The influence of parasites on host sexual selection

In 1982 Hamilton and Zuk(1) proposed a provocative solution for the unexplained fact that the males of many species exhibit 'showy' traits such as brightly coloured plumage or vigorous courtship displays. They suggested that showy traits are fully expressed only by males who are resistant to parasites and that females examine such traits in order to choose resistant males as mates. Hamilton and Zuk's proposal has been the topic of extensive research and vigorous debate for nearly a decade. This article reviews the research, relevant criticisms and unanswered questions pertaining to the influence of parasites on sexual selection.     

MALE MATE CHOICE AND THE EVOLUTION OF FEMALE PLUMAGE COLORATION IN THE HOUSE FINCH

The house finch (Carpodacus mexicanus) is a sexually dichromatic passerine in which males display colorful plumage and females are generally drab brown. Some females, however, have a subdued version of the same pattern of ornamental coloration seen in males. In previous research, I found that female house finches use male coloration as an important criterion when choosing mates and that the plumage brightness of males is a reliable indicator of male nest attentiveness. Male house finches invest substantially in the care of young and, like females, stand to gain by choosing high-quality mates. I therefore hypothesized that a female's plumage brightness might be correlated with her quality and be the basis for male mate choice. In laboratory mate choice experiments, male house finches showed a significant preference for the most brightly plumaged females presented. Observations of a wild population of house finches, however, suggest that female age is the primary criterion in male choice and that female plumage coloration is a secondary criterion. In addition, yearling females tended to have more brightly colored plumage than older females, and there was no relationship between female plumage coloration and overwinter survival, reproductive success, or condition. These observations fail to support the idea that female plumage coloration is an indicator of individual quality. Male mate choice for brightly plumaged females may have evolved as a correlated response to selection on females to choose brightly colored males.     

Air pollution fades the plumage of the Great Tit

1. Great Tits ( Parus major ) derive the carotenoid pigments for their yellow plumage via the prey items in their diet. Air pollution is known to affect the abundance of many forest insects, e.g. green caterpillars, which are an important source of food and pigments for tits. This study investigates whether air pollutants indirectly affected the intensity of the yellow colour in P. major plumage via the reduced access to carotenoid sources.
2. The intensity of the yellow colour in the plumage of P. major nestlings was scored and the relative abundance of green herbivorous larvae in territories around a polluting copper smelter in SW Finland was simultaneously measured.
3. Both the intensity of yellow colour in nestling plumage and caterpillar abundance increased with increasing distance from the pollution source. The colour intensity correlated significantly with the density of green herbivorous larvae in a territory.
4. Parus major nestlings were significantly heavier at distant sites than close to the pollution source which suggests that the future survival probability of pale nestlings may be lowered.
5. Young birds, after their first moult, were studied for the relationships between condition, size and plumage colour by the means of ptilochronology. The plumage colour intensity did not correlate with the size corrected width of the growth bars in fifth rectrix (condition at moult) but was correlated positively with the length of the rectrix (size).
6. The implications of colour change for survival and mate choice are discussed.     

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.     

Fat soluble antioxidants in brood-rearing great tits Parus major: relations to health and appearance

The concept of parasite-mediated sexual selection assumes that females may improve offspring fitness by selecting mates on the basis of sexual ornaments that honestly reveal the health state of a partner. Expression of such signals may be particularly sensitive to oxidative damage caused by excess production of oxidative metabolites and free radicals. To control and neutralise free radicals, animals rely heavily on dietary fat-soluble antioxidants such as vitamin E and A, and carotenoids. However, the organism's need for free radical scavenging may interfere with the opposite need to generate oxidative stress for fighting parasitic infections. We investigated plasma concentrations of carotenoids and vitamin A and E in brood-rearing great tits Parus major in relation to carotenoid-based plumage coloration, sex, habitat, leukocyte hemoconcentrations and infection status with Haemoproteus blood parasites. Rural great tits differed from urban ones and males from females with respect to the hue of the yellow ventral feathers. However, plasma antioxidant concentrations were not related to sex, habitat or plumage coloration. Plasma carotenoid concentration correlated positively with indices of immune system activation as measured by blood counts of lymphocytes and eosinophils. Birds with gametocytes of Haemoproteus in their blood had higher plasma concentrations of carotenoids and vitamin E than unparasitized individuals. These results are consistent with the idea that maintenance of high blood antioxidant levels might conflict with individual needs to rely on oxidative stress for fighting infections.     

