EFFECT OF ECTOPARASITIC MITES ON SEXUAL SELECTION IN A SONORAN DESERT FRUIT FLY

We conducted a field study and a laboratory experiment to test whether ectoparasitic mites, Macrocheles subbadius, generate parasite-mediated sexual selection in the Sonoran desert endemic fruit fly, Drosophila nigrospiracula. Male flies gather on the outer surfaces of necrotic saguaro cacti where they engage in male–male competitive interactions and vigorous female-directed courtship. At these sites, operational sex ratios were significantly skewed toward males. The degree to which mites were aggregated among flies varied across the 25 fly populations sampled. The degree of mite aggregation across fly populations was strongly positively related to the mean number of mites per fly (intensity of infestation). Both the intensity and prevalence of infestation (fraction of flies infested) increased with the age of the cactus necrosis. Infested flies of both sexes were significantly less likely to be found in copula than uninfested flies, and mean intensity of infestation was significantly more pronounced in noncopulating than in copulating flies. The effect of attached mites on copulatory success exhibited dose-dependency, and this effect was more stringent in males: males or females with more than two and four mites, respectively, were never found in copula. The magnitude of parasite-mediated sexual selection was estimated for 12 fly populations by calculating selection differentials for each sex separately. The relation between intensity of infestation and magnitude of parasite-mediated sexual selection was stronger in males but significant for both sexes. We also assayed copulatory success of field-caught males in the laboratory, both during infestation and after experimental removal of mites. Males infested with two mites copulated less frequently than uninfested individuals, and in mating trials after mites had been removed, previously infested males copulated as many times as flies with no history of infestation. These findings, and the lack of difference in the number of mite-induced scars on copulating and single individuals in nature, strongly suggest that the reduced copulatory success of infested flies is attributable to an effect of mites per se, rather than to a character correlated with parasitism or previous parasite infestation.     

An evolutionary limit to male mating success

The well-known phenotypic diversity of male sexual displays, and the high levels of genetic variation reported for individual display traits have generated the expectation that male display traits, and consequently male mating success, are highly evolvable. It has not been shown however that selection for male mating success, exerted by female preferences in an unmanipulated population, results in evolutionary change. Here, we tested the expectation that male mating success is highly evolvable in Drosophila bunnanda using an experimental evolution approach. Female D. bunnanda exhibit a strong, consistent preference for a specific combination of male cuticular hydrocarbons (CHCs). We used female preference to select for male mating success by propagating replicate populations from either attractive or unattractive males over 10 generations. Neither the combination of CHCs under sexual selection (the sexual signal) nor male mating success itself evolved. The lack of a response to selection was consistent with previous quantitative genetic experiments in D. bunnanda that demonstrated the virtual absence of genetic variance in the combination of CHCs under sexual selection. Persistent directional selection, such as applied by female mate choice, may erode genetic variance, resulting in multitrait evolutionary limits.     

Postmating sexual selection: the effects of male body size and recovery period on paternity and egg production rate in a water strider

The role of male body size in postmating sexual selection wasexplored in a semiaquatic insect, the water strider Gerris lateralis.To separate effects of male size per se from those due to numericsperm competition, male recovery period (shown here to be proportionalto ejaculate size) was manipulated independently of body sizein a factorial experiment where virgin females were mated firstwith sterile males and then with focal males. Both relativemale fertilization success and female reproductive rate were measured.The number of sperm transferred increased with male recoveryperiod, an effect that was mediated by longer copulation duration,but there were no effects of body size on ejaculate size. Neithermale size nor recovery period had any significant direct effectson male fertilization success. However, copulation durationinfluenced relative fertilization success, suggesting that malesable to transfer more sperm also achieved higher fertilizationsuccess. Females exercised cryptic female choice by modulatingtheir reproductive rate in a manner favoring large males andmales that were successful in terms of achieving high relativefertilization success. Thus, successful males gained a twofoldadvantage in postmating sexual selection. This study has important implicationsfor previous estimates of sexual selection in this group of insectsbecause pre- and postmating sexual selection will be antagonisticdue to limitations in male sperm production: males mating frequently(high mating success) will on average transfer fewer sperm ineach mating and will hence tend to fertilize fewer eggs permating (low fertilization success).     

