Sexual ornamentation relates to immune function in male red grouse Lagopus lagopus scoticus

Sexual ornaments may enable females to discriminate amongst potential mates and choose those having either fewer parasites, or those which are more immunocompetent, or better able to cope with parasites. Tetraonid birds exhibit supra-orbital combs that function in both intra-sexual competition and mate choice. Through a correlative and experimental approach we investigated whether comb size of male red grouse Lagopus lagopus scoticus was related to infection intensity by their main parasite, the gastro intestinal nematode Trichostrongylus tenuis , and to immune function. We first looked at the relationships between immune function, parasite infection and condition. We found that spleen mass, an indirect measure of immune response, correlated positively with T. tenuis load, and negatively with condition. Cell-mediated immunity, a measure of immune defence, correlated positively with condition, and although not significantly related to T. tenuis load, increased when nematode parasites were experimentally reduced. Secondly, we investigated whether comb size was related to condition, T. tenuis load or immune function. Comb size was not significantly related to T. tenuis infection and did not change significantly after nematode parasite removal. However, males with bigger combs were in better condition, had a lighter spleen, a lighter spleen than expected from their T. tenuis load and had greater cell-mediated immunity. The findings suggest that comb size relates to immune function rather than T. tenuis parasite infection intensity. Males with bigger combs are likely to be of higher phenotypic quality because they are more immunocompetent and might be better able to cope with the detrimental effects of parasites.     

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

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

Different mate preferences by parasitized and unparasitized females potentially reduces sexual selection

Parasite‐mediated models of sexual selection predict that females should avoid parasitized mates, thereby generating selection on male traits revealing health. The strength of this selection, however, may depend on the prevalence of parasitism among females if their infection status alters their mate preferences. We evaluated the effects of a socially transmitted parasite on male traits and female behaviour in spadefoot toads. Parasitized males were larger and in better condition than unparasitized males. Moreover, better condition males produced longer calls. Unparasitized females preferred longer calls indicative of good‐condition males that are more likely parasitized. By contrast, parasitized females as a group possessed no preference for call duration. Presumably because of reduced selection by these parasitized females, male mating success was not associated with any measured traits. Thus, when females are parasitized, sexual selection on condition‐dependent traits is potentially reduced.     

Age‐related parasite load and longevity patterns in the sedge warbler Acrocephalus schoenobaenus

We report the results from a nine‐year study on parasite infection in males of a small migrant passerine, the sedge warbler Acrocephalus schoenobaenus. Every year, for each male caught during territory establishment we estimated infection intensity of two lineages of Haemoproteus belopolskyi (SW1 and SW3), using molecular methods. We found a significant relationship between infection intensity and males’ longevity in both studied lineages. There was severe mortality of second‐year sedge warblers after their first breeding season, with lower parasite load in survivors. The lower infection intensity in older age classes was related to between‐individual change in both lineages, but was also a result of differences in infection intensity during the lifetime of individual males in the SW3. The relation between parasite load and longevity suggests that parasite load may be an age‐dependent factor influencing individual survival.     

Effects of a parasitic nematode on male mate choice in a livebearing fish with a coercive mating system (western mosquitofish, Gambusia affinis)

I examined the effects of the parasitic larval nematode, Eustrongylides ignotus, on male mate choice in the western mosquitofish, Gambusia affinis. I hypothesized that parasite presence influences male mate choice either directly (via reduction in male mating behavior due to presence of parasite in females) or indirectly (via reduction in male mating behavior due to reduced condition of infected females). Specifically, I tested the predictions that (1) males would mate preferentially with uninfected over infected females (scoring both mating attempts and association time with females); (2) parasitized females would be in poorer condition than non-parasitized females (measured as soluble fat stores); and (3) parasitized females would have reduced fecundity (measured as number of developing embryos). Males preferred to mate with non-parasitized over parasitized females, but showed no differences in association time between females. The nematode did not decrease female body condition, but did decrease female mass, and appeared to decrease female fecundity via reduction in broods (# embryos). Results support that parasites affect male mate choice in mosquitofish; however, the mechanisms used by males to differentiate between parasitized and non-parasitized females remain untested. This study provides the first empirical evidence of parasite affects on male mate choice in livebearing fishes, and suggest a potentially important role for parasite-mediated sexual selection in organisms that use coercive mating as the primary mechanism of obtaining mates.     

ABSOLUTE VERSUS RELATIVE MEASUREMENTS OF SEXUAL SELECTION: ASSESSING THE CONTRIBUTIONS OF ULTRASONIC SIGNAL CHARACTERS TO MATE ATTRACTION IN LESSER WAX MOTHS,ACHROIA GRISELLA (LEPIDOPTERA: PYRALIDAE)

When females choose a mate among a group of signaling males concentrated in a small area, a male's mating success is often determined not only by his absolute attractiveness but by the attractiveness of his neighbors as well. Multivariate analyses of sexual selection measurements based on absolute values of predictor variables are then misleading, because such analyses assume that the fitness of a given individual is not influenced by others. We addressed this problem of relative fitness in sexual selection by developing two adjustments of the predictor variables in the multivariate analyses by including group means in addition to absolute values and by using relative values, deviations from group means. In the lesser wax moth, Achroia grisella (Lepidoptera: Pyralidae), aggregated males produce ultrasonic signals attractive to females in the vicinity of honey bee colonies. Playback experiments showed that females prefer signals whose pulses are louder, longer, delivered at a faster rate, and include lengthy silent gaps within pulse pairs (long asynchrony intervals). To measure sexual selection on ultrasonic signals, attractiveness was assessed by observing the number of females orienting toward given males in four-choice trials. The various signal characters of the males were computed from ultrasound recordings. Multivariate regression and nonparametric analyses revealed that peak amplitude, asynchrony interval, and pulse rate were the direct targets of selection. Nonlinear stabilizing and correlational selection were also detected. Comparisons of results from multivariate analyses based on absolute values and on the two relative adjustments indicated that the quality of a four-male group did not affect the strength or direction of linear selection but changed the strength of nonlinear selection. Both relative adjustments improved the prediction of male attractiveness. Three-dimensional surface plots generated by the nonparametric regression analyses showed that attractiveness increased monotonically with any combination of the signal characters. This graphical technique also showed that female choice in A. grisella was based on a relative, as opposed to a threshold, decision rule. Overall, male attractiveness for the population remained consistent between testing days. However, attractiveness values for some individual males changed between successive testing days. In these cases, the change in attractiveness was related only to the change in peak amplitude.     

HOW CAN SEX RATIO DISTORTERS REACH EXTREME PREVALENCES? MALE‐KILLING WOLBACHIA ARE NOT SUPPRESSED AND HAVE NEAR‐PERFECT VERTICAL TRANSMISSION EFFICIENCY IN ACRAEA ENCEDON

Abstract.— Maternally transmitted bacteria that kill male hosts early in their development are found in many insects. These parasites typically infect 1–30% of wild females, but in a few species of insects, prevalences exceed 95%. We investigated one such case in the butterfly Acraea encedon , which is infected with a male-killing Wolbachia bacterium. We measured three key parameters that affect the prevalence of the parasite: transmission efficiency, rate of survival of infected males, and the direct cost of infection. We observed that all wild females transmit the bacterium to all their offspring and that all infected males die in wild populations. We were unable to detect any physiological cost to infection in lab culture. These observations explain the high prevalence of the A. encedon male killer, as theory predicts that under these conditions the parasite will spread to fixation. This will occur provided the death of males provides some benefit to the surviving infected females. The problem therefore becomes why the bacterium has not reached fixation and driven the butterfly extinct due to the shortage of males. We therefore investigated whether males choose to mate with uninfected rather than infected females, as this would prevent the bacterium from reaching fixation. We tested this hypothesis in the "lekking swarms" of virgin females found in the most female-biased populations, and were unable to detect any evidence of mate choice. In conclusion, this male killer has spread to high prevalence because it has a high transmission efficiency and low cost, but the factors maintaining uninfected females in the population remain unknown.     

Ultra-violet reflectance of male and female red grouse, Lagopus lagopus scoticus, sexual ornaments reflect nematode parasite intensity

In many birds, females prefer males with the biggest or brightest sexual ornaments, which might reflect a higher phenotypic quality, such as fewer parasites. Unlike humans, most birds detect near-ultraviolet (UV) light, and UV signals can play an important role in sexual signalling and mate choice. Using a spectrophotometer, we analysed the colour of red grouse Lagopus lagopus scoticus sexual ornaments (their combs). We first show that combs reflect both in the red (600–700 nm) and UV (300–400 nm) part of the spectrum. Second, we investigated whether comb size and colour, and UV reflectance in particular, reflected an aspect of individual quality: the intensity of infection by a main nematode parasite, the caecal threadworm Trichostrongylus tenuis . We first analysed comb size and colour variation, and parasite intensity variation, in relation to sex and age. Males had bigger and redder combs than females, but UV brightness was greater for female than for male combs. Comb colour also differed between age groups, with young birds of both sexes showing brighter UV than old birds. Young grouse also had fewer T. tenuis worms than old grouse. We further tested whether intensity of infection could be predicted from comb characteristics (size and colour) in male and female red grouse. We found that parasite intensity was not significantly related to comb size or red brightness, but fewer worms were predicted from brighter UV in combs, in both males and females. The results indicate that UV reflectance of combs have a quality revealing function and might play an important role in grouse mate choice: UV brightness of combs could enable both male and female red grouse to assess the parasite loads of a potential mate.     

Parasites and Bright Male Plumage in the Satin Bowerbird (Ptilonorhynchus violaceus)

Results from our field studies of the satin bowerbird (Ptilonorhynchusviolaceus) suggest that females choose males as mates basedon their level of infection with the ectoparasite (Myrsideaptilonorhynchi: Menoponidae). We evaluated predictions fromthree hypotheses for why this pattern of choice might evolve.The bright male and correlated infection models both suggestthat females choose parasite free males because these malesare more likely to sire parasite resistant offspring. The brightmale hypothesis suggests that females are able to gauge infectionbased on plumage brightness. The correlated infection hypothesisclaims that females assess resistance to endoparasites througha correlated effect on ectoparasites. In the parasite avoidancemodel female choice is shaped by the proximate benefits of avoidinginfection. Six predictions from these models were tested usinginformation on patterns of infection in satin bowerbirds. Ofthese models the parasite avoidance model was best supportedby the available data.     

Epizootiology of blood parasites in an Australian lizard: a mark-recapture study of a natural population

The dynamics of a naturally endemic blood parasite (Hepatozoon hinuliae) were studied in a lizard (Eulamprus quoyii) host population, using 2 years of longitudinal data. We investigated how parasite abundance in the population varied over time, examined whether certain host sub-populations were more prone to infection, and compared parasite loads in relation to host reproductive behaviour. We recorded blood parasite infections of 331 individuals, obtained in 593 captures. Prevalence (the proportion of the host population infected) of blood parasites was high; approximately 66% of the lizard population was infected. Probability of infection increased with host age and size, but did not differ between the sexes. Within individuals, parasite load (the intensity of infection within individuals) did not vary over time, and was independent of host reproductive behaviour. Parasite load was significantly higher in males compared to females.     

Male-biased parasitism by common helminths is not explained by sex differences in body size or spleen mass of breeding cormorants Phalacrocorax auritus

In vertebrates, males are often more parasitised than conspecific females. This bias in parasitism might result from sex differences in parasite exposure and/or susceptibility to infection. Such information is important for testing hypotheses about allocation of resources to life histories of males and females and for testing hypotheses about factors thought to influence parasite fitness and parasite dynamics. We tested whether double-crested cormorants Phalacrocorax auritus exhibit male-biased parasitism by gut helminths. The prevalence of nematode Contracaecum spp. and trematode Drepanocaphalus spathans infections was ∼90% and 39%, respectively. Cestode, primarily Paradilepis caballeroi and acanthocephalan Andracantha gravida infections were less common (<10%). Male and female cormorants did not differ in prevalence of infection by any helminth species. However, males had twice the abundance and intensity of Contracaecum spp. infections and twice the intensity of D. spathans infections than found in females. For common parasites showing male-biased parasitism, degree of parasitism was also unrelated to body size or mass in either sex. Males and females did not differ in spleen mass and spleen mass was unrelated to abundance of common parasites. Furthermore, abundance of trematodes and nematodes was not correlated. At present, male biases in parasitism by nematodes and trematodes in cormorants are independent patterns that remain unexplained, but are most likely attributable to sex differences in exposure and/or immunological differences not yet assessed.     

艾美耳球虫对高原鼠兔繁殖的影响

寄生物对宿主繁殖的影响取决于宿主对当前繁殖值和剩余繁殖值的权衡。球虫为微型寄生物,而微型寄生物对宿主当前繁殖值的影响较剩余繁殖值要大。因此,本研究检验了寄生在高原鼠兔肠道内的艾美耳球虫可影响其当前繁殖的假设。在繁殖早、中、晚期,野外共观测高原鼠兔170只。结果表明,不同繁殖期感染率有显著差异。在繁殖中期,未感染雌性的妊娠率显著高于感染雌性。且未妊娠雌性较妊娠雌性有更高的感染强度,但在另外两个繁殖期没有发现此效应。在雄性中,任何繁殖期的感染强度和感染率与睾丸和附睾指数均无显著相关性,且感染和未感染球虫雄性睾丸及附睾指数无显著差异。此外,野外观测实验结果表明,感染雌性的胚胎重较未感染雌性显著降低,与野外感染对胚胎重量影响的实验结果相一致。说明艾美耳球虫感染可影响胚胎的发育。上述结果说明,艾美耳球虫对高原鼠兔繁殖的影响随繁殖期而有不同效应,且存在性别间差异,这种效应可能与不同性别间的繁殖对策有关。     

Common Wall Lizard Females (Podarcis muralis) do not Actively Choose Males Based on their Colour Morph

Identifying the processes that lead to the evolution and maintenance of links between colour morphs and behavioural strategies has implications for the evolution of reproductive isolation and sympatric speciation. Sexual selection may play a significant role in the evolution of colour pattern complexity in reptiles, particularly when there are fitness consequences associated with mating with males of different colour morphs. In this article, we explored if common wall lizard females (Podarcis muralis) actively select males according to their morph in a colour‐assortative pattern using a multiple‐choice experiment with both visual and chemical cues. We failed to identify female active mate choice, as females did not choose males based on male colouration or femoral pore secretions. Indeed, females equally entered the three preference compartments and spent nearly the same amount of time within them, irrespective of both colour and odour of males. Consequently, our results do not support the hypothesis that colour polymorphism in this species may be driven by colour‐assortative mating promoted by females. However, we cannot exclude the possibility that females may choose males according to their colour following a flexible choice strategy, nor the possibility that females actively discriminate among males according to qualities that are not directly related to morph‐specific strategies.     

Pheromonal markers as indicators of parasite load: parasite-mediated behavior in salamanders (Plethodon angusticlavius)

Assessment of parasite load of conspecifics may be important during social interactions such as courtship and aggressive encounters. We used a correlational study to test whether pheromonal markers can be used to assess parasite load of conspecifics, and whether the parasite load of the pheromone receivers affected their responses. We tested the responses of parasitized and nonparasitized Ozark zigzag salamanders, Plethodon angusticlavius, to territorial markers (fecal pellets) from conspecific males. Males and females were simultaneously exposed to fecal pellets placed in front of two artificial burrows located at the opposite ends of their chambers. The treatments were (1) fecal pellet of male with low parasite load versus fecal pellet of male with high parasite load, (2) fecal pellet of male with low parasite load versus control pellet (chemical blank), and (3) fecal pellet of male with high parasite load versus control pellet. Nonparasitized females spent significantly more time near fecal pellets of males with low parasite load in test condition 1, whereas the behavior of parasitized females was not significantly different from random in any test condition. Males responded differently to treatments only in condition 3; males with low parasite loads spent significantly more time near control pellets, whereas males with high parasite loads spent significantly more time near fecal pellets of males with high parasite loads. This study demonstrates that pheromonal markers may be used for assessment of parasite load of conspecifics and that responses by both males and females may be influenced by their own level of infection. Received: 21 January 1999 / Received in revised form: 17 March 2000 / Accepted: 13 November 2000     

Reduced blood parasite prevalence with age in the Seychelles Warbler: selective mortality or suppression of infection?

Avian malaria can affect survival and reproduction of their hosts. Two patterns commonly observed in birds are that females have a higher prevalence of malaria than do males and that prevalence decreases with age. The mechanisms behind these patterns remain unclear. However, most studies on blood parasite infections are based on cross-sectional analyses of prevalence, ignoring malaria related mortality and individual changes in infection. Here, we analyse both within-individual changes in malaria prevalence and long-term survival consequences of infection in the Seychelles Warbler (Acrocephalus sechellensis). Adults were less likely to be infected than juveniles but, contrary to broad patterns previously reported in birds, females were less likely to be infected than males. We show by screening individual birds in two subsequent years that the decline with age is a result both of individual suppression of infection and selective mortality. Birds that were infected early in life had a lower survival rate compared to uninfected birds, but among those that survived to be screened twice the proportion of infected birds had also decreased. Uninfected birds did not become infected later in life. Males were found to be more infected than females in this species possibly because, unlike most birds, males are the dispersing sex and the cost of dispersal may have to be traded against immunity. Infected males took longer to suppress their infection than did females. We conclude that these infections are indeed costly, and that age-related patterns in blood parasite prevalence are influenced both by suppression and selective mortality.     

Environmental conditions influence red grouse ornamentation at a population level

Theory suggests that condition‐dependent sexual displays should be more weakly expressed under adverse conditions than under more favourable ones. Here, we tested this hypothesis in wild red grouse Lagopus lagopus scoticus using a data set of nearly 1500 individuals from nine populations over 8 years, covering varying environmental conditions. We analysed whether male and female ornament expression (i.e. comb size) in a given site and year varied with various indices of environmental conditions: population density, Trichostrongylus tenuis nematode infection at the population level, and climate conditions [measured as winter North Atlantic oscillation (NAO) index]. We found that average comb size in males, but not in females, negatively correlated with population density, parasite infection levels, and winter NAO index. Furthermore, the coefficient of variation (CV) of comb size was higher in females than in males. CVs in both males and females were not clearly associated with the studied environmental variables. Our results support the idea that the expression of condition‐dependent sexual traits should be lower under more stressful environmental conditions, but only in males. We discuss the potential reasons behind the effect of environmental conditions on secondary sexual traits, and why these effects differ between sexes. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Do male hoots betray parasite loads in Tawny Owls?

Bird song structure may honestly reveal the health and vigour of individual males to potential mates and competitors. If this is the case then song may reflect the level of parasitic infections in males. We initially examined the relationship between blood parasite infections and the time taken to respond by 22 male Tawny Owls to a broadcast hoot. We then examined the call structure (total length and frequency) in relation to parasite infection, an index of owl condition and an index of food abundance. Owls with higher parasite loads responded more slowly to an intruder, although this relationship was not significant once condition and vole abundance were controlled for. We found no relationship between call length and any of the measured variables. However, the high frequency and the range of frequencies used in calls decreased with increasing parasite load. Thus, there was the potential for individuals to assess male parasite load from the speed of response and the structure of the call. Experimental tests of these relationships are now required.     

Migration distance does not predict blood parasitism in a migratory songbird

Migration can influence host–parasite dynamics in animals by increasing exposure to parasites, by reducing the energy available for immune defense, or by culling of infected individuals. These mechanisms have been demonstrated in several comparative analyses; however, few studies have investigated whether conspecific variation in migration distance may also be related to infection risk. Here, we ask whether autumn migration distance, inferred from stable hydrogen isotope analysis of summer‐grown feathers (δ²H_f) in Europe, correlates with blood parasite prevalence and intensity of infection for willow warblers (Phylloscopus trochilus) wintering in Zambia. We also investigated whether infection was correlated with individual condition (assessed via corticosterone, scaled mass index, and feather quality). We found that 43% of birds were infected with Haemoproteus palloris (lineage WW1). Using generalized linear models, we found no relationship between migration distance and either Haemoproteus infection prevalence or intensity. There was spatial variation in breeding ground origins of infected versus noninfected birds, with infected birds originating from more northern sites than noninfected birds, but this difference translated into only slightly longer estimated migration distances (~214 km) for infected birds. We found no relationship between body condition indices and Haemoproteus infection prevalence or intensity. Our results do not support any of the proposed mechanisms for migration effects on host–parasite dynamics and cautiously suggest that other factors may be more important for determining individual susceptibility to disease in migratory bird species.     

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

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

     

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.