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     

Blood parasites and male fitness in the pied flycatcher

In vertebrates the effect of parasites on host ecology has almost been ignored. Recently the view that well-adapted parasites do not harm their hosts has been challenged and there is growing evidence that parasites do have a present-day effect on a great variety of host fitness components. The pied flycatcher is a small migratory passcrine bird. Any decrease in condition caused by disease should affect its ability to cope with physical demands of migration. Here we examine whether blood parasites have any effect on male arrival time. Males infected with Trypanosoma arrived on average 2 days later than males with no Trypanosoma infection. Infected males also had shorted tails and tended to have shorter wings. By contrast, there was no difference in male arrival time between males infected with Haemoproteus and healthy males. It seems that Trypanosoma infection lowered male condition and consequently the ability to moult and migrate. The difference in length of feathers may have generated the difference in arrival times. Early arrival is highly important for males, since only the first males become polygynous and breeding prospects deteriorate rapidly with any delay in egg laying. Estimated reduction in breeding success for infected males was about 20%.     

Pairing success and sperm reserve of male Gammarus pulex infected by Cyathocephalus truncatus (Cestoda: Spathebothriidea)

Manipulative parasites with complex life cycles are known to induce behavioural and physiological changes in their intermediate hosts. Cyathocephalus truncatus is a manipulative parasite which infects Gammarus pulex as intermediate host. G. pulex males display pre-copulatory mate guarding as a response to male-male competition for access to receptive females. In this paper, we tested the influence that C. truncatus-infection might have on male G. pulex sperm number and pairing success. We considered 3 classes of G. pulex males in our experiments: (i) uninfected males found paired in the field, (ii) uninfected males found unpaired in the field, or (iii) infected males found unpaired in the field. Both infected males and uninfected unpaired males paired less with a new female than uninfected paired males did. Furthermore, infected males appear to be at a strong disadvantage when directly competing for females with a healthy rival male, and had fewer sperm in their testes. We discuss the potential effect of male and female mating strategies on such male host mating alteration.     

Assortative pairing with respect to parasite load in the beetle Timarcha maritima (Chrysomelidae)

Because of their effects on host reproductive behaviour, parasites are theoretically expected to create sometimes assortative mating among hosts, with heavily parasitized individuals pairing together and lightly parasitized ones pairing among themselves. We investigated the influence of protozoan gut parasites on the pairing pattern of the chrysomelid beetle Timarcha maritima. In the field, fecundity was negatively correlated with the parasite load of females, unpaired males were significantly more heavily infected than paired ones and, among pairs, males and females were matched for parasite load. Mate choice experiments in the laboratory showed that males have some ability to avoid heavily infected partners when given the choice between two females. Male competitiveness, measured as their mobility, was also negatively correlated with parasite load. These results indicate that parasite-related assortative pairing in this beetle could result from parasitized females being less fecund and parasitized males less competitive.     

Experimental evidence for a hierarchy of mate- and host-induced cues in a fish ectoparasite, Argulus coregoni (Crustacea: Branchiura)

Argulus coregoni is an ectoparasite primarily infesting freshwater salmonids. Sexually reproducing parasites such as A. coregoni are confronted with a dilemma between finding a mate and the costs involved in doing so; if mating partners are unavailable on a host, by leaving to search for a mate on a new host, the parasite is exposed to risks such as predation and energy loss. The utilization of chemical cues could enhance the probability of finding a host and/or a suitable mating partner and thus decrease the level of costs associated with detachment from the host. In this study we constructed a Y-maze arena to determine if adult A. coregoni respond to mate- and host-related chemical cues. We also tested the directional response towards light, since it has been suggested that photic cues are the most important cues for juvenile A. coregoni locating a host. Our results showed that both sexes were attracted to light and fish odour. Free-swimming A. coregoni males responded to chemical cues produced by adult females but not vice versa. The hierarchy of these stimuli was analyzed by pitting the cues against one another in the Y-maze, showing that light was the most salient stimulus for both male and female parasites. Moreover, male parasites were more strongly attracted towards light and fish odour than female odour. In another experiment in a semi-natural environment, we examined whether the ability of A. coregoni males to detect female odour influences their host choice. Free-swimming males did not preferentially infest fish infected with female parasites over parasite-free fish. We suggest that a hierarchy of stimulus responses exists, whereby free-swimming parasites first respond to host-related signals and most dominantly to visual cues. However, cues connected to mate finding may become a priority for late adult stages and/or once the parasite has attached to the host.     

