Sexual selection in an isopod with Wolbachia‐induced sex reversal: males prefer real females

A variety of genetic elements encode traits beneficial to their own transmission. Despite their ‘selfish’ behaviour, most of these elements are often found at relatively low frequencies in host populations. This is the case of intracytoplasmic Wolbachia bacteria hosted by the isopod Armadillidium vulgare that distort the host sex ratio towards females by feminizing the genetic males they infect. Here we tested the hypothesis that sexual selection against Wolbachia‐infected females could maintain a polymorphism of the infection in populations. The infected neo‐females (feminized males) have lower mating rates and received less sperm relative to uninfected females. Males exhibited an active choice: they interacted more with uninfected females and made more mating attempts. A female behavioural difference was also observed in response to male mating attempts: infected neo‐females more often exhibited behaviours that stop the mating sequence. The difference in mating rate was significant only when males could choose between the two female types. This process could maintain a polymorphism of the infection in populations. Genetic females experimentally infected with Wolbachia are not exposed to the same sexual selection pressure, so the infection alone cannot explain these differences.     

Parasitized female mice display reduced aversive responses to the odours of infected males.

The present study showed that parasites influence both the responses of uninfected females to males and the responses of female hosts to infected males. In female laboratory mice one of the consequences of exposure to the olfactory cues associated with an infected male was a reduction of the reactivity to a thermal surface, i.e. pain inhibition or analgaesia. Uninfected oestrous and non-oestrous female mice displayed marked analgaesic responses after exposure to the odours of males infected with either the enteric single-host nematode parasite, Heligmosomoides polygyrus, or the protozoan parasite, Eimeria vermiformis. The uninfected oestrous females distinguished between infected and physically stressed males, displaying a greater analgaesic response to the odours of infected males. These analgaesic responses and their anxiety/ fearfulness-associated behavioural correlates could elicit either a reduced interest in, or avoidance of, parasitized males by females. Oestrous female mice infected with H. polygyrus displayed a reduced analgaesic response to the odours of the infected males and differentially responded to the odours of males infected with either the same (H. polygyrus) or a different parasite (E. vermiformis). An exposure time of 1 min elicited minimal responses to the odours of males infected with the same parasite, H. polygyrus, and an attenuated, though significant, non-opioid peptide-mediated analgaesic response to males infected with E. vermiformis. An exposure time of 30 min elicited similar markedly reduced endogenous opioid peptide-mediated analgaesic responses to the odours of both of the categories of infected males. The responses to the odours of a stressed male were, however, unaffected by the parasitic infection. The reduced analgaesic responses of the parasitized females to the odours of infected males may involve either enhanced odour familiarity and responses to group odour templates and/or neuromodulatory shifts resulting in reduced fearfulness and potentially greater interest in the infected males.     

Mate Choice in Captive American Kestrels,Falco sparverius,Parasitized by a Nematode,Trichinella pseudospiralis

The American kestrel (Falco sparverius) — Trichinella pseudospiralis host-parasite association was used as a laboratory model to study the effect of a nematode infection on (1) mate choice of female kestrels and (2) competitive abilities of male kestrels during the breeding season. Females were given the opportunity to choose between infected and uninfected males. There was no significant difference in the proportion of females that chose uninfected (n = 18) over infected (n = 16) males. Eight of 11 competitions between infected and uninfected males exposed to a caged female and a nest box were dominated by uninfected males. Female kestrels seemed to base their choices on the intensity of display effort by the males; the experimental level of infection did not affect male courtship behaviour. Although T. pseudospiralis is known to debilitate American kestrels, parasitized males in mate-choice tests may have diverted energy from less important functions to court the females.     

The impact of Wolbachia,male age and mating history on cytoplasmic incompatibility and sperm transfer in Drosophila simulans

Most insects harbour a variety of maternally inherited endosymbionts, the most widespread being Wolbachia pipientis that commonly induce cytoplasmic incompatibility (CI) and reduced hatching success in crosses between infected males and uninfected females. High temperature and increasing male age are known to reduce the level of CI in a variety of insects. In Drosophila simulans, infected males have been shown to mate at a higher rate than uninfected males. By examining the impact of mating rate independent of age, this study investigates whether a high mating rate confers an advantage to infected males through restoring their compatibility with uninfected females over and above the effect of age. The impact of Wolbachia infection, male mating rate and age on the number of sperm transferred to females during copulation and how it relates to CI expression was also assessed. As predicted, we found that reproductive compatibility was restored faster in males that mate at higher rate than that of low mating and virgin males, and that the effect of mating history was over and above the effect of male age. Nonvirgin infected males transferred fewer sperm than uninfected males during copulation, and mating at a high rate resulted in the transfer of fewer sperm per mating irrespective of infection status. These results indicate that the advantage to infected males of mating at a high rate is through restoration of reproductive compatibility with uninfected females, whereas uninfected males appear to trade off the number of sperm transferred per mating with female encounter rate and success in sperm competition. This study highlights the importance Wolbachia may play in sexual selection by affecting male reproductive strategies.     

