AN EXPERIMENTAL STUDY OF PATERNITY AND TAIL ORNAMENTATION IN THE BARN SWALLOW (HIRUNDO RUSTICA)

Previous studies of the socially monogamous barn swallow (Hirundo rustica) have shown that males that most frequently engage in extrapair copulations and whose partners are least involved in copulations with extrapair males are those with long tail ornaments. In this study, through the use of three highly polymorphic microsatellite markers, we analyze the relationships between length of tail ornaments of male barn swallows and proportion of nestlings fathered in own broods, number of offspring fathered in broods of other pairs, and total number of offspring fathered, using both a correlational and an experimental approach. Consistent with our predictions, we show that males with either naturally long or experimentally elongated tails have higher paternity (proportion of biological offspring in own broods), and they produce more biological offspring during the whole breeding season than males with naturally short or experimentally shortened tails. Males with naturally long tails also had more offspring in extrapair broods than short-tailed males, but the effect of tail manipulation on the number of offspring fathered in extrapair broods, although being in the predicted direction, was not statistically significant. Cuckolded males that did not fertilize extrapair females had smaller postmanipulation tail length than cuckolders. We conclude that there is a causal, positive relationship between male tail length and paternity. Since female barn swallows have extensive control over copulation partners and heritability of tail length is high, this study shows that female choice is a component of selection for larger male ornaments. Benefits from extrapair fertilizations to females may arise because they acquire “good” genes for sexual attractiveness or high viability for their offspring.     

Experimental manipulation of tail length in female barn swallows (Hirundo rustica) affects their future reproductive success

Previous studies have shown no significant effect of experimentaltail length manipulation in female barn swallows (Hirundo rustica)at the beginning of a breeding season on reproductive successor behavior during that breeding season. In the present study,we investigate if tail length manipulation had any effect onreproductive performance the following year, the so-called long-termeffect, in contrast to the short-term effects already studied.We found that females with experimentally elongated externaltail feathers at the beginning of a breeding season producedless offspring during the breeding season the following yearthan did females with shortened or unmanipulated tails. Theseresults suggest that tail elongation caused flight deficienciesthat deteriorated the condition of females and eventually reducedreproductive success. The finding of long-term effects but nosignificant short-term effects for female tail elongation suggeststhat female barn swallows have the ability to adjust immediateparental investment. Detrimental effects of long tails in femalesin terms of decreased reproductive success might explain whyfemale tails are not as long as those of males. Finally, femalesmated to long-tailed (sexually attractive) males decreased theirreproductive success the following year more than did femalesmated to short-tailed males, possibly owing to differentialparental effort causing a deterioration of their condition.     

DIFFERENTIAL COSTS OF A SECONDARY SEXUAL CHARACTER: AN EXPERIMENTAL TEST OF THE HANDICAP PRINCIPLE

The evolution of reliable signaling can be explained by the handicap principle, which assumes that (1) the cost of a signal guarantees its reliability, and (2) cheating is prevented because the cost of a unit of display is greater for low-quality than for high-quality individuals. A test of these two assumptions was performed using manipulations of the length of the outermost tail feathers of male barn swallows Hirundo rustica, a trait currently subject to a directional female mate preference. We found that survival decreased with tail elongation and increased with tail shortening of males, supporting the assumption that the secondary sexual character is costly. Naturally long-tailed males were better able to survive with an elongated tail, whereas naturally short-tailed males improved their survival following tail shortening. This observation supports the second assumption of a differential cost of a signal. One mechanism imposing differential costs on sexually signaling barn swallows is foraging. Males with elongated tails captured smaller, less profitable Diptera, whereas males with shortened tails captured large, profitable prey items. The conditions for reliable sexual signaling by the tail ornament of male barn swallows are thus fulfilled.     

Symmetrical male sexual ornaments, paternal care, and offspring quality

Simultaneous manipulation of tail length and tail asymmetryin male barn swallows (Hirundo rustica) has revealed that femalesprefer maJes with both long and symmetrical tail ornaments overmales with short and asymmetrical ornaments. Fluctuating asymmetryin tail length has a negative effect on the maneuvering abilityof male barn swallows, and females may prefer males with symmetricaltail ornaments because they thereby acquire more direct fitnessbenefits in terms of paternal care. The least preferred maleswith short tails with high asymmetry performed an absolutelyand relatively larger share of feeding of nestlings than themost preferred males. However, the combined feeding rate ofthe pair was not statistically significantly different betweentreatment groups. Fully grown tarsus length and body mass ofoffspring on day 15 did not differ between treatments. Theseresults indicate that females do not prefer males with symmetricaltail ornaments because such males contribute a relatively orabsolutely larger share of parental duties. Although these resultsdo not explain the basis of female choice for long and symmetricaltails, the results are consistent with a hypothesis that femalesof species with biparental care should invest differentiallyin their offspring relative to the quality of their mates. Theresults are also consistent with a hypothesis that preferredmales have access to mates with superior parenting abilities     

