Parasites and Sexual Selection in Birds of Paradise

We studied blood parasite infections in relation to aspectsof sexual selection and mate choice in 10 species of birds ofparadise. Across species there was a significant, positive correlationbetween relative parasite intensity and showiness in males.Parasite infections also correlated across species with thedegree of sexual dimorphism and varied with mating systems.Promiscuous species were showier and had significantly higherparasite prevalences than monogamous species. Within one species,Lawes' Parotia (Parotia lawesii), parasite intensity was negativelycorrelated with all phenotypic traits examined, a pattern significantlydifferent than random. The mating success of males with lowparasite intensities varied, but males with high intensitiesdid not mate. Sampling of individual males on repeated occasionsrevealed large temporal differences in parasite counts whichspanned the range believed to affect behavior and mating success.Whereas the interspecific correlations support one predictionof the Hamilton and Zuk hypothesis on parasites and sexual selection,the intraspecific data are equivocal with respect to a secondprediction of this hypothesis. Parasites appear to influencethe behavior of Lawes' Parotia, but alternative explanationsto that of Hamilton and Zuk for this effect are equally plausibleand there is no evidence of a link between female choice andthe traits in males indicative of parasite loads. We suggestthat female Lawes' Parotia may be avoiding highly infected malesrather than actively choosing parasite-resistant males.     

Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba)

The hypothesis that extravagant ornaments signal parasite resistancehas received support in several species for ornamented malesbut more rarely for ornamented females. However, recent theorieshave proposed that females should often be under sexual selection,and therefore females may signal the heritable capacity toresist parasites. We investigated this hypothesis in the sociallymonogamous barn owl, Tyto alba, in which females exhibit on average more and larger black spots on the plumage than males,and in which males were suggested to choose a mate with respectto female plumage spottiness. We hypothesized that the proportionof the plumage surface covered by black spots signals parasiteresistance. In line with this hypothesis, we found that theectoparasitic fly, Carnus hemapterus, was less abundant onyoung raised by more heavily spotted females and those flieswere less fecund. In an experiment, where entire clutches werecross-fostered between nests, we found that the fecundity ofthe flies collected on nestlings was negatively correlatedwith the genetic mother's plumage spottiness. These resultssuggest that the ability to resist parasites covaries with theextent of female plumage spottiness. Among females collecteddead along roads, those with a lot of black spots had a smallbursa of Fabricius. Given that parasites trigger the developmentof this immune organ, this observation further suggests thatmore spotted females are usually less parasitized. The same analyses performed on male plumage spottiness all provided non-significant results. To our knowledge, this study is the first one showingthat a heritable secondary sexual characteristics displayedby females reflects parasite resistance.     

Mate choice based on static versus dynamic secondary sexual traits in the dark-eyed junco

Some secondary sexual traits (SSTs) such as structural characteristicsare semi-permanent or static, while others, such as courtshipdisplay, are more labile or dynamic. In this paper we reportresults from two experiments designed to test the relative attractivenessto female dark-eyed juncos (Junco hyemalis, Passeriformes, Aves)of a relatively static plumage trait, the amount of white inthe tail, and a relatively dynamic behavioral trait, courtshipintensity. The experiments derived from a study showing that femalejuncos prefer males that court more vigorously. We asked whether femalesalso base their preferences on plumage traits and how they respond whenpresented with a choice between attractive traits that are eitherstatic (plumage) or dynamic (courtship) in nature. In the firstexperiment we presented males to females in paired mate-choicetrials and found that males enhanced with more white in theirtails were more attractive to females than controls with unenhancedtails. Females spent more time with enhanced males and directedmore sexual displays toward them. In the second experiment we testedwhether females preferred males with enhanced tails (a staticSST) or males with enhanced hormone-mediated courtship behavior(a dynamic SST). In this experiment females did not demonstratea consensus preference for either the static or the dynamictrait. Instead, some females preferred the male whose courtshipperformance was enhanced with testosterone, while others preferredthe male with an enhanced tail. We conclude that both kindsof traits are important in junco mate choice, but that somefemales apparently weigh static traits more heavily than dynamicones, while other females use opposite weightings.     