Sexual selection and condition dependence of courtship display in three species of horned dung beetles

Sexual selection has traditionally been divided into competitionover mates and mate choice. Currently, models of sexual selectionpredict that sexual traits are expressed in proportion to thecondition of their bearer. In horned beetles, male contestcompetition is well established, but studies on female preferencesare scarce. Here I present data on male mating success and condition dependence of courtship rate in three species of horn-dimorphicdung beetles, Onthophagus taurus, Onthophagus binodis, andOnthophagus australis. I found that in the absence of malecontest competition, mating success of O. taurus and O. australiswas unrelated to their horn length and body size, whereas inO. binodis horn size had a negative effect but body size hada positive effect on male mating success. Overall, in O. binodismajor morph males had greater mating success than minor morphmales. In all three species male mating success was affectedby courtship rate, and the courtship rate was condition dependent such that when males were manipulated to be in poor conditionthey had lower courtship rates than males that were manipulatedto be in good condition. My findings provide new insight intothe mating systems of horned dung beetles and support an importantassumption in indicator models of sexual selection.     

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.     

SEXUALLY TRANSMITTED DISEASE AND PARASITE-MEDIATED SEXUAL SELECTION

Few studies have investigated the consequences of parasite-mediated sexual selection on the parasites involved. In some cases parasite-mediated sexual selection could lead to increased virulence, but I develop a simple model that shows that, if a parasite is sexually transmitted (i.e., is a sexually transmitted disease, or STD) and if mating success of the host is adversely affected by the parasite, then less virulent STDs will be selected for because transmission of the STD depends on the mating success of the host. This selection for reduced virulence could have important consequences for the role of STDs in sexual selection.     

Survival costs and reproductive benefits of floral display in a sexually dimorphic dioecious shrub, Leucadendron xanthoconus

The evolutionary causes of sexual dimorphism in plants have not been as widely studied as in animals and the importance of sexual selection in causing dimorphism remains controversial. Sexual selection is most obvious when it favours the evolution of a trait which enhances mating success at the expense of decreased viability. We studied the relationship between floral display (number of inflorescences), pollinator attraction and plant survival in a dioecious shrub, Leucadendron xanthoconus. Pollinator attraction, measured as the number of insect pollinators, increased linearly with floral display in males. However, males with extravagant displays had a higher probability of dying. Our data suggest that male plants are undergoing selection on floral display for increased mating success counterbalanced by selection against plants with extravagant displays. Seed set in females did not increase with floral display, except at very low inflorescence numbers. Nor was female survival correlated with floral display. Because inflorescences are terminal in the species, selection for more inflorescences in males causes increased ramification, thinner terminal branches and smaller leaves. Thus vegetative dimorphism in this species appears to be caused by selection for extravagant floral display in males, but not females. Limits to dimorphism are imposed by survival costs of elaborate display.     

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.     

Sexual selection in a moth: effect of symmetry on male mating success in the wild

Sexual selection is generally caused by female choice and male–malecompetition. In female choice process, female preference isfavored indirectly and/or directly by sexual selection. In indirectselection, females expressing the preference might gain indirectgenetic benefits. In direct selection, females expressing thepreference might gain direct benefits or avoid male-imposedcosts. The white-tailed zygaenid moth Elcysma westwoodii ismonandrous, and males often gather around a female to mate withher, suggesting a high opportunity for sexual selection on maletraits. We quantified phenotypic selection on male morphologyin this species in the field. The morphological characters analyzedincluded body weight, antenna length, forewing length, hindwing length, hind wing tail length, genital clasper length,and the fluctuating asymmetry (FA) of these bilateral traits.In E. westwoodii, selection favored males with more symmetricgenital claspers, as well as longer and more symmetrical hindwings and antennae. Negative correlations between FA and sizewere also detected in the clasper and the antenna. Our resultssuggest that FAs of male traits, in particular the genital clasper,may have indirect and direct influences on mating success. Duringa copulatory attempt, an E. westwoodii male will try to graspthe female's abdominal tip with his claspers but often failto do so because of the female's reluctance to mate. The femaleabdominal tips are smooth and strongly sclerotized and couldthus be difficult for males to grasp. We hypothesize that moresymmetrical male claspers are more efficient in overcoming femalereluctance.     