Wolbachia affects oviposition and mating behaviour of its spider mite host

Wolbachia bacteria are transmitted from mother to offspring via the cytoplasm of the egg. When mated to males infected with Wolbachia bacteria, uninfected females produce unviable offspring, a phenomenon called cytoplasmic incompatibility (CI). Current theory predicts that ‘sterilization’ of uninfected females by infected males confers a fitness advantage to Wolbachia in infected females. When the infection is above a threshold frequency in a panmictic population, CI reduces the fitness of uninfected females below that of infected females and, consequently, the proportion of infected hosts increases. CI is a mechanism that benefits the bacteria but, apparently, not the host. The host could benefit from avoiding incompatible mates. Parasite load and disease resistance are known to be involved in mate choice. Can Wolbachia also be implicated in reproductive behaviour? We used the two‐spotted spider mite – Wolbachia symbiosis to address this question. Our results suggest that uninfected females preferably mate to uninfected males while infected females aggregate their offspring, thereby promoting sib mating. Our data agrees with other results that hosts of Wolbachia do not necessarily behave as innocent bystanders – host mechanisms that avoid CI can evolve.     

Parasite-related pairing success in an intermediate host, Caecidotea intermedius (Isopoda): effects of male behavior and reproductive physiology

The acanthocephalan parasite Acanthocephalus dirus develops from the egg to the cystacanth stage inside the freshwater isopod Caecidotea intermedius. We have shown previously that cystacanth-infected male C. intermedius are less likely to initiate mating attempts with females than uninfected males in competitive situations. Here, we used a field-based experiment to examine whether cystacanth-infected males were also less likely to initiate mating attempts with females in noncompetitive situations. We found that infected males were less responsive to females than uninfected males, and we propose that the cystacanth-related change in male mating behavior is mediated by a change in the mating response of males to females rather than male-male competition. We then examined whether cystacanth-related changes in reproductive function, i.e., sperm content and fertilization ability, could explain this variation in male mating behavior. We found that cystacanth-infected males contained both developing and mature sperm and fertilized as many eggs as uninfected males. Thus, we propose that changes in reproductive function are unlikely to explain cystacanth-related variation in male mating behavior in C. intermedius.     

Intrasexual mounting in the beetle Diaprepes abbreviatus (L.).

The weevil Diaprepes abbreviatus shows three kinds of same-sex mountings: males mount other unpaired males, males mount males already engaged in copulation and females mount other females. Four hypotheses were evaluated in order to explain same-sex matings by males: (i) female mimicry by inferior males, (ii) dominance of larger males which affects the behaviour of small males, (iii) sperm transfer in which smaller males gain some reproductive success by 'hitchhiking' their sperm with the sperm of larger males, and (iv) poor sex recognition. Data from mate choice and sperm competition experiments rejected the female mimicry, dominance and sperm transfer hypotheses and supported the poor sex recognition hypothesis. We tested three hypotheses in order to explain female mounting behaviour: (i) females mimic male behaviour in order to reduce sexual harassment by males, (ii) females mount other females in order to appear larger and thereby attract more and larger males for mating, and (iii) female mimicry of males. The results of our mate choice experiments suggested that the female mimicry of males hypothesis best explains the observed female mounting behaviour. This result is also consistent with the poor sex recognition hypothesis which is the most likely explanation for male and female intrasexual mating behaviour in many insect species.     

