Interspecific differences in hematozoan infection in Sonoran desert Aimophila sparrows

Numerous studies have identified factors that control avian hematozoan infections, but the mechanisms that account for host differences in parasitemia remain largely speculative. To address this issue, we compared the prevalence of these parasites in stained blood smears from four conspecific Sonoran desert Aimophila sparrow species sampled during their breeding season: rufous-winged (Aimophila carpalis; RWSP), rufous-crowned (Aimophila ruficeps; RCSP), Cassin's (Aimophila cassinii, CASP), and Botteri's (Aimophila botterii; BOSP) sparrows. Blood smears contained Haemoproteus fringillae (RWSP), Trypanosoma everetti (RWSP, RCSP, BOSP), Trypanosoma avium (CASP), and microfilariae (all species). Most (92.5%) RWSP (n=40) were infected with Haemoproteus, but this parasite was not detected in RCSP (n=20) or BOSP (n=20) and was found only in one (2.5%) CASP (n=40). Trypanosoma spp. and microfilariae were detected in all species, but prevalence differed between these four sparrow species. Species differences in parasite prevalence were not due to difference in sex, age, adult body mass, incubation period, breeding habitat, or plumage colorfulness. However, differences in Haemoproteus sp. prevalence correlated with preferred nesting height, as RWSP generally nest above ground, whereas the other species nest on or close to the ground. Elevated H. fringillae prevalence in breeding-condition RWSP presumably does not result from a seasonal relapse associated with breeding or require new infection because 1) this prevalence did not differ in males sampled during and outside (n=21) the breeding season, and 2) all male RWSP (n=25) that we held in captivity and shielded from new infections and influence of natural photoperiod for 1 yr had viable blood H. fringillae gametocytes. H. fringillae prevalence in fall-sampled hatch-year male RWSP (n=11) was 63.6%, demonstrating that this parasite can be transmitted on the breeding grounds and during the first months of life. T. everetti prevalence in RWSP was lower in winter than in summer and also in long-term captive than in free-ranging adults. Presence of this parasite in the blood of breeding males may depend on recrudescence of existing infections or new infections.     

Sex-biased,but not plumage color-based,prevalence of haemosporidian parasites in free-range chickens

Previous studies found a relationship between blood parasite infection and bird gender, with higher prevalence in males. Some studies also found a relationship between host plumage color and parasitic infection, while others did not. Here, we investigated the blood parasite prevalence in correlation with sex and plumage color in free-range chickens (Gallus gallus domesticus) in China. We analyzed a total of 297 blood samples, out of which 234 chickens tested positive for haemosporidian parasites, with 78.5% parasite prevalence. Out of 139 males, 118 tested positive with 84.8% parasite prevalence while 116 of 158 female samples tested positive (73.4%). Leucocytotozoon was the most frequent genus isolated (193 infected individuals /234 birds), followed by Plasmodium (41 infected individuals/234 birds), with no Haemoproteus parasites being detected. There were no significant differences in the body parameters and chicken color plumages with regards to the infection status. Our study indicated that blood parasite infection was significantly different between male and female chickens, with infection prevalent in males.     

Mate Choice in Experimentally Parasitized Rock Doves: Lousy Males Lose

A recent model by Hamilton and Zuk (1982) suggests that exaggeratedsecondary sexual traits facilitate mate choice for genetic resistanceto parasites. The model predicts that individuals discriminateagainst parasitized mates by scrutinizing traits indicativeof parasite load. In the case of birds and their feather-feedinglice, for example, individuals might avoid parasitized matesbydetecting reduced plumage brightness, reduced courtship display,or increased grooming. I conducted a series of mate choice trialsin which female Rock Doves (Columba livia) were allowed to choosebetween "clean" males without lice and "lousy" males with experimentallyincreased loads. Clean males displayed significantly more oftenthan lousy males and females demonstrated a significant preferencefor clean males. Lousy males were subject to plumage damage;however, none of the damage was externally visible, and thetime spent grooming by clean and lousy males did not differsignificantly. Female louse loads, which were also manipulated,were not significantly related to female mating preferences.These results are consistent with the Hamilton-Zuk model. Theyare also consistent with a model of sexual selection for theavoidance of parasite transmission, which is discussed. Thegeneral relevance of lice and other ectoparasites to modelsof parasite-mediated sexual selection is reviewed.     

