Post-copulatory guarding,female choice and the levels of gregarine infections in the field cricket,Gryllus bimaculatus

Summary A recent model in sexual selection has proposed a role for parasites in maintaining heritable fitness variation. Females are envisaged as benefitting from preferentially mating with males that show resistance to infection. The post-copulatory guarding behaviour characteristic of many species of field cricket, has been envisaged as a means by which females assess male health and vigour. This hypothesis was tested in a field cricket, G. bimaculatus, which harbours a protozoan gut parasite. In enclosed arena trials, no direct correlations between female behaviours and levels of infection in males were found. However, there were significant correlations between the intensity of male guarding and the number of parasites found in the gut; infected males guarded more intensely in order to maintain contact with the female. In a second experiment simulating open field conditions, females left heavily parasitized males sooner than mildly or uninfected individuals. These data are discussed in relation to female choice for male health and vigour.     

Satin bowerbird parasites: a test of the bright male hypothesis

Summary The number of a common parasite (Cuclotogaster sp.) on male satin bowerbirds was related to male mating success in a test of Hamilton and Zuk's (1982) bright male hypothesis. The data do not show the expected inverse correlation between female mating preferences and the level of parasitic infection of males predicted by that model. Nearly all matings are accomplished by bower-holding males (Borgia 1985a), but the vast majority of these males were uninfected. There were large differences in mating success among the uninfected bower holders, but this could not be explained by between male differences in the level of parasitic infection. From this I conclude that levels of parasitic infection are not now an important direct cause of intermale variation in mating success. The results are, however, consistent with a hypothesis that a low level of infection is indicative of the overall healthy condition of a male. If this is true, it supports the hypothesis that the ability to hold a bower may be an indicator of male condition to females.     

Threat-sensitive feeding strategy of immature sticklebacks (Gasterosteus aculeatus) in response to recent experimental infection with the cestode Schistocephalus solidus

Threat-sensitive decision-making might be changed in response to a parasitic infection that impairs future reproduction. Infected animals should take more risk to gain energy to speed up their growth to achieve early reproduction and/or to strengthen their immune response. To avoid correlational evidence, we experimentally infected and sham-infected randomly selected immature three-spined sticklebacks with the cestode Schistocephalus solidus. For 7 weeks we determined the threat-sensitive foraging decisions and growth of individual sticklebacks in the presence of a live pike (Esox lucius). The experimenters were blind with respect to the infection status of the fish. In contrast to previous studies, our recently infected fish should have been almost unconstrained by the parasite and thus have been able to adopt an appropriate life history strategy. We found a strong predator effect for both infected and uninfected fish: the sticklebacks’ risk-sensitive foraging strategy resulted in significantly reduced growth under predation risk. Infected fish did not grow significantly faster under predation risk than uninfected fish. Since infected fish consumed much less prey in the presence of the predator than did infected fish in its absence, they obviously did not use the opportunity to maximize their growth rate to reach reproduction before the parasite impairs it. Received: 21 June 1999 / Revised: 27 November 1999 / Accepted: 5 September 2000     

Altered responses to female odors in parasitized male mice: neuromodulatory mechanisms and relations to female choice

