Evidence for differential maternal allocation to eggs in relation to manipulated male attractiveness in the pied flycatcher (Ficedula hypoleuca)

We present evidence of differential maternal allocation to eggs in response to manipulated male attractiveness in the migratory pied flycatcher (Ficedula hypoleuca). We manipulated the size of a male secondary sexual trait, the white forehead patch, right after male arrival to the breeding area and before female arrival. Patch size was (1) enlarged to the maximum observed in the population, (2) reduced by 40% or (3) kept constant by painting with indelible felt markers over the natural feather patch. Male behaviour was affected by the experimental manipulation, as individuals with enlarged patches performed more approaches to the nestbox in response to song playback during the territory occupation and nest-site presentation phases. Females paired with males with reduced forehead patches laid significantly smaller eggs than those paired with males in the control and enlarged-patch treatments. Laying date and clutch size did not differ among the experimental groups. We discuss that manipulations of ornaments designed to study differential allocation at laying should reduce as well as enlarge their expression.     

POPULATION DIVERGENCE IN SEXUAL ORNAMENTS: THE WHITE FOREHEAD PATCH OF NORWEGIAN PIED FLYCATCHERS IS SMALL AND UNSEXY

Models of sexual selection suggest that populations may easily diverge in male secondary sexual characters. Studies of a Spanish population of the pied flycatcher, Ficedula hypoleuca, and a Swedish population of the closely related collared flycatcher, F. albicollis, have indicated that the white forehead patch of males is a sexually selected trait. We studied the white forehead patch of male pied flycatchers (n = 487) in a Norwegian population over seven years. Males with large forehead patches were in general more brightly colored, but patch height was not correlated to body mass, body size, or parasite loads. Conditions during the nestling period did not seem to influence patch height as an adult. Patch height increased slightly from the first to the second year as adults, but then remained relatively constant at higher ages. Patch height was not related to survival. Year-to-year changes showed that males who increased in patch height also increased in body mass, suggesting that expression of the forehead patch may be partly condition dependent. However, changes in body mass explained only a small proportion of the variance in patch height between males. Thus, patch height would not be a good indicator of male quality. Furthermore, patch size was also not related to male ability to feed nestlings, indicating that females would not obtain direct benefits by choosing males with large patches. However, patch height could be a Fisher trait, but this requires heritability and there was no significant father-son resemblance in patch height. Comparisons of the males visited by each female during the mate sampling period indicated that chosen males did not have larger forehead patches than rejected males. Experimental manipulation of patch height did not affect male mating success. These results indicate that females do not use patch size as a mate choice cue. Finally, patch height did not predict the outcome of male contests for nestboxes, suggesting that the forehead patch is not an intrasexually selected cue of status. Norwegian pied flycatchers have smaller forehead patches than both Spanish pied flycatchers and Swedish collared flycatchers. We suggest that this pattern may be explained by the lack of sexual selection on the forehead patch in the Norwegian population as compared to the other populations, where the patch is apparently sexually selected. We discuss possible reasons for these population divergences, such as female choice on an alternative secondary sexual character (general plumage color) and speciation among Ficedula flycatchers.     

Female ornaments in the Pied Flycatcher Ficedula hypoleuca: associations with age, health and reproductive success

Female ornamentation has received little attention in studies of sexual selection. Traditionally, female ornaments have been explained as a genetically correlated response to selection in males. However, recent findings suggest that female ornaments may be adaptive. Southern populations of Pied Flycatchers Ficedula hypoleuca are suited for studies of female ornamentation because, in addition to the white wing patch, some females also express the white forehead patch characteristic of males. We thus addressed the associations of these two ornaments with female age and with some health and breeding parameters in a Spanish population of Pied Flycatchers. Female ornament expression was not associated with haemoparasite prevalences, clutch size or parental provisioning effort. However, females expressing the white forehead patch raised more fledglings, and females with larger wing patches bred earlier, had higher number of hatchlings and showed increased levels of total serum immunoglobulins. Thus, these two unrelated epigamic ornaments may indicate some aspects of female quality. Further experimental studies could test the possibility that these plumage traits might function as signals to the males or might be used during female–female aggressive encounters in competition for nest-sites and mates.     