Sexual advertisement and immune function in an arachnid species (Lycosidae)

A simple version of the immunocompetence handicap hypothesizesthat through condition-dependence, the size of the sexual traitmay be positively related to immune function at the populationlevel. In the present study, we investigated the relationshipbetween sexual advertisement and immune function in a naturalpopulation of male wolf spiders, Hygrolycosa rubrofasciata (Araneae:Lycosidae). Males of H. rubrofasciata have a costly and condition-dependentacoustic signal, courtship drumming. In the mating season, malesdrum against dry leaves while wandering around the habitat searchingfor receptive females. Males increase their mating success byincreasing their drumming rate and mobility. We used drummingrate and mobility measured without female proximity as estimatesof sexual advertisement. As estimates of male immune function,we used encapsulation rate and lytic activity. Encapsulationrate is a common challenging technique, which measures immuneresponse against multicellular parasites. Lytic activity isa monitoring technique, which measures immune response againstpathogens. Our results show that males with higher drummingrate had higher encapsulation rate. This suggests that femalesmight use drumming rate as a signal for choosing males withgood immunocompetence. Moreover, our results show that maleswith higher mobility had higher lytic activity. As females aremore likely to encounter those males that have higher mobility,this might also select males with better immune function. Ourresults suggest that the immunocompetence handicap might workalso among spiders, although we could not assess the causalityof the relationship between sexual selection and immune functionin this correlational study.     

Anisogamy,sexual selection,and the evolution and maintenance of sex

Summary In the present paper we distinguish between two aspects of sexual reproduction. Genetic recombination is a universal features of the sexual process. It is a primitive condition found in simple, single-celled organisms, as well as in higher plants and animals. Its function is primarily to repair genetic damage and eliminate deleterious mutations. Recombination also produces new variation, however, and this can provide the basis for adaptive evolutionary change in spatially and temporally variable environments.The other feature usually associated with sexual reproduction, differentiated male and female roles, is a derived condition, largely restricted to complex, diploid, multicellular organisms. The evolution of anisogamous gametes (small, mobile male gametes containing only genetic material, and large, relatively immobile female gametes containing both genetic material and resources for the developing offspring) not only established the fundamental basis for maleness and femaleness, it also led to an asymmetry between the sexes in the allocation of resources to mating and offspring. Whereas females allocate their resources primarily to offspring, the existence of many male gametes for each female one results in sexual selection on males to allocate their resources to traits that enhance success in competition for fertilizations. A consequence of this reproductive competition, higher variance in male than female reproductive success, results in more intense selection on males.The greater response of males to both stabilizing and directional selection constitutes an evolutionary advantage of males that partially compensates for the cost of producing them. The increased fitness contributed by sexual selection on males will complement the advantages of genetic recombination for DNA repair and elimination of deleterious mutations in any outcrossing breeding system in which males contribute only genetic material to their offspring. Higher plants and animals tend to maintain sexual reproduction in part because of the enhanced fitness of offspring resulting from sexual selection at the level of individual organisms, and in part because of the superiority of sexual populations in competition with asexual clones.     

Red Queen dancing in the lek: effects of mating skew on host–parasite interactions

The RQH (Red Queen hypothesis), which argues that hosts need to be continuously finding new ways to avoid parasites that are able to infect common host genotypes, has been at the center of discussions on the maintenance of sex. This is because diversity is favored under the host–parasite coevolution based on negative frequency‐dependent selection, and sexual reproduction is a mechanism that generates genetic diversity in the host population. Together with parasite infections, sexual organisms are usually under sexual selection, which leads to mating skew or mating success biased toward males with a particular phenotype. Thus, strong mating skew would affect genetic variance in a population and should affect the benefit of the RQH. However, most models have investigated the RQH under a random mating system and not under mating skew. In this study, I show that sexual selection and the resultant mating skew may increase parasite load in the hosts. An IBM (individual‐based model), which included host–parasite interactions and sexual selection among hosts, demonstrates that mating skew influenced parasite infection in the hosts under various conditions. Moreover, the IBM showed that the mating skew evolves easily in cases of male–male competition and female mate choice, even though it imposes an increased risk of parasite infection on the hosts. These findings indicated that whether the RQH favored sexual reproduction depended on the condition of mating skew. That is, consideration of the host mating system would provide further understanding of conditions in which the RQH favors sexual reproduction in real organisms.     