There is accumulating evidence that females may preferentially select parasite-free or -resistant males. Minimal attention has, however, been paid to the mate preferences and responses of the parasitized male hosts themselves. Here, we considered the effects of parasitic infection on male host mate responses, the neuromodulatory correlates of these responses, and the relations of these responses to female mate choice. Using an odor “preference” test, we examined the effects of different stages of an acute, sub-clinical infection with the naturally occurring, enteric, single host, protozoan parasite, Eimeria vermiformis, on the responses of male mice, Mus musculus domesticus, to the odors of estrous females along with the responses of uninfected females to the parasitized males. At 4 days post-infection (non-infective, pre-patent stage) E. vermiformis-infected male mice showed a significantly decreased preference for the odors of estrous females, whereas at 10 days post-infection (infective, patent stage) infected males showed a significantly increased preference for the odors of estrous females. Parasitized males displayed no significant changes in their responses to the odors of non-estrous females, supporting effects on the reproductively related responses of the host. In parallel, estrous females displayed a reduced interest in the odors of infected males. Least interest was expressed in the odors of the patent, infective males, consistent with the avoidance of contagion. Using selective opioid peptide receptor agonists and antagonists we found evidence that enhanced kappa opioid peptide (e.g., dynorphin) activity was related to the decreased sexual interest of the pre-infective males, while augmented delta opioid peptide (e.g., enkephalin) activity was associated with the enhanced responses of the infective males to females. We further showed that acute kappa opiate administration reduced the responses of uninfected males to females and that uninfected females displayed modified responses to the odors of uninfected males subject to acute modifications of opioid activity. We suggest that these differential shifts in endogenous opioid activity in the parasitized males are associated with and, or related to alterations in neuro-immune and endocrine functions. These findings show that parasitic infection can have, depending on the stage of infection and associated neuromodulatory changes, either significant facilitatory or inhibitory effects on male host preferences for and responses to females. Received: 22 April 1996 / Accepted after revision: 15 March 1997     

The effects of two acanthocephalan parasites, Pomphorhynchus laevis and Polymorphus minutus, on pairing success in male Gammarus pulex (Crustacea: Amphipoda)

Parasites can decrease male mating success in host species in various ways, in particular by affecting male competitive ability for access to females. However, male-male competition can take different forms (i.e. interference vs exploitation competition) and which type of competition is most affected by parasites is not always clear. We investigated the influence of two acanthocephalan parasites Pomphorhynchus laevis and Polymorphus minutus on the pairing success of their intermediate host, Gammarus pulex, using field-based studies and complementary laboratory-based studies. We first studied male pairing success in the field using four large samples of paired and unpaired individuals collected at different dates. In three of the samples, the effects of size and parasite infection were significant, whereas for one sample only male size had a significant effect. There was no difference in size distributions between infected and uninfected gammarids. Large males were paired more often than smaller males, and uninfected males were paired more frequently than infected males, the pairing success of P. minutus-infected males being more severely affected than that of P. laevis-infected males. We then experimentally tested the ability to enter into precopula with a receptive female in the presence or absence of competitors. In competitive situations, the pairing success of P. laevis- and P. minutus-infected males was significantly lower than that of uninfected males, with pairing success being more affected in P. laevis-infected than in P. minutus-infected males. In the absence of competition, males infected with P. laevis were significantly less likely to enter into precopula compared with uninfected males and P. minutus-infected males, whereas there was no difference between uninfected and P. minutus-infected males in their inclination to pair with a receptive female. However, for both parasites, latency time to pair formation was significantly shorter for uninfected than for infected males. In a third experiment, we tested for a potential effect of vertical segregation on the pairing success of infected and uninfected males, but found no evidence for it. We conclude that infected males may be less competitive than uninfected males in competition by exploitation between males for females.     

Do microsporidian parasites affect courtship in two-spotted gobies?

Courtship and body condition of male two-spotted gobies (Gobiusculus flavescens) harbouring naturally acquired microsporidian infections were compared with those of microsporidian-free males under standardized conditions in the lab. Although parasite infection had no apparent effect on individual condition, it significantly affected male courtship intensity. This effect, however, was affected by the intensity of the female courtship. Our study is one of the first to demonstrate a sub-lethal behavioural effect of a microsporidian parasite that could negatively affect the reproductive success of infected individuals. Our results also suggest that secondary sexual traits like courtship may be more sensitive to moderately detrimental effects of parasite infection than classical condition indices.     