Different mate preferences by parasitized and unparasitized females potentially reduces sexual selection

Parasite‐mediated models of sexual selection predict that females should avoid parasitized mates, thereby generating selection on male traits revealing health. The strength of this selection, however, may depend on the prevalence of parasitism among females if their infection status alters their mate preferences. We evaluated the effects of a socially transmitted parasite on male traits and female behaviour in spadefoot toads. Parasitized males were larger and in better condition than unparasitized males. Moreover, better condition males produced longer calls. Unparasitized females preferred longer calls indicative of good‐condition males that are more likely parasitized. By contrast, parasitized females as a group possessed no preference for call duration. Presumably because of reduced selection by these parasitized females, male mating success was not associated with any measured traits. Thus, when females are parasitized, sexual selection on condition‐dependent traits is potentially reduced.     

Effects of blood parasites on sexual and natural selection in the pied flycather

The occurrence of the blood parasites Haemoproteus and Trypanosoma in the pied flycatcher, Ficedula hypoleuca , was examined to test current hypotheses that parasites reduce the expression of secondary sexual traits, mating success, breeding success, and survival of infected individuals. The results showed that there was no significant relationship between male plumage brightness and Trypanosoma infection, but males infected with Haemoproteus tended to be brighter than uninfected males, partly because first-year males were less often infected than older males. Polygynous males did not have fewer parasites than monogamous males. Females did not choose uninfected males among those they had sampled. Clutch size and laying date were not related to female infection status, and the number and quality of nestlings was not related to parasite infections of either male or female parent. The ability of males to provide parental care was not related to their infection status. The return rate from one breeding season to the next of infected males was not lower than that of uninfected males. The lack of correlations between parasites and male plumage colour and female mate choice apparently do not support the Hamilton-Zuk hypothesis of sexual selection. However, the absence of demonstration of any negative effects of parasites suggests that infection status may not be a direct measure of parasite resistance, or the degree to which the host suffers. Instead, the results support the alternative view that infected individuals have demonstrated their ability to survive and to cope with the parasites, while uninfected individuals are probably not yet tested for their resistance. This points to problems in using parasite prevalences and distributions, at least of some protozoan blood parasites, for tests of Hamilton-Zuk hypothesis, even though this was done in the first test by Hamilton and Zuk and by many later researchers     

Effects of a parasitic nematode on male mate choice in a livebearing fish with a coercive mating system (western mosquitofish, Gambusia affinis)

I examined the effects of the parasitic larval nematode, Eustrongylides ignotus, on male mate choice in the western mosquitofish, Gambusia affinis. I hypothesized that parasite presence influences male mate choice either directly (via reduction in male mating behavior due to presence of parasite in females) or indirectly (via reduction in male mating behavior due to reduced condition of infected females). Specifically, I tested the predictions that (1) males would mate preferentially with uninfected over infected females (scoring both mating attempts and association time with females); (2) parasitized females would be in poorer condition than non-parasitized females (measured as soluble fat stores); and (3) parasitized females would have reduced fecundity (measured as number of developing embryos). Males preferred to mate with non-parasitized over parasitized females, but showed no differences in association time between females. The nematode did not decrease female body condition, but did decrease female mass, and appeared to decrease female fecundity via reduction in broods (# embryos). Results support that parasites affect male mate choice in mosquitofish; however, the mechanisms used by males to differentiate between parasitized and non-parasitized females remain untested. This study provides the first empirical evidence of parasite affects on male mate choice in livebearing fishes, and suggest a potentially important role for parasite-mediated sexual selection in organisms that use coercive mating as the primary mechanism of obtaining mates.     

Colourful male European Serins Serinus serinus are more careful with their plumage

Ornamental traits typically advertise individual condition and can be costly to maintain. Plumage maintenance behaviour can increase plumage quality and positively influence female mate preference. We investigated this prediction by performing female mate‐choice trials and measuring male plumage maintenance behaviour in the European Serin Serinus serinus. More colourful males spent more time in plumage maintenance than less colourful males, but this was not correlated with body condition or ectoparasite load. Females preferred more colourful males, although this was not influenced by male plumage maintenance. Our findings highlight the fact that investment in plumage maintenance depends on individual coloration and this may reinforce the honesty of ornamental plumage and convey positive information for mate choice.     

