The Sicker Sex: Understanding Male Biases in Parasitic Infection,Resource Allocation and Fitness

The “sicker sex” idea summarizes our knowledge of sex biases in parasite burden and immune ability whereby males fare worse than females. The theoretical basis of this is that because males invest more on mating effort than females, the former pay the costs by having a weaker immune system and thus being more susceptible to parasites. Females, conversely, have a greater parental investment. Here we tested the following: a) whether both sexes differ in their ability to defend against parasites using a natural host-parasite system; b) the differences in resource allocation conflict between mating effort and parental investment traits between sexes; and, c) effect of parasitism on survival for both sexes. We used a number of insect damselfly species as study subjects. For (a), we quantified gregarine and mite parasites, and experimentally manipulated gregarine levels in both sexes during adult ontogeny. For (b), first, we manipulated food during adult ontogeny and recorded thoracic fat gain (a proxy of mating effort) and abdominal weight (a proxy of parental investment) in both sexes. Secondly for (b), we manipulated food and gregarine levels in both sexes when adults were about to become sexually mature, and recorded gregarine number. For (c), we infected male and female adults of different ages and measured their survival. Males consistently showed more parasites than females apparently due to an increased resource allocation to fat production in males. Conversely, females invested more on abdominal weight. These differences were independent of how much food/infecting parasites were provided. The cost of this was that males had more parasites and reduced survival than females. Our results provide a resource allocation mechanism for understanding sexual differences in parasite defense as well as survival consequences for each sex.     

Are sexes equally parasitized in damselflies and dragonflies?

Parasitism plays an essential part in ecology and evolution of host species and understanding the reasons for differential parasitism within and among hosts species is therefore important. Among the very important factors potentially affecting parasitism is the gender of the host. Here, we studied whether either females or males are more likely to harbour parasites among Odonatan insects, by relying on an extensive literature review and new field data. We collected data on numerous dragonfly and damselfly species and their ectoparasites (water mites) and endoparasites (gregarines) to examine the generality of similarities and differences in prevalence, intensity and maximum number of parasites of male and female hosts. We found three main results. Firstly, most of the odonate host species showed no differences between sexes in either gregarine or water mite prevalence and intensity. The only exception was female damselflies’ higher gregarine prevalence and intensity compared to conspecific males. These inequalities in gregarine parasitism may be due to behavioral and physiological differences between conspecific males and females. In comparison, there were no differences in dragonflies between sexes in water mite or gregarine prevalence and intensity. Secondly, damselflies had higher prevalence and intensity levels of both gregarine and water mite parasites compared to dragonflies. Finally, we found a strong species level pattern between female and male parasitism: a certain level of gregarine or water mite parasitism in one sex was matched with a similar parasitism level for the other. This indicates similar exposure and susceptibility to parasites on both sexes. Even though significant differences of parasite levels between the sexes were observed within certain host species, our results strongly suggest that on a general level a more parasitized sex does not exist in the order, Odonata.     

No Correlation Between Ectoparasitism and Male Mating Success in a Damselfly: Why Parasite Behavior Matters

The mating success of individually marked male damselflies parasitized by water mites was closely followed. The number of ectoparasites could be determined exactly from knowledge of the parasite's life cycle. In contrast to previous studies, no correlation between water mite infestation and male mating success was revealed. The reasons for this discrepancy may be explained by the inclusion of the parasite's behavior. The body fat content of the males was negatively correlated with the mite load, indicating that parasitism reduces host's condition. It is hypothesised that the water mites damselfly system is not valuable for testing the Hamilton and Zuk hypothesis. Furthermore, selection exerted or mediated by parasites should act during the teneral phase.     