The effects of parasites on male ornaments and female choice in the lek-breeding black grouse (Tetrao tetrix)

Summary We describe the results of two studies of parasitic infection in the black grouse (Tetrao tetrix). The first deals with our own observations of lekking black grouse in which the parasite levels of two blood parasites, the protozoan Leucocytozoon lovati and microfilaria, probably produced by a nematode worm Splendidofilaria tuvensis, were scored. We also obtained measures of age, survival, number of copulations, body mass and length of the ornamental tail feathers (the lyre) of the lekking males. The second study analysed the data from Lund (1954) which involved eight gut parasites obtained from birds which were killed. In the first study we found higher levels of infection of Leucocytozoon in adults relative to young birds. Parasites had no effect on male survival and there was no correlation in infection between the two types of parasites. Birds infected with microfilaria had shorter tail ornaments. There was no relationship between parasitic infection and mating success. However, the data indicated that such a trend indeed may exist for Leucocytozoon and the most successful males on the leks were less often infected by Leucocytozoon than other males. Results of the second study showed a negative relationship between parasite load (a combined measure of all parasites) and both ornamental tail feather length and body mass. These observations are compatible with, but not conclusive evidence for, the hypothesis of Hamilton and Zuk (1982) on the evolution of secondary sexual characters, where females choose to mate with genetically resistant males which show their resistance by expressing larger and more showy secondary sexual characters. Alternative explanations for the observed patterns are: females avoid infected males for some immediate benefit; and/or parasite loads are indicators of general stress rather than genetical resistance. Under the latter hypothesis females could mate with more vigorous males for reasons unrelated to parasite resistance.     

Trichinella spiralis infection in voles alters female odor preference but not partner preference

Females may choose mates based on secondary sex traits that reflect disease resistance. Accordingly, females should be able to distinguish between unparasitized and parasitized males, and should prefer to mate with unparasitized individuals. Mate and odor preferences for uninfected males or males infected with the nematode, Trichinella spiralis, were examined among prairie voles (Microtus ochrogaster) and meadow voles (M. pennsylvanicus). In a 15-min odor preference test, only female meadow voles distinguished between bedding from parasitized and unparasitized conspecific males, and preferred to spend time with bedding from unparasitized males. Although T. spiralis infection influenced odor preference in female meadow voles, there was no effect of infection status on mate preference among either species. Testosterone and corticosterone concentrations were not different between parasitized and unparasitized males. However, among prairie voles, males that spent an increased amount of time with females during the mate preference test had elevated testosterone concentrations. Taken together, these data suggest that (1) female meadow voles can discriminate between unparasitized and parasitized males, (2) the effects of infection on steroid hormone concentrations may be masked by the effects of social interactions, and (3) parasites may represent a selective constraint on partner preference in voles; however, the life cycle of parasites may influence female preference and should be considered in studies of female preference. Received: 23 April 1998 / Accepted after revision: 25 October 1998     

Parasite distribution and virulence: implications for parasite-mediated sexual selection

The Hamilton-Zuk hypothesis states that females choosing males with more developed secondary sexual traits, i.e. brighter males, achieve greater fitness if variability in brightness reflects heritable variation in resistance to parasites. However, several factors will affect the likelihood that parasites play a role in sexual selection in given species. Here, using simple models, we show that because of parasite aggregation on a few hosts, only few breeding males would suffer from reductions in brightness due to parasites. Only in cases where parasites are abundant and show low levels of aggregation among their hosts would there be sufficient variability in brightness among breeding males for female choice of bright, resistant males to evolve. In addition, sufficient parasite-induced variability in brightness among breeding males will only occur in host-parasite systems where pathology is linearly related to the number of parasites per host. The presence of males that are uninfected and bright but genetically susceptible to parasites will also influence the fitness advantages obtained by females choosing bright males. If genetic immunity against parasites is rare in the host population, females can probably only benefit from choosing bright males if parasites are common and little aggregated among males. These results greatly limit the generality of the Hamilton-Zuk hypothesis, and suggest that only a small fraction of host-parasite associations could promote the evolution of host mate choice for resistance based on brightness. Correspondence to: R. Poulin     

Prospecting at conspecific nests and exploration in a novel environment are associated with reproductive success in the jackdaw