Pairing success of male Gammarus lacustris infected by two acanthocephalans: a comparative study

The costs of parasitism to host reproduction can be best assessedusing field studies to determine overall mating success andexperimental studies to examine how parasites may affect matingbehavior. We compared the influence of two parasites, Polymorphusparadoxus and P. marilis (Acanthocephala), on the pairing successof their intermediate host (Gammarus lacustris, Crustacea) inboth the field and laboratory. Parasitism significantly loweredthe pairing success of male gammarids. In the field, P. paradoxus-infectedmales paired significantly less often than P. marilis-infectedor uninfected males. Those infected by P. marilis were alsofound in precopula significandy less often than uninfected ones.In the laboratory, the pairing success of males infected byeither parasite was significantly reduced in both competitiveand noncompetitive situations. As in the field studies, thepairing success of P. paradoxus-infected males was significantlylower than that of P. marilis-infected and uninfected males.Polymorphus marilis-infected males were also outcompeted byuninfected individuals, however, their pairing success improvedwhen alone with a female (noncompetitive experiments). We relatethe differential influence of the two parasites on the pairingsuccess of male gammarids to their effects on the physiologyand behavior of G. lacustris.     

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.     

Patterns of gastrointestinal parasitism among five sympatric prairie carnivores: are males reservoirs?

Male vertebrates are believed to be disproportionately vulnerable to parasites, but empirical support for this contention is mixed. We tested the hypothesis of higher levels of parasitism in males with the use of counts of gastrointestinal helminths in 5 sympatric mammalian carnivores (American badgers, coyotes, red foxes, raccoons, striped skunks) from central Saskatchewan. Parasite burdens for females and males of each host species were compared with the use of prevalence (percentage of hosts infected), intensity (parasites per infected host), and overdispersion (proportion of heavily infected hosts that were male). Of 30 comparisons (13 each for prevalence and intensity, 4 for overdispersion), male bias was detected 8 times (27%), whereas female bias was detected only once (3%), adding some support to the notion that male mammals are more susceptible to parasitism. However, most of the statistical comparisons we undertook revealed no sexual bias (n=21, 70%), suggesting that differential patterns of infection are not ubiquitous in mammals. Moreover, when detected, the magnitude and direction of bias varied among host species, helminth species, and metrics of infection. We conclude that sympatric and ecologically similar mammal species will not always share the tendency for males to be more susceptible to parasitism, and that studies incorporating multiple parasites and metrics of infection are more likely to detect sex bias.     

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

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

Carotenoid trade-off between parasitic resistance and sexual display: an experimental study in the blackbird (Turdus merula)

Many parasites depress the expression of the carotenoid-based colour displays of their hosts, and it has been hypothesized that animals face a trade-off in carotenoid allocation between immune functions and 'degree of ornamentation'. While numerous correlative studies suggest that parasite infection decreases the intensity of carotenoid-based colour displays, the existence of this trade-off has never been demonstrated experimentally in a host-parasite model. In this study, we used the blackbird (Turdus merula) and Isospora (an intestinal parasite) to assess whether this trade-off does indeed exist. Blackbirds were supplemented with carotenoids while simultaneously being exposed to parasites. Supplemented males circulated more carotenoids in the blood and developed more brightly coloured bills than unsupplemented males. In addition, supplementation slowed down the replication rate of parasites. Supplementation with carotenoids enabled infected birds to maintain their bill coloration, whereas birds that were infected but not supplemented showed reduced bill coloration. At the same time, infection slowed carotenoid assimilation in the blood. Overall, we demonstrated that bill colour reflects a bird's health, and that only males with a carotenoid-rich diet are capable of coping with costs associated with parasitic infection. Carotenoids are thus traded off between host physiological response to parasites and secondary sexual traits. Further investigations are required to determine the physiological mechanisms that govern this trade-off.     

Sex-specific response of a mosquito to parasites and crowding

Host-parasite interactions are significantly influenced by the sex of the host and the environment in which the host is found. Sex-specific responses to parasite infection, however, may change according to the host environment. I examine the combined effect of parasite infection and crowding on males and females of the mosquito Aedes albopictus. At a high larval density, infected males experienced a greater relative reduction in body size than did infected females, whereas the pattern was reversed at low density. This experiment demonstrates the importance of the environment on sex-specific responses to parasites and contributes to a growing body of work examining sources of variation in host-parasite interactions.     

