Female choice for parasite-free male satin bowerbirds and the evolution of bright male plumage

Summary Hamilton and Zuk proposed that bright male plumage may have evolved in males of polygynous species as a result of female preferences for males that are able to demonstrate their resistance to disease. They predicted an inverse correlation between female mating preferences and the level of parasitic infection of males. We found such a correlation between the level of infection by a common ectoparasite (Myrsidea ptilonorhynchi: Menoponidae) and mating success of male satin bowerbirds (Ptilonorhynchus violaceus). In addition, we tested and were able to confirm three other predictions derived from their model: that (1) older males had fewer parasites than their younger counterparts, (2) levels of individual parasitic infection are highly correlated between years, and (3) that individuals resighted in successive years are less parasitized than those that fail to return. These results support the bright male model, but they are also consistent with two other hypotheses that may explain plumage dimorphism based on the level of parasitic infection. The correlated infection model suggests that females choose males with few ectoparasites because of a correlation between the level of ectoparasitic infection and heritable resistance to internal infections. In the parasite avoidance model, females favor parasitefree males because it lowers their own prospects for parasitic infection. Our data did not show the predicted relationship between parasite numbers with plumage quality that is needed to support the bright male hypothesis, nor did it show the inverse correlation between male condition and parasite numbers that is predicted by both the bright male and correlated infection hypotheses. Our results are most consistent with the parasite avoidance hypothesis.     

Personality and parasites: sex-dependent associations between avian malaria infection and multiple behavioural traits

The evolution and ecology of consistent behavioural variation, or personality, is currently the focus of much attention in natural populations. Associations between personality traits and parasite infections are increasingly being reported, but the extent to which multiple behavioural traits might be associated with parasitism at the same time is largely unknown. Here, we use a population of great tits, Parus major, to examine whether infection by avian malaria (Plasmodium and Leucocytozoon) is associated with three behavioural traits assayed under standardized conditions. All of these traits are of broad ecological significance and two of them are repeatable or heritable in our population. Here, we show weak correlations between some but not all of these behavioural traits, and sex-dependent associations between all three behavioural traits and parasite infection. Infected males showed increased problem-solving performance whereas infected females showed reduced performance; furthermore, uninfected females were four times more likely to solve problems than uninfected males. Infected females were more exploratory than uninfected females, but infection had no effect on males. Finally, infected males were more risk-averse than uninfected males but females were unaffected. Our results demonstrate the potential for complex interactions between consistent personality variation and parasite infection, though we discuss the difficulty of attributing causality in these associations. Accounting for complex parasite-behaviour associations may prove essential in understanding the evolutionary ecology of behavioural variation and the dynamics of host–parasite interactions.     

Altered responses to female odors in parasitized male mice: neuromodulatory mechanisms and relations to female choice

There is accumulating evidence that females may preferentially select parasite-free or -resistant males. Minimal attention has, however, been paid to the mate preferences and responses of the parasitized male hosts themselves. Here, we considered the effects of parasitic infection on male host mate responses, the neuromodulatory correlates of these responses, and the relations of these responses to female mate choice. Using an odor “preference” test, we examined the effects of different stages of an acute, sub-clinical infection with the naturally occurring, enteric, single host, protozoan parasite, Eimeria vermiformis, on the responses of male mice, Mus musculus domesticus, to the odors of estrous females along with the responses of uninfected females to the parasitized males. At 4 days post-infection (non-infective, pre-patent stage) E. vermiformis-infected male mice showed a significantly decreased preference for the odors of estrous females, whereas at 10 days post-infection (infective, patent stage) infected males showed a significantly increased preference for the odors of estrous females. Parasitized males displayed no significant changes in their responses to the odors of non-estrous females, supporting effects on the reproductively related responses of the host. In parallel, estrous females displayed a reduced interest in the odors of infected males. Least interest was expressed in the odors of the patent, infective males, consistent with the avoidance of contagion. Using selective opioid peptide receptor agonists and antagonists we found evidence that enhanced kappa opioid peptide (e.g., dynorphin) activity was related to the decreased sexual interest of the pre-infective males, while augmented delta opioid peptide (e.g., enkephalin) activity was associated with the enhanced responses of the infective males to females. We further showed that acute kappa opiate administration reduced the responses of uninfected males to females and that uninfected females displayed modified responses to the odors of uninfected males subject to acute modifications of opioid activity. We suggest that these differential shifts in endogenous opioid activity in the parasitized males are associated with and, or related to alterations in neuro-immune and endocrine functions. These findings show that parasitic infection can have, depending on the stage of infection and associated neuromodulatory changes, either significant facilitatory or inhibitory effects on male host preferences for and responses to females. Received: 22 April 1996 / Accepted after revision: 15 March 1997     