Sexual conflict and female immune suppression in the cricket, Allonemobious socius

In many animal systems, females exhibit a localized immune response to insemination that helps defend against sexually transmitted disease. However, this response may also kill sperm, reducing a male's reproductive potential. If males could suppress this response, they may be able to increase their sperm's representation in the female's reproductive tract, thereby increasing their fitness. Here we address the hypothesis that, under conditions of sperm competition, males interfere with female immunity. To test our hypothesis, we manipulated levels of female mating frequency (single vs. multiply mated) and seminal diversity (monandrous vs. polyandrous) in the cricket, Allonemobius socius and measured female immune response. As mating frequency increased, female hemocyte load decreased, indicating a general reproductive cost. As seminal diversity increased, phenoloxidase (PO) activity (in vitro measure of 'potential' macroparasitic defense) increased and encapsulation ability (in vivo measure of 'realized' macroparasitic defense) decreased in polyandrous females. These results suggest that males may manipulate female immunity by interrupting the pro-PO cascade, which begins with the activation of PO and ends in the encapsulation of invading foreign bodies. In other words, female immune function may serve as a battleground over which a sexual conflict is fought.     

Ontogenetic colour change signals sexual maturity in a non-territorial damselfly

Conspicuous colouration increases male reproductive success through female preferences and/or male–male competition. Despite the advantages of conspicuous colouration, inconspicuous male morphs can exist simultaneously in a population due to genetic diversity, condition dependence or developmental constraints. We are interested in explaining the male dichromatism in Xanthagrion erythroneurum damselflies. We reared these damselflies in outdoor insectaries under natural conditions and showed that this species undergoes ontogenetic colour changes. The younger males are yellow and change colour to red 6–7 days after their emergence. We took red and yellow male reflectance spectra and found that red males are brighter than yellow males. Next, we aimed to determine whether ontogenetic colour change signals sexual maturity with field observations and laboratory experiments. Our field observational data showed that red males are in higher abundance in the breeding territory, and they have a higher mating frequency than yellow males. We confirmed these field observations by enclosing a red and a yellow male with two females and found that yellow males do not mate in presence of red males. To determine whether colour change signals sexual maturity, we measured mating success of males before and after colour changes by enclosing a single male at different age (day 3-day 7) and colour (yellow, intermediate and red) with a single female in a mating cage. Males did not mate when yellow but the same male mated after it changed colour to red, suggesting the ontogenetic colour change signals sexual maturity in this species. Our study shows that male dichromatism can be age-dependent and ontogenetic colour change can signal age and sexual readiness in non-territorial insects.     

Female reproductive decisions and parasite burden in a calopterygid damselfly (Insecta: Odonata)

There is currently a gap in sexual selection theory about how much the environment drives female mating decisions. We present field data that suggest that female sexual behaviour in the damselfly Calopteryx haemorrhoidalis is influenced by parasite burden. Male wing pigmentation in Calopteryx is a sexually selected trait that signals a male's ability to cope with eugregarine parasites (an intestinal parasite that feeds on the adult's ingested food). Because adult C. haemorrhoidalis females also show wing pigmentation, we examined whether this trait is similarly influenced by parasite burden and whether it may signal the female's reproductive value. MaleC. haemorrhoidalis defend riverine substrates that females use for oviposition. After copulation and during oviposition, females are guarded by the copulating male against intruder males. Alternatively, females may avoid mating and ‘steal’ an oviposition site within a male's territory. In the present study, we found that the amount of female wing pigmentation was negatively correlated with the number of eugregarines present. Females with more parasites produced fewer eggs, survived fewer days, spent less time during courtship, ‘inspected’ fewer males before mating, had a lower mating success, were guarded for less time during oviposition and engaged in fewer ‘stealing’ events during oviposition. The reduced egg production and survival of heavily infected females may result from eugregarine depletion of the females' consumed food reserves. Thus, to offset reduced longevity, heavily infected females may accept a mating more rapidly and mate with fewer males. ‘Stealing’ behaviour may be related to the female's differential use of sperm from some males, particularly high-quality males. Interestingly, males that mated with low-pigmented females showed greater variance in wing pigmentation than did males that mated with high-pigmented females. Possibly, female wing pigmentation may signal a female's reproductive value, which provides females with longer mate-guarding episodes and reduced interference from intruder males. This study points out one possible constraint, intestine parasites, that females may face during mating decisions. Because females in bad condition mate with males in both good and bad condition, this constraint may be pervasive enough to weaken the intensity of selection for a male sexually selected trait, wing pigmentation, and help to maintain its variation in phenotypic expression. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Correlation between Male Social Status,Testosterone Levels,and Parasitism in a Dimorphic Polygynous Mammal