Individual Quality and Extra-Pair Paternity in the Blue Tit: Sexy Males Bear the Costs

Adaptive explanations for the evolution of extra-pair paternity (EPP) suggest that females seek extra-pair copulations with high quality males. Still, the link between ornamentation, individual quality, and paternity remains unclear. Moreover, honest signaling is essential when explaining EPP because it is needed for sexual selection to occur; yet, it is understudied in multiple ornaments. Because blue tits (Cyanistes caeruleus) show variable color expression in several plumage patches, we tested: (i) over two seasons, whether males in better condition, more ornamented and less infected by blood parasites gain EPP and have higher reproductive success, and (ii) over three seasons, whether mating patterns affect color change. Males with more saturated yellow feathers, brighter tails, and in better condition had higher reproductive success in one of the seasons. Contrary to expectation, in another season, males that gained EPP were parasitized by blood parasites, suggesting increased vector exposure during extra-pair copulations. Our results for two seasons show that males siring more extra-pair young were older and grew brighter cheek or tail feathers for the following season. Despite the increased mating costs, in socially monogamous avian systems, high quality males incur in EPP without compromising traits that may be under sexual selection.     

Sexual selection in the barn swallow Hirundo rustica. VI. Aerodynamic adaptations

Secondary sexual characters are assumed to be costly to produce and maintain, and this will select for morphological modifications that reduce the magnitude of such costs. Here we test whether a feather ornament, the sexually exaggerated outermost tail feathers of male barn swallows Hirundo rustica, a trait currently subject to a directional female mate preference, and other aspects of the morphology used for flight have been modified to increase aerodynamic performance. This was done by making comparisons among sexes within populations, among individuals varying in tail length within populations, and among populations from different parts of Europe. Male barn swallows experienced reduced drag from their elongated tail feathers by morphological modifications of the ornamental feathers as compared to females. Morphological features of the outermost tail feathers were unrelated to tail length in both males and females within populations. Wing and tail morphology (length of central tail feathers and wings, wing span, wing area, wing loading, and aspect ratio) was modified in males compared to females. Barn swallows with long tails had morphological tail and wing modifications that reduced the cost of a large ornament, and similar modifications were seen among populations. The costs of the exaggerated secondary sexual character were therefore reduced by the presence of cost-reducing morphological modifications. The assumptions of reliable signalling theory, that signals should be costly, but more so to low than to high quality individuals, were not violated because long-tailed male barn swallows had the largest cost-reducing morphological characters.     

FEMALE REPRODUCTIVE EFFORT DEPENDS ON THE DEGREE OF ORNAMENTATION OF THEIR MATES

Sexual selection theory assumes that secondary sexual characters do not influence female reproductive effort. Female animals may invest relatively more in reproduction if they acquire mates of high phenotypic quality, because offspring sired by preferred males may be relatively more viable than offspring sired by less preferred males. Here we report for the first time in a field study that females of the monogamous barn swallow Hirundo rustica adjust their reproductive effort to the attractiveness of their mates. Experimental manipulation of male tail length, which is a trait currently subject to a directional female mating preference, affected the reproductive effort by females in single broods as well as their decision on the seasonal number of clutches. These results, and those of previous experiments, demonstrate that female barn swallows assess the quality of their mates throughout the reproductive season and adjust their reproductive decisions accordingly. This result has important implications for the theory of sexual selection and for the possibility of testing current models of female mate preferences, because the viability of offspring will be confounded by differential reproductive effort.     

The function of long tails in female barn swallows (Hirundo rustica): an experimental study

The outermost tail feathers in male barn swallows (Hirundo rustica)are the target of a strong directional female mate preference.The tail ornament is also expressed in females, since femaleshave considerably longer tails than juveniles, either due to(1) a strong genetic correlation between the characters in thetwo sexes, or (2) direct sexual selection on females. To discriminatebetween these two hypotheses, we manipulated the length of theoutermost tail feathers in female barn swallows shortly afterarrival by either shortening or elongating the outermost tailfeathers, or maintaining their length among control individuals.Start of laying of the first clutch, reproductive performance,or provisioning of offspring did not show any significant differencesamong treatments. Original female tail length before manipulationwas unrelated to reproductive performance, while male tail lengthexplained some variation in the number of clutches and, to someextent, the total number of eggs laid per year. Females withlonger tails arrived earlier at the breeding grounds. Manipulatedfemale tail length was positively correlated to the tail lengthof their mates. Our results support the correlated responsehypothesis but do not support the sexual selection explanationfor the existence of exaggerated tail feathers in female barnswallows.     