Status signalling in male but not in female Eurasian Tree Sparrows Passer montanus

Male ornaments, such as plumage coloration, frequently serve as signals. The signalling function of similar ornaments in females has, however, received much less attention despite the fact that conspicuousness of their ornaments is often comparable to those of males. In this study we tested the signalling function of a plumage trait present in both sexes in the Eurasian Tree Sparrow Passer montanus. The black throat patch has been repeatedly found to have a signal function in the closely related House Sparrow Passer domesticus, where only males bear the ornamental trait. However, the function of the black throat patch in the females of Passer species that have sexually monomorphic ornament expression has never, to our knowledge, been considered. We investigated the outcomes of aggressive encounters in foraging flocks of free‐living Tree Sparrows, and assessed whether throat patch size and measurements of body size predicted fighting success in these flocks. We found that male throat patch size predicted fighting success against both male and female opponents. However, female throat patch size did not correlate with fighting success against either sex. Among the morphological traits studied, wing length was the best predictor of fighting success in females. Our findings suggest a status signalling function of throat patch size in males but not in females, although further experimental studies are necessary to corroborate these correlative results.     

Phenotypic plasticity in breeding plumage signals in both sexes of a migratory bird: responses to breeding conditions

Adaptive phenotypic plasticity may respond to present ambient conditions. Sexual and social signals in both sexes may express phenotype performance. Plumage signals that change discontinuously allow relating discrete variation to previous performance. Both sexes of the pied flycatcher Ficedula hypoleuca present white patches on the wings and on the forehead, which constitute sexual and social signals. Forehead patches are moulted together with body plumage in Africa, while wing patches are partly moulted in Africa and partly in the breeding area soon after breeding. We studied individual inter‐year changes (corrected for regression to the mean) in the size of forehead and wing patches of both sexes in seven years for females or six years for males in two nearby study areas in central Spain. We found that initial signal extent strongly delimits the possible subsequent changes negatively. There is a negative association of male age with forehead patch changes. Cold and rainy springs are associated in females with decreases in both patch areas and vice versa, while no association with climate is observed in male wing patch changes. Cold pre‐breeding conditions predict positive changes in female wing and male forehead patches. Breeding success is positively associated with forehead patch changes in females. Late‐breeding males experience more positive changes in forehead patch size than early‐breeding males. Some of these trends can be explained by variable costs of breeding in certain conditions for subsequent signal production and/or maintenance, while absence of trends in some cases may be explained by sex differences in costs of breeding and interactions with phenotypic quality of breeders.     

Females Paired with More Attractive Males Show Reduced Oxidative Damage: Possible Direct Benefits of Mate Choice in Pied Flycatchers

Direct benefits of female mate choice may concern female fertility and fecundity but also physiological status. In birds with biparental care, males may contribute to improve the condition and health of their pair‐mates through help in constructing nests, incubation or incubation feeding and nestling provisioning. They may also reduce harassment of females by non‐pair males. A consequence of these male activities could be expressed in terms of oxidative damage, which may depend on metabolic effort and social stress. Here, we have related male contribution to parental and territorial duties to female oxidative status in the pied flycatcher Ficedula hypoleuca, a species where preferred males present darker dorsal plumage and, in Iberian populations, a large white forehead patch. Darker males were paired with females with high incubation attendance and reduced nestling provisioning rates, which may lead to reduced female exertion. These males owned nest boxes at which there were fewer visits by non‐pair males. Although females paired with dark mates worked less hard, they were able to raise more fledglings. Female oxidative damage measured as malondialdehyde (MDA) level in plasma declined with increasing incubation attendance and male incubation feeding. Moreover, levels of MDA in females declined with both darkness of male dorsal plumage and male forehead patch size when controlling for female forehead patch size and male age. The effect of male plumage darkness was especially strong. Females paired with middle‐aged males (2–3 yr) showed reduced levels of MDA compared with those paired with 1‐yr‐old and more than 3‐yr‐old males. Male age could not explain the effects of male attractiveness. Females paired with attractive males were more successful in reproduction while suffering reduced oxidative damage, possibly mediated by help during incubation and nestling rearing from their pair‐mates. Although correlative, the evidence suggests direct benefits of females paired with more attractive males.     