Life history trade-offs have often been assumed to be the consequence of restrictions in the availability of critical resources such as energy and nutrients, which necessitate the differential allocation of resources to costly traits. Here, we examined endocrine (testosterone) and health (parasite burdens) parameters in territorial and non-territorial New Zealand fur seal males. We documented intra-sexual differences in sexual behaviours, testosterone levels, and parasitism that suggest a trade-off exists between reproductive success and physical health, particularly susceptibility to helminths and acanthocephalans, in males displaying different mating tactics (i.e., territorial and non-territorial tactics). Levels of testosterone were higher in territorial males and correlated positively with reproductive effort (i.e., intra- and inter-sexual interactions). However, these territorial males also exhibited high levels of parasitic infection, which may impair survival in the long-term. Our study, while limited in sample size, provides preliminary evidence for a link between male mating tactics, testosterone levels and parasite loads, and potential effects on reproductive success and life history that should be explored further.     

Temporal change in mite abundance and its effect on barn swallow reproduction and sexual selection

The tropical fowl mite Ornithonyssus bursa parasitizing barn swallows Hirundo rustica in a Danish population demonstrated a dramatic change in abundance during 1982–2000. Prevalence of mites in nests showed a decrease from 66% in 1987 to a minimum of 1% in 1999. Two parasite manipulation experiments of barn swallow nests in 1988 and 1999 revealed a strong effect of parasites on host reproductive success in the first year (with an average reduction in seasonal reproductive success of 30% when 50 mites were added to nests as compared with controls), but only a weak effect the last year. This pattern was paralleled by a positive relationship between reduction in host reproductive success between egg laying and fledging and mite prevalence during different years of the study period. Mite abundance on adult hosts was negatively related to tail length of males (a secondary sexual character) at the peak of mite abundance in 1988, while that relationship became weaker in the beginning of the 1990s and disappeared at the end of the 1990s. Assortative mating with respect to mite loads in the 1980s also disappeared in the 1990s. Mean tail length of male hosts increased by 1.3 standard deviations during the study period because of changes in phenotype‐dependent patterns of mortality outside the breeding season. This microevolutionary change in mean male phenotype of the host was accompanied by a correlated response in mite abundance. These results are consistent with the hypothesis that the host has become more resistant to the mite during the study period, and that the mite from earlier playing an important role in natural and sexual selection of the host now is of little importance.     

Effects of water mites on the damselfly Ceriagrion tenellum

1. Water mite parasitism is expected to have an important effect on damselfly survivorship and reproductive success, because mites drain considerable amounts of body fluids from their hosts. This study tests the effect of water mite parasitism in a marked population of the damselfly Ceriagrion tenellum during 1995 (individuals marked as mature adults) and 1996 (individuals marked as tenerals).
2. Almost all teneral individuals were parasitized (98%) and mites were aggregated strongly on some individuals. Parasite load increased during the season.
3. Parasites had no effect on the probability of recapture of hosts as mature adults. The average daily survival rate of lightly- and heavily-parasitized individuals, estimated with Jolly's stochastic method, did not differ significantly.
4. In 1995 parasites had a significant effect on host mating success. The probability of mating was about 25% lower for heavily-parasitized males than for lightly-parasitized males. Lightly-parasitized males also mated more times than heavily-parasitized males, even if heavily-parasitized males lived longer. In 1996, parasitism did not have an effect on male mating success. In both years mites had no effect on female lifetime mating success.
5. These results indicate that water mite parasitism does not reduce damselfly survivorship, but it could reduce male mating success in some circumstances. Further long-term studies are needed, especially in populations with a lower incidence of parasitism.     