Nonrandom pairing by male barn owls (Tyto alba) with respect to a female plumage trait

In socially monogamous species it is rare for females to bemore intensely colored than males. The barn owl (Tyto alba)is one of the exceptions, as females usually exhibit more andlarger black spots on the plumage. The evolution of sexual dimorphismin plumage traits is commonly assumed to be the result of sexualselection. I therefore examined the prediction that male barnowls do not pair randomly with respect to female plumage spottinessduring a 5-year study in Switzerland. The prediction was supported,as males that changed mates acquired a new female that was similarlyspotted to the previous one, and pairing with respect to plumage spottinesswas positively assortative. Significant repeatability in male pairingwas presumably neither the consequence of sharing the same habitats withfemales displaying a given plumage spottiness nor of morphological characteristicsof the males that could influence mate sampling. A resemblance inplumage spottiness between the mates of sons and of their fathersuggests that repeatability could have resulted from sexualimprinting and/or heritable variance in male preference forspotted females. To test whether males assess female plumagespottiness, I either cut off black spots or small pieces of feathersbut not the spots of already mated females. Males mated to females withreduced plumage spottiness fed their brood at a lower cadencyand achieved a lower reproductive success than other males.This experiment further suggests that female plumage spottinessis a stimulus for males.     

Fitness correlates of male coloration in a Lake Victoria cichlid fish

Sexual selection by female choice has contributed to the rapidevolution of phenotypic diversity in the cichlid fish speciesflocks of East Africa. Yet, very little is known about the ecologicalmechanisms that drive the evolution of female mating preferences.We studied fitness correlates of male nuptial coloration ina member of a diverse Lake Victoria cichlid lineage, Pundamilianyererei. In this species, male red coloration is subject tointraspecific sexual selection by female mate choice. Male nuptialcoloration plays a critical role also in reproductive isolationbetween this species and the closely related sympatric speciesP. pundamilia. Here, we show that P. nyererei male colorationis carotenoid based, illustrating the potential for honest signalingof individual quality. In a wild population, we found that variationin male coloration was not associated with variation in a setof strongly intercorrelated indicators of male dominance: malesize, territory size, and territory location. Instead, the 2male characters that predominantly determine female choice,territory size and red coloration, may be independent predictorsof male quality: males with bright red coloration and largeterritories had lower parasite infestation rates. As a result,female preferences tended to select against heavily parasitizedmales. Consistent with parasite-mediated sexual selection, maleshad higher and more variable parasite loads than females.     

The relative importance of male tail length and nuptial plumage on social dominance and mate choice in the red-backed fairy-wren Malurus melanocephalus: evidence for the multiple receiver hypothesis

Understanding why males of many species exhibit two or more sexual ornaments depends upon identifying both the information conveyed and the intended receiver(s) for each signal. Here we focus on identifying the intended receivers for two sexual signals exhibited by male red-backed fairy-wrens Malurus melanocephalus , extent of nuptial plumage and tail length. In doing so we test the multiple receiver hypothesis, which predicts that each trait is directed toward a different type of receiver (e.g., males vs females). Male red-backed fairy-wrens in nuptial plumage exhibit reversed sexual dimorphism for tail length in the breeding season, when their tails are significantly shorter than those of females or males in eclipse plumage. Using both aviary-based experiments and indices of mate choice and social dominance from a natural population, we found that extent of nuptial plumage and age primarily affected female mate choice and that shorter tails were primarily associated with male:male dominance signaling. The field and aviary studies combined are consistent with the multiple receiver hypothesis, in that each trait appears to be directed primarily to a different set of receivers (plumage for females and tail length for males), though each trait may also signal information to the other set of receivers as well. We propose that sexual selection may favor shorter tail lengths in male red-backed fairy-wrens through social competition mechanisms.     

Sexual selection in an anadromous population of threespine sticklebacks — no role for parasites

Summary We examined the hypothesis that trematode parasites played a role in the evolution of the red colour of male threespine sticklebacks (Gasterosteus aculeatus L.) and whether the parasites affected female fitness. Parasites (blackspot disease) played no role either in determining the outcome of male—male competition for breeding territories or in female mate choice. Among males with territories, mating success was highly variable. Some males obtained over 3000 eggs (approximately 10 matings) whereas others received none. In 1 year of the 2 year study, males with the greatest amount of red nuptial coloration had the greatest mating success. Although male colour may sometimes affect female choice in this system, this preference has probably not evolved because of the Hamilton—Zuk mechanism of sexual selection. The parasites had small, but statistically significant effects on female fitness. Females with high parasite loads were in poorer condition and produced fewer eggs than less parasitized fish.     

