MHC,parasites and antler development in red deer: no support for the Hamilton & Zuk hypothesis

The Hamilton‐Zuk hypothesis proposes that the genetic benefits of preferences for elaborated secondary sexual traits have their origins in the arms race between hosts and parasites, which maintains genetic variance in parasite resistance. Infection, in turn, can be reflected in the expression of costly sexual ornaments. However, the link between immune genes, infection and the expression of secondary sexual traits has rarely been investigated. Here, we explored whether the presence and identity of functional variants (supertypes) of the highly polymorphic major histocompatibility complex (MHC), which is responsible for the recognition of parasites, predict the load of lung and gut parasites and antler development in the red deer (Cervus elaphus). While we found MHC supertypes to be associated with infection by a number of parasite species, including debilitating lung nematodes, we did not find support for the Hamilton‐Zuk hypothesis. On the contrary, we found that lung nematode load was positively associated with antler development. We also found that the supertypes that were associated with resistance to certain parasites at the same time cause susceptibility to others. Such trade‐offs may undermine the potential genetic benefits of mate choice for resistant partners.     

Parasite load and brightness in lizards: an interspecific test of the Hamilton and Zuk hypothesis

Hamilton & Zuk (1982) hypothesized a positive correlation between a species' sexual showiness and its level of parasitic infection. We tested the hypothesis in 26 species of lizards, members of a class of vertebrates never before used to test the model. The prevalence of parasites was determined using published lists of parasites found in wild lizard populations. An index of showiness (brightness) was derived by scoring photographs of lizards in natural settings. Contrary to expectations of Hamilton & Zuk (1982), we found an inverse correlation between a lizard species' brightness and parasite prevalence. No correlation was found between a species' brightness and the number of parasite genera, species, or percentage of individual infecting parasite taxa. These results are discussed in relation to other interspecific tests of the hypothesis.     

MHC VARIATION IS RELATED TO A SEXUALLY SELECTED ORNAMENT,SURVIVAL, AND PARASITE RESISTANCE IN COMMON YELLOWTHROATS

Hamilton and Zuk proposed that females choose mates based on ornaments whose expression is dependent on their genetically based resistance to parasites. The major histocompatibility complex (MHC) plays an important role in pathogen recognition and is a good candidate for testing the relationships between immune genes and both ornament expression and parasite resistance. We tested the hypothesis that female common yellowthroats prefer to mate with more ornamented males, because it is a signal of their MHC‐based resistance to parasites and likelihood of survival. In this species, females prefer males that have larger black facial masks as extrapair mates. Using pyrosequencing, we found that mask size was positively related to the number of different MHC class II alleles, as predicted if greater variation at the MHC allows for the recognition of a greater variety of pathogens. Furthermore, males with more MHC class II alleles had greater apparent survival, and resistance to malaria infection was associated with the presence of a particular MHC class II allele. Thus, extrapair mating may provide female warblers with immunity genes that are related to parasite resistance, survival, and the expression of a male ornament, consistent with good genes models of sexual selection.     

Sexual selection and the role of parasites

Six years ago, William Hamilton and Marlene Zuk(1) proposed a novel and - on the face of it - bizarre explanation for the evolution of secondary sexual characters. Contrary to most theories of sexual selection through female choice(2), Hamilton and Zuk suggested that the bright colours and elaborate ornaments of many animal species have a utilitarian function: they allow females to assess a potential mate's ability to resist parasites. Recently, several studies have begun to test the hypothesis directly, and the idea has been discussed at two meetings(3,4). Here I review the work to date, and discuss the difficulties involved in gathering and interpreting the evidence still required.     