Cost of reproduction in Callosobruchus maculatus: effects of mating on male longevity and the effect of male mating status on female longevity

One of the most studied life-history trade-offs is that resulting from the cost of reproduction: a trade-off arises when reproduction diverts limited resources from other life-history traits. We examine the cost of reproduction in male, and the effect of male mating status on female Callosobruchus maculatus seed beetles. Cost of reproduction for male C. maculatus was manifested as reduced longevity. There was also a positive relationship between male body size and male longevity. Females mated to males that had already copulated twice did not live as long as females mated to males that had copulated once or not at all. The third copulation of males also lasted longer than the two previous ones. We conclude that even though the cost of reproduction for males has been studied much less than that in females, there is growing evidence that male reproductive effort is more complex than has traditionally been thought.     

Male Drosophila melanogaster show adaptive mating bias in response to female infection status

Given the non-trivial cost of reproduction for males and substantial variation in female quality, males have been predicted to show mating bias as an evolved strategy. Using a large outbred population of Drosophila melanogaster, we test this prediction and show that males may adaptively bias their mating effort in response to the infection status of females. Given a simultaneous choice between females infected with pathogenic bacteria and sham infected females, males preferentially mated with the latter, who had a higher reproductive output compared to infected females. This may provide evidence for pre-copulatory male mate choice. Assessment of the reproductive behaviour ensured that the observed pattern of mating bias was not due to differences in receptivity between females infected with pathogenic bacteria and sham infected females. Further, there was no evidence for post-copulatory male mate choice measured in terms of copulation duration.     

Males mate with females even after sperm depletion in the two-spotted spider mite

Generally, males increase their reproductive success by mating with as many females as possible, whereas females increase their reproductive success by choosing males who provide more direct and indirect benefits. The difference in reproductive strategy between the sexes creates intense competition among males for access to females, therefore males spend much energy and time for competition with rival males for their reproduction. However, if they do not need to engage themselves into male competition and females are in no short supply, how many females can a male mate with and fertilize? We address this question in the two-spotted spider mite, Tetranychus urticae Koch. In this study, we investigated how many females a young, virgin male mated in 3 h, and checked whether the mated females were fertilized. We found that on average males mated with 12–13 females (range: 5–25). As latency to next mating did not change with the number of matings, the males are predicted to engage in even more matings if the mating trial were continued beyond 3 h. Copulation durations decreased with the number of matings and typically after 11 copulations with females any further copulations did not lead to fertilization, suggesting that males continued to mate with females even after sperm depletion. We discuss why spider mite males continue to display mating and copulation behaviour even after their sperm is depleted.

     

Effects of eugregarine parasites on adult longevity in the polymorphic damselfly Mnais costalis Selys

Abstract.  1. The relationship between the abundance of midgut parasites (eugregarine trophozooites) and the survival of hosts (field-collected damselflies, Mnais costalis ) was investigated under laboratory conditions.
2. Males of M. costalis are morphologically and behaviourally polymorphic, typically existing as clear-winged non-territorial sneaks and orange-winged territorial fighters (the latter are larger in size). The survival cost of eugregarine infection for the two morphs was compared.
3. Orange-winged males showed shorter longevity compared to clear-winged males when they were fed at levels lower than the natural feeding rate, or when they were deprived of food. In contrast, morph longevity did not differ when they were fed until satiation every day.
4. Within each morph, the survival of damselflies was negatively correlated with the parasite abundance except when damselflies were fed until satiation.
5. The results suggest that the abundance of eugregarine parasites exerts a substantial cost, which is associated with the maintenance of alternative mating strategies, together with the higher developmental cost and energy expenditure of the fighter morph.     