Experimentally reduced male attractiveness increases parental care in the pied flycatcher Ficedula hypoleuca

This study reports effects of experimental manipulations ofreproductive effort and the size of the male's white foreheadpatch (a secondary sexual trait), on provisioning rates, reproductivesuccess, and parental breeding dispersal distance in the piedflycatcher, Ficedula hypoleuca. Parents caring for enlargedbroods resulting from manipulated clutches provisioned nestsat higher rates than parents with reduced broods. Males with a reduced forehead patch fed their nestlings more in relationto males with an unmanipulated forehead patch, and their youngfledging with a longer tarsi. This suggests that males witha reduced attractiveness may perceive their own attractivenessand they devote more time available for parental effort given their poorer prospects in male contest competition and/or femaleattraction for extra-pair copulations. However, their femalesdid not alter their provisioning effort and this runs counterto both the differential allocation and the partner-compensationhypotheses. An artificial decrease in a male secondary sexualtrait led to a wider breeding dispersal distance between successiveyears.     

Female ornamentation, parental quality, and competitive ability in the rock sparrow

The evolution of female ornaments is poorly understood. Recent evidence suggests not only that female ornaments may be genetic correlates of selection on males but may also have evolved through male mate choice and/or through female–female aggressive interactions. In the rock sparrow, Petronia petronia, both sexes have a carotenoid-based yellow patch that is sexually selected by both sexes. The benefits that male may gain from choosing an attractive female remain unidentified. Both parents participate in caring for the young, so there should be mutual mate choice because males and females should both benefit from choosing a good parent (good parent hypothesis; GPH). Moreover, it has already been demonstrated that the yellow patch in males is also a badge of status (armament). Therefore, the yellow patch could also serve as both ornament and armament in females (dual utility hypothesis; DUH). We investigated the hypothesis that male and female yellow patch size signals parental quality in the field. We tested by an experiment in captivity the signal function of the yellow patch in female–female aggressive interactions for access to food. Yellow patch size correlated with paternal, but not maternal, feeding rates. Thus, this study supports the hypothesis that yellow patch dimension signals male parental quality, but there is no evidence for the GPH to explain female ornamentation. In the experiment females with relatively large yellow patches had earlier access to food than those with small patches. These results seem to suggest that a sexually selected carotenoid-feather signal may be used in female–female competition, in agreement with the DUH. Males may benefit from choosing well ornamented females because these may be superior competitors.     

The effect of parental quality and malaria infection on nestling performance in the Collared Flycatcher (Ficedula albicollis)

Plumage ornamentation often signals the quality of males and, therefore, female birds may choose elaborately ornamented mates to increase their fitness. Such mate choice may confer both direct and indirect benefits to the offspring. Males with elaborate ornaments may provide good genes, which can result in better nestling growth, survival or resistance against parasitic infections. However, these males may also provision their offspring with more food or food of better quality, resulting in nestlings growing at a higher rate or fledging in better condition. In this study, we examined if there was an association between male ornamentation and malaria infection in Collared Flycatchers (Ficedula albicollis). We also investigated offspring performance in relation to malaria infection in the parents and the quality of the genetic and rearing fathers (assessed by the size of two secondary sexual characters) under simulated good and bad conditions (using brood size manipulation). We found that secondary sexual characters did not signal the ability of males to avoid parasitic infections, and malaria infection in the genetic and the rearing parents had no effect on nestling growth and fledging size. Our results do show, however, that it may be beneficial for the females to mate with males with a large forehead patch because wing feathers of nestlings reared by large-patched males grew at a higher rate. Fast feather growth can result in earlier fledging which, in turn, could improve nestling survival in highly variable environments or under strong nest predation.     