Effects of social experience on subsequent sexual performance in naïve male Japanese quail (Coturnix japonica)

On their first sexual encounter, naïve male Japanese quail will attend to and approach a female; they sometimes mount but they do not always copulate. During the second encounter, most males successfully copulate. Although sexual experience facilitates subsequent sexual interactions, sensory cues provided by females, independent of any sexual encounter, may also enhance sexual performance. To investigate whether previous exposure to a conspecific affects subsequent sexual behavior, we allowed inexperienced males to observe an empty box, or a conspecific consisting of either an experienced female or male for 2.5 min/day on 7 days. Measures of appetitive sexual behavior were recorded during these tests. On day 8, subjects were allowed to copulate with a novel female for 5 min. On the following days, all subjects were repeatedly provided with visual access to a female and allowed to mate. In the pre-copulatory trials males initially exhibited a high frequency of appetitive responses that dissipated with repetition. Pre-copulatory experience also significantly affected motivation to mate with subjects exposed to females copulating more quickly than other subjects. Post-copulatory appetitive behavior also differed between groups: control subjects showed the highest behavioral frequency followed by males exposed to females and finally males exposed to males. These data indicate that pre-copulatory social experience profoundly influences subsequent sexual behavior and probably reproductive success. This experience effect is independent of any hormonal effect (such as one resulting from changes in secretion following different social interactions) given that the subjects were castrates chronically treated with testosterone.     

Mating Status Effects on Sexual Response of Males and Females in the Parasitoid Wasp <Emphasis Type="Italic">Urolepis rufipes</Emphasis>

Although mate preferences are most commonly examined in females, they are often found in both sexes. In the parasitoid wasp Urolepis rufipes, both female and male mating status affected certain aspects of sexual interactions. Female mating status mattered only in the later stages of mating. Males did not discriminate between virgin and mated females in terms of which they contacted or mounted first. However, once mounted, most virgin females were receptive to copulation, whereas very few mated females were. Whether a male’s mating status affected his own sexual response depended on the female’s ability to respond and the stage of mating. Examining male behavior toward dead females allowed elimination of the role of female behavior in how males responded. Virgin and mated males are both attracted to dead females as evidenced by their fanning their wings at such females. However, mated males were quicker than virgin males to contact and to mount in an experiment with dead females, whereas there was no such differential response in an experiment with live females. This difference is consistent with greater female sexual responsiveness to virgin males. Male mating status also affected female receptivity to copulate. Once mounted, live virgin females were less likely to become receptive to copulation by mated males than to virgin males, but only in a choice experiment, not in a no-choice experiment.     

The effects of Trichinella spiralis infection on social interactions in mixed groups of infected and uninfected male mice

The presence of Trichinella spiralis infection in groups of male mice caused behavioural changes in both infected and uninfected mice. Also, for some behaviours, the extent of behavioural change in infected mice appeared to be determined by the number of muscle larvae they harboured. Infected mice showed a reduced frequency of exploratory and social behaviours compared with uninfected mice while uninfected mice performed more social investigatory activities towards those that were infected. Social interactions between infected and uninfected mice were also affected by familiarity. Behavioural differences shown to result from infection in mice familiar with each other were similar but more pronounced when the mice were unfamiliar. These results suggest that other factors may influence the behavioural effects of parasites on their hosts. For some behaviours, the greatest alterations in behaviour apparently caused by infection coincided with the period of infectivity to another host. The significance of this in relation to parasite transmission is considered.     

The effects of exposure to seaweed on willingness to mate, oviposition, and longevity in seaweed flies

Abstract  1. Large male seaweed flies (Diptera: Coelopidae) are more likely to mate than smaller males. This is due to sexual conflict over mating, by which females physically resist male attempts to copulate. In some species, large males are simply more efficient at overpowering female resistance.
2. Female reluctance to mate is likely to have evolved due to the costs of mating to females. In many dipterans, males manipulate female behaviour through seminal proteins that have evolved through sperm competition. This behavioural manipulation can be costly to females, for example forcing females to oviposit in sub-optimal conditions and increasing their mortality.
3. Previous work has failed to identify any ubiquitous costs of mating to female coelopids. The work reported here was designed to investigate the effects of exposure to oviposition sites ( Fucus algae) on the reproductive behaviour of four species of coelopid. Algae deposition in nature is stochastic and females mate with multiple males in and around oviposition sites. Spermatogenesis is restricted to the pupal stage and there is last-male sperm precedence. It was predicted that males would avoid wasting sperm and would be more willing to mate, and to remain paired with females for longer, when exposed to oviposition material compared with control males. Females were predicted to incur longevity costs of mating if mating increased their rate of oviposition, especially in the presence of algae.
4. The behaviour of males of all four species concurred with the predictions; however mating did not affect female receptivity, oviposition behaviour, or longevity. Exposure to algae induced oviposition and increased female mortality in all species independently of mating and egg production. The evolutionary ecology of potential costs of mating to female coelopids are discussed in the light of these findings.     