Sexual selection for white tail spots in the barn swallow in relation to habitat choice by feather lice

Many bird species have white spots in their tails or wing feathers, and such characters have been hypothesized to be either reliable signals (handicaps) or amplifiers that facilitate the message of a signal. In barn swallows, Hirundo rustica, the size of the white spots in the tail feathers is sexually dimorphic and positively correlated with feather length. We tested whether such spots act as handicaps or amplifiers. These white spots affect sexual selection in barn swallows, as shown by an experiment in which we randomly subjected males to (1) a considerable reduction of the size of all the spots by the use of a black permanent marker pen, (2) a small reduction of the size of the spots, or (3) no reduction. There was a positive association between spot size and the number of offspring produced per season. The white tail spots were preferred by feather-eating Mallophaga as a feeding site: holes made by Mallophaga were more abundant in the white spots than expected by chance. A habitat choice experiment with Mallophaga on barn swallow tail feathers revealed that they preferred white spots over black parts of the tail feathers. We therefore expected long-tailed male barn swallows to have more Mallophaga than short-tailed males. However, the opposite relationship was observed, indicating that long-tailed males may reliably signal their quality by the presence of large white tail spots without parasite damage. Thus white tail spots in barn swallows appear to be a reliable signal of phenotypic quality. Copyright 1999 The Association for the Study of Animal Behaviour.     

SEXUAL SELECTION IN THE BARN SWALLOW HIRUNDO RUSTICA. III. FEMALE TAIL ORNAMENTS

Male secondary sexual characters are often expressed in females, and the maintenance of the character in females can be due to either direct selection on females favoring the maintenance of the trait, or a correlated response to selection in males. Here I report on determinants of and phenotypic selection on tail length of female barn swallows Hirundo rustica. The homologous trait in males is under strong directional sexual selection. Female tail length was positively associated with several reproductive parameters including total seasonal reproductive success, even when controlling for year and age effects. A change in female tail length from one year to another was often associated with a change in the reproductive parameters correlated with absolute tail length. There was little evidence for an association between female tail length and the duration of the incubation period (only females incubate) and absolute and relative female provisioning rates of offspring, and subsequent size of offspring. Tail length of female barn swallows was positively correlated with that of their mates. Female tail length was a heritable trait as determined from regression of the tail trait of offspring on that of their mother and their father, and there was a positive genetic correlation between the tail trait in males and females. In conclusion, female tail length reliably reflects female reproductive potential, and the trait appears to be under directional selection, which may result in an evolutionary response to selection because of the heritability of the tail trait.     

Experimental manipulation of tail ornament size affects the hematocrit of male barn swallows (Hirundo rustica)

Ornamental tail feathers of male barn swallows (Hirundo rustica) confer an advantage in sexual selection because long-tailed males are preferred by females. However, the size of tail ornaments exceeds the natural selection optimum and males are predicted to pay an energetic cost for flying, directly related to tail length. An increase in hematocrit is an adaptive response to enhance oxygen uptake, for example during periods of intense locomotory activity. In this study, we analyzed the effect of experimental manipulation of tail length on the hematocrit of male barn swallows from an Italian and a Spanish population. We predicted that the natural decrease in hematocrit during the breeding season would be reduced by experimental elongation and enhanced by experimental shortening of tail ornaments. The results showed that the decrease in hematocrit was significantly different among tail treatments, and tail-elongated males had the smallest hematocrit reduction. In Italy, the hematocrit of tail-elongated males did not change after tail manipulation, while that of two control groups and tail-shortened males decreased. A comparatively high hematocrit in males with experimentally enlarged tail ornaments may be a response to increased energetic requirements and, hence, to oxygen demands for flying imposed by their tail morphology. Received: 22 June 1996 / Accepted: 23 October 1996     

Intrusion into neighboring home range by male Madagascar paradise flycatchers, Terpsiphone mutata: a circumstantial evidence for extra-pair copulation

The seasonal change in home range size and distribution of the male Madagascar paradise flycatcher, Terpsiphone mutata, was studied in deciduous dry forest of the Ampijoroa Forest Station, northwestern Madagascar. Male home ranges were spaced out in the prebreeding period but overlapped during the breeding period; this change resulted from male intrusion into neighboring home ranges. Male intrusion was often observed during the prelaying and laying stages of females in invaded home ranges. These stages are assumed to be in a fertile period of females. Intruder males tended to have longer tails as compared to resident males. Intruder males may be seeking extra-pair copulations. Females may prefer long-tailed males to short-tailed males as extra-pair partners, or long-tailed males may be dominant to short-tailed males. Received: February 17, 2000 / Accepted: April 25, 2000     