Carotenoid-based plumage colouration is associated with blood parasite richness and stress protein levels in blue tits (Cyanistes caeruleus)

Carotenoids are molecules that birds are not able to synthesize and therefore, must be acquired through their diet. These pigments, besides their function of giving birds red and yellow colouration when deposited in feathers, seem to act as immune-stimulators and antioxidants in the organism. Hence, only the healthiest individuals would be able to express carotenoid-based ornaments to a larger extent without compromising the physiological functions of carotenoids. Various studies have reported that birds infected by parasites are paler than those uninfected, but, to our knowledge, none of them has assessed the possible effect of multiple infections by blood parasites on plumage colour. By comparing the yellow colour in the breast plumage of blue tits, Cyanistes caeruleus, between birds infected by different numbers of blood parasite genera, we found that those birds infected by more than one genus were paler than those parasitized just by one. In addition, we examined the potential role of carotenoid-based plumage colour of blue tits as a long-term indicator of other parameters of health status, such as body condition and immunoglobulin and heat shock protein (HSP) levels. Our results indicate that more brightly coloured birds had lower HSP70 levels than paler birds, but we did not find any significant association between colour and body condition or immunoglobulin levels. In addition, we found a positive significant association between Haemoproteus density of infection and HSP60 levels. Overall, these results support the role of carotenoid-based colours as indicators of health status in blue tits and show detrimental effects of parasitism on this character.     

Sexual Signals of the Male American Goldfinch

Male American goldfinches (Carduelis tristis) exhibit conspicuous yellow plumage, orange bills, and black caps during the breeding season. These secondary sexual characteristics may serve as criteria by which females evaluate males as potential mates because the traits vary among individuals and are likely to be costly. We quantified plumage and bill color and cap characteristics of wild, free‐ranging American goldfinches during the breeding season and tested for relationships between those features, body condition and individual genetic diversity in males. Overall, male and female goldfinches were highly sexually dichromatic, with plumage saturation and brightness and bill brightness contributing strongly to the dimorphism. Body condition decreased significantly with Julian date, even over the 2‐wk period immediately prior to the onset of nesting during which we collected our color and cap measurements. Principal components describing color of the back and the bill significantly predicted date‐corrected body condition based on quadratic regressions, suggesting that there is reliable information in back and bill color that females could use when choosing mates. In a subset of captive males, we found that bill hue faded from orange to yellow within 24 h of capture, suggesting that bill color may reflect short‐term changes in health status or carotenoid availability. Individual genetic diversity based on a panel of eight microsatellite loci was correlated with back brightness and perhaps with cap symmetry. Based on the results of this field study, ornamentation of male American goldfinches appears to signal both long‐ and short‐term aspects of phenotypic quality.     

PARTHENOGENESIS IN A FRESHWATER SNAIL: REPRODUCTIVE ASSURANCE VERSUS PARASITIC RELEASE

Two alternative (but not mutually exclusive) hypotheses were contrasted for their abilities to explain the distribution of parthenogenesis in the freshwater snail Potamopyrgus antipodarum: the reproductive assurance hypothesis, which predicts that parthenogenesis will be favored in sparse populations where mates are difficult to find, and the Red Queen hypothesis, which predicts that parthenogenesis will be favored in populations that have a low risk of parasitism. The results were inconsistent with the prediction of the reproductive assurance hypothesis; male frequency was not significantly or positively correlated with snail density. Thus, there was no support for any of the hypotheses for the maintenance of sex that rely on selection for reproductive assurance to explain the distribution of parthenogenesis (e.g., recombinational repair). The results, however, were consistent with the Red Queen hypothesis; male frequency was positively and significantly correlated with the frequency of individuals infected by trematodes. This correlation suggests that parthenogenetic females have replaced sexual females in populations where parasites are rare, and that sexual females have persisted in populations where parasites are common.     

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.     

Evidence that plumage bacteria influence feather coloration and body condition of eastern bluebirds Sialia sialis

Parasites influence the expression of secondary sexual traits and the health of infected individuals. We set out to test the influence of reputed exogenous parasites, plumage bacteria, including feather-degrading bacteria (FDB), on secondary sexual characteristics and body condition of wild adult eastern bluebirds Sialia sialis . Previous work has shown that FDB alter the coloration of structurally-colored bluebird feathers in vitro ( Shawkey et al. 2007 ). In a correlational study of how bacteria affect birds in the wild, we found that female plumage got duller with increasing FDB intensity. Males tended to get brighter with increasing FDB intensity, but the relationship was not significant. We also found significant associations between plumage bacteria intensity and body condition, but, again, with gender-based differences. Female body condition was negatively associated with plumage bacteria intensity, while male body condition was positively associated with plumage bacteria intensity. Interestingly, plumage bacteria intensity of males and females in nesting pairs was significantly positively correlated. We also report the highest prevalence of FDB measured in a wild bird population, with FDB detected on 67/68 (99%) of individuals. Further work is needed to fully understand the relationships between plumage bacteria and birds, but our data indicate that plumage bacteria may have sex-dependent effects on multiple phenotypic traits.     