Blood parasites of Nearctic-Neotropical migrant passerine birds during spring trans-Gulf migration: impact on host body condition

To test the hypothesis that migrants infected with blood parasites arrive on the northern coast of the Gulf of Mexico in poorer condition than uninfected birds, we examined 1705 migrant passerine birds representing 54 species of 11 families from 2 Gulf Coast sites for blood parasites. Three hundred and sixty (21.1%) were infected with 1 or more species of 4 genera of blood parasites. The prevalence of parasites was as follows: Haemoproteus spp. (11.7%), Plasmodium spp. (6.7%), Leucocytozoon spp. (1.3%), and Trypanosoma spp. (1.2%). Both prevalence and density of Haemoproteus spp. infection varied among species. We found no relationship of gender or age with the prevalence of Haemoproteus spp. infection or Plasmodium spp. infection, with the exception of the orchard oriole (Icterus spurius) for which older birds were more likely to be infected with Haemoproteus spp. than younger birds. We also found that scarlet tanagers and summer tanagers infected with species of Haemoproteus have lower fat scores than uninfected individuals and that rose-breasted grosbeaks and Baltimore orioles infected with Haemoproteus spp. have a smaller mean body mass than uninfected individuals. Blood parasites do seem to pose a physiological cost for Neotropical migrant passerines and may be important components of the ecology of these species.     

Age-specific patterns of infection with haemosporidians and trypanosomes in a warbler: implications for sexual selection

Although the selective loss of individuals susceptible to disease can favor the evolution of female preference for older males, the interrelationship between age, infection, longevity, and mating success remains poorly characterized in natural populations. In a longitudinal study of 61 male common yellowthroats (Geothlypis trichas), we found that the probability of infection with hematozoa increased as males aged from 1 to 5 years. Despite a significant, negative association between infection and longevity that partially masked age-effects, the odds that a male was infected with Trypanosoma, Plasmodium, or Leucocytozoon increased 71–212% per year. Nearly 75% of males in their first breeding season were either uninfected or infected with only a single parasite, while 50% of older males were infected with at least two parasites and 16% were infected with all three. No males escaped infection after their second breeding season. Older males were also more likely to sire extra-pair young (EPY) and, as a consequence, infection with multiple parasites was associated with a fourfold increase in the odds of producing EPY. Unlike younger males, 80% of the oldest males had a history of either surviving chronic infection or recovering. Combined with previous work showing higher diversity at the major histocompatibility complex among older males, our results suggest that the song and plumage traits that signal male age in common yellowthroats also, perforce, signal resistance to parasites. By preferring older males, females may obtain good genes for disease resistance even in the absence of any effect of infection on male ornamentation.     

Association between haematozoan infections and reproduction in the Pied Flycatcher

1. Parasites may affect breeding success of their host since they compete for the same resources as their hosts. Reproduction may also increase the susceptibility of a host to parasite infections owing to lowered resistance to parasites during breeding.
2. We studied the association between breeding performance and haematozoan parasite infection in the Pied Flycatcher ( Ficedula hypoleuca ) by using both natural data on reproduction and data from clutch size manipulations.
3. The most frequent blood parasites of the Pied Flycatcher in central Finland were Haemoproteus pallidus , Haemoproteus balmorali and Trypanosoma avium complex.
4. We did not find evidence that these haematozoan parasites have any debilitating effects on either reproduction or survival. The variation in reproductive effort did not seem to influence susceptibility to new blood parasite infections.
5. The intensity of Haemoproteus balmorali tended to increase in infected males as the brood size was artificially enlarged. Also, in females intensity of H. pallidus infection tended to increase with the level of clutch size manipulation. Thus, increased reproductive effort seems to debilitate the ability of Pied Flycatcher to control chronic infections.
6. Individuals with enlarged clutches/broods increased their reproductive effort at the expense of defence towards parasites. The cost of current reproduction may then be at least partly mediated by haematozoan infections.     

