Parasite-mediated Sexual Selection Research Articles

Defensive tolerance to parasitism is correlated with sexual selection in swallows.

Parasite-mediated sexual selection has been the topic of extensive research and enthusiastic debate for more than three decades. Here, we suggest that secondary sexual characters may not only signal parasite resistance but also defensive tolerance. We exemplify this possibility by analysing information on two sexually selected traits, annual reproductive success, and ectoparasitism in a barn swallow Hirundo rustica population followed for more than 30years. For each individual, we estimated the slope of the association between reproductive success and parasitism as an index of tolerance and subsequently explored the association with the expression of the sexually selected traits. In accordance with expectations of parasites playing a role in sexual selection, tail length was negatively related to load of chewing lice and nest size was positively related to tolerance to chewing lice. We discuss the importance of considering defensive tolerance for understanding the role of parasite-mediated sexual selection.

Ornaments indicate parasite load only if they are dynamic or parasites are contagious.

Choosing to mate with an infected partner has several potential fitness costs, including disease transmission and infection-induced reductions in fecundity and parental care. By instead choosing a mate with no, or few, parasites, animals avoid these costs and may also obtain resistance genes for offspring. Within a population, then, the quality of sexually selected ornaments on which mate choice is based should correlate negatively with the number of parasites with which a host is infected ("parasite load"). However, the hundreds of tests of this prediction yield positive, negative, or no correlation between parasite load and ornament quality. Here, we use phylogenetically controlled meta-analysis of 424 correlations from 142 studies on a wide range of host and parasite taxa to evaluate explanations for this ambiguity. We found that ornament quality is weakly negatively correlated with parasite load overall, but the relationship is more strongly negative among ornaments that can dynamically change in quality, such as behavioral displays and skin pigmentation, and thus can accurately reflect current parasite load. The relationship was also more strongly negative among parasites that can transmit during sex. Thus, the direct benefit of avoiding parasite transmission may be a key driver of parasite-mediated sexual selection. No other moderators, including methodological details and whether males exhibit parental care, explained the substantial heterogeneity in our data set. We hope to stimulate research that more inclusively considers the many and varied ways in which parasites, sexual selection, and epidemiology intersect.

Is Color Related to Parasite Load in a Sexually Dichromatic Neotropical Toad?

Research on anuran parasites often focuses on the description and identification of parasites and demonstrating that parasitic infection can have deleterious effects on the health of amphibians. There is comparatively little research on how parasitism influences evolutionary dynamics such as sexual selection. Here, we explore anuran blood parasites with a focus on parasite-mediated sexual selection. The Hamilton–Zuk hypothesis posits that parasite–host coevolution drives sexual ornamentation of hosts, and that the degree of ornament expression honestly signals heritable parasite resistance. Although the Hamilton–Zuk hypothesis has received support in a number of animal taxa, it has received little attention in amphibians. Neotropical Yellow Toads (Incilius luetkenii) are sexually dichromatic toads with an unusual sexual ornament: males turn from cryptic brown to bright lemon yellow for a very short period during the brief breeding season. In this study, we identify blood parasites in male Neotropical Yellow Toads, and we investigate one component of the Hamilton–Zuk hypothesis by comparing skin color and body condition to blood parasite levels. We found four types of parasites. Apicomplexa and frog erythrocytic virus were the most common, infecting 73% and 46% of toads, respectively, whereas Nematoda and bacteria were found in 27% and 36% of toads, respectively. We found negative relationships between parasites and male color: males infected with fewer Apicomplexa and Nematoda had higher yellow saturation, and males with fewer Nematoda had longer-wavelength hue. In contrast, we found one positive relationship between parasites and male color: males infected with higher levels of frog erythrocytic virus had higher brightness. Our results suggest that parasites may influence sexual traits in this species, but that the relationship is complex. This research contributes to our understanding of amphibian host–parasite coevolution by demonstrating a relationship between parasites and host coloration.

When sexual selection in hosts benefits parasites.