Parasites and Sexual Selection in Birds of Paradise

We studied blood parasite infections in relation to aspectsof sexual selection and mate choice in 10 species of birds ofparadise. Across species there was a significant, positive correlationbetween relative parasite intensity and showiness in males.Parasite infections also correlated across species with thedegree of sexual dimorphism and varied with mating systems.Promiscuous species were showier and had significantly higherparasite prevalences than monogamous species. Within one species,Lawes' Parotia (Parotia lawesii), parasite intensity was negativelycorrelated with all phenotypic traits examined, a pattern significantlydifferent than random. The mating success of males with lowparasite intensities varied, but males with high intensitiesdid not mate. Sampling of individual males on repeated occasionsrevealed large temporal differences in parasite counts whichspanned the range believed to affect behavior and mating success.Whereas the interspecific correlations support one predictionof the Hamilton and Zuk hypothesis on parasites and sexual selection,the intraspecific data are equivocal with respect to a secondprediction of this hypothesis. Parasites appear to influencethe behavior of Lawes' Parotia, but alternative explanationsto that of Hamilton and Zuk for this effect are equally plausibleand there is no evidence of a link between female choice andthe traits in males indicative of parasite loads. We suggestthat female Lawes' Parotia may be avoiding highly infected malesrather than actively choosing parasite-resistant males.     

Sexual dichromatism and parasitism in british and irish freshwater fish

Hamilton & Zuk (1982) predicted that there should be a relationship between a species' parasite load and its sexual showiness. The relationship between the number of parasite genera reported from a fish family and its sexual dichromatism was examined in British and Irish freshwater fish. Eleven other ecological and life history variables which may also cause sexual dichromatism were also examined. The changes in appearance that take place are always more marked in males and occur only during the breeding season. This strongly implicates sexual selection as an important selective determinant. There was a significant positive correlation between a fish family's sexual dichromatism and the number of parasite genera reported from it. This remained significant when the influences of near-significantly correlated ecological and life history variables were removed. Using more detailed published parasite data on six species, there was also a significant correlation between the mean number of parasite species per host individual and host sexual dichromatism. These results support Hamilton & Zuk's bright, parasiteresistant male and choosy female hypothesis.     

Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus).

The Hamilton and Zuk hypothesis on haemoparasite-mediated sexual selection and certain studies of reproductive costs are based on the assumption that avian blood parasite infections are detrimental to their hosts. However, there is no experimental evidence demonstrating harmful effects of blood parasites on fitness in wild populations, it even having been suggested that they may be non-pathogenic. Only an experimental manipulation of natural blood parasite loads may reveal their harmful effects. In this field experiment we reduced through medication the intensity of infection by Haemoproteus majoris and the prevalence of infection by Leucocytoazoon majoris in blue tits (Parus caeruleus), and demonstrated detrimental effects of natural levels of infection by these common parasite species on host reproductive success and condition. The fact that some of the costs of infection were paid by offspring indicates that blood parasites reduce parental working capacity while feeding nestlings. Medicated females may be able to devote more resources to parental care through being released from the drain imposed upon them by parasites and/or through a reduced allocation to an immune response. Therefore, this work adds support to previous findings relating hosts' life-history traits and haematozoan infections.     

Parasitism and Heterozygosity Influence the Secondary Sexual Characters of the European Minnow,Phoxinus phoxinus (L.) (Cyprinidae)

The Hamilton & Zuk hypothesis (Hamilton & Zuk 1982) was tested in the European minnow, Phoxinus phoxinus (L.), where the male breeding characters include tubercles, which are horny growths on the skin of the head, and a bright red abdomen. Two trematode parasite species, neither directly transmitted, were present: Diplostomum phoxini in the brains of 100% of the fish and Macrolecithus papilliger in the guts of 44%. The heterozygosity of the fish at 11 loci was determined. The number of M. papilliger was negatively related to redness and positively related to the size of tubercles. The number of D. phoxini was not related to redness but was also positively related to the size of tubercles. Heterozygosity was positively related to redness and negatively related to the size of tubercles. This is the first report of such inverse relationships with heterozygosity. The number of tubercles was positively related to the size and condition of a fish. We suggest that males unable to develop exaggerated characters to display to females, e.g. a bright red abdomen, have the alternative strategy of emphasizing weapons for use in male-male competition. This effect could explain other reported positive correlations between parasite burden and sexual display.     