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.     

Haematozoa infections in a Great Tit Parus major population in Central Portugal: relationships with breeding effort and health

Blood parasites may act as modulators of their hosts' ecology, life histories and fitness. We studied the prevalence of Plasmodium sp., Haemoproteus sp. and Leucocytozoon sp. and their effects on morphological, biochemical and haematological variables and on breeding effort of Great Tits Parus major . Total prevalence (percentage of individuals infected by any parasite) ranged from 7.7% to 61.1%. There was an overall positive association in prevalence between the three haematozoan parasites. No effect of sex or age on infection status was observed. Negative impacts of infection on physiological condition depended largely on year and/or season and included effects on body condition index, plasma protein and haemoglobin index. There were also indications that parasite infection increased immune response and stress levels and activated antioxidant defence mechanisms. Males with higher fledging success had a higher probability of Haemoproteus infection, and females laying heavier eggs had a higher probability of Plasmodium infection. However, clutch size was negatively associated with the probability of infection by Leucocytozoon and Haemoproteus . Surprisingly, males raising second broods had a lower prevalence of both Haemoproteus and Leucocytozoon . Only 5.7% of first-brood nestlings were infected, but those in infected nestboxes had a lower heterophil/lymphocyte ratio. This study confirms the pathogenicity of blood parasites to the host by demonstrating negative effects of infection on both physiology and breeding performance.     

Parasites make male pipefish careless

Parasite-mediated sexual selection is expected to favour the avoidance of matings with infected individuals. However, the extent to which the costs and benefits of discriminating against parasitized mates trade off may depend upon numerous factors. I investigated the effects of sex and infection status on choosiness in sex-role reversed deep-snouted pipefish (Syngnathus typhle L.) that were either artificially infected with the trematode parasite Cryptocotyle sp. or sham-infected. Sham-infected males were significantly more likely to associate with a sham-infected female rather than with a Cryptocotyle-infected female. Infected males failed to discriminate against infected potential partners. Males were choosier the larger they were relative to the females available for choice. Females were not discriminatory, regardless of their infection status. Given an inverse relation between female fecundity and parasite load, choosy unparasitized males may gain enhanced reproductive success from their choice decisions. In contrast, more heavily infected wild-caught males gave birth to slightly fewer, but not smaller offspring than did uninfected or lightly infected males, suggesting only a low direct premium on choosy females. The detrimental effects of parasitism on male choosiness, and the lack of female discrimination against infected males likely have profound repercussions on the strength of sexual selection acting on the two sexes and on the dynamics of host-parasite interactions in this system.     

Altered behavior of the snail Biomphalaria glabrata as a result of infection with Schistosoma mansoni

In this comparative behavioral study, the effect of infection with Schistosoma mansoni on its snail intermediate host Biomphalaria glabrata was investigated. Three groups of snails were compared for their activity: (1) uninfected, (2) infected with male parasites, and (3) infected with female parasites. In solitary movement trials, uninfected snails traveled greater distances at faster rates, explored more surface area, and had shorter rest periods than snails infected with either male or female schistosomes. In Y-maze experiments designed to determine attraction, the uninfected snails more often and more quickly moved toward other snails than the infected individuals. Snails from all 3 groups were more attracted to infected individuals than to uninfected ones. There was no difference in attraction toward snails infected with male or female parasites. These experiments provide evidence that behavioral alterations as a result of infection may lead to aggregation of infected snails in the field. We propose that such an effect may result in enhanced parasite transmission.     