An investigation of mate choice based on manipulation of multiple ornaments in Kentish plovers

Many animals have multiple sexual ornaments, a fact variously explained as signalling of multiple attributes, or nonadaptive retention of now redundant, but previously informative, signals. Despite the widespread occurrence of multiple ornaments, and the theoretical interest in how they are maintained by selection, there have been few experimental studies of the phenomenon. We investigated the role of two ornaments, each plausibly signalling different male attributes, in attracting a new mate in the Kentish plover, Charadrius alexandrinus. Previously we have shown that male Kentish plovers vary in how long they take to acquire a new mate, and we hypothesized that this variation may relate to their attractiveness or parental ability. We created single males by removing their mate and clutch, and then manipulated both their badge size (a presumed signal of either their genetic quality or their dominance status and hence defensive abilities) and the length of their flank feathers (a presumed signal of their parental quality in incubation) in a 2×2 factorial design. We found no difference in remating times between manipulated and control males. Furthermore, neither body size nor body condition of males was related to their remating times, although males with enlarged badges spent less time fighting than control males. Taken together, our results suggest that female Kentish plovers do not use either badge size or the length of flank feathers as cues in their mate choice decisions. However, badge size may influence male-male competition.     

Reproductive effort of both male and female Bar‐throated Apalis Apalis thoracica is predicted by ornamentation of self and mate

Melanin‐based plumage ornaments have been shown to play an important role in male–male competition, but also influence inter‐sexual communication. Consequently, ornaments may be associated with reproductive effort of both males and females. Females mated to males with larger melanin ornaments may acquire access to better territories or benefit from increased paternal care. Here we investigated whether the melanin‐based breast‐band of male and female Bar‐throated Apalis Apalis thoracica is a signal of information about its bearer and is associated with male and female reproductive effort. Breast‐band size was a highly variable morphometric trait in both sexes, but only in males was it associated with body mass. We then assessed whether male and female breast‐band size predicted maternal and paternal investment. Egg mass increased with male breast‐band size, but decreased with female breast‐band size. Whether females adjust maternal hormone allocation in response to their partner's ornamentation remains a contentious issue. We found that yolk testosterone and androstenedione concentrations were not predicted by male ornamentation or body mass. Finally, males with larger breast‐bands provided their mates with more food, allowing those females to spend more time incubating. Reproductive effort of both parents is therefore predicted by their own and their mate's ornamentation in Bar‐throated Apalis, and thus breast‐band size potentially acts as a signal of reproductive performance in both sexes. These results highlight the need for more comprehensive analyses of a relationship between melanin‐based ornaments and fitness, incorporating multiple behavioural variables associated with reproductive effort.     

Carry‐over effects of conditions at the wintering grounds on breeding plumage signals in a migratory bird: roles of phenotypic plasticity and selection

To understand the consequences of ever‐changing environment on the dynamics of phenotypic traits, distinguishing between selection processes and individual plasticity is crucial. We examined individual consistency/plasticity in several male secondary sexual traits expressed during the breeding season (white wing and forehead patch size, UV reflectance of white wing patch and dorsal melanin coloration) in a migratory pied flycatcher (Ficedula hypoleuca) population over an 11‐year period. Furthermore, we studied carry‐over effects of three environmental variables (NAO, a climatic index; NDVI, a vegetation index; and rainfall) at the wintering grounds (during prebreeding moult) on the expression of these breeding plumage traits of pied flycatcher males at individual and population levels. Whereas NAO correlates negatively with moisture in West Africa, NDVI correlates positively with primary production. Forehead patch size and melanin coloration were highly consistent within individuals among years, whereas the consistency of the other two traits was moderate. Wing patch size decreased with higher NAO and increased with higher rainfall and NDVI at the individual level. Interestingly, small‐patched males suffered lower survival during high NAO winters than large‐patched males, and vice versa during low NAO winters. These counteracting processes meant that the individual‐level change was masked at the population level where no relationship was found. Our results provide a good example of how variation in the phenotypic composition of a natural population can be a result of both environment‐dependent individual plasticity and short‐term microevolution. Moreover, when plasticity and viability selection operate simultaneously, their impacts on population composition may not be evident.     

Male rock sparrows adjust their breeding strategy according to female ornamentation: parental or mating investment?