Trichinella spiralis infection in voles alters female odor preference but not partner preference

Females may choose mates based on secondary sex traits that reflect disease resistance. Accordingly, females should be able to distinguish between unparasitized and parasitized males, and should prefer to mate with unparasitized individuals. Mate and odor preferences for uninfected males or males infected with the nematode, Trichinella spiralis, were examined among prairie voles (Microtus ochrogaster) and meadow voles (M. pennsylvanicus). In a 15-min odor preference test, only female meadow voles distinguished between bedding from parasitized and unparasitized conspecific males, and preferred to spend time with bedding from unparasitized males. Although T. spiralis infection influenced odor preference in female meadow voles, there was no effect of infection status on mate preference among either species. Testosterone and corticosterone concentrations were not different between parasitized and unparasitized males. However, among prairie voles, males that spent an increased amount of time with females during the mate preference test had elevated testosterone concentrations. Taken together, these data suggest that (1) female meadow voles can discriminate between unparasitized and parasitized males, (2) the effects of infection on steroid hormone concentrations may be masked by the effects of social interactions, and (3) parasites may represent a selective constraint on partner preference in voles; however, the life cycle of parasites may influence female preference and should be considered in studies of female preference. Received: 23 April 1998 / Accepted after revision: 25 October 1998     

Male greenfinches (Carduelis chloris) with brighter ornaments have higher virus infection clearance rate

Hamilton and Zuk proposed that bright plumage in birds indicates genetic resistance to parasites, and that by selecting brighter males as mates, females can increase their offspring’s fitness due to this inherited resistance. The theory predicts a negative relationship between parasite load and plumage brightness in males. We used Sindbis virus clearance rate after an experimental infection to quantify parasite resistance in male greenfinches (Carduelis chloris) and related variation in clearance rate with variation in male plumage brightness. We found that certain aspects of brightness of the male plumage (i.e. tail-patch area) could be used to predict the virus infection clearance rate. Wing brightness was uninformative of virus clearance rate, but revealed age class. We found no clear relationship between antibody production rate and virus clearance rate or total viraemia. However, males with large tail patches tended to have a higher antibody production rate. The results suggest that the size of the male tail patch may function as an indicator of an individual male’s ability to resist parasite infections, thus supporting the Hamilton-Zuk theory for a novel taxon of parasites, a virus. Received: 11 November 1999 / Received in revised form: 13 March 2000 / Accepted: 1 April 2000     

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.     

Post-copulatory guarding,female choice and the levels of gregarine infections in the field cricket,Gryllus bimaculatus

Summary A recent model in sexual selection has proposed a role for parasites in maintaining heritable fitness variation. Females are envisaged as benefitting from preferentially mating with males that show resistance to infection. The post-copulatory guarding behaviour characteristic of many species of field cricket, has been envisaged as a means by which females assess male health and vigour. This hypothesis was tested in a field cricket, G. bimaculatus, which harbours a protozoan gut parasite. In enclosed arena trials, no direct correlations between female behaviours and levels of infection in males were found. However, there were significant correlations between the intensity of male guarding and the number of parasites found in the gut; infected males guarded more intensely in order to maintain contact with the female. In a second experiment simulating open field conditions, females left heavily parasitized males sooner than mildly or uninfected individuals. These data are discussed in relation to female choice for male health and vigour.     

Parasite load predicts mate choice in guppies

Summary The influence of parasites on mate selection and on a secondary sexual character was studied in guppies (Poecilia reticulata). In fish infected with Camallanus cotti or Gyrodactylus, females were found to prefer males with relatively few parasites, and this preference was associated with a higher display rate in less parasitised males.     

Patterns of host switching in the fish ectoparasite <Emphasis Type="Italic">Argulus coregoni</Emphasis>

Mating is essential for sexually reproducing species to pass on their genes. For sexual parasites, this implies a need to switch the host in the search for a mate when potential partners are not available on the same host, although host switching includes risks like starvation and predation. Studies of mate-searching behavior predict that commonly only one sex searches for mating partners while the other remains stationary. In the present work, we experimentally infected rainbow trout (Oncorhynchus mykiss) with the fish ectoparasite Argulus coregoni and determined whether the sex, age and the presence of mating partners influenced the host switching activity. Our results show that increased host switching by A. coregoni occurred only after the parasite reached the adult stage and a difference between the sexes was also recorded. Host switching by mature males was enhanced when no mating partners were present on the same host, whereas females remained mainly stationary on their host regardless of male presence or absence. Our data therefore support the hypothesis that there is a strategic difference in reproductive behavior between males and females; males invest energy in mate searching while females are rather stationary and invest into body size and hence increased fecundity. Our data also showed that leaving the host to find a mate is potentially costly in terms of predation since a substantial number of free-swimming parasites were eaten by fish.     