Fat soluble antioxidants in brood‐rearing great tits Parus major: relations to health and appearance

The concept of parasite‐mediated sexual selection assumes that females may improve offspring fitness by selecting mates on the basis of sexual ornaments that honestly reveal the health state of a partner. Expression of such signals may be particularly sensitive to oxidative damage caused by excess production of oxidative metabolites and free radicals. To control and neutralise free radicals, animals rely heavily on dietary fat‐soluble antioxidants such as vitamin E and A, and carotenoids. However, the organism's need for free radical scavenging may interfere with the opposite need to generate oxidative stress for fighting parasitic infections. We investigated plasma concentrations of carotenoids and vitamin A and E in brood‐rearing great tits Parus major in relation to carotenoid‐based plumage coloration, sex, habitat, leukocyte hemoconcentrations and infection status with Haemoproteus blood parasites. Rural great tits differed from urban ones and males from females with respect to the hue of the yellow ventral feathers. However, plasma antioxidant concentrations were not related to sex, habitat or plumage coloration. Plasma carotenoid concentration correlated positively with indices of immune system activation as measured by blood counts of lymphocytes and eosinophils. Birds with gametocytes of Haemoproteus in their blood had higher plasma concentrations of carotenoids and vitamin E than unparasitized individuals. These results are consistent with the idea that maintenance of high blood antioxidant levels might conflict with individual needs to rely on oxidative stress for fighting infections.     

The social significance of plumage variability in wintering turnstone Arenaria interpres

Wintering turnstone, Arenaria interpres, have individually variable plumage. This paper examines the possibility that individual differences in plumage signal differences in dominance status (status signalling hypothesis) and/or allow individuals to be recognized by conspecifics (individual recognition hypothesis). The status signalling hypothesis was rejected on the basis of several lines of evidence: (1) differences in status between males and females, and between adults and juveniles, were not reflected by significant differences in plumage characteristics; (2) features of the plumage of adults remain the same from year to year yet the status of the adults probably changes; (3) in two flocks of wild turnstones dominance rank orders were not correlated with rank orders predicted by individual differences in three plumage variables. The individual recognition hypothesis was supported by tests showing that when the plumage of captive turnstone was experimentally altered, flock mates acted more aggressively towards them, irrespective of the form of the alteration.     

Signals of status in wintering white-crowned sparrows, Zonotrichia leucophrys gambelii

The possibility of plumage status signalling within the social systems of wintering birds has been a controversial issue. Our results are the first to demonstrate conclusively the reality of such signalling. Data from eight groups of captive white-crowned sparrows (Zonotrichia leucophrys gambelii), each with 8 to 11 different individuals, show that immature and adult females with crowns painted to resemble more brightly coloured, dominant adult males consistently win encounters with control birds of their own age and sex. These experiments demonstrate that signals that correlate with age (adult versus immature) and sex (adult male versus adult female) are used by the birds as reliable indicators of relative dominance position. Our demonstration of status signalling draws attention to the need to explain how such a system can be evolutionarily stable and we discuss some suitable models.     

Coloration,Paternity, and Assortative Mating in Western Bluebirds

Coloration in birds can act as an important sexual signal in males, yet in many species, both sexes display bright colors. Social selection may account for this pattern, with more brightly colored individuals pairing together on the best territories. Mutual mate choice may also explain this, as males investing a great deal of parental care in the offspring should be choosy about their social mates. It is less clear whether this pattern of mate choice can apply to extra‐pair partners as well. We examined western bluebirds (Sialia mexicana) to determine whether more colorful individuals tended to pair with one another, both in social pairs and between females and their extra‐pair partners. Both male and female western bluebirds display both UV‐blue structural plumage and a melanin‐based chestnut breast patch, although females are duller than males. Social pairs mated assortatively with regard to UV‐blue brightness, but not chestnut coloration. There was no evidence that extra‐pair partners mated assortatively, but males with brighter UV‐blue coloration had fewer extra‐pair offspring in their nests. Older males were more successful at siring extra‐pair offspring, despite displaying no differences in coloration compared to younger males. Coloration did not play a role in determining extra‐pair male success. These results suggest that coloration plays a role in the formation of social pairs, but not mate choice for extra‐pair partners.     