We investigated the relations between female quality and ornamentation and between male breeding investment and female ornamentation in the rock sparrow, Petronia petronia, a passerine in which both sexes have a yellow breast patch. Breast patch size in females was positively correlated with body mass and breeding status; double-brooding and primary females of polygynous males had a larger patch, and patch size could therefore be an indicator of female phenotypic quality. We conducted a field experiment to test whether males allocate their parental effort in relation to female quality, as predicted by the differential allocation hypothesis. We increased and reduced the ornament sizes of paired females and compared the behaviour of their males before and after manipulation. Frequency of brood feeding by the male was not affected by female ornament manipulation; there was a nonsignificant trend for females with enlarged ornaments, contrary to predictions, to increase their feeding rate. Reducing female ornaments resulted in a decrease in male nest attendance, a measure of passive brood defence, whereas enlarging the ornament had no effect. Males concurrently reduced their territorial (song output) and sexual activity (courtship and copulation). The reduction in sexual activity suggests that males may have changed their nest attendance in response to their mate's renesting probability. Whatever the interpretation, these results provide some of the first evidence that not only female, but also male, birds change breeding strategy according to their mate's phenotype in the wild. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Experimentally increased badge size increases male competition and reduces male parental care in the collared flycatcher

Experimental enlargement of sexually selected traits that are energetically cheap to produce is expected to reveal costs resulting from increased risk of predation or social competition. Given a trade-off between sexually selected traits and life history traits such costs may be expected to affect not only the males themselves but also their offspring. In this study I manipulated the size of the forehead patch, a sexually selected trait that functions as a badge of status in male collared flycatchersFicedula albicollis). First, I found that a male''s likelihood to establish a breeding territory with respect to his original badge size was affected by the treatment such that old males (older than or equal to two years) with relatively small original badges enjoyed an increased likelihood of establishing a breeding territory while young males (yearlings) suffered a reduced likelihood of establishment when their badges were enlarged as compared to unchanged. Second, young males with enlarged badges that were able to establish a territory fed their nestlings less in relation to their females compared to the control males. However, the females adjusted their parental effort to such an extent that no significant differences were observed in total feeding rate nor in reproductive success between the two groups of males. These results suggest that experimentally enlarged badge size in the collared flycatcher may result in increased male competition and that males have to trade their effort spent in male contest against their parental effort.     

High brood patch temperature of less colourful,less pheomelanic female Barn Swallows Hirundo rustica

In birds, even a minor difference in egg temperature (1–1.5 °C) has been shown to affect the fitness of offspring by changing hatching success, incubation period and nestling quality. Female, but not male, passerines develop brood patches. Thus if there are traits, such as plumage ornamentation, that indicate optimal egg temperature, males should pair with females that exhibit those traits. However, no study has yet investigated the relationship between female brood patch temperature, which would directly affect egg temperature, and female plumage ornamentation. In this study, we examined the surface temperature of female brood patches during nocturnal incubation and examined its relationship with female plumage ornaments in Asian Barn Swallows Hirundo rustica gutturalis. After controlling for ambient air temperature, brood patch temperature was negatively associated with colour saturation of the female throat patch. No other female ornaments, such as tail‐length, white tail spots or throat patch size, predicted brood patch temperature. When oral (mouth) temperature was statistically controlled, females with less colourful throats and longer tails showed higher brood patch temperature, indicating that these females had hotter brood patches in relation to the temperature of other body parts. Furthermore, we found a negative relationship between pheomelanin pigmentation and brood patch temperature after controlling for ambient air temperature or oral temperature. To our knowledge, this is the first study to show that female ornaments can predict the absolute/relative thermal investment in brood patches. This relationship, together with other aspects of female quality, may affect male mate preference and female ornamentation.     

Age-Dependent Expression of Song in the Collared Flycatcher, Ficedula albicollis

Theory suggests that male ornaments should be reliable signals of age, with more elaborated ornaments reflecting superior quality in terms of experience and/or viability. Bird song is immensely involved in sexual selection, thus not‐surprisingly, it usually shows age‐dependent variation. Although the collared flycatcher Ficedula albicollis has been intensively studied for its sexual traits, and female preference for male age is expected to be strong, there is no quantitative information on age‐dependent expression of song in this species. Here, we fill this gap and, based on phenotypic correlations, we report the relationship between age and several song features. Repertoire size was consistently smaller in yearlings than in older males, but it also tended to increase after the second year of breeding. In a meta‐analysis of effect sizes using data from the literature, we found that the strength of the relationship between age and repertoire size in the collared flycatcher is similar to patterns observed in other passerines. Song rate was inversely related to age, as yearlings sang at higher rates than older males. Generally, effect sizes for the relationship between age and other song traits were of medium level on average, and had broad confidence intervals. Song traits covaried with survival in a direction suggesting that differences in song between age categories are unlikely to result from phenotype dependent survival. Our results generally support the hypothesis that song holds the potential to function as a reliable indicator of male age in the collared flycatcher. However, it seems that not all song traits are unambiguously more expressed in older males than in yearlings.     