In host-parasite coevolution, the parasite is selected to increase its infectivity while host is selected to resist the parasite infection. It is widely held that parasite-mediated sexual selection can further amplify the selective pressure on the host to overcome parasite infection. In this paper we focus on certain types of parasites, those that can impair the activity of the host immune function to prevent signs of sickness. We show that the effect of sexual selection can actually reduce the selective pressure on the host immune response to adapt to the parasite infection. We design a simple mathematical model for a population of sexually reproducing organism in which individuals are choosy, preferring traits that are correlated negatively with immune system activity. We introduce to this population a parasite that can suppress activation of the host's immune response. Our results show that even though the host immune system is likely to ultimately evolve and adapt to the parasite infection, when sexual selection is part of this process, it can slow down this evolution on the host and give the parasite more time to get established.

Male-Male Competition Causes Parasite-Mediated Sexual Selection for Local Adaptation.

AbstractSexual selection has been suggested to accelerate local adaptation and promote evolutionary rescue through several ecological and genetic mechanisms. Condition-dependent sexual selection has mainly been studied in laboratory settings, while data from natural populations are lacking. One ecological factor that can cause condition-dependent sexual selection is parasitism. Here, we quantified ectoparasite load (Arrenurus water mites) in a natural population of the common bluetail damselfly (Ischnura elegans) over 15 years. We quantified the strength of sexual selection against parasite load in both sexes and experimentally investigated the mechanisms behind such selection. Then we investigated how parasite resistance and tolerance changed over time to understand how they might influence population density. Parasites reduced mating success in both sexes, and sexual selection was stronger in males than in females. Experiments show that male-male competition is a strong force causing precopulatory sexual selection against parasite load. Although parasite resistance and male parasite tolerance increased over time, suggestive of increasing local adaptation against parasites, no signal of evolutionary rescue could be found. We suggest that condition-dependent sexual selection facilitates local adaptation against parasites and discuss its effects in evolutionary rescue.

Extending the ecology of fear: Parasite-mediated sexual selection drives host response to parasites

The ‘ecology of fear’ describes the negative effects natural enemies have on potential victims even when those victims are not consumed or infected. Although recent work has demonstrated parasites have non-consumptive effects (NCE) on potential hosts, how these effects vary within host populations is not well understood. We investigated how NCE vary based on host risk of infection and relative cost of infection by measuring the metabolic rate (MR) of naive Drosophila nigrospiracula exposed to an ectoparasite, Macrocheles subbadius. We tested two mutually exclusive hypotheses: 1) asymmetrical costs of infection drive adaptions for stronger responses to parasite exposure; or 2) asymmetrical risks of infection drive adaptions for stronger responses to parasite exposure. In this system, male flies have higher costs of infection relative to female flies due to parasite-mediated sexual selection; similarly, virgin females experience higher costs of infection relative to mated females. Risk of infection also varies among flies because mites preferentially infect female flies over males, and mites preferentially infect mated females over virgin females. Our results were compatible with the hypothesis that costs of infection drive the strength of response to mite risk. Female flies responded to parasite exposure with a 15.1% increase in MR, while exposed males showed a stronger response with a 31.3% increase in MR. Mated females increased their MR by 34.8% during mite exposure whereas virgin females experienced an increase of 61.2%. Our findings suggest that NCE of parasites can vary based on state-dependent costs of infection.

Parasite Prevalence and Income Inequality Positively Predict Beardedness Across 25 Countries

Sexually dimorphic characteristics can signal high genetic fitness and parasite resistance in intersexual selection; and individuals choose and prefer mates who appear resistant to parasites. Furthermore, sexually dimorphic traits can indicate intrasexual competitiveness. Beards are a sexually dimorphic trait, and in the current study we investigate the relationship between pathogen prevalence, income inequality and beardedness in men. Using publicly available data from The World’s Muslims’ dataset (PEW Research Center), encompassing more than 14,000 individuals from 25 countries, we test the hypotheses that men wear beards where the pathogen stress is higher and male-male competition is more prevalent. Our results show that beardedness in men is predicted by pathogen prevalence as well as GINI coefficient. Overall, the results of this study provide support for the Hamilton-Zuk parasite-mediated sexual selection hypothesis, indicating that men wear beards in environments where the parasitic stress is higher (in order to signal their vigor, health, and ability to resist parasites in such environments), and where there is more prevalence of male-male competition (indicated by higher wealth inequality).