Sex‐dependent infection causes nonadditive effects on kissing bug fecundity

The influence of parasites on host reproduction has been widely studied in natural and experimental conditions. Most studies, however, have evaluated the parasite impact on female hosts only, neglecting the contribution of males for host reproduction. This omission is unfortunate as sex‐dependent infection may have important implications for host–parasite associations. Here, we evaluate for the first time the independent and nonindependent effects of gender infection on host reproductive success using the kissing bug Mepraia spinolai and the protozoan Trypanosoma cruzi as model system. We set up four crossing treatments including the following: (1) both genders infected, (2) both genders uninfected, (3) males infected—females uninfected, and (4) males uninfected—females infected, using fecundity measures as response variables. Interactive effects of infection between sexes were prevalent. Uninfected females produced more and heavier eggs when crossed with uninfected than infected males. Uninfected males, in turn, sired more eggs and nymphs when crossed with uninfected than infected females. Unexpectedly, infected males sired more nymphs when crossed with infected than uninfected females. These results can be explained by the effect of parasitism on host body size. As infection reduced size in both genders, infection on one sex only creates body size mismatches and mating constraints that are not present in pairs with the same infection status. Our results indicate the fitness impact of parasitism was contingent on the infection status of genders and mediated by body size. As the fecundity impact of parasitism cannot be estimated independently for each gender, inferences based only on female host infection run the risk of providing biased estimates of parasite‐mediated impact on host reproduction.     

Assortative pairing in Gammarus insensibilis (Amphipoda) infected by a trematode parasite

We have investigated the influence of Microphallus papillorobustus (Trematoda) on the reproductive biology and mating patterns of its intermediate host Gammarus insensibilis (Amphipoda). Infected Gammarus species show altered behaviour which renders them more susceptible to predation by Charadriiform birds, the parasite's definitive hosts. In a natural population of G. insensibilis, mean parasite intensity was higher for unpaired individuals than for paired individuals. Fecundity was reduced in infected amphipods. Size-assortative pairing was significant, although infected males were found with smaller females compared to uninfected males of the same size. There was also a positive assortative pairing by parasitic prevalence. Vertical segregation between infected and uninfected individuals, male-male competition for access to uninfected females, and female choice may explain assortative mating for prevalence. This study provides the first empirical evidence that parasites can have a direct effect on patterns of mating in gammarids.     

Learning decreases heterospecific courtship and mating in fruit flies

Recent theory and data suggest that adaptive use of learning in the context of sexual behaviour could contribute to assortative mating. Experiments examining this issue indicated that male Drosophila persimilis that experienced courtship and rejection by heterospecific females exhibited significantly lower levels of heterospecific courtship and mating compared with those of inexperienced males. These results indicate that experience in the context of sexual behaviour in fruit flies could reduce gene flow between diverging populations, which may contribute to incipient speciation.     

Increased male mating rate in Drosophila is associated with Wolbachia infection

The maternally inherited bacterium Wolbachia pipientis infects 25-75% of arthropods and manipulates host reproduction to improve its transmission. One way Wolbachia achieves this is by inducing cytoplasmic incompatibility (CI), where crosses between infected males and uninfected females are inviable. Infected males suffer reduced fertility through CI and reduced sperm production. However, Wolbachia induce lower levels of CI in nonvirgin males. We examined the impact of Wolbachia on mating behaviour in male Drosophila melanogaster and D. simulans, which display varying levels of CI, and show that infected males mate at a higher rate than uninfected males in both species. This may serve to increase the spread of Wolbachia, or alternatively, may be a behavioural adaptation employed by males to reduce the level of CI. Mating at high rate restores reproductive compatibility with uninfected females resulting in higher male reproductive success thus promoting male promiscuity. Increased male mating rates also have implications for the transmission of Wolbachia.     