Consistent behavioural differences between individuals of the same population (“personality” variation) might arise if individuals follow different life-history strategies. Thus, it would be important to determine how personality variation relates to behaviours potentially associated with life-history strategies, such as those related to the use of information about the state of the environment. Little is, however, known about how personality is associated with information use and reproductive success. We tested whether wild social jackdaws, Corvus monedula, show consistent behavioural differences in their exploratory behaviour (in a novel environment in the lab and in their reaction towards a novel object in the wild) and prospecting behaviour (number of visits to conspecific nests). We furthermore examined whether these behavioural traits are linked with each other and predictors of reproductive success. Breeding jackdaws were consistent in their exploratory behaviour within, and in their prospecting behaviour between, years. Exploratory behaviour in the novel environment was correlated with the latency to approach a novel object in the wild but not with the frequency of prospecting at conspecific nests. Highly exploratory males and females and frequently prospecting males produced fewer fledglings than less exploratory individuals or less prospecting males, respectively. We discuss the importance of consistent individual differences in exploration and information sampling on individual fitness.     

Mate preferences in <Emphasis Type="Italic">Drosophila</Emphasis> infected with <Emphasis Type="Italic">Wolbachia</Emphasis>?

The maternally inherited bacterium Wolbachia pipientis generates strong reproductive incompatibilities between uninfected females and infected males (cytoplasmic incompatibility), significantly reducing both female and male reproductive success. Such fitness costs are thought to place selective pressure on hosts to evolve pre-copulatory preferences for mating with compatible mates, thereby enabling them to avoid the reproductive incompatibilities associated with Wolbachia. Therefore, uninfected females are predicted to prefer mating with uninfected males, whereas infected males are predicted to prefer mating with infected females. Despite these predictions, previous investigations of pre-copulatory mate preferences in Wolbachia-manipulated Drosophila have not found evidence of female preference for uninfected or compatible males. However, none of these studies utilised a design where focal individuals are provided with a simple choice in a relatively non-competitive situation. We examined both female and male pre-copulatory mate preference based on mate infection status in Drosophila simulans and D. melanogaster using simple choice assays involving between 30–50 replicates per treatment. Although we found no evidence of female pre-copulatory mate preferences in either species, male D. simulans exhibited some preference for mating with females of the same infection status. However, this preference was not evident when we repeated the experiment to confirm this finding. Consequently, we conclude that neither male nor female D. melanogaster and D. simulans exhibit significant Wolbachia-associated pre-copulatory mate preferences.     

The social network structure of a wild meerkat population: 2. Intragroup interactions

Knowledge of the structure of networks of social interactions is important for understanding the evolution of cooperation, transmission of disease, and patterns of social learning, yet little is known of how environmental, ecological, or behavioural factors relate to such structures within groups. We observed grooming, dominance, and foraging competition interactions in eight groups of wild meerkats (Suricata suricatta) and constructed interaction networks for each behaviour. We investigated relationships between networks for different social interactions and explored how group attributes (size and sex ratio), individual attributes (tenure of dominants), and ecological factors (ectoparasite load) are related to variation in network structure. Network structures varied within a group according to interaction type. Further, network structure varied predictably with group attributes, individual attributes, and ecological factors. Networks became less dense as group size increased suggesting that individuals were limited in their number of partners. Groups with more established dominant females were more egalitarian in their grooming and foraging competition interactions, but more despotic in their dominance interactions. The distribution of individuals receiving grooming became more skewed at higher parasite loads, but more equitable at low parasite loads. We conclude that the pattern of interactions between members of meerkat groups is not consistent between groups but instead depends on general attributes of the group, the influence of specific individuals within the group, and ecological factors acting on group members. We suggest that the variation observed in interaction patterns between members of meerkat groups may have fitness consequences both for individual group members and the group itself.     