The evolution of immune defense and song complexity in birds

Abstract There are three main hypotheses that explain how the evolution of parasite virulence could be linked to the evolution of secondary sexual traits, such as bird song. First, as Hamilton and Zuk proposed a role for parasites in sexual selection, female preference for healthy males in heavily parasitized species may result in extravagant trait expression. Second, a reverse causal mechanism may act, if sexual selection affects the coevolutionary dynamics of host-parasite interactions per se by selecting for increased virulence. Third, the immuno-suppressive effects of ornamentation by testosterone or limited resources may lead to increased susceptibility to parasites in species with elaborate songs. Assuming a coevolutionary relationship between parasite virulence and host investment in immune defense we used measures of immune function and song complexity to test these hypotheses in a comparative study of passerine birds. Under the first two hypotheses we predicted avian song complexity to be positively related to immune defense among species, whereas this relationship was expected to be negative if immuno-suppression was at work. We found that adult T-cell mediated immune response and the relative size of the bursa of Fabricius were independently positively correlated with a measure of song complexity, even when potentially confounding variables were held constant. Nestling T-cell response was not related to song complexity, probably reflecting age-dependent selective pressures on host immune defense. Our results are consistent with the hypotheses that predict a positive relationship between song complexity and immune function, thus indicating a role for parasites in sexual selection. Different components of the immune system may have been independently involved in this process.     

EFFECTS OF A HAEMATOPHAGOUS MITE ON THE BARN SWALLOW (HIRUNDO RUSTICA): A TEST OF THE HAMILTON AND ZUK HYPOTHESIS

I tested three assumptions of the Hamilton and Zuk hypothesis (1982), which suggests that the extravagant male plumage of many bird species allows females to choose mates that are resistant to the parasites exploiting the host population at a given time. By choosing such males as mates, females will rear offspring carrying the genes for resistance. I tested three necessary conditions for the Hamilton and Zuk model: (1) whether parasites affect the fitness of their hosts; (2) whether there is heritable variation in parasite resistance, and (3) whether the expression of the sexual ornament varies with parasite burden. The haematophagous mite Ornithonyssus bursa (Macronyssidae, Gamasida) sucks blood from their Barn Swallow (Hirundo rustica) hosts. Experimental manipulation of mite loads and partial cross-fostering experiments on Barn Swallows, where half of the nestlings in the brood were exchanged with nestlings from another nest, shows that parasite burdens and origin, but not rearing conditions, of Bam Swallow nestlings, affected their adult tarsus length and maximum body weight shortly before fledging. Mite loads of adult Barn Swallows at spring arrival were more similar to mite loads of their own offspring, whether reared in their own or in foster nests inoculated with mites, than to loads of foster offspring. Parent Barn Swallows with long tail ornaments had offspring with smaller mite loads in the partial cross-fostering experiments. The amount of increase in male tail ornaments from one year to another was negatively related to experimentally manipulated mite loads of Barn Swallow nests during the preceding breeding season. In conclusion, the three assumptions of the hypothesis were supported by the experimental tests.     

A rare study from the wintering grounds provides insight into the costs of malaria infection for migratory birds

Malaria parasites can have strong effects on the population dynamics and evolution of migratory bird species. In many species, parasite transmission occurs on the wintering grounds, but studies to determine the consequences of infection have taken place during the breeding season, when malaria parasites circulate at chronic levels. We examined the predictors of malarial infections for great reed warblers during the northern winter in Africa, where active parasite transmission is thought to occur and naïve individuals experience acute infections. Counter to expectations, we found that winter infection intensities were lower than those encountered on the breeding grounds. One potential explanation is that reduced immune function during breeding allows parasites to persist at higher chronic intensities. We found no relationships between the incidence or intensity of infection on condition (as measured by scaled mass index, plasma metabolites, and feather corticosterone), spring migration departure dates, or home range sizes. We also tested a prediction of the Hamilton–Zuk hypothesis and found that male ornament (song) quality was unrelated to parasitic infection status. Overall, our results provide the first evidence that long‐distance migrants captured on their wintering grounds are in the chronic stage of infection, and suggest that winter studies may fare no better than breeding studies at determining the costs of acute malarial infection for great reed warblers.     