Female pied flycatchers trade between male quality and mating status in mate choice

According to mate choice theory, females should consider both male quality and mating status when choosing a mate. In birds, strong experimental evidence indicates that females prefer males with elaborate traits. No comparable evidence exists to determine whether females take male mating status into account or how they may trade between male quality and male mating status. We studied mate choice of female pied flycatchers (Ficedula hypoleuca) in outdoor aviaries where the effect of territory quality could be eliminated and where we could control which males were mated and which were unmated. We used male plumage colour as our measure of male quality. In the aviaries, focal females could easily compare males and assess their plumage colour and mating status, and resident females were prevented from attacking prospecting females because of separation in different compartments. The study provided evidence for a trade-off in mate choice. Females may compromise by choosing an already mated male if he is more brightly coloured and, presumably, of higher quality than available unmated males. The study did not support the idea that polygyny is based on male deception of females, but the results were consistent with the female aggression hypothesis.     

Secondary sexual traits, parasites, and polygyny in red-winged blackbirds, Agelaius phoeniceus

Data from a 3-year study of red-winged blackbirds (Agelaiusphoeniceus) were used to test the hypothesis that parasites(in this case, haematozoa) reduce male fitness and cause diminishedexpression of secondary sexual traits, which, in turn, are usedby females to select parasite-free males as mates. There wasno evidence indicating a fitness cost to being parasitized becauseparasitized males were as likely as unparasitized males to acquirea territory and to survive from one year to the next. Similarly,parasitized and unparasitized females did not differ with regardto how early they started nesting, how many eggs they laid,or their year-to-year survival. Secondary sexual traits, particularlyintrasexual aggression, did reliably (>80%) reveal the parasitestatus of males. Plumage and morphological traits also alloweddiscrimination of parasitized and unparasitized females. However,apparent mating patterns were unrelated to either the males'or the females' parasite status. Only if genetic analyses revealthat unparasitized males actually realize higher productivesuccess will these results potentially provide support for theparasite hypothesis of sexual selection.     

Choosy females and indiscriminate males: mate choice in mixed populations of sexual and hybridogenetic water frogs (Rana lessonae, Rana esculenta)

For several decades, behavioral ecologists have studied theeffects of the environment on the behavior of individuals;but only fairly recently they have started to ask the reversequestion: how do the behavioral strategies of individuals affectthe composition and dynamics of populations and communities?Although intuitively obvious, this feedback from individualto higher levels is difficult to demonstrate, except in systemswith exceptionally fast and marked responses of the populationsto the behavior of its members. Such a system exists in sperm-dependentspecies. In European water frogs, for instance, successfulreproduction of a hybrid species (R. esculenta, genotype LR)requires mating with one of its parental species (R. lessonae,genotype LL), except in the rare cases where hybrids are triploid.The sexual host LL, however, should avoid matings with the sexual parasite LR, because the resulting LR offspring willeliminate the L genome from their germ line. In this studywe investigate how this conflict is solved. Since water froghybrids come in both sexes, rather than as females only likein other sperm-dependent systems, we performed the tests withboth females and males. One individual was given a choice betweentwo individuals of the opposite sex, one an LL and the otheran LR. In both species, females showed the predicted preferencefor LL males, whereas males did not discriminate between LLand LR females. On the individual level, we interpret the sexdifference in choosiness by the lower costs from mating withthe wrong species (LR) and the higher benefits from matingwith large individuals in males than in females. In "normal"species, male preference for large (i.e. more fecund) femalesis advantageous, but in this system such a choice can resultin mating with the larger LR females. With respect to the structureand dynamics of mixed populations, we discuss that the observed female preference is consistent with the higher mating successof LL males found in nature. Hence, mate female choice is astrong candidate for a mechanism promoting coexistence of thesperm-dependent hybrid and its sexual host. This confirms predictionsfrom previous theoretical models.     

Parasites and mate choice in red jungle fowl

Captive flocks of red jungle fowl (Gallus gallus) experimentallyinfected with the intestinal nematode Ascaridia galli were usedto test Hamilton and Zuk's (1982) hypothesis that parasitesadversely affect male secondary sex characters and that femalesprefer unparasitized over parasitized males. Infected chicksgrew more slowly than uninfected controls, with the effect particularlypronounced on comb length rather than tarsus length or bodyweight. At sexual maturity, infected roosters had duller combsand eyes, shorter combs and tail feathers, and paler hacklefeathers than control roosters. In experimental mate choicetests, females preferred unparasitized over parasitized roostersby about 2: 1, and an analysis of covariance revealed that thehens were using the traits on which the two groups differedto make their mate choice decisions. Finally, in a test of anextension of the Hamilton and Zuk hypothesis, control and infectedmales were not distinguishable based on non sexually-selectedcharacters such as bill size, suggesting that parasites havea disproportionately larger effect on ornamental traits.     