Sigma virus and male reproductive success in Drosophila melanogaster

The risk of disease transmission can affect female mating rate, and thus sexual conflict. Furthermore, the interests of a sexually transmitted organism may align or diverge with those of either sex, potentially making the disease agent a third participant in the sexual arms race. In Drosophila melanogaster, where sexual conflict over female mating rate is well established, we investigated how a common, non-lethal virus (sigma virus) might affect this conflict. We gave uninfected females the opportunity to copulate twice in no-choice trials: either with two uninfected males, or with one male infected with sigma virus followed by an uninfected male. We assessed whether females respond behaviorally to male infection, determined whether male infection affects either female or male reproductive success, and measured offspring infection rates. Male infection status did not influence time to copulation, or time to re-mating. However, male infection did affect male reproductive success: first males sired a significantly greater proportion of offspring, as well as more total offspring, when they were infected with sigma virus. Thus viral infection may provide males an advantage in sperm competition, or, possibly, females may preferentially use infected sperm. We found no clear costs of infection in terms of offspring survival. Viral reproductive success (the number of infected offspring) was strongly correlated with male reproductive success. Further studies are needed to demonstrate whether virus-induced changes in reproductive success affect male and female lifetime fitness, and whether virus-induced changes are under male, female, or viral control.     

Do brain parasites alter host personality? — Experimental study in minnows

Despite that the existence of animal personalities is widely recognized, no consensus has been reached on the relative importance of different ecological factors behind their expression. Recently, it has been suggested that parasites may have a crucial role in shaping animal personalities, but only a very few studies have experimentally tested the idea. We infected Eurasian minnows (Phoxinus phoxinus) with the brain-encysted trematode parasite, Diplostomum phoxini, and studied whether infection could modify the personality of their hosts. Our results show that D. phoxini infection did not affect the mean levels of boldness, activity or exploration, but infected minnows showed higher repeatability in boldness and activity, and reduced repeatability in exploration. We also found that D. phoxini may be able to break the associations (behavioral syndromes) between behavioral traits, but that this effect may be dependent on parasite intensity. Furthermore, the effect of D. phoxini infection on personality of the hosts was found to be nonlinearly dependent on infection intensity. Taken together, our results suggest that D. phoxini parasites may shape the personality of their hosts, but that behavioral consequences of ecologically relevant infection levels may be rather subtle and easily remain undetected if only the mean trait expressions are compared.     

Female choice for parasite-free male satin bowerbirds and the evolution of bright male plumage

Summary Hamilton and Zuk proposed that bright male plumage may have evolved in males of polygynous species as a result of female preferences for males that are able to demonstrate their resistance to disease. They predicted an inverse correlation between female mating preferences and the level of parasitic infection of males. We found such a correlation between the level of infection by a common ectoparasite (Myrsidea ptilonorhynchi: Menoponidae) and mating success of male satin bowerbirds (Ptilonorhynchus violaceus). In addition, we tested and were able to confirm three other predictions derived from their model: that (1) older males had fewer parasites than their younger counterparts, (2) levels of individual parasitic infection are highly correlated between years, and (3) that individuals resighted in successive years are less parasitized than those that fail to return. These results support the bright male model, but they are also consistent with two other hypotheses that may explain plumage dimorphism based on the level of parasitic infection. The correlated infection model suggests that females choose males with few ectoparasites because of a correlation between the level of ectoparasitic infection and heritable resistance to internal infections. In the parasite avoidance model, females favor parasitefree males because it lowers their own prospects for parasitic infection. Our data did not show the predicted relationship between parasite numbers with plumage quality that is needed to support the bright male hypothesis, nor did it show the inverse correlation between male condition and parasite numbers that is predicted by both the bright male and correlated infection hypotheses. Our results are most consistent with the parasite avoidance hypothesis.     

The multidimensionality of behavioural defences against brood parasites: evidence for a behavioural syndrome in magpies?

Studies of antiparasite defences against cuckoo parasites have largely neglected the possibility that behavioural components of host defence may correlate giving rise to a behavioural syndrome. Furthermore, the different contribution of the host’s sex in nest defence has traditionally been disregarded. Here, we studied magpie (Pica pica) mobbing behaviour towards dummies of great spotted cuckoo (Clamator glandarius) and non-harmful hoopoes (Upupa epops) and egg rejection of parasite eggs in a population of colour-banded magpies. We predicted a positive correlation between the intensity of nest defence and egg rejection within each sex and that females respond more intensely than males to the threat of brood parasitism as they undertake incubation. Magpie males, but not females, defended their nests more intensely in those nests in which cuckoo model eggs were rejected. Individual magpies did significantly differ in their baseline level of nest attentiveness; however, there were no individual differences once pair identity was considered. Males and females defended their nests more intensely when it was exposed to the presence of a great spotted cuckoo dummy. Males, but not females, were more prone to appear at their nests, and females, but not males, were more prone to defend more intensely when their nests were challenged by a parasite threat. Our results thus agree with the view that mobbing behaviour and egg rejection in magpies may actually constitute a pseudosyndrome and highlight the necessity to integrate interindividual variation and the sex of the host in studies of the evolution of host defences.     