Sexual functionality of Leptopilina clavipes (Hymenoptera: Figitidae) after reversing Wolbachia-induced parthenogenesis

Females infected with parthenogenesis-inducing Wolbachia bacteria can be cured from their infection by antibiotic treatment, resulting in male production. In most cases, however, these males are either sexually not fully functional, or infected females have lost the ability to reproduce sexually. We studied the decay of sexual function in males and females of the parasitoid Leptopilina clavipes. In western Europe, infected and uninfected populations occur allopatrically, allowing for an investigation of both male and female sexual function. This was made by comparing females and males induced from different parthenogenetic populations with those from naturally occurring uninfected populations. Our results indicate that although males show a decay of sexual function, they are still able to fertilize uninfected females. Infected females, however, do not fertilize their eggs after mating with males from uninfected populations. The absence of genomic incompatibilities suggests that these effects are due to the difference in mode of reproduction.     

Sexually transmitted disease and the evolution of mating systems

Sexually transmitted diseases (STDs) have been shown to increase the costs of multiple mating and therefore favor relatively monogamous mating strategies. We examine another way in which STDs can influence mating systems in species in which female choice is important. Because more popular males are more likely to become infected, STDs can counteract any selective pressure that generates strong mating skews. We build two models to investigate female mate choice when the sexual behavior of females determines the prevalence of infection in the population. The first model has no explicit social structure. The second model considers the spatial distribution of matings under social monogamy, when females mated to unattractive males seek extrapair fertilizations from attractive males. In both cases, the STD has the potential to drastically reduce the mating skew. However, this reduction does not always happen. If the per contact transmission probability is low, the disease dies out and is of no consequence. In contrast, if the transmission probability is very high, males are likely to be infected regardless of their attractiveness, and mating with the most attractive males imposes again no extra cost for the female. We also show that optimal female responses to the risk of STDs can buffer the prevalence of infection to remain constant, or even decrease, with increasing per contact transmission probabilities. In all cases considered, the feedback between mate choice strategies and STD prevalence creates frequency-dependent fitness benefits for the two alternative female phenotypes considered (choosy vs. randomly mating females or faithful vs. unfaithful females). This maintains mixed evolutionarily stable strategies or polymorphisms in female behavior. In this way, a sexually transmitted disease can stabilize the populationwide proportion of females that mate with the most attractive males or that seek extrapair copulations.     

Robust calling performance in frogs infected by a deadly fungal pathogen

Reproduction is an energetically costly behavior for many organisms, including species with mating systems in which males call to attract females. In these species, calling males can often attract more females by displaying more often, with higher intensity, or at certain frequencies. Male frogs attract females almost exclusively by calling, and we know little about how pathogens, including the globally devastating fungus, Batrachochytrium dendrobatidis, influence calling effort and call traits. A previous study demonstrated that the nightly probability of calling by male treefrogs, Litoria rheocola, is elevated when they are in good body condition and are infected by B. dendrobatidis. This suggests that infections may cause males to increase their present investment in mate attraction to compensate for potential decreases in future reproduction. However, if infection by B. dendrobatidis decreases the attractiveness of their calls, infected males might experience decreased reproductive success despite increases in calling effort. We examined whether calls emitted by L. rheocola infected by B. dendrobatidis differed from those of uninfected individuals in duration, pulse rate, dominant frequency, call rate, or intercall interval, the attributes commonly linked to mate choice. We found no effects of fungal infection status or infection intensity on any call attribute. Our results indicate that infected males produce calls similar in all the qualities we measured to those of uninfected males. It is therefore likely that the calls of infected and uninfected males should be equally attractive to females. The increased nightly probability of calling previously demonstrated for infected males in good condition may therefore lead to greater reproductive success than that of uninfected males. This could reduce the effectiveness of natural selection for resistance to infection, but could increase the effectiveness of selection for infection tolerance, the ability to limit the harm caused by infection, such as reductions in body condition.     

Sexual interaction in adult laboratory rats: importance of female's stimuli and of male's experience

Precopulatory behaviour of adult male rats towards the passively receptive and towards the ovariectomized females was observed in dyadic interaction, first, at the time when the males were sexually inexperienced and later on after they had gained small and uniform copulatory experience (with a darting female). It was found that precopulatory activity of the sexually inexperienced males towards the ovariectomized female was "higher and richer" than that of males exposed to the passively receptive female. When the males were sexually experienced the frequency of precopulatory behavior increased and the patterns changed only in the animals exposed to the passively receptive female. Precopulatory activity of males weakened during the interaction under all experimental conditions. It is remarkable, however, that the weakening of precopulatory activity of sexually inexperienced males exposed to the ovariectomized female was reinforced again after the female temporarily exhibited behaviour typical of the male. We concluded that both the quality of the female's precopulatory behaviour and the quantity of previous male's experience are the decisive factors in successful interaction.