Temporal and microspatial variation in the intensities of natural and sexual selection in the yellow dung fly Scathophaga stercoraria

Studies of phenotypic selection in natural populations often concentrate only on short time periods and do not quantify selection intensities. We quantified temporal and microspatial variation in the intensities of natural and sexual selection for body size in the yellow dung fly over 2 years. Female fecundity selection intensity remained approximately constant over the season with an overall mean ± SE of 0.187 ± 0.014. Selection intensity for male reproductive success, defined as eggs obtained by mating males, did not differ from zero, indicating there was no assortative mating by size. Sexual selection intensity for male mating success favouring large males was variable but overall strong in the two years (0.499 ± 0.053 and 0.510 ± 0.051). As theoretically expected for male–male competition, sexual selection intensity increased with competitor density and reached an asymptote at about 250 males per pat; it also decreased with time in spring and increased again in autumn as a function of density. Small males had the best chance of obtaining a female at very low male densities. Greater selection intensity for large size in males than females is consistent with, and might be responsible for, the observed sexual size dimorphism in this species, as males are larger. The seasonal pattern of mean male body size (smallest at the beginning and end of the season) most likely reflects mere environmental (primarily temperature) influences on phenotypic size.     

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.     

A mixed model of the evolution of polygyny and sexual size dimorphism in mammals

The theory of sexual selection is the most widely accepted theory explaining the evolution of mating systems and secondary sexual characters. Polygyny is the most common mating system in mammals, and there is a strong correlation between the degree of polygyny and the degree of sexual size dimorphism skewed towards males. Sexual selection theory posits that polygyny in mammals has evolved through direct, precopulatory, intrasexual selection in males, and that sexual size dimorphism is a result of male competition for mates. New results that are being obtained with the use of molecular techniques and with comparative phylogenetic methods do not appear to support predictions from this classical model in full. In this article, an expansion of the classical model is presented that combines the effects of at least four forms of selection: natural, precopulatory intrasexual, postcopulatory intrasexual, and intersexual selection. This mixed model consists of an initial phase in which natural selection operates on body size, followed by a second phase dominated by sexual selection and involving increases in sexual dimorphism and coercive behaviour of males towards females. Sexual harassment induces female aggregation, thus creating social potential for polygyny. Males compete for access to the groups of females, following two possible evolutionary scenarios, directional or equilibrium sexual selection, both producing similar behavioural polygyny, but with differences in the intensity of intra-male precopulatory sexual selection. Predictions of the mixed model are as follows: 1) polygyny can exist without high variance in male reproductive success (a fundamental requirement in the classical model); 2) extra-group fertilisation can be common; 3) sexual size dimorphism evolved prior to polygyny; 4) sexual coercion is widespread; and 5) females reduce levels of sexual coercion by joining groups.     

Correlates of male mating success in the lekking great snipe (Gallinago media): results from a four-year study

To investigate behavioral or morphological traits importantas mate choice cues, we measured selection differentials (s)as the covariances between each trait and male mating success,and directional selection gradients (J3) from multiple linearregression of the standardized traits on male mating success.Data from two leks in four consecutive years were included,and the annual data were analyzed separately. The main findingsare: (1) the distribution of male mating success proved to beless skewed than those found in many other lekking species,(2) only a few traits yielded significant selection gradients,(3) the importance of age on male mating success changed acrossyears, (4) females may use traits with a high variance as matechoice cues, and (5) individual males achieved similar matingsuccesses between years. Attendance and age were the traitsmost consistently correlated with male mating success, but notraits showed significant selection gradients in all years.Our results indicate that variable sexual selection pressuresexisted between years, but the high correlation found betweenthe mating success of individual males in successive seasonsalso indicates that permanent differences in male traits areimportant. Key words: lek, mate choice, sexual selection.     