A link between heritable parasite resistance and mate choice in dung beetles

AbstractParasites play a central role in the adaptiveness of sexual reproduction. Sexual selection theory suggests a role for parasite resistance in the context of mate choice, but the evidence is mixed. The parasite-mediated sexual selection (PMSS) hypothesis derives a number of predictions, among which that resistance to parasites is heritable, and that female choice favors parasite resistance genes in males. Here, we tested the PMSS hypothesis using the dung beetle Onthophagus taurus, a species that can be heavily parasitized by Macrocheles merdarius mites, which are known to affect adult survival. We investigated the heritability of resistance to M. merdarius, as well as whether female O. taurus impose a mating bias against males susceptible to mite infestation. Female choice for parasite resistance is difficult to disentangle from the possibility that females are simply choosing less parasitized males due to naturally selected benefits of avoiding contracting those parasites. This is especially likely for ectoparasites, such as mites. We tackled this problem by performing a mate choice trial first, and then measuring a male’s resistance to mite infestation. Resistance to mite infestation exhibited significant levels of additive genetic variance. Although we found no relationship between mating success and parasite resistance, males with greater resistance to infestation mated for longer. If females control copula duration, given that short copulations often result in mating failure, female choice could act on parasite resistance.

Age and infection history are revealed by different ornaments in a warbler.

Female preference for older or more disease-resistant males are both possible outcomes of parasite-mediated sexual selection, but the extent to which infection alters the development of ornaments to yield signals of male age and health has rarely been explored. In a longitudinal study of 61 male common yellowthroats (Geothlypis trichas), age-related increases in the size of the melanin-based mask and carotenoid-based bib were not correlated among young males, likely owing to differences in how blood parasites affect ornament development. Infection with trypanosomes and hemosporidians in a male's first breeding season was associated with slower growth of the mask; uninfected males attained large masks in their second breeding season, while infected males attained large masks in their third breeding season. In contrast, the bib size of males increased every year regardless of infection. As a consequence, different populations of males are identified by the largest ornaments-older males in the case of bib and a combination of older males and young, uninfected males in the case of mask. Although mask is thus the more informative trait with respect to male health, females prefer large bibs in our population. If infection is opportunistic, young, uninfected males may not possess good genes for parasite resistance but simply good luck, and it may benefit females to prefer older males who are more likely to have withstood prior episodes of selection. A "pure" signal of age may be a more reliable signal of resistance to parasites than an ornament whose expression is modulated by infection.

Infestation with the parasitic nematode Philometra ovata does not impair behavioral sexual competitiveness or odor attractiveness of the male European minnow (Phoxinus phoxinus)

Our understanding on the role of chemical signals in parasite-mediated sexual selection is still limited, and only some existing studies have focused on fish. Furthermore, published studies on the effect of parasite infection on behavioral sexual competition of the male hosts have yielded contradictory results. Here, we examined whether the infection of the body cavity-dwelling parasitic nematode Philometra ovata influences odor-based female choice and behavioral sexual competition (dominance and courtship behavior) between males in the European minnow (Phoxinus phoxinus), the cyprinid fish host. In contrast to our predictions, we found that naive females showed no preference between the odors of infected and non-infected males, thus indicating that P. ovata infection may not affect odor-based female choice. Moreover, P. ovata did not impair sexual competitiveness of their hosts either. Our results indicate that despite its relatively large size, P. ovata may not alter sexual cues and the success of the male hosts in sexual selection.