Diet, sex, and death in field crickets

Senescence is shaped by age-dependent trade-offs between fitness components. Because males and females invest different resources in reproduction, the trade-offs behind age-dependent reproductive effort should be resolved differently in the sexes. In this study, we assess the effects of diet (high carbohydrate and low protein vs. equal carbohydrate and protein) and mating (once mated vs. virgin) on lifespan and age-dependent mortality in male and female field crickets (Teleogryllus commodus), and on male calling effort. Females always had higher actuarial ageing rates than males, and we found a clear lifespan cost of mating in females. Mated males, however, lived longer than virgin males, possibly because virgins call more than mated males. The fastest age-dependent increases in mortality were among mated males on the high-carbohydrate diet. Males on a high-carbohydrate diet showed a faster increase in calling effort earlier in life, and a more pronounced pattern of senescence once they reached this peak than did males on a diet with equal amounts of protein and carbohydrates. Our results provide evidence that the cost of mating in this cricket species is both diet and sex-dependent, and that the underlying causes of sex differences in life-history traits such as lifespan and senescence can be complex.     

Impact of body reserves on energy expenditure, water flux, and mating success in breeding male northern elephant seals

In capital breeders, individual differences in body size and condition can impact mating effort and success. In addition to the collateral advantages of large body size in competition, large nutrient reserves may offer advantages in endurance rivalry and enable the high rates of energy expenditure associated with mating success. We examined the impacts of body reserves and dominance rank on energy expenditure, water flux, mating success, and breeding tenure in the adult male northern elephant seal, a polygynous, capital breeder. Adult males expended energy at a rate of 159 ± 49 MJ d (-1), which is equivalent to 3.1 times the standard metabolic rate predicted by Kleiber's equation. Despite high rates of energy expenditure and a long fasting duration, males spared lean tissue effectively, deriving a mean of 7% of their metabolism from protein catabolism. Body composition had a strong impact on the ability to spare lean tissue during breeding. When controlling for body size, energy expenditure, depletion of blubber reserves, and water efflux were significantly greater in alpha males than in subordinate males. Large body size was associated with increased reproductive effort, tenure on shore, dominance rank, and reproductive success. Terrestrial locomotion and topography appeared to strongly influence energy expenditure. Comparisons with conspecific females suggest greater total seasonal reproductive effort in male northern elephant seals when controlling for the effects of body mass. In polygynous capital breeding systems, male effort may be strongly influenced by physiological state and exceed that of females.     

Evidence for adaptive male mate choice in the fruit fly Drosophila melanogaster

Theory predicts that males will benefit when they bias their mating effort towards females of higher reproductive potential, and that this discrimination will increase as males become more resource limited. We conducted a series of experiments to test these predictions in a laboratory population of the fruitfly, Drosophila melanogaster. In this species, courtship and copulation have significant costs to males, and females vary greatly in fecundity, which is positively associated with body size. When given a simultaneous choice between small and large virgin females, males preferentially mated with larger, more fecund, females. Moreover, after males had recently mated they showed a stronger preference for larger females. These results suggest that male D. melanogaster adaptively allocate their mating effort in response to variation in female quality and provide some of the first support for the theoretical prediction that male stringency in mate choice increases as resources become more limiting.     

FITNESS TRADE-OFFS MEDIATED BY IMMUNOSUPPRESSION COSTS IN A SMALL MAMMAL

Trade-offs are widespread between life-history traits, such as reproduction and survival. However, their underlying physiological and behavioral mechanisms are less clear. One proposed physiological factor involves the trade-off between investment in male reproductive effort and immunity. Based on this hypothesis, we investigated differences in fitness between artificially selected immune response bank vole groups, Myodes glareolus . Significant heritability of immune response was found and a correlated response in testosterone levels to selection on immune function. Male reproductive effort, reproductive success, and survival of first generation offspring were assessed and we demonstrate a relationship between laboratory measured immune parameters and fitness parameters in field enclosures. We identify a trade-off between reproductive effort and survival with immune response and parasites as mediators. However, this trade-off results in equal male fitness in natural conditions, potentially demonstrating different male signaling strategies for either reproductive effort or survival. Females gain indirect genetic benefits for either genetic disease resistance or male reproductive effort, but not both. Immune response is genetically variable, genetically linked to testosterone and may indirectly maintain genetic variation for sexually selected traits. Evidence for both a genetic and a field trade-off between reproductive effort and survival indicates an evolutionary constraint on fitness traits.     