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

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

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.     

Inter- and intraspecific conflicts between parasites over host manipulation

Host manipulation is a common strategy by which parasites alter the behaviour of their host to enhance their own fitness. In nature, hosts are usually infected by multiple parasites. This can result in a conflict over host manipulation. Studies of such a conflict in experimentally infected hosts are rare. The cestode Schistocephalus solidus (S) and the nematode Camallanus lacustris (C) use copepods as their first intermediate host. They need to grow for some time inside this host before they are infective and ready to be trophically transmitted to their subsequent fish host. Accordingly, not yet infective parasites manipulate to suppress predation. Infective ones manipulate to enhance predation. We experimentally infected laboratory-bred copepods in a manner that resulted in copepods harbouring (i) an infective C plus a not yet infective C or S, or (ii) an infective S plus a not yet infective C. An infective C completely sabotaged host manipulation by any not yet infective parasite. An infective S partially reduced host manipulation by a not yet infective C. We hence show experimentally that a parasite can reduce or even sabotage host manipulation exerted by a parasite from a different species.     

Taking the Myc is bad for Theileria

It is commonly acknowledged that intracellular parasites manipulate the survival pathways of the host cells to their own ends. Theileria are masters of this because they invade bovine leukocytes and immortalize them. Host-cell survival depends on the presence of live parasites, and parasite death results in the leukocyte undergoing programmed cell death. The parasite, therefore, activates several anti-apoptotic pathways in host cells to ensure its own survival. In B cells that are infected by Theileria parva, one of the main mechanisms involves the induction of c-Myc and the subsequent activation of the anti-apoptotic protein Mcl-1. Activation of Myc might occur in other types of leukocyte that are infected by Theileria and in other host cells that are infected with different parasites.     

Monoxenous and heteroxenous parasites of fish manipulate behavior of their hosts in different ways

Adaptive host manipulation hypothesis is usually supported by case studies on trophically transmitted heteroxenous endoparasites. Trematodes and cestodes are among efficient manipulators of fish, their common intermediate hosts. In this review paper, new data on modifications of host fish behavior caused by monoxenous ectoparasitic crustaceans are provided together with a review of effects caused by heteroxenous parasites. Differences in modifications of host behavior caused by heteroxenous and monoxenous parasites are discussed. Manipulation by heteroxenous parasites enhances availability of infected fish to predators--definitive hosts of the parasites. Fine-tuned synchronization of modified anti-predator behavior with a certain phase of the trematode Diplostomum spathaceum development in the eyes of fish, their second intermediate host, was shown. Modifications of behavior are habitat specific. When juvenile salmonids are in the open water, parasites impair their cooperative anti-predator behavior; in territorial bottom-dwelling salmonids, individual defense behavior such as sheltering is the main target of manipulation. It was shown that monoxenous ectoparasitic crustaceans Argulus spp. decreased motor activity, aggressiveness and increased shoal cohesiveness of infected fish. Such a behavior facilitates host and mate searching in these parasites, which often change their hosts, especially during reproduction. Reviewed experimental data suggest that heteroxenous parasites manipulate their host mainly through impaired defense behavior, e.g. impairing shoaling in fish. Alternatively, monoxenous parasites facilitate shoaling that is profitable for both parasites and hosts. Coordination of modified host behavior with the parasite life cycle, both temporal and spatial, is the most convincing criterion of the adaptive value of host manipulation.     

The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation

Numerous parasites with complex life cycles are able to manipulate the behaviour of their intermediate host in a way that increases their trophic transmission to the definitive host. Pomphorhynchus laevis, an acanthocephalan parasite, is known to reverse the phototactic behaviour of its amphipod intermediate host, Gammarus pulex, leading to an increased predation by fish hosts. However, levels of behavioural manipulation exhibited by naturally-infected gammarids are extremely variable, with some individuals being strongly manipulated whilst others are almost not affected by infection. To investigate parasite age and parasite intensity as potential sources of this variation, we carried out controlled experimental infections on gammarids using parasites from two different populations. We first determined that parasite intensity increased with exposure dose, but found no relationship between infection and host mortality. Repeated measures confirmed that the parasite alters host behaviour only when it reaches the cystacanth stage which is infective for the definitive host. They also revealed, we believe for the first time, that the older the cystacanth, the more it manipulates its host. The age of the parasite is therefore a major source of variation in parasite manipulation. The number of parasites within a host was also a source of variation. Manipulation was higher in hosts infected by two parasites than in singly infected ones, but above this intensity, manipulation did not increase. Since the development time of the parasite was also different according to parasite intensity (it was longer in doubly infected hosts than in singly infected ones, but did not increase more in multi-infected hosts), individual parasite fitness could depend on the compromise between development time and manipulation efficiency. Finally, the two parasite populations tested induced slightly different degrees of behavioural manipulation.     