Nuptial gift in the spider Pisaura mirabilis maintained by sexual selection

The nuptial prey gift in the spider Pisaura mirabilis has been suggested to function as a male protection against sexual cannibalismduring courtship and mating. This hypothesis together withtwo alternatives—male mating effort and paternal investment hypotheses—were tested in a laboratory experiment withsexually inexperienced males and females. One group of malesoffered no gift to the female while three groups of males offeredsmall, medium, or large sized gifts, respectively. No malewas cannibalized among 82 trials. Aggression was observed onlyin encounters where a gift was presented. Males without a gift courted females, and 40% of these males managed to copulate,compared to 90% of males offering a gift. The copulation durationwas positively correlated with gift size. In general, the femaleterminated the copulation and ran away with the gift. The proportionof eggs fertilized increased with copulation time. Presenceor size of the nuptial gift did not affect female fecundityor spiderling size significantly. The results refute the hypothesesof sexual cannibalism and paternal investment. The nuptialgift represents a male mating effort; it entices the femaleto copulate, facilitates coupling during copulation, and byprolonging copulation it may increase the amount of sperm transferred.I conclude that the nuptial prey gift in Pisaura mirabilisis maintained by sexual selection.     

Male reproductive success and sexual selection in northern water snakes determined by microsatellite DNA analysis

Male northern water snakes (Nerodia sipedon) have high variancein reproductive success relative to females. We used DNA-basedpaternity analyses from a 3-year study of two marsh populationsof water snakes to investigate the factors that contributeto variation in male success. Male traits investigated includedbody size, condition, tail length, home range size, activityduring the mating season, and genetic profile (genetic similarityto females, heterozygosity, and genetic variability [d²]).We successfully assigned > 80% of offspring to sires froma sample of 811 offspring from 45 litters. Male reproductivesuccess did not vary significantly with body size, tail length,condition, home range size, or the number of microsatelliteloci at which males were heterozygous, nor with other featuresof their genetic profiles. However, we found evidence of positive assortative mating by size in the marsh in which receptive femaleswere not spatially clumped. Also, males that were most activeduring the mating season were more successful, particularlywhere females were not clumped. We failed to find evidenceof selection acting on male size through variance in reproductivesuccess, indicating that sexual selection does not have an important influence on sexual size dimorphism in this species(males are smaller than females). We propose that males aresmaller than females because the lack of advantage to largesize allows males to adopt a low-energy, low-growth strategythat reduces their risk of predation outside the mating season.     

Male mating success in a North American pitviper: influence of body size,testosterone, and spatial metrics

Males with enhanced traits relative to conspecifics often show increased mating and reproductive success and thus have a fitness advantage. The opportunity or potential for sexual selection is predicted to occur under these conditions. Here, we investigated proximate determinants of mating success in male copperhead snakes (Agkistrodon contortrix), a medium‐sized pitviper of North America. Specifically, we investigated the relationships of body size (snout‐vent length, body mass), body condition index, spatial metrics (total distance moved, home range size), and plasma testosterone concentration on mating success in males. The single mating season lasts from August through September. We compared a set of candidate linear mixed models and selected the best‐fitting one using the adjusted Akaike Information Criterion (AICc). The AICc‐selected model (model 2), with testosterone, body condition index, and home range size as predictor variables, showed that male mating success was positively correlated with testosterone. To our knowledge, this is the first report to show the relationship of testosterone and individual mating success in any snake species. A parallel study conducted on male fitness in A. contortrix of the same population used microsatellite markers to assign parentage of fathers (known mothers). Unlike our study, they found that snout‐vent length was positively correlated with reproductive success and that males were experiencing greater sexual selection. This relationship has been detected under natural conditions in other species of snakes. Although behavioural data are important in any mating system analysis, they should not stand alone to infer parentage, relationships or selection metrics (e.g. Bateman gradients). Long‐term sperm storage by females, female cryptic choice, and other factors contribute to the complexity of mating success of males. Accordingly, we thus conclude that estimates of reproductive success and fitness in cryptic species, such as copperheads and other snakes, require robust molecular methods to draw accurate conclusions regarding proximate and evolutionary responses. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 185–194.