A selective trade-off for territoriality and non-territoriality in the polymorphic damselfly Mnais costalis

Males of the damselfly Mnais costalis occur as territorial orange-winged 'fighter' males or non-territorial clear-winged 'sneaker' males. Their morph life histories differ considerably but the estimated lifetime reproductive success is the same for the two morphs. In this study we compared the developmental and reproductive costs associated with the two morphs. Orange-winged male and female reproductive costs resulted in a decline in adult fat reserves with increasing age. In contrast, the fat reserves of clear-winged males remained constant with adult age. Body size was positively correlated with mating success in orange-winged males, but had no influence on the mating success of clear-winged males. The orange-winged male flight muscle ratios (FMRs) were significantly higher than the clear-winged male and female FMRs. However, there was no difference in the size-corrected fat reserves of the two morphs; both had higher fat reserves than females. The gain in mass between eclosion and reproduction in orange-winged males and females was almost double the mass gained by clear-winged males, suggesting that clear-winged male development is less costly. An experiment in which pre-reproductive levels of nutrition were manipulated confirmed this.     

Vibratory courtship in a web-building spider: signalling quality or stimulating the female?

Courtship behaviour in spiders in the form of premating vibrations by males may function (1) as a male identity signal used for species recognition, (2) in suppression of female aggressiveness, (3) to stimulate female mating behaviour, or (4) as a quality signal used in female choice. We investigated the function of web vibration by male Stegodyphus lineatus in a series of experiments. Regardless of vibratory performance, all males mated successfully with virgin females but only 56.4% of males mated with nonvirgin females. Vibratory performance did not influence male mating success, but heavier males had a higher probability of mating with mated females. Males vibrated less often and produced fewer vibrations when introduced on the web of a mated female. Males that vibrated webs of virgin females mated faster than nonvibrating males, but there was no effect of vibration rate or body mass. There was no effect of male vibratory effort or vibration rate on female reproductive success measured as time to egg laying, clutch size, number of hatched young, number of dispersed young and offspring body mass after a single mating. Males vibrated on abandoned virgin female webs but the response decreased with increasing duration of female absence, suggesting that females produce a web-borne pheromone, which elicits male vibrating behaviour. Mated females were less receptive and not stimulated by male vibrating behaviour. We conclude that male premating vibrations in S. lineatus do not function as a male quality signal selected via female choice. Rather, the primary function of this behaviour may be to stimulate a receptive female to mate. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Multiple Mating Increases Fecundity, Fertility and Relative Clutch Mass in the Female Leopard Gecko (Eublepharis macularius)

Females across many taxa may mate with several males or mate more than once with the same male within one reproductive event. Although many researchers have discussed the effects of multiple mating on reproductive success of females, few studies have attempted to disentangle whether the reproductive success of females differs with respect to whether females mate with multiple males or mate more than once with one male. In this study, we hypothesized that female leopard geckos (Eublepharis macularius) increase aspects of their reproductive success, such as fecundity, fertility and relative clutch mass, by mating more than once within one reproductive event, either by mating repeatedly with the same male or multiply mating with different males. We controlled for the potentially confounding variables of mating frequency and mate number by allowing females to mate once with one male, twice with the same male, or twice with two different males. We found that females that mated with more than one male laid more clutches, exhibited increased egg fertility and invested more in clutches relative to females that mated only once with one male, whereas females that mated twice to the same male were intermediate for these variables. Thus, reproductive success is higher among female leopard geckos that mated with more than one male compared to female leopard geckos that mated only once.