Parasites reduce attractiveness and reproductive success in male grain beetles

Sexual characters may reveal the quality of a potential mate, including the mate's level of infection with parasites. Females that prefer males with low levels of infection or no infection may benefit in several ways. Direct benefits may include avoidance of infection, acquistition of larger nuptial gifts or enhancement in fecundity due to differences in male fertility. Females may also benefit indirectly by producing offspring that are more resistant to infections. We measured female preference for odours produced by male grain beetles, Tenebrio molitor, that were either infected by a tapeworm, Hymenolepis diminuta, or uninfected. This parasite is not transmitted directly between conspecifics. Females were attracted to odours of all males, but they were less attracted to those from parasitized males. To the contrary, females were preferentially attracted to infected females. Males did not show any biased attraction to odours from infected and uninfected male beetles. Females that mated with highly infected males produced fewer offspring than females mated to uninfected males, indicating parasitic infection inflicts multiple costs to males. These results are consistent with models of parasite-mediated sexual selection. Copyright 2000 The Association for the Study of Animal Behaviour.     

Health impact of blood parasites in breeding great tits

Hypotheses of hemoparasite-mediated sexual selection and reproductive costs rely on the assumption that avian blood parasite infections are harmful to their hosts. To test the validity of this assumption, we examined the health impact of Haemoproteus blood parasites on their great tit (Parus major) host. We hypothesised that if blood parasites impose any serious health impact on their avian hosts, then infected individuals must differ from uninfected ones in respect to hemato-serological general health and immune parameters. A 3-year study of two great tit populations, breeding in contrasting (urban and rural) habitats in south-east Estonia, revealed that Haemoproteus blood parasites affected the health state of their avian hosts. Infected individuals had elevated lymphocyte hemoconcentration and plasma gamma-globulin levels, indicating that both cell-mediated and humoral immune response mechanisms are involved in host defence. The effect of parasites on cell-mediated immunity was both age- and sex-specific, as infection status affected peripheral blood lymphocyte counts only in males, and among these, the magnitude of response was greater in old individuals than yearlings. Heterophile hemoconcentration and plasma albumin levels were not affected by infection status, suggesting that blood stages of Haemoproteus infection do not cause a severe inflammatory response. Parasitism was not related to hematocrit values, indicating that Haemoproteus infection does not cause anemia. In two years, infected individuals were heavier than uninfected ones in the urban but not in the rural study area. This suggests, that under certain circumstances (possibly related to reproductive tactics), breeding great tits may avoid losing body mass in order to save resources for an anti-parasite immune response. Received: 16 February 1998 / Accepted: 22 May 1998     

Prevalence of blood parasites in European passeriform birds

Variation in the prevalence of blood parasites among species of birds has been used to test hypotheses about the effects of sexual selection and parental investment on disease resistance, and how vector abundance influences infection. However, the factors causing this variation are still poorly understood. We assessed the statistical effects of biogeographic, plumage-related and life-history traits on the prevalence of the blood parasites Plasmodium, Haemoproteus, Leucocytozoon and Trypanosoma in European passerine birds. Most of the variation in parasite prevalence occurred at low taxonomic levels. Brighter male plumage and greater host body mass were associated with higher prevalence, explaining 32% of the total variation. Male plumage brightness remained a significant factor when we controlled for phylogenetic effects. These relationships were driven primarily by simuliid-transmitted parasites (Leucocytozoon, Trypanosoma), which were more frequent in species with northern distributions. Host species with greater maximum longevity and shorter nestling periods had higher prevalences of Plasmodium; however, the effect was not stable after controlling for phylogeny using pairwise contrasts. Coevolution between hosts and parasites appears to create temporal and spatial variation that disconnects haematozoan prevalence from evolutionarily conservative life-history traits while creating some positive associations with traits that are phylogenetically labile. Clearly, ecologists should be cautious in relating patterns of variation in haematozoan prevalence to particular host traits.     