Indications for female mate choice in grey-cheeked mangabeys <Emphasis Type="Italic">Lophocebus albigena johnstoni</Emphasis> in Kibale National Park,Uganda

Female sexual strategies affect male strategies and can play an important role in shaping mating systems. We investigated female sexual behaviour within five groups of grey-cheeked mangabeys in Kibale National Park, Uganda, and tested the hypothesis that females exhibit mate choice using as indications the prevalence of (1) females soliciting matings by presenting to males and (2) females refusing to mate with approaching males. In addition, we describe how these behaviours as well as grooming and copulation calls are distributed over high-ranking, low-ranking and migrating males and discuss these patterns with regard to trade-offs that could play a roll in female mate choice in multi-male groups. Females were promiscuous and initiated almost half of the matings, with both resident and migrating males. More than half of male mating approaches were refused by peak females. Female mate choice in this species may depend on individual female preferences, oestrus phase and male tactic.     

The evolution of female mate choice by sexual conflict

Although empirical evidence has shown that many male traits have evolved via sexual selection by female mate choice, our understanding of the adaptive value of female mating preferences is still very incomplete. It has recently been suggested that female mate choice may result from females evolving resistance rather than attraction to males, but this has been disputed. Here, we develop a quantitative genetic model showing that sexual conflict over mating indeed results in the joint evolution of costly female mate choice and exaggerated male traits under a wide range of circumstances. In contrast to tradition explanations of costly female mate choice, which rely on indirect genetic benefits, our model shows that mate choice can be generated as a side-effect of females evolving to reduce the direct costs of mating.     

Pairing success relative to male plumage redness and pigment symmetry in the house finch: temporal and geographic constancy

Male house finches (Carpodacus mexicanus) have carotenoid-based ornamentalplumage coloration. In previous research it was shown that fora single population of house finches in a single year, malesthat paired were on average redder in plumage coloration thanmales that did not pair, and males with redder plumage tendedto nest earlier than males with less red plumage. Here we showthat these patterns continued over 6 years and at two widely separatedlocations. We also tested whether the symmetry of carotenoid-based crownpigmentation differed between paired and unpaired males andfound that paired males have, on average, more perfect symmetryof crown pigmentation than males not paired. These observationssupport the idea that expression of carotenoid-based plumagecoloration by males is a persistent and widespread criterionin female mate choice in the house finch.     

Parasites and Bright Male Plumage in the Satin Bowerbird (Ptilonorhynchus violaceus)

Results from our field studies of the satin bowerbird (Ptilonorhynchusviolaceus) suggest that females choose males as mates basedon their level of infection with the ectoparasite (Myrsideaptilonorhynchi: Menoponidae). We evaluated predictions fromthree hypotheses for why this pattern of choice might evolve.The bright male and correlated infection models both suggestthat females choose parasite free males because these malesare more likely to sire parasite resistant offspring. The brightmale hypothesis suggests that females are able to gauge infectionbased on plumage brightness. The correlated infection hypothesisclaims that females assess resistance to endoparasites througha correlated effect on ectoparasites. In the parasite avoidancemodel female choice is shaped by the proximate benefits of avoidinginfection. Six predictions from these models were tested usinginformation on patterns of infection in satin bowerbirds. Ofthese models the parasite avoidance model was best supportedby the available data.     

Female barn owls (Tyto alba) advertise good genes

The good genes hypothesis of sexual selection postulates that ornamentation signals superior genetic quality to potential mates. Support for this hypothesis comes from studies on male ornamentation only, while it remains to be shown that female ornamentation may signal genetic quality as well. Female barn owls (Tyto alba) display more black spots on their plumage than males. The expression of this plumage trait has a genetic basis and it has been suggested that males prefer to mate with females displaying more black spots. Given the role of parasites in the evolution of sexually selected traits and of the immune system in parasite resistance, we hypothesize that the extent of female plumage 'spottiness' reflects immunological defence. We assessed the genetic variation in specific antibody production against a non-pathogenic antigen among cross-fostered nestlings and studied its covariation with the plumage spottiness of genetic parents. The magnitude of the antibody response was positively correlated with the plumage spottiness of the genetic mother but not of the genetic father. Our study thereby provides the first experimental support, to our knowledge, for the hypothesis that female ornamentation signals genetic quality.