Coevolution of parasite virulence and host mating strategies

Parasites are thought to play an important role in sexual selection and the evolution of mating strategies, which in turn are likely to be critical to the transmission and therefore the evolution of parasites. Despite this clear interdependence we have little understanding of parasite-mediated sexual selection in the context of reciprocal parasite evolution. Here we develop a general coevolutionary model between host mate preference and the virulence of a sexually transmitted parasite. We show when the characteristics of both the host and parasite lead to coevolutionarily stable strategies or runaway selection, and when coevolutionary cycling between high and low levels of host mate choosiness and virulence is possible. A prominent argument against parasites being involved in sexual selection is that they should evolve to become less virulent when transmission depends on host mating success. The present study, however, demonstrates that coevolution can maintain stable host mate choosiness and parasite virulence or indeed coevolutionary cycling of both traits. We predict that choosiness should vary inversely with parasite virulence and that both relatively long and short life spans select against choosy behavior in the host. The model also reveals that hosts can evolve different behavioral responses from the same initial conditions, which highlights difficulties in using comparative analysis to detect parasite-mediated sexual selection. Taken as a whole, our results emphasize the importance of viewing parasite-mediated sexual selection in the context of coevolution.

Male Mate Choice for Unparasitized Females in Drosophila melanogaster

Parasite-mediated sexual selection theory suggests that females may choose male partners who possess a relatively low pathogen load in order to maximize their reproductive investment (e.g. by avoiding pathogens or producing pathogen-resistant offspring). However, males might also maximize their reproductive investment by preferring unparasitized females; even in non-sex-role-reversed systems where female choice predominates. We address this hypothesis in the fruit fly Drosophila melanogaster where female choice plays a major selective role. Females in this system exhibit reduced fecundity when parasitized, creating the opportunity for simultaneous parasite-mediated male choice. To address our hypothesis, virgin females were either prick-injected with a sub-lethal dose of the gram-negative bacteria Pseudomonas aeuginosa (pricked-parasitized group, PP), prick-injected with sterile media (pricked-unparasitized group, PU) or unpricked and unparasitized (UU group). Twenty-four hours post-infection, females were decapitated to minimize the confounding effects of female behavior on male preference (decapitated females will stand upright, but lack reproductive behavior). Males were then assigned to one of two different two-choice trials (experiment A: PU versus UU females or experiment B: PP versus UU females) and their courtship behavior monitored. In experiment A, males exhibited no courtship preference for either female. However, experiment B males preferentially courted UU females more often than PP females. These results suggest that males prefer unparasitized mates, which could play a significant role in shaping disease resistance in this system. These data also provide some of the first evidence that males prefer unparasitized females in systems that do not exhibit sex-role reversal.

Effect of an immune challenge on the functional performance of male weaponry

Theories of parasite-mediated sexual selection predict a positive association between immune function and the expression of sexually selected ornaments. Few studies, however, have investigated how an immune challenge affects the performance of sexually selected weaponry. Male Wellington tree weta (Hemideina crassidens) (Orthoptera: Anostostomatidae) possess enlarged mandibles that are used as weapons in fights for access to females residing in tree galleries. Intense sexual competition appears to have favoured the evolution of alternative male mating strategies in this species as males have a trimorphic phenotype in which weapon size varies across morphotype: 8th instar males have the smallest jaws, 10th instar males have the largest and 9th instar males being intermediate to the other two. After injecting males and females with either lipopolysaccharide (LPS; immune challenge) or saline (control) I measured over a 24h period each weta's body mass to assess whether they responded immunologically to the LPS and their bite force to assess the functional performance of their jaws. Both sexes responded immunologically to the immune-challenge as LPS-injected individuals lost significantly more body mass than saline-injected controls with females losing more mass than males. Female bite force was significantly reduced 8h after LPS-injection whereas male bite force did not significantly decline. Both sexes regained pre-injection functional performance of their jaws 24h after the immune challenge. My results suggest that females trade-off bite force for immune function whereas males do not.This article is part of a Special Issue entitled: insert SI title.