Qualitative population divergence in proximate determination of a sexually selected trait in the collared flycatcher

We examined proximate determination of sexually selected forehead patch size in a Central‐European population of Ficedula albicollis, the collared flycatcher, using a 9‐year database, and compared our results with those obtained in other populations of the same and the sister species. Between‐individual variation of forehead patch size was large, its repeatability larger than, and heritability similar to the Swedish population. Unlike in the other populations, the trait proved unaffected by body condition, and only very slightly influenced by age. There was no relationship between forehead patch size and breeding lifespan, and a marginal negative association with survivorship in adult males. Our results suggest that additive genetic variance of the trait in this population is large, but genes act independently of body condition, and there is no viability indicator value of the trait. This is the first report of a qualitative intraspecific difference in proximate determination of a sexually selected trait.     

Female collared flycatchers choose neighbouring and older extra‐pair partners from the pool of males around their nests

Extra‐pair copulation is common among passerine birds. Females might engage in this behavior to obtain direct or indirect benefits. They may choose extra‐pair males with larger ornaments, especially if they are costly to produce. Here we studied extra‐pair paternity in the collared flycatcher. Genetic analysis allowed us to identify the presence or absence of extra‐pair young in the focal nests, and to identify extra‐pair fathers. We also identified potential males available as extra‐pair sires around the nests of females who had extra‐pair young. First, we tested the relationship between paternity in own nest and ornament size (wing patch and/or forehead patch), morphological traits and age of social males and females. Second, we compared the same suite of traits among social mates, extra‐pair males and all potential extra‐pair mates. Finally, we investigated the effect of the size of ornaments on the distance between the social nest and that of nest the extra‐pair father. Contrary to our prediction, males with larger ornaments and longer wings lost more paternity in their nests. We also found that early breeders lost less paternity in their nests. Extra‐pair males were older and had longer wings than social and potential extra‐pair males. Females mainly obtained extra‐pair mates near their nests but the distance did not vary according to ornamentation. These results could potentially be explained by differences in mate guarding strategy as older males may be more experienced in guarding their mate and attract other females more easily. More data about mate guarding and prospecting are needed to increase our understanding of mechanisms underlying the extra‐pair paternity in birds.     

拟环纹豹蛛雄蛛触肢上黑白相间毛饰物的功能

狼蛛科雄蛛附肢上多样化的饰装往往与求偶行为相偶联,这些特殊的饰装通常被认为是雌性选择的结果。拟环纹豹蛛Pardosa pseudoannulata,属狼蛛科豹蛛属,雄蛛触肢胫节密被白毛,跗舟密被黑毛,具有典型的性二型现象;同时,只有成熟的雄蛛才展现触肢黑白相间的毛饰物。推测拟环纹豹蛛雄蛛触肢这种黑白相间的毛饰物可能在物种识别中具重要作用。在室内我们拟通过涂抹操作对拟环纹豹蛛雄蛛触肢黑白相间毛饰物的功能进行分析。实验分为4组,分别是对照组(A组,雄蛛不做任何处理)、雄蛛触肢白色胫节全部涂成黑色(B组)、雄蛛触肢黑色跗舟全部涂成白色(C组)和雄蛛触肢的黑色跗舟被涂成黑色(D组),然后采用雌雄配对进行求偶交配行为测定。实验结果表明,B组雄蛛的交配成功率显著低于A、C和D组的雄蛛,而后3组雄蛛的交配成功率无显著差异。相反,B组雄蛛被雌蛛相食百分率显著高于其它3组。可见拟环纹豹蛛雄蛛触肢上黑白相间毛饰物,尤其是其胫节上的白色饰物在雌蛛种间识别中起重要作用。