Female throat ornamentation does not reflect cell-mediated immune response in bluethroats Luscinia s. svecica

The brilliantly coloured throat patch in male bluethroats, Luscinia s. svecica, influences their social mating success and both within- and extra-pair paternity. Female bluethroats are highly variable in their extent of throat coloration, from entirely drab to almost male-like. The ornament in females could be due to a genetic correlation between the sexes. However, it has been shown that male bluethroats prefer brightly coloured females, suggesting that female ornamentation has evolved by direct sexual selection on females through male choice. Males may prefer extravagant traits in females if these reliably signal female quality, such as resistance to disease. We investigated whether variation in the extent of structural and melanin plumage ornamentation in female bluethroats reflects cell-mediated immune response. We caught the females at their nests and measured their immune response as a swelling following a challenge by phytohemagglutinin. An analysis of the data from two years of study revealed that the cell-mediated immune response was not related to female ornamentation. However, the immune response was strongly correlated with female body condition. Thus, our results do not support the hypothesis that female ornament expression signals quality in terms of cell-mediated immunity.     

Paternal care as a conditional strategy: distinct reproductive tactics associated with elaboration of plumage ornamentation in the house finch

When individuals in a population differ in physiological conditionand residual reproductive value, selection should favor phenotypicplasticity in reproductive investment such that individualsare able to adopt the reproductive tactic that results in thehighest fitness under given conditions. Here we examined reproductivetactics in relation to the elaboration of condition-dependentsexual ornamentation (carotenoid breast coloration) in a Montanapopulation of the house finches (Carpodacus mexicanus). Malesused distinct reproductive tactics depending on elaborationof their sexual ornamentation. Males with red pigmentation (maximum ornament elaboration) paired with females that nestedearlier, but these males did little provisioning of incubatingfemales and nestlings. In contrast, males with yellow colorationpaired with females that nested later, but these males fedfemale and nestlings more. Consequently, for red males offspringrecruitment was primarily affected by earlier nest initiation, whereas in yellow males it was affected most by male provisioning.In males with intermediate plumage coloration, all measuredcomponents, nest initiation, provisioning of incubating female,and nestling feeding, strongly contributed to offspring recruitment.The fitness consequences of alternative reproductive tacticsof males were influenced by breeding experience and fidelityof their mates. Among first-time breeders, red males achievedthe highest fecundity because of the advantage gained throughearly nesting and pairing with more experienced females andbecause of compensation by their mates for low male provisioningof nestlings. Among experienced breeders, males with intermediateplumage coloration achieved the highest fecundity because ofthe combined benefits of relatively early pairing and high parental care. High variation in sexual ornamentation in a Montana populationof house finches may favor distinct associations of sexualdisplays with a particular set of reproductive behaviors.     

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.     

Brighter yellow blue tits make better parents

Whether or not bird ornaments are a signal for direct (e.g. good parents) or indirect (e.g. good genes) benefits to prospective partners in sexual selection is controversial. Carotene coloration in Parus species is directly related to the ingestion of caterpillars, so that a brightly carotene-coloured tit may be signalling its ability to find caterpillars, a main high-quality food source for good fledgling development, and hence its parental abilities. If carotene-based plumage coloration is related to the good-parent hypothesis, we predict that yellow plumage brightness of tit fathers should be positively correlated to their investment in offspring provisioning. Here, we use cross-fostering experiments in blue tits (Parus caeruleus) to show that chick development (as measured by tarsus length) is related to yellowness of the foster father, but not to that of the genetic parents. Using these data, we were able to measure, for the first time to our knowledge, the separate contribution of genetic and environmental factors (i.e. parental plumage coloration) to chick development, and hence parental investment. Our data, which relate carotenoid coloration to models of good parents, and data from other authors, which relate ultraviolet coloration to good-genes models, stress that different kinds of coloration within an individual may provide different units of information to prospective females.     

Parental Effort in Relation to Structural Plumage Coloration in the Mountain Bluebird (Sialia currucoides)

Indicator models of sexual selection suggest that costly ornaments signal reliable information regarding an individual's quality to potential mates. In species that produce altricial offspring, the amount of parental care provided by both males and females can impact reproductive success. The Good Parent Hypothesis proposes that ornamentation in biparental species can act as an honest signal of parental ability to potential mates. We tested this hypothesis using the mountain bluebird (Sialia currucoides), a sexually dichromatic, socially monogamous species in which both sexes have structurally based ornamental plumage coloration. A male's plumage color predicted neither the rate at which it provisioned nestlings nor brood growth rate. The same was true for females. We also found no indication of assortative mating by color or body condition. Feeding rates within pairs were positively correlated, which we suggest may be due to pairs responding similarly to the perceived needs of nestlings or to local area prey availability. In sum, our results do not support the Good Parent Hypothesis as an explanation for the evolution of ornamental plumage color in mountain bluebirds. We suggest alternative hypotheses for the evolution of ornamental plumage color in this species.