Short-term nutrient deprivation affects immune function

Abstract Measurement of insect immune effector system function aimed at identifying costs has largely been stimulated by the ideas of Hamilton & Zuk (1982) , who proposed that choosy females may derive some genetic benefit from selecting parasite-resistant males. Field studies of such systems assume that most variation in measured immune traits is affected strongly by genes and pay little attention subsequently to the role of nutritional status in determining the magnitude of assayed immune effector systems. In this paper the effects of nutrient deprivation on immune function are measured in the mealworm beetle ( Tenebrio molitor L.) reared in otherwise ideal conditions. The results suggest that immune effector system function is down-regulated during short-term nutritional deprivation, but is rapidly up-regulated to pre-deprivation levels after animals are allowed access to food. This rapid modulation of immune function in the context of nutritional status has important implications for measuring immune function in the field, as well as the interpretation of those measures.     

Sexual showiness and parasite load: correlations without parasite coevolutionary cycles

Hamilton & Zuk (1982, Science 218, 384-387.) produced a model of sexual selection in which coevolutionary cycles of host and parasites generate consistently positive correlations between parent and offspring viability, and that animals choose mates for genetic disease resistance by scrutinizing characters whose full expression is dependent on health and vigour. They predicted a positive correlation between sexual showiness and parasite burden across species, and a negative correlation within a species. First, recent suggestions that interspecific correlations in the opposite direction to that indicated above are consistent with the mechanisms of Hamilton & Zuk's model are discussed. Second, it is shown that the model's predictions can be produced by heritable variation maintained by non-parasite fluctuating selection. In this case, the parasites associated with degree of sexual showiness are those able to amplify any initial heritable differences in vigour. Alternative sources of positive correlation between parent and offspring viability, which include the indirect effects of climatic change and exclude the need for host-parasite coevolutionary cycles, are also proposed.     

Sex differences in immune responses: Hormonal effects,antagonistic selection,and evolutionary consequences

Males and females differ in both parasite load and the strength of immune responses and these effects have been verified in humans and other vertebrates. Sex hormones act as important modulators of immune responses; the male sex hormone testosterone is generally immunosuppressive while the female sex hormone estrogen tends to be immunoenhancing. Different sets of T-helper cells (Th) have important roles in adaptive immunity, e.g. Th1 cells trigger type 1 responses which are primarily cell-mediated, and Th2 cells trigger type 2 responses which are primarily humoral responses. In our review of the literature, we find that estrogen and progesterone enhance type 2 and suppress type 1 responses in females, whereas testosterone suppresses type 2 responses and shows an inconsistent pattern for type 1 responses in males. When we combine these patterns of generally immunosuppressive and immunoenhancing effects of the sex hormones, our results imply that the sex differences in immune responses should be particularly strong in immune functions associated with type 2 responses, and less pronounced with type 1 responses. In general the hormone-mediated sex differences in immune responses may lead to genetic sexual conflicts on immunity. Thus, we propose the novel hypothesis that sexually antagonistic selection may act on immune genes shared by the sexes, and that the strength of this sexually antagonistic selection should be stronger for type 2- as compared with type 1-associated immune genes. Finally, we put the consequences of sex hormone-induced effects on immune responses into behavioral and ecological contexts, considering social mating system, sexual selection, geographical distribution of hosts, and parasite abundance.     

Comparative evidence for a positive correlation between haematozoan prevalence and mortality in waterfowl

Hamilton and Zuk (1982) suggested a new hypothesis to explain the evolution of secondary sexual characters, namely that male ornaments may represent honest signals of male capacity to resist parasites. Since then several authors have addressed the question of the role played by parasites in the evolution of host secondary sexual characters. Comparative analyses of Hamilton and Zuk's hypothesis have, however, failed to show the predicted positive association between parasitism levels and sexually-selected traits. One possible explanation for this discrepancy involves a low pathogenicity of the parasites used to test the hypothesis. Here we show that haemosporidians are positively correlated with mortality rates in a sample of waterfowl, and that the correlation between the two variables is of similar magnitude in both males and females. Contrary to the expectations based on the Hamilton and Zuk's hypothesis, we did not find any correlation between plumage brightness and haemosporidian prevalence. These results indicate that haemosporidians may have a pathogenic effect on their avian hosts and that plumage brightness is likely to have evolved in response to ecological factors other than parasitism infections.     

