impacts the evolutionary dynamics of phenotypic change within each sex. We performed a QTL analysis on Silene latifolia to evaluate the contribution of sex‐specific QTL to phenotypic variation in 46 traits, whether traits involved in trade‐offs had colocalized QTL, and whether the distribution of sex‐specific loci can explain differences between the sexes in their variance/covariance matrices. We used a backcross generation derived from two artificial‐selection lines. We found that sex‐specific QTL explained a significantly greater percent of the variation in sexually dimorphic traits than loci expressed in both sexes. Genetically correlated traits often had colocalized QTL, whose signs were in the expected direction. Lastly, traits with different genetic correlations within the sexes displayed a disproportionately high number of sex‐specific QTL, and more QTL co‐occurred in males than females, suggesting greater trait integration. These results show that sex differences in QTL patterns are congruent with theory on the resolution of sexual conflict and differences based on G ‐matrix results. They also suggest that trade‐offs and trait integration are likely to affect males more than females.     

Synergistic effects of seasonal rainfall, parasites and demography on fluctuations in springbok body condition

1. Seasonality of rainfall can exert a strong influence on animal condition and on host-parasite interactions. The body condition of ruminants fluctuates seasonally in response to changes in energy requirements, foraging patterns and resource availability, and seasonal variation in parasite infections may further alter ruminant body condition. 2. This study disentangles the effects of rainfall and gastrointestinal parasite infections on springbok (Antidorcas marsupialis) body condition and determines how these factors vary among demographic groups. 3. Using data from four years and three study areas, we investigated (i) the influence of rainfall variation, demographic factors and parasite interactions on parasite prevalence or infection intensity, (ii) whether parasitism or rainfall is a more important predictor of springbok body condition and (iii) how parasitism and condition vary among study areas along a rainfall gradient. 4. We found that increased parasite intensity is associated with reduced body condition only for adult females. For all other demographic groups, body condition was significantly related to prior rainfall and not to parasitism. Rainfall lagged by two months had a positive effect on body condition. 5. Adult females showed evidence of a 'periparturient rise' in parasite intensity and had higher parasite intensity and lower body condition than adult males after parturition and during early lactation. After juveniles were weaned, adult females had lower parasite intensity than adult males. Sex differences in parasitism and condition may be due to differences between adult females and males in the seasonal timing of reproductive effort and its effects on host immunity, as well as documented sex differences in vulnerability to predation. 6. Our results highlight that parasites and the environment can synergistically affect host populations, but that these interactions might be masked by their interwoven relationships, their differential impacts on demographic groups, and the different time-scales at which they operate.     

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.     

EVOLUTION OF INCOMPATIBILITY-INDUCING MICROBES AND THEIR HOSTS

In many insect species, males infected with microbes related to Wolbachia pipientis are “incompatible” with uninfected females. Crosses between infected males and uninfected females produce significantly fewer adult progeny than the other three possible crosses. The incompatibility-inducing microbes are usually maternally transmitted. Thus, incompatibility tends to confer a reproductive advantage on infected females in polymorphic populations, allowing these infections to spread. This paper analyzes selection on parasite and host genes that affect such incompatibility systems. Selection among parasite variants does not act directly on the level of incompatibility with uninfected females. In fact, selection favors rare parasite variants that increase the production of infected progeny by infected mothers, even if these variants reduce incompatibility with uninfected females. However, productivity-reducing parasites that cause partial incompatibility with hosts harboring alternative variants can be favored once they become sufficiently abundant locally. Thus, they may spread spatially by a process analogous to the spread of underdominant chromosome rearrangements. The dynamics of modifier alleles in the host are more difficult to predict, because such alleles will occur in both infected and uninfected individuals. Nevertheless, the relative fecundity of infected females compared to uninfected females, the efficiency of maternal transmission and the mutual compatibility of infected individuals all tend to increase under within-population selection on both host and parasite genes. In addition, selection on host genes favors increased compatibility between infected males and uninfected females. Although vertical transmission tends to harmonize host and parasite evolution, competition among parasite variants will tend to maintain incompatibility.     

The effect of parasites on sex differences in selection

The life history strategies of males and females are often divergent, creating the potential for sex differences in selection. Deleterious mutations may be subject to stronger selection in males, owing to sexual selection, which can improve the mean fitness of females and reduce mutation load in sexual populations. However, sex differences in selection might also maintain sexually antagonistic genetic variation, creating a sexual conflict load. The overall impact of separate sexes on fitness is unclear, but the net effect is likely to be positive when there is a large sex difference in selection against deleterious mutations. Parasites can also have sex-specific effects on fitness, and there is evidence that parasites can intensify the fitness consequences of deleterious mutations. Using lines that accumulated mutations for over 60 generations, we studied the effect of the pathogenic bacterium Pseudomonas aeruginosa on sex differences in selection in the fruit fly Drosophila melanogaster. Pseudomonas infection increased the sex difference in selection, but may also have weakened the intersexual correlation for fitness. Our results suggest that parasites may increase the benefits of sexual selection.     