Haemosporidian parasites depress breeding success and plumage coloration in female barn swallows Hirundo rustica

Parasites are major effectors of natural selection and also play a role in sexual selection processes. Haemosporidian blood parasites are common in vertebrates and have been shown to vary in their effects depending on both the parasite and host species, on the host trait investigated as well as on host condition and stage of infection. Here we investigated infection of adult barn swallows Hirundo rustica by Plasmodium, Leucocytozoon and Haemoproteus species during the chronic stage of infection and the consequences for host fitness traits. Prevalence was higher than 10% only for Plasmodium. Chronic stage infection by Plasmodium was associated with reduced female breeding success, but did not affect breeding dates. Infection did not affect the expression of male secondary sexual traits (tail length and melanin‐based plumage coloration), but was associated with paler coloration of females. Finally, we found a negative effect of infection by Plasmodium on feather growth rate in older but not in yearling individuals. Because feathers are moulted during wintering in sub‐Saharan Africa where infection of barn swallows by Plasmodium occurs, our results suggest that male secondary sexual traits have little potential to reveal acute‐stage infection whereas plumage coloration of females may advertise their infection status. In addition, these results suggest that infection by Plasmodium can influence the course of plumage moult. Thus, our results add to the observations of negative effects of haemosporidian infection on fitness traits in birds and provides evidence that these effects can vary among traits and in relation to age and sex.     

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.     

Seasonal and age-related changes in blood parasite prevalence in Dark-eyed Juncos (Junco hyemalis, Aves, Passeriformes)

We determined seasonal changes in blood parasite infections in a free-living population of Dark-eyed Juncos (Junco hyemalis) breeding in interior Alaska (65 degrees N; 148 degrees W). The common parasites found in blood smears were Leucocytozoon fringillinarum (56%), Trypanosoma avium (33%), and Haemoproteus fringillae (9%). In males, parasite prevalences were relatively high at arrival on breeding grounds and increased during the breeding season. Intensity of infection with Leucocytozoon also increased between spring and summer, and then decreased at the time of migration (September). This decrease did not occur in adult females. Elevated prevalences during the breeding season probably reflected the addition of new cases via vector activity to positive status resulting from spring relapse. We observed neither an association between parasite species nor a consistent relationship between parasite intensity and body condition. To further study relationships between reproductive system activity and parasite infections, we compared prevalences in adult males that were undergoing their first cycle of gonadal development and regression (males in their second calendar year, or SY) with those of older males (males in their third or more calendar year, i.e., after-second-year males or ASY). Circulating testosterone concentrations declined in both groups between arrival on breeding grounds (end of April-early May) and the end of the reproductive period (July), and they were higher in May in ASY than in SY males. At the peak of the breeding season (June), ASY males also had a higher parasite prevalence than SY males. This difference may have resulted from immunosuppressive effects of gonadal hormones and/or from behavioral differences between SY and ASY males such that older males were exposed to more insect vectors than younger males. .     

Testosterone levels and gular pouch coloration in courting magnificent frigatebird (Fregata magnificens): variation with age-class, visited status and blood parasite infection

Male magnificent frigatebirds (Fregata magnificens) possess a seasonally expressed skin ornament, namely the red and inflatable gular pouch, and are, therefore, a convenient model for the study of some theories related to the evolution of possible testosterone-dependent sexual skin coloration. Here we report the findings of a study performed over four consecutive mating seasons in the Mexican national park Isla Isabel. We investigated differences in testosterone level and gular pouch coloration in courting males in relation to the categories: age-class, visited status and blood parasite infection. Gular pouch color saturation increased with age-class. Investigated frigatebirds were infected only with Haemoproteus iwa (Haemosporida, Haemoproteidae), with an overall prevalence infection of 15.5%. Prevalence of the infection increased with birds' age-class. Testosterone levels were significantly higher in infected males, who also had lighter colored gular pouches. In non-infected males, those visited by a female had higher testosterone levels than non-visited males. Gular pouch lightness and redness were negatively correlated but only redness in non-visited non-infected males was positively correlated with testosterone levels. Gular pouch saturation in visited and infected males was positively correlated with body mass, which also increased with age-class. Mated males had lower testosterone levels and lighter, less red and saturated gular pouch coloration than courting males. In summary, we found that coloration of the male skin ornament could reflect age-class (saturation), parasite infection (lightness) and mated status (all), together with indications of condition and testosterone dependency of ornament expression.     