Mate sampling behaviour of black grouse females (Tetrao tetrix)

We studied female mate sampling behaviour in lekking black grouse (Tetrao tetrix). Females mainly visited males occupying territories in the centre of the lek with relatively large territories. They were also more likely to visit males that had high attendance. The same factors were also correlated with male mating success. A multiple regression model including these factors explained more of the variance in female visits per male (53%) than in mating success (33%). The pattern of female sampling conformed with a pool comparison (best-of-n) tactic. Such a tactic is expected if the costs of sampling are low. Females of high body mass visited more males than lighter females, however, which indicates that females may vary in their search tactics and suggests that there may be search costs. The existence of costs is further suggested by the fact that if the mate from a previous year was still present, females always mated with the same male in the following year. Though search costs were not measured directly, our findings suggest that some costs are negligible (e.g. energetic exhaustion or predation) whereas others (timing of mating) may be more important.     

Mate preferences in <Emphasis Type="Italic">Drosophila</Emphasis> infected with <Emphasis Type="Italic">Wolbachia</Emphasis>?

The maternally inherited bacterium Wolbachia pipientis generates strong reproductive incompatibilities between uninfected females and infected males (cytoplasmic incompatibility), significantly reducing both female and male reproductive success. Such fitness costs are thought to place selective pressure on hosts to evolve pre-copulatory preferences for mating with compatible mates, thereby enabling them to avoid the reproductive incompatibilities associated with Wolbachia. Therefore, uninfected females are predicted to prefer mating with uninfected males, whereas infected males are predicted to prefer mating with infected females. Despite these predictions, previous investigations of pre-copulatory mate preferences in Wolbachia-manipulated Drosophila have not found evidence of female preference for uninfected or compatible males. However, none of these studies utilised a design where focal individuals are provided with a simple choice in a relatively non-competitive situation. We examined both female and male pre-copulatory mate preference based on mate infection status in Drosophila simulans and D. melanogaster using simple choice assays involving between 30–50 replicates per treatment. Although we found no evidence of female pre-copulatory mate preferences in either species, male D. simulans exhibited some preference for mating with females of the same infection status. However, this preference was not evident when we repeated the experiment to confirm this finding. Consequently, we conclude that neither male nor female D. melanogaster and D. simulans exhibit significant Wolbachia-associated pre-copulatory mate preferences.     

Parasite distribution and virulence: implications for parasite-mediated sexual selection

The Hamilton-Zuk hypothesis states that females choosing males with more developed secondary sexual traits, i.e. brighter males, achieve greater fitness if variability in brightness reflects heritable variation in resistance to parasites. However, several factors will affect the likelihood that parasites play a role in sexual selection in given species. Here, using simple models, we show that because of parasite aggregation on a few hosts, only few breeding males would suffer from reductions in brightness due to parasites. Only in cases where parasites are abundant and show low levels of aggregation among their hosts would there be sufficient variability in brightness among breeding males for female choice of bright, resistant males to evolve. In addition, sufficient parasite-induced variability in brightness among breeding males will only occur in host-parasite systems where pathology is linearly related to the number of parasites per host. The presence of males that are uninfected and bright but genetically susceptible to parasites will also influence the fitness advantages obtained by females choosing bright males. If genetic immunity against parasites is rare in the host population, females can probably only benefit from choosing bright males if parasites are common and little aggregated among males. These results greatly limit the generality of the Hamilton-Zuk hypothesis, and suggest that only a small fraction of host-parasite associations could promote the evolution of host mate choice for resistance based on brightness. Correspondence to: R. Poulin     

Some constraints on reproduction for male bushcrickets,Requena verticalis (Orthoptera : Tettigoniidae) diet,size and parasite load

Summary Reproduction for male bushcrickets is energetically expensive. Male Requena verticalis invest 70% of their daily energy reserves in calling to attract a female and providing her with a nutritious spermatophore. Males are thereby likely to be constrained in their mating frequency. I investigated constraints on reproduction imposed by body size and the levels of a protozoan gut parasite when males were fed diets that differed in their nutritional value. Males suffered a cost of reproduction in terms of an increasing interval between matings that was independent of diet and parasitic infection. After three successive matings, males decreased the magnitude of investment in courtship feeding when fed a diet poor in protein. Furthermore, these males suffered a reduction in the number of times they were capable of mating relative to males fed a diet rich in protein. Male size constrained mating frequency on both rich and poor diets; small males were able to mate less frequently than large males. There was an interaction between the effects of diet and parasitic infection on male mating frequency. Heavily infected males mated less frequently than uninfected individuals when fed the poor diet. However, males fed the rich diet were able to overcome the constraints imposed by parasitic infection. Reproductive constraints are discussed in relation to the costs of reproduction and their effects on courtship roles.     