Patterns of infection by intestinal parasites in sympatric howler monkey (Alouatta palliata) and spider monkey (Ateles geoffroyi) populations in a tropical dry forest in Costa Rica

In primate populations, endoparasite species richness and prevalence are associated with host traits such as reproductive and social status, age, sex, host population density, and environmental factors such as humidity. We analyzed the species richness and prevalence of intestinal parasites in two sympatric primate populations, one of Alouatta palliata and one of Ateles geoffroyi, found in a tropical dry forest in Costa Rica. We identified three species of intestinal parasites (Controrchis sp., Trypanoxyuris sp., and Strongyloides sp.) in these two primate species. We did not find any differences in species richness between the primate species. However, the prevalences of Controrchis sp. and Trypanoxyuris sp. were higher in Alouatta palliata. Similarly, males and lactating females of Alouatta palliata showed higher Controrchis sp. prevalences. We did not observe any differences in parasite richness and prevalence between seasons. Infectious diseases in endangered primate populations must be considered in conservation strategies, especially when defining protected areas.     

Partitioning of resources: the evolutionary genetics of sexual conflict over resource acquisition and allocation

Fitness depends on both the resources that individuals acquire and the allocation of those resources to traits that influence survival and reproduction. Optimal resource allocation differs between females and males as a consequence of their fundamentally different reproductive strategies. However, because most traits have a common genetic basis between the sexes, conflicting selection between the sexes over resource allocation can constrain the evolution of optimal allocation within each sex, and generate trade‐offs for fitness between them (i.e. ‘sexual antagonism’ or ‘intralocus sexual conflict’). The theory of resource acquisition and allocation provides an influential framework for linking genetic variation in acquisition and allocation to empirical evidence of trade‐offs between distinct life‐history traits. However, these models have not considered the emergence of trade‐offs within the context of sexual dimorphism, where they are expected to be particularly common. Here, we extend acquisition–allocation theory and develop a quantitative genetic framework for predicting genetically based trade‐offs between life‐history traits within sexes and between female and male fitness. Our models demonstrate that empirically measurable evidence of sexually antagonistic fitness variation should depend upon three interacting factors that may vary between populations: (1) the genetic variances and between‐sex covariances for resource acquisition and allocation traits, (2) condition‐dependent expression of resource allocation traits and (3) sex differences in selection on the allocation of resource to different fitness components.     

Variations in the parasite fauna of the Patagonian toothfish (Dissostichus eleginoides Smitt, 1898), with length, season, and depth of habitat around the Falkland Islands

The parasite fauna of Dissostichus eleginoides was examined from locations around the Falkland Islands. In total, of 11,362 individual parasites of 27 taxa were recovered from 105 fish. Two species, Ceratomyxa dissostichi and Sphaerospora dissostichi, represent new host records. The nematode Ascarophis nototheniae and the larval acanothocephalan Corynosoma bullosum were found to be new locality records and add to the knowledge of the biogeography and host specificity of parasites on the Patagonian Shelf. There were no significant differences in the mean abundance and prevalence of parasites recovered between sexes. Therefore, sex was not considered in further analysis and the data were pooled. Cysts of unknown etiology (CUE), the monogenean Neopavlovskioides georgianus, the larval acanthocephalan Corynosoma bullosum, and the digenean Neolepidapedon magnatestis had significant positive correlations with increasing host length. The larval Trypanorhynch cestode Grillotia erinaceus and the digenean Elytrophalloides oatesi showed significant negative correlations with increasing host length. CUEs, N. georgianus, the digenean Gonocerca physidis and E. oatesi showed statistically significant prevalence between summer, winter, and spring. The effect of depth on parasite communities was also examined, initially using a linear discriminant function analysis. The prevalence of individual parasites was then compared between depth strata using the chi-square test. The parasite communities on the shelf and deep water (> 1,000 m) were found to be different, whereas those caught at intermediate depths on the shelf slope were found to have parasite communities that were intermediate, containing a mixture of shelf and deeper-water parasites. The causes of the variations in parasite faunas in association with these intrinsic and extrinsic factors are discussed.     

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.