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- Materials and methods
Fundamental biological differences between genders may explain why susceptibility to parasites often differs between females and males. First, sex-specific behaviour may affect exposure to parasites, one sex being more vulnerable than the other (Reimchen & Nosil 2001; Krasnov et al. 2005a). Such behaviours that increase the likelihood of becoming infected may be, for instance, aggressions between males for mating opportunities, decreased male grooming rate during the mating season (Mooring & Hart 1995; Mooring et al. 2006) or spatial aggregation within the members of one sex (Zuk & McKean 1996). Secondly, negative association between steroid hormones, particularly testosterone, and immune responses are thought to play a major role in this difference (Grossman 1985; Zuk 1990; Folstad & Karter 1992; Roberts, Buchanan & Evans 2004).
In this study, we take advantage of the particular social habit of bats to investigate whether spatial aggregation within the members of one sex favours differential susceptibility to parasites, eventually leading to preference for a given host sex in parasites. Females of most temperate zone bat species usually aggregate during the breeding season in nursery colonies, whereas males are mainly solitary and occupy satellite roosts (Lewis 1995). Colonial habits of female bats during reproduction favour vertical and horizontal parasite transmission (Christe, Arlettaz & Vogel 2000). Moreover high temperature of nursery roost sites, including the heat generated by tight associations among individuals in a colonial cluster, may favour parasites’ reproductive output (Marshall 1981). These two factors could lead to a strong sex-linked difference in the opportunity to become infested. Two recent studies have shown that under natural conditions, females of some temperate zone bat species have higher prevalence and intensity of parasitism than males and that these differences vary with season (Zahn & Rupp 2004; Lucan 2006). It remains unknown, however, whether differential encounter probability due to spatial aggregation selects for an active choice on more profitable hosts by the parasite.
Ectoparasitic mites of the genus Spinturnix represent a good model to investigate the effect of sex on host susceptibility to parasites. These parasites complete their entire life cycle on their hosts and are thus strictly dependent on close contact between individuals to disperse and infect new hosts (Rudnick 1960). Individual bats cannot be infected by Spinturnix while visiting empty roosts, contrary to other parasite taxa that undergo developmental stage irrespective of host presence (Lewis 1995; Reckardt & Kerth 2006). Randomly choosing a male as host could lead to a drastic reduction in reproductive success in an individual Spinturnix because, once installed on a male, dispersal opportunities are much lower than on a female. One would therefore expect a strong selection for female hosts in these parasites.
To assess whether parasites are able to actively select one, more profitable gender, we performed dual choice experiments with wild-caught bats kept for a while in captivity. Males and females Myotis daubentoni and the mite Spinturnix andegavinus were used as a model system. Host's nutritional status was standardized so as to remove any confounding factors as far as possible (Christe et al. 2003; Krasnov et al. 2005b).
Because temperate zone bats typically mate during the fall, testosterone reaches its highest level during an entire year cycle between mid summer and early autumn. One could therefore expect seasonal variation in parasite preference because parasites could take advantage of the immunosuppressor effect of testosterone for infecting males during mating when opportunities for parasite transmission between sexes are high.
Among juveniles prior to weaning, equal parasite loads should be observed in males and females due to similar behaviours and hormone profiles at that early life stage in the two genders. However, if mites have other cues than hormones to identify host sex at that young bat age, they should preferentially settle on females if exploiting female hosts increases their future survival prospect.
The aims of the present paper are thus manifold. We tested: (1) whether there is a natural bias in parasite prevalence and intensity between male and female hosts in five bat species; (2) whether juveniles within colonies harbour different parasite loads according to host sex; (3) if the patterns of parasite choice observed in natural conditions, with respect to host sex and/or sexual maturity, can be replicated under experimental laboratory conditions with captive bats; (4) if parasite choice fluctuates seasonally in laboratory conditions; and (5) if the mid-term survival functions of parasites differ with respect to host gender, this under experimental conditions where mites cannot switch between female and male hosts.
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- Materials and methods
The sex-biased parasitic load observed in this study is in accordance with previous results obtained from various ectoparasite species infesting European vespertilionid bats (Zahn & Rupp 2004; Lucan 2006). The present study adds data for two new, so far noninvestigated species, P. auritus and M. blythii. Female bats have thus higher ectoparasite prevalence than males, which strikingly contrasts with the pattern observed in other vertebrate taxa (Poulin 1996; Klein 2004; Morand et al. 2004; Amo et al. 2005; Krasnov et al. 2005b). We could further experimentally demonstrate that parasites contribute to this bias by actively selecting female host. Therefore, if differences in host's exposure to parasitism remain a key factor for explaining sex-biased parasitic load, strong selection for sex recognition within Spinturnix species has evolved as evidenced here by our survival experiments, which established that settling on females strongly increases parasite survival prospect.
Sex bias in parasite rate most likely stems from sex-specific differences in host social behaviour, with female aggregation during the reproductive period being likely to play a central role for the evolution of this pattern. In a previous study (Christe et al. 2000), we have demonstrated that Spinturnix myoti show a strong preference for hosts with either low behavioural antiparasite defences (juveniles), or lowered cell-mediated immunity (reproductive females over non-reproductive females). Thus, a combination of immunosuppression during reproduction and aggregation in nursery colonies facilitates both horizontal and vertical parasite transmission among favourable hosts. Male solitary lifestyle decreases transmission probability of Spinturnix, which in turn may result in adaptive parasite choice. Moreover, sex-specific thermal roosting conditions in most temperate-zone bat species may be an additional important factor, with the high temperature prevailing in nursery roosts potentially boosting parasite transmission and reproduction (Solick & Barclay 2006). However, in the case of Spinturnix spp., which complete their entire life cycle on the host, abiotic factors are likely to play a minor role, contrary to biotic factors. Biotic factors concern mainly bats’ peculiar physiology. In effect, bats aggregating in reproductive clusters remain the whole day homeothermic. This enables them to sustain a high metabolism, thereby maximizing embryo growth and lactation. In contrast, non-reproductive females and males, especially when roosting solitarily, enter regular phases of torpor, even during the summer (Kurta & Kunz 1988). These phases of lethargy would correspondingly slow down the metabolism of ectothermic ectoparasites such as mites.