MEASURING THE EFFECTS OF PAIRING SUCCESS,EXTRA-PAIR COPULATIONS AND MATE QUALITY ON THE OPPORTUNITY FOR SEXUAL SELECTION

Sexual selection can act through variation in the number of social mates obtained, variation in mate quality, or variation in success at obtaining extra-pair fertilizations. Because within-pair fertilizations (WPF) and extra-pair fertilizations (EPF) are alternate routes of reproduction, they are additive, rather than multiplicative, components of fitness. We present a method for partitioning total variance in reproductive success (a measure of the opportunity for selection) when fitness components are both additive and multiplicative and use it to partition the variance into components that correspond to each mechanism of sexual selection. Computer simulations show that extra-pair fertilizations can either increase or decrease total variance, depending on the covariance between within-pair and extra-pair success. Simulations also suggest that for socially monogamous species, extra-pair fertilizations have a greater effect than variation in mate quality or pairing status on the opportunity for selection. Application of our model to data gathered for a population of red-winged blackbirds (Agelaius phoeniceus) indicates that most of the variance in male reproductive success was attributable to within-pair sources of variance. Nevertheless, extra-pair copulations increased the opportunity for selection because males varied both in the proportion of their social young that they sired and in the number of extra-pair mates that they obtained. Furthermore, large and positive covariances existed between the number of extra-pair mates a male obtained and both social pairing success and within-pair paternity, indicating that, in this population, males preferred as social mates also were preferred as extra-pair mates.     

SEXUAL SELECTION IN THE BARN SWALLOW (HIRUNDO RUSTICA). IV. PATTERNS OF FLUCTUATING ASYMMETRY AND SELECTION AGAINST ASYMMETRY

The patterns of variation in fluctuating asymmetry were studied in four morphological characters of the barn swallow Hirundo rustica. The level of absolute and relative asymmetry was larger in the secondary sexual character “outer tail length” than in three nonsexual morphological traits (wing, central tail, and tarsus length). The extent of individual asymmetry in outer tail length was negatively correlated with tail-ornament size, whereas the relationship between asymmetry of all other morphological characters and their size was flat or U-shaped. Asymmetry in outer tail length was unrelated to asymmetry in other morphological characters, whereas asymmetries in the length of wing, central tail, and tarsus were positively correlated. Male bam swallows exhibited larger asymmetry in outer tail length than females. Asymmetry of most morphological traits exhibited intermediate repeatabilities between years, with the exception of male and female outer tail length, which were highly repeatable. Tail asymmetry of offspring weakly, though significantly, resembled that of their parents. Asymmetry in wing and outer tail length was also significantly related to several fitness components. Male barn swallows that acquired a mate were less asymmetric in wing and outer tail length than unmated males. Females with more asymmetrical tails laid eggs significantly later. Annual reproductive success was unrelated to fluctuating asymmetry. Male barn swallows that survived were less asymmetric in wing and outer tail length than nonsurvivors, whereas female survivors were less asymmetric in outer tail length than nonsurvivors. These results suggest that levels of fluctuating asymmetry in barn swallows are associated with differences in fitness.     

Paternity analysis reveals opposing selection pressures on crown coloration in the blue tit (Parus caeruleus)

In socially monogamous species, extra-pair paternity can increase the variance in reproductive success and thereby the potential for sexual selection on male ornaments. We studied whether male secondary sexual ornaments are selected through within- and/or extra-pair reproductive success in the blue tit (Parus caeruleus). Male blue tits display a bright blue crown plumage, which reflects substantially in the ultraviolet (UV) and previously has been indicated to be an important sexual signal. We show that males with a more UV-shifted crown hue were less cuckolded, which probably resulted from female preference for more ornamented mates. By contrast, however, older males and males with a less UV-shifted hue sired more extra-pair young. This probably did not reflect direct female preference, since cuckolders were not less UV-ornamented than the males they cuckolded. Alternatively, a trade-off between UV ornamentation and other traits that enhance extra-pair success could explain this pattern. Our results might reflect two alternative male mating tactics, where more UV-ornamented males maximize within-pair success and less UV-ornamented males maximize extra-pair success. Since crown colour was selected in opposite directions by within-pair and extra-pair paternity, directional selection through extra-pair matings seemed weak, at least in this population and breeding season. Reduced intensity of sexual selection due to alternative mating tactics constitutes a potential mechanism maintaining additive genetic variance of male ornaments.     