Reproductive success of parasitized males in a marine reef fish

Parasitism is hypothesized to reduce reproductive success in heavily parasitized males because females may preferentially mate with less parasitized males (parasite-mediated sexual selection) or parasites may compromise male competitiveness. In marine systems, this hypothesis is largely unexplored. This paper provides the first confirmed record of a copepod ectoparasite (Caligus buechlerae Hewitt 1964) on the common triplefin (Forsterygion lapillum) and evaluates the hypothesis that males parasitized with C. buechlerae experience lower reproductive success than unparasitized males (as determined by the presence and area of eggs within male nests). We found that 38 % of males we surveyed were infected with at least one C. buechlerae, with a median of two individuals per infected male. About 32 % of males were defending eggs, with 62.5 % of those males infected with at least one parasite. Males of greater total length (TL) were both more likely to be infected and more likely to be defending eggs. However, when statistically accounting for the effects of TL, parasite infection had no effect on the probability of defending eggs, or the average surface area of eggs when present. Positive covariation in fish length, the presence of eggs and parasite infection observed here potentially suggest that the importance of parasitic infection on reproductive success may depend upon the strength of selection for larger male body size. Our study is one of the few studies to investigate the effects of ectoparasites on reproductive success in reef fish and also provides a quantitative measure of infection for a widespread species within New Zealand.

Plumage Coverage is Related to Body Condition and Ectoparasitism in Blue-black Grassquits

Females may prefer elaborate sexual ornaments in males as these can be costly and may honestly indicate male viability. We used a wild population of the Blue-black Grassquit (Volatinia jacarina) in central Brazil to test whether more ornamented males have lower parasite loads (parasite-mediated sexual selection) and/or better body condition (condition-dependent sexual selection) compared with less ornamented males. We predicted that blue-black plumage coverage should be positively correlated to body condition (weight/tarsus) and negatively correlated to parasite load (Mallophaga lice). We found that blue-black plumage coverage of grassquit males was positively related to body condition score and negatively related to ectoparasite load. However, body condition was not correlated with ectoparasite load in these males. Our data are consistent with the hypothesis of sexual selection mediated by parasites as well as with the hypothesis of sexual selection mediated by body condition, indicating that nuptial plumage coverage can be an honest signal of male quality in Blue-black Grassquits, and could thus be used by females during mate choice.

Calling Behavior and Parasite Intensity in Treefrogs,Hypsiboas prasinus

Abstract A negative relationship between parasite intensity and male ornament condition or sexual display rate is one of the conditions of the parasite-mediated sexual selection model. In anurans, temporal properties of calling behavior, and particularly calling rates, are the best candidates to express a negative relationship with parasite intensity, given the high energy costs of calling and the fact that calls are potentially under strong intersexual selection. We studied the relationship between call parameters and helminth parasite intensity in males of a Brazilian subtropical treefrog, Hypsiboas prasinus. We tested the hypotheses that: 1) calling characteristics are correlated negatively to parasite intensity; and 2) the relationship between calling performance and parasite intensity is more pronounced when dynamic properties are considered. According to our predictions, only rate, the most important dynamic property of calling behavior, is associated with individual variation in parasite intensity....

Negative correlation between nuptial throat colour and blood parasite load in male European green lizards supports the Hamilton–Zuk hypothesis

During female mate choice, conspicuous male sexual signals are used to infer male quality and choose the best sire for the offspring. The theory of parasite-mediated sexual selection (Hamilton-Zuk hypothesis) presumes that parasite infection can influence the elaboration of sexual signals: resistant individuals can invest more energy into signal expression and thus advertise their individual quality through signal intensity. By preferring these males, females can provide resistance genes for their offspring. Previous research showed that nuptial throat colour of male European green lizard, Lacerta viridis, plays a role in both inter- and intrasexual selections as a condition-dependent multiple signalling system. The aim of this study was to test the predictions of the Hamilton-Zuk hypothesis on male European green lizards. By blood sampling 30 adult males during the reproductive season, we found members of the Haemogregarinidae family in all but one individual (prevalence = 96%). The infection intensity showed strong negative correlation with the throat and belly colour brightness in line with the predictions of the Hamilton-Zuk hypothesis. In addition, we found other correlations between infection intensity and other fitness-related traits, suggesting that parasite load has a remarkable effect on individual fitness. This study shows that throat patch colour of the European green lizards not only is a multiple signalling system but also possibly acts as an honest sexual signal of health state in accordance with the Hamilton-Zuk hypothesis.