Reproductive trade-offs from mating with a successful male: the case of the tephritid fly Anastrepha obliqua

In lekking species, females may become sperm-limited when mating with sexually successful males, and this may be exacerbated by a poor male diet. Polygynous males may also be limited by the amount of accessory gland products (AGPs) they can transmit to females, which in turn may influence the females’ refractory period and longevity. Here, we tested the effect of male mating history, larval and adult diet on copula duration, mating intervals, female fecundity, fertilisation success, life span and likelihood to remate using sexually successful males of the lekking tephritid fly Anastrepha obliqua. Flies originated from either a native or exotic host fruit and were protein-fed or deprived. Male diet and larval host influenced copula duration, while the time elapsed between matings was affected by the interaction of mating order and male adult diet. Female fecundity was not influenced by female position in mating order or protein inclusion into the male diet. However, mating order and male larval diet influenced female fertilisation success. Importantly, as males mated successively they were less able to induce a refractory period on females, as the last females to mate with a male were more likely to remate and had slightly longer life spans than the first females to mate with males. These results might be attributed to a decrease in male AGPs with increasing male mating frequency. We discuss the role of conditional expression of male mating frequency with respect to A. obliqua’s life history, the trade-off that females face when mating with a successful male, the effect of larval diet on adult sexual performance and the possibility for sexual conflict to occur due to high male mating rates and fitness costs to females.     

An experimental test of female choice relative to male structural coloration in eastern bluebirds

Several experimental studies have shown that female birds use ornamental melanin and carotenoid plumage coloration as criteria in mate choice. Whether females choose mates based on natural variation in structural coloration, however, has not been well established. Male eastern bluebirds (Sialia sialis) display brilliant ultraviolet (UV)-blue plumage coloration on their head, back, wings, and tail, which is positively correlated with condition, reproductive effort, and reproductive success. We experimentally tested the hypothesis that female eastern bluebirds prefer as mates males that display brighter structural coloration by presenting breeding-condition females with males of variable coloration. We conducted two types of mate-choice experiments. First, females chose between males whose coloration was manipulated within the natural range of variation in the population; feathers were either brightened with violet marker or dulled with black marker. Second, females chose between males with naturally dull or bright plumage coloration. In both manipulated and unmanipulated coloration trials, female choice did not differ significantly from random with respect to structural coloration. We found no support for the hypothesis that the UV–blue coloration of male eastern bluebirds functions as a criterion in female mate choice.     

Bat predation and the evolution of leks in acoustic moths

Theories of lek evolution generally invoke enhanced mating success experienced by males signalling in aggregations. Reduced predation has also been acknowledged as a potential factor driving lek formation, but its role is more ambiguous. Although lekking is a complex behaviour, few empirical studies have investigated the role of both claims. We studied the potential pressures imposed by mating success and predation in an acoustic moth, Achroia grisella, in which males gather in leks and broadcast a calling song attractive to females. We exploited the ability to manipulate the distribution of singing males in laboratory arenas to create different-sized leks and tested female preferences for these aggregations. Because A. grisella are vulnerable to predation by bats while in flight and on the substrate, we also tested the responses of a potential predator, Rhinolophus ferrumequinum, a bat species that feeds on moths, to the experimental leks. We found that the per capita attractiveness of A. grisella males to females rose with increasing lek size. R. ferrumequinum also oriented toward experimental A. grisella leks, but this attraction did not increase at larger leks. Thus, a male’s per capita exposure to predation risk declined as more moths joined the lek. A. grisella males appear to benefit from advertising in larger leks in terms of both increased mate attraction and reduced predation risk. Our results support the idea that multiple factors operating simultaneously may maintain lekking behaviour.     