Female Barn Swallows Gain Indirect but not Direct Benefits through Social Mate Choice

Female mate choice is responsible for the evolution of male secondary sexual ornaments. If male ornamental traits reflect indirect, genetic benefits and/or direct, material benefits to females, choosy females may benefit from their choice, indirectly and/or directly. We examined a breeding population of Japanese barn swallows Hirundo rustica gutturalis to determine whether male tail streamer length reflected indirect and/or direct benefits to females. There was no significant positive relationship between male streamer length and the number of extra-pair young (EPY) sired, suggesting that male tail streamers are not a signal of indirect benefits (i.e. good genes theory). In addition, we found no evidence that males with longer streamers fed their offspring more frequently or sired more within-pair young (WPY). The result indicates that male streamer length probably does not act as a signal of direct benefits. Our finding that the length of tail streamers in Japanese barn swallows plays no role in sexual selection is not consistent with studies on European subspecies, but is consistent with studies on North American subspecies where sexual selection on tail streamer is weak. The present study supports the recent suggestion that the pattern of sexual selection on tail streamer length in barn swallows varies geographically. Instead of tail length, males in better condition sired more EPY and WPY. Males in better condition, however, did not feed their nestling more frequently. These results indicate that females gain indirect benefits but not direct benefits, in terms of feeding of young, on choosing social mates.     

Fitness consequences of divorce in the azure-winged magpie depends on the breeding experience of a new mate

Sexual conflict in producing and raising offspring is a critical issue in evolutionary ecology research.Individual experience affects their breeding performance,as measured by such traits of provisioning of offspring and engagement in extra-pair copulations,and may cause an imbalance in sexual conflict.Thus,divorce is hypothesized to occur within aged social pairs,irrespective of current reproductive success.This concept was explored in the azure-winged magpie Cyanopica cyanus by investigating the divorce of a social pair and its relationship to their changes in breeding performance with prior experience.Females engaging in extra-pair copulation may intensify sexual conflicts and may be the main reason for divorce.Once divorced,females repairing with an inexperienced male realized higher reproductive success than that repairing with an experienced male;males repairing with an experienced female realized higher reproductive success than that repairing with an inexperienced female.This finding indicates that the fitness consequence of divorce depends on the breeding experience of new mates.Divorced females can obtain more extra-pair copulations,whereas divorced males cannot,when they repair with inexperienced breeders.Divorced females provisioned a brood at lower rates than inexperienced females whereas divorced males had no such difference.It appears that divorced females can obtain an advantage in sexual conflicts with inexperienced mates in future reproduction.Consequently,females are probably more active than males in divorcing their aged mates so as to select an inexperienced male as a new mate.Azure-winged magpies thus provide novel insights into the implicaticns of sexual conflict in birds.     

Haematocrit correlates with tail ornament size in three populations of the Barn Swallow (Hirundo rustica)

1. Handicap models of sexual selection propose that male ornaments are indicators of male quality and that honesty is enforced by the costs imposed by the exaggerated ornamental traits. In long-distance migratory birds that feed on the wing, the aerodynamic cost of exaggerated ornamental characters should be particularly high because the size of the ornaments deviates from the natural selection optimum. During migration, birds are expected to raise their oxygen consumption in relation to the energetic demands imposed by their morphology. An increase of haematocrit is an adaptive response to enhance oxygen uptake and efficiency of transfer to the muscular tissues during spells of intense muscular activity.
2. The change of haematocrit of Barn Swallows ( Hirundo rustica ) after their arrival to the breeding sites, and the relationships between haematocrit values recorded after migration and the size of ordinary and sexually selected morphological characters in three Barn Swallow populations were analysed.
3. Males had higher haematocrit values than females. Individual haematocrit values declined after arrival to the breeding sites. Haematocrit values of males were significantly and positively correlated with the size of their ornamental tail but not correlated with other characters, thus suggesting that well-ornamented males, in order to arrive early, have to raise their haematocrit above the level of short-tailed males.
4. Males and females of similar tail length did not differ in their haematocrit, thus suggesting that sexual dimorphism in haematocrit might be functionally related to dimorphism in tail length.
5. Our results are consistent with the handicap principle because long-tailed males experience lower mortality and larger seasonal reproductive success compared with short-tailed males.     

Promiscuity drives sexual selection in a socially monogamous bird

Many socially monogamous species paradoxically show signs of strong sexual selection, suggesting cryptic sources of sexual competition among males. Darwin argued that sexual selection could operate in monogamous systems if breeding sex ratios are biased