Antioxidant supplementation during early development reduces parasite load but does not affect sexual ornament expression in adult ring-necked pheasants

Summary 1. The ‘parasite-mediated sexual selection’ (PMSS) hypothesis predicts that exaggerated male ornamentation could provide a signal to females of a male’s ability to resist parasites. Empirical tests of the PMSS have been largely equivocal, however, which may be because most have not considered the role of early life-history effects. 2. Many sexually selected traits are carotenoid-based. Allocation of dietary-derived carotenoids to sexual ornaments may trade-off with allocation to pro-inflammatory immune response andUor antioxidant functions, mediated by the oxidative status of individuals. Exposure to parasites can increase oxidative stress, so under this scenario, sexually selected traits indicate ability to resist oxidative stress rather than ability to resist parasites per se . Such life-history trade-offs, mediated by oxidative status of individuals, are particularly acute during growth and development. 3. Here, we use ring-necked pheasants, Phasianus colchicus, a strongly sexually selected species, to test whether supplementation with dietary antioxidants (vitamin E) can mitigate the effects of early exposure to parasites (the nematode, Heterakis gallinarum ), via alteration of the oxidative status of individuals, and positively affect the expression of sexual ornaments at adulthood. 4. We found that vitamin E mediated the effect of early exposure to parasites on levels of oxidative damage at 8 weeks of age and reduced the parasite load of individuals at adulthood as predicted. However, the expression of sexual ornaments, immune function and growth were unaffected by either early vitamin E supplementation or manipulation of parasite load. In contrast to the predictions of the PMSS hypothesis, the intensity of sexual ornament expression was not related to either parasite load or oxidative status of individuals (current or long-term). Consequently, there was no evidence that the expression of sexual ornaments provided information on the ability of males to resist infection from parasites.

Is plasticity in mating preferences adapted to perceived exposure to pathogens?

Humans are unique among primates due to a lack of typical thermally insulating fur. The ectoparasite avoidance mediated by the mate choice hypothesis suggests that the loss of body hair reduces the risk of infection by ectoparasites and that the movement toward nudity may have been enforced by parasite-mediated sexual selection. In this study, we investigated two possible predictions of this hypothesis: (1) that preferences for hairless bodies increase with exposure to environmental pathogens and (2) that disgust sensitivity to the pathogens’ threat predicts the degree to which a woman will prefer hairless bodies. Using an experiment comparing the preferences of 88 women for shaved vs. hairy pictured versions of 20 male torsos, we found that exposure to the visual cues of pathogens does not predict preferences for a male chest nor does the individual disgust sensitivity to disease-related invertebrates. Overall, the results suggest that female perception of male trunk hair is not associated with a risk of contamination, which questions the salience of the ectoparasite avoidance hypothesis in explaining the loss of body hair in humans.

Resource allocation trade-off between sperm quality and immunity in the field cricket, Teleogryllus oceanicus

Mounting an immune response is costly, requiring an animal to draw on its limited nutrient pool at a cost to future growth and reproduction. A trade-off between immunity and reproduction is central to parasite-mediated models of sexual selection. In this study, I examine a prediction of postcopulatory models of parasite-mediated sexual selection that males face a nutrient allocation trade-off between immunity and ejaculate quality. I experimentally induced an antibacterial immune response in juvenile crickets held on either a restricted diet or allowed ad libitum access to food. Immune-challenged crickets took longer to reach adult eclosion, and crickets on a restricted diet had a greatly reduced ability to encapsulate a foreign body. Neither juvenile immune challenge nor diet influenced adult antibacterial activity. Crickets with restricted access to food had reduced sperm viability after upregulation of their antibacterial immunity when juvenile, whereas crickets fed ad libitum did not suffer a cost of reduced sperm viability. This finding provides evidence for a nutrient allocation trade-off between antibacterial immunity and ejaculate quality. However, the genetic correlation between these traits is negative, rendering any indirect genetic benefits from sperm competition unlikely. Key words: ecological immunology, ejaculate quality, invertebrate immunity, sperm competition, trade-off. [Behav Ecol]