Factor Affecting Sex Ratios of a Mermithid Parasite of Mosquitoes

The ratio of male to female Reesimermis nielseni Tsai and Grundmann, a nematode parasite of mosquito larvae, increased as the number of parasites per host increased. Hosts with a single nematode produced 9% males compared with essentially 100% males in hosts with more than 7 parasites; hosts with 3 nematodes produced about equal numbers of males and females. Males of R. nielseni generally emerged before females because of the earlier death of multiple-infected mosquitoes. The species of the host mosquito influenced the sex ratio, but the size of a specific host at the time of invasion did not. Host diet also had a noticeable influence on the sex ratio of the nematode: singly infected hosts from a starved population produced 92% males compared with 13% in the normally fed group. The importance of these factors in the mass rearing of R. nielseni is discussed.     

Competitive advantages of Caedibacter-infected Paramecia

Intracellular bacteria of the genus Caedibacter limit the reproduction of their host, the freshwater ciliate Paramecium. Reproduction rates of infected strains of paramecia were significantly lower than those of genetically identical strains that had lost their parasites after treatment with an antibiotic. Interference competition occurs when infected paramecia release a toxic form of the parasitic bacterium that kills uninfected paramecia. In mixed cultures of infected and uninfected strains of either P tetraurelia or of P novaurelia, the infected strains outcompeted the uninfected strains. Infection of new host paramecia seems to be rare. Infection of new hosts was not observed in either mixtures of infected with uninfected strains, or after incubation of paramecia with isolated parasites. The competitive advantages of the host paramecia, in combination with their vegetative reproduction, makes infection of new hosts by the bacterial parasites unnecessary, and could be responsible for the continued existence of "killer paramecia" in nature. Caedibacter parasites are not a defensive adaptation. Feeding rates and reproduction of the predators Didinium nasutum (Ciliophora) and Amoeba proteus (Amoebozoa, Gymnamoebia) were not influenced by whether or not their paramecia prey were infected. Infection of the predators frequently occurred when they preyed on infected paramecia. Caedibacter-infected predators may influence competition between Paramecium strains by release of toxic parasites into the environment that are harmful to uninfected strains.     

Persistence of Dactylogyrus eucalius (Monogenea: Dactylogyridae) on the short-lived host Culaea inconstans (Pisces: Gasterosteiformes)

The monogene Dactylogyrus eucalius Mizelle and Regensberger, 1945 and its ability to maintain a population from year to year on the annual fish Culaea inconstans Kirkland was examined in a small lake in central Ontario. Fish were sampled toward the end of their annual breeding season, at a time when the host population consisted of 2 cohorts, i.e., young-of-the-year (0+) and mature adults (1+). Prevalence of infection was 94%, with a mean intensity of 8.8 +/- 9.6; neither measure varied significantly with host length or between cohorts (P > 0.05). At necropsy, parasites were characterized as juveniles that included postoncomiracidia (immature, with a ventrally directed haptor) as well as developing protandrous males (body with a near-complete haptor and with little or no pigmented vitellaria), or as adults (with testis, ovarium, darkened vitellaria, and occasionally bearing a tanned egg). The proportion of juvenile to adult parasites differed significantly between cohorts (P < 0.05), with 0+ fish infected with a mixture of juveniles and adults, whereas 1+ fish had almost exclusively adult parasites. Since adult (1+) brook stickleback typically die after spawning, the increased frequency of juvenile parasites exploiting juvenile hosts may represent an evolutionary adaptation, maximizing the chances of parasites infecting hosts that will enter winter. It is suspected that 0+ fish can be infected in the nest within 2 wk of hatching and persist by effectively infecting new host recruits when they are sympatric with their parents.