Chemical ornaments of male lizards <Emphasis Type="Italic">Psammodromus algirus</Emphasis> may reveal their parasite load and health state to females

Evidence for parasite-mediated sexual selection has been found in many species that use visual ornaments to attract females. However, in many animals, variation in female responses to scents of parasitized males suggests that parasitic infections might also affect information conveyed by pheromones (i.e., chemical ornaments). Thus, pheromones might also function in parasite-mediated sexual selection. We show here that female lizards Psammodromus algirus responded differently to femoral gland secretions of males according to the parasite load and health of these males. Scents of healthier males elicited more tongue flicks (a chemosensory behavior) by females, suggesting that these scents were more attractive. Chemical analyses showed that parasite load and the T-cell-mediated immune response were related to the variability in the proportions of some lipids in secretions of males. Further trials testing the chemosensory responses of females to chemical standards indicated that females actually discriminated the chemicals related to males’ health from other chemicals found in secretions. We suggest that these chemical ornaments may provide reliable information on the health and degree of parasitic infection of a male.     

Intraspecific brood parasitism in the moorhen: parentage and parasite-host relationships determined by DNA fingerprinting

Parasitic female moorhens (Gallinula chloropus) lay from one to six eggs in the nests of conspecific neighbours. DNA fingerprinting was used to show that parasitic eggs could be correctly identified when they appeared in addition to or outside the host’s laying sequence. Moorhen hosts accept all parasitic eggs laid after the 2nd day of their laying period. To understand why moorhen hosts tolerate parasitic eggs, we tested two hypotheses. (1) The quasi-parasitism hypothesis: females lay their eggs in the evening when the host males are normally in attendance at the nest, so host males may allow parasitic females to lay in their nests in exchange for fertilizing their eggs. However, DNA fingerprinting showed that all the parasitic eggs were sired by the parasites’ mates. Parasitic moorhens frequently continue laying a clutch in their own nest, without a break in the laying sequence after a parasitic laying bout. The eggs laid by brood parasites in their own nests were also sired by their own mates. Therefore this hypothesis was rejected. (2) The kin selection hypothesis: if one or both members of the host pair are close relatives of the parasite, the costs of rearing parasitic chicks will be to some degree offset by inclusive fitness benefits. We examined the genetic relationships between parasites and their hosts using DNA fingerprinting and genealogical data. Natal philopatry by both sexes was relatively common in this population, and the probability that a neighbour of either sex was a first-order relative (parent-offspring) was calculated as 0.18. Although first-order relatives were not preferentially chosen as hosts over individuals that were not first-order relatives, even through random host selection there is almost a one-in-five chance that brood parasites in this population are closely related to their hosts. This may facilitate host tolerance of parasitic eggs. Other hypotheses are also discussed. Received: 3 February 1995/Accepted after revision: 27 August 1995     

The effect of perceived female parasite load on post-copulatory male choice in a sex-role-reversed pipefish

The last several decades of research in behavioral ecology have resulted in a deeper appreciation of post-mating processes and sexual conflict in sexual selection. One of the most controversial aspects of sexual selection is cryptic mate choice. Here, we take advantage of male pregnancy in a sex-role-reversed pipefish (Syngnathus typhle) to quantify cryptic choice based on perceived parasite load and other sources of variance in female fitness. Studies have shown that S. typhle males preferentially mate with females with lower parasite loads and that a male’s perception of female parasite load can be altered by tattooing females. We manipulated the apparent parasite load of females in controlled mating experiments to test the hypothesis that post-copulatory sexual selection is dependent on a male’s perception of female parasite load in pipefish. Our results provided no evidence for cryptic male choice based on perceived female parasite load. However, we found evidence that eggs from larger females were more likely to result in viable offspring than eggs from smaller females and that the first female to mate with a male transferred more eggs per copulation on average. Overall, our results show that potential for post-copulatory sexual selection does exist in pipefish, but the male’s perception of female parasite load does not play a major role in this process.     

The basis for female choice in an avian brood parasite

Summary Behavioral observation and experimental manipulation of a marked population of brood parasitic brown-headed cowbirds (Molothrus ater) were conducted to determine whether or not females exhibit mate choice and to elucidate the ultimate basis for any such choice. Female choice was indicated by the fact that each female copulated with only one male, although most were courted by several. Patterns of female aggression towards males also revealed that females had the opportunity to display choice. Courtship by males was sometimes treated by females as harassment, but there was no conclusive evidence that a male provided his mate with protection from harassment by other males. Nor was there any indication of other proximate benefits or services males might have provided for females. Thus, there is no evidence that males provide females with anything other than their genes. An experimental removal of mated males and the pattern of subsequent remating of widowed females are consistent with female choice for male genetic quality. Offprint requests to: D.A. Yokel at the present address