Parasitism in a social wasp: effect of gregarines on foraging behavior, colony productivity, and adult mortality

Behavior in eusocial insects likely reflects a long history of selection imposed by parasites and pathogens because the conditions of group living often favor the transmission of infection among nestmates. Yet, relatively few studies have quantified the effects of parasites on both the level of individual colony members and of colony success, making it difficult to assess the relative importance of different parasites to the behavioral ecology of their social insect hosts. Colonies of Polybia occidentalis, a Neotropical social wasp, are commonly infected by gregarines (Phylum Apicomplexa; Order Eugregarinida) during the wet season in Guanacaste, Costa Rica. To determine the effect of gregarine infection on individual workers in P. occidentalis, we measured foraging rates of marked wasps from colonies comprising both infected and uninfected individuals. To assess the effect of gregarines on colony success, we measured productivity and adult mortality rates in colonies with different levels of infection prevalence (proportion of adults infected). Foraging rates in marked individuals were negatively correlated with the intensity of gregarine infection. Infected colonies with high gregarine prevalence constructed nests with fewer brood cells per capita, produced less brood biomass per capita, and, surprisingly, experienced lower adult mortality rates than did uninfected or lightly infected colonies. These data strongly suggest that gregarine infection lowers foraging rates, thus reducing risk to foragers and, consequently, reducing adult mortality rates, while at the same time lowering per-capita input of materials and colony productivity. In infected colonies, queen populations were infected with a lower prevalence than were workers. Intra-colony infection prevalence decreased dramatically in the P. occidentalis population during the wet season.An erratum to this article can be found at     

Black spots and female association preferences in a sexual/asexual mating complex (Poecilia, Poeciliidae, Teleostei)

We investigated whether female association preferences for males are influenced by black spot disease (BSD), a parasite induced change of the host phenotype. We compared three different species of fish: a gynogenetic hybrid species, Poecilia formosa (amazon molly) and two sexual species (Poecilia latipinna and Poecilia mexicana), which were involved in the natural hybridisation leading to the amazon molly. Contrary to their sexual relatives, asexual amazon mollies significantly avoided images of males infected with black spot disease. We propose that amazon molly females have direct fitness benefits from choosing healthy males. The adaptive significance of the preference for BSD-uninfected males in the asexual amazon molly is yet unclear but may involve avoidance of predation or parasite infection as well as increased sperm availability.     

A fungus infecting domestic flies manipulates sexual behaviour of its host

The Enomopathogenic fungus Entomophthora muscae infects and kills domestic flies Musca domestica, and rates of transmission are higher at high population densities. I tested whether features of parasitized hosts increased the likelihood of transmission of the fungus in a series of experiments. Individual flies contacting an infected conspecific had a much higher probability of becoming infected than had flies contacting a dead fly without signs of infection. Males especially were attracted to and behaved sexually towards dead, infected flies even when a choice was available between a dead, infected fly and a dead, uninfected individual. The abdomen of infected flies swelled considerably as a consequence of infection, and uninfected female flies with larger abdomens are more fecund than the average female and maybe more attractive. Experiments in which abdomens of infected and uninfected flies were cut off and glued back on other flies demonstrated that the abdomens of infected flies were highly attractive to males. When the size of the abdomen of infected and uninfected individual flies was held constant, infected dead flies were still more attractive than corpses of uninfected flies. This result suggests that features other than the size of the swollen abdomen enhanced the attractivity of infected flies. Features of infected hosts therefore increased the likelihood of transmission of the parasitic fungus.