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.     

Parasites and showy males: malarial infection and color variation in fence lizards

Summary Hamilton and Zuk (1982) proposed that the quality of male showy traits reflects genetically-based resistance to parasites and can be used by females to select mates that are less prone to parasitic attack. The hypothesis requires that a particular state of a variable showy trait should be associated with parasite infection. We tested this idea with a population of western fence lizards, Sceloporus occidentalis, infected with the malarial parasite, Plasmodium mexicanum. Ventral color pattern is strongly dimorphic in fence lizards and varies greatly among males in this population. Malaria-infected males exhibited significantly more black and less pale on their ventral surface than did noninfected males of similar body size. This difference was not a function of differing ages of infected and noninfected animals of the same body size. However, logistic regression demonstrated that females using male ventral color as a gauge of infection status would only marginally improve their chance of choosing a noninfected lizard over random selection of mates.     

Melanin‐based coloration is related to parasite intensity and cellular immune response in an urban free living bird: the feral pigeon Columba livia

Melanin‐based coloration is widespread among vertebrates, but the adaptive function of this trait remains poorly known. Recently, it has been shown that differently coloured individuals have different abilities to cope with parasites. This correlation between melanin‐based coloration and immunity could be explained by the pleiotropic effects of genes coding for melanin pigmentation on the immune system (‘genetic link’ hypothesis) but also because differently coloured individuals may exploit alternative habitats varying in parasite exposure, which leads to different development of the immune function (‘exposure’ hypothesis). As feral pigeons Columba livia are genetically polymorphic with respect to melanic coloration, they constitute an ideal model system to address such hypotheses. In this study, we showed that darker melanic individuals had a lower endoparasite intensity (reflecting host susceptibility) and had a greater cellular immune response to PHA injection than paler ones, whereas parasite prevalence (reflecting exposure to vectors) was similar between colorations. These results provide a correlative support of the ‘genetic link’ hypothesis: differently coloured individuals might be similarly exposed to parasites but darker ones might have a better ability to control the infection. This suggests that parasitism could play a crucial role in the maintenance of colour polymorphism in natural populations, which opens the interesting possibility that differently coloured individuals could be adapted to alternative environments varying in parasite diversity and exposure.     

Effects of blood parasites on sexual and natural selection in the pied flycather

The occurrence of the blood parasites Haemoproteus and Trypanosoma in the pied flycatcher, Ficedula hypoleuca , was examined to test current hypotheses that parasites reduce the expression of secondary sexual traits, mating success, breeding success, and survival of infected individuals. The results showed that there was no significant relationship between male plumage brightness and Trypanosoma infection, but males infected with Haemoproteus tended to be brighter than uninfected males, partly because first-year males were less often infected than older males. Polygynous males did not have fewer parasites than monogamous males. Females did not choose uninfected males among those they had sampled. Clutch size and laying date were not related to female infection status, and the number and quality of nestlings was not related to parasite infections of either male or female parent. The ability of males to provide parental care was not related to their infection status. The return rate from one breeding season to the next of infected males was not lower than that of uninfected males. The lack of correlations between parasites and male plumage colour and female mate choice apparently do not support the Hamilton-Zuk hypothesis of sexual selection. However, the absence of demonstration of any negative effects of parasites suggests that infection status may not be a direct measure of parasite resistance, or the degree to which the host suffers. Instead, the results support the alternative view that infected individuals have demonstrated their ability to survive and to cope with the parasites, while uninfected individuals are probably not yet tested for their resistance. This points to problems in using parasite prevalences and distributions, at least of some protozoan blood parasites, for tests of Hamilton-Zuk hypothesis, even though this was done in the first test by Hamilton and Zuk and by many later researchers