Parasites and Mate Choice in Gray Treefrogs, Hyla versicolor

A fundamental assumption of the Hamilton and Zuk (1982) modelof sexual selection is that parasite-free males should producemate attracting displays that are substantially more vigorousand effective than those of their parasitized counterparts.Further, the model predicts that parasite-free males shouldbe preferred as mating partners by females and, as a consequence,should have higher reproductive success than their parasitizedcompetitors. Gray treefrogs (Hyla versicolor) constitute anideal species for testing both assumptions and predictions ofthe Hamilton-Zuk model in that: (i) mate attraction by malesrequires the production of energetically costly calls and (ii)males of this species have been shown to harbor a wide rangeof helminth parasites. The present paper summarizes resultsof analyses of calling and mating behavior by male gray treefrogsin relation to their parasite infection levels. In general,these analyses revealed no consistent relationship between thenumber and kinds of parasites harbored by males and either theduration or duty-cycle (a direct measure of energetic cost)of their calls. Furthermore, males found in amplexus (i.e.,males actually selected as mating partners by females) showeda slightly higher prevalence of parasite infection (but a slightlylower intensity of infection) than did a comparable sample ofunmated males. In sum, the present study failed to support themajor within-species prediction of the Hamilton-Zuk model ofsexual selection and also calls into question one of the fundamentalassumptions of the model.     

Effects of tapeworm infection on male reproductive success and mating vigor in the red flour beetle,Tribolium castaneum

Parasites may exert negative effects on host survivorship and reproductive success. The effects of parasites on female host fitness have been well documented; however, the effects of parasites on the reproductive success of male hosts and particularly the underlying mechanisms that alter male fitness are not well understood. Previous studies demonstrated that infection by rat tapeworm (Hymenolepis diminuta) reduced the fitness of male red flour beetles (Tribolium castaneum) in an environment of female mate choice and strong male-male competition. The present study determined the role of female mate choice and male insemination capacity on observed fitness reduction of male beetles by the tapeworm parasites. We found that infected males showed reduced mating vigor and consequently inseminated fewer females than did uninfected males. Specifically, tapeworm infection reduced the number of offspring sired by a male by 14-22% even when male-male competition and female mate choice were absent. Further, the insemination capacity of males diminished by 30% because of infection. Female beetles did not discriminate against infected males in precopulatory mate choice experiments. Copulatory courtship, a determinant of postcopulatory female choice, was not significantly different between infected and uninfected males. Hence, we concluded that female beetles did not show either pre- or postcopulatory choice against tapeworm-infected males. Therefore, tapeworm-induced reduction in the reproductive success of male beetles possibly results from altered reproductive biology, such as lower mating vigor and decreased sperm quantity or quality.     

Parasites and sexual selection: a macroevolutionary perspective.

The Hamilton-Zuk hypothesis postulates a causal link between parasitism and the evolution of epigamic traits by intersexual selection. Oversimplified assumptions about basic parasite biology, ambiguous formulation of the hypothesis, and poor communication between ethologists and parasitologists have hampered its testing. The hypothesis is supported at the microevolutionary level if females show significant preference for lightly or uninfected males, if intensity of infection reflects host resistance to parasites that depress host fitness by causing disease, and if intensity of infection is related to the degree of epigamic development. It must be shown that particular parasites cause disease, that the host population is polymorphic for resistance to infection by those species, and that female hosts are capable of distinguishing male hosts with low parasite loads due to heritable aspects of host resistance from males that are uninfected due to chance. The macroevolutionary prediction of the hypothesis, that species displaying strongly developed epigamic characters should host "more parasites" than species with weakly developed epigamic traits, contradicts the microevolutionary dynamic of the hypothesis, and is too ambiguous. We propose a macroevolutionary prediction based on understanding the evolutionary origin of epigamic traits and the evolutionary origin of each host-parasite association. Associations originating in the ancestor in which the epigamic trait appeared corroborate the hypothesis most strongly; those originating prior to the evolution of the epigamic trait corroborate it weakly; those beginning after the origin of the epigamic trait could not have been involved in the origin and spread of the epigamic trait.