The difference in parasitism could be attributed to differences in grooming rate between males and females. Because grooming activity is energetically costly (Giorgi et al. 2001), mothers may reduce grooming activity, which is traded-off against other components of maternal care (McLean & Speakman 1997). Consistent with this hypothesis, it has been shown that reproductive female bats groom less than non-reproductive females (McLean & Speakman 1997). Similarly, rutting male impalas and bisons engage in much less grooming than females, presumably to increase vigilance towards herding females and bachelor males (Mooring & Hart 1995; Mooring et al. 2006). Although we cannot exclude differential, sex-specific grooming rate in most situations in this study, grooming ability – or at least its efficiency – was certainly hampered if not totally suppressed in the flat, small-sized boxes we used for our dual choice experiments. Overall, if males would be more inclined than females to perform grooming, this would further bias parasite adaptive preference for females; the pattern observed would thus in no case be reversed but reinforced.
Gender differences in parasite infestation have also been attributed to possible resource-based trade-offs between growth and immunity in species with sexual dimorphism (Sheldon & Verhulst 1996; Møller, Sorci & Erritzøe 1998; Zuk & Stoehr 2002; Tschirren, Fitze & Richner 2003) and/or to the immunosuppressive effect of androgens, particularly in species with a high level of sexual selection (Alexander & Stimson 1988; Zuk 1990). The five bats species studied here all exhibited sexual size dimorphism in favour of females. Our findings thus conform to the pattern observed in a comparative analysis, which revealed that mammal species in which the female is the larger sex exhibit female-biased parasitism, whereas the opposite trend is found when males are the larger sex (Moore & Wilson 2002). We could thus not exclude the possibility that during growth, females allocate resources differently than males. This difference in resource allocation would lead to difference in future sex-specific defences against parasites.
Mites survived better and reproduced significantly better on females than on males. As suggested by the outcome of our experiments, sex-biased parasitism observed in free-ranging bats would be a mere consequence of both parasite preference and differential survival according to host status. Male and female bats seem to represent different types of hosts and thus parasites may evolve ‘habitat’ choice strategies to infect better quality hosts (Gandon 2004; Hawlena, Abramsky & Krasnov 2005). Male and female noctule bats spend the winter in common hibernation roosts. Despite close body contact during this long period of inactivity, we found a significant difference in prevalence and intensity of parasites already soon after the end of the hibernating period (Table 1). This suggests a permanently readjusted, active choice on the side of the parasites. Previous experiments had demonstrated that Spinturnix are able to precisely detect, and select almost immediately, the ‘right’ host, i.e. their native host species (Giorgi et al. 2004). In addition, individual hosts with an excellent nutritional status were at once recognized and chosen (Christe et al. 2003). As there is no clear sexual dimorphism (e.g. partial fur coverage on the wings of one sex only), i.e. no external recognition signal usable by the parasite, steroid level is the most probable candidate as regards host selection cues. In this respect, we speculate that hormone concentrations could indirectly translate into differential (e.g. sex specific) metabolic rates that might theoretically be detected by body temperature or other biochemicals (Osterkamp et al. 1999). In the absence of appropriate tests, however, the stimuli involved in host sex recognition remain unknown.
In our choice experiments, we first found marked seasonal effects in host selection, with strong female preference at the beginning of the season and random choice during the mating period. During mating, testosterone levels are high in males, and this period also corresponds to a high probability of transmission of parasites between males and females due to the constitution of pairs in the mating alcoves. Second, we could document a random choice between adult females and sexually immature, subadult males. These results support the hypothesis of subtle cues used by Spinturnix for host selection. In natural populations of M. daubentoni, prevalence in adult females (94·5%) was significantly higher than in subadult females (83·4%). The inverse was true for males with a prevalence of 60·8% on subadults, vs. 35·4% on adults.
There was no difference in parasite intensities between juveniles of either sex within colonies, probably due to similar parasite exposure and identical hormone profiles at this early stage of life. A similar result has been shown for juvenile M. daubentoni (Lucan 2006). These two studies are thus in accordance with two studies on juvenile birds (Møller et al. 1998; Bize et al. 2005) but contrast with a study on great tit nestlings in which males showed a reduced cellular immunity (Tschirren et al. 2003).
In conclusion, this study adds to the exceptions to the female host supremacy paradigm in parasitic infections of mammals (Morales-Montor et al. 2004) as it reveals distinct female-biased parasitism in five different bat species. The particular social life of bats, compared with other mammals on which most host–parasite studies have been carried out so far, is likely to imply different selective pressures leading to a largely female-biased parasite preference. For hosts, this difference in parasite susceptibility is expected to select for different life-history traits according to sex. For parasites, our results suggest first that male and female hosts represent different types of ‘habitats’, and, second, that parasites have evolved subtle cues to detect and infest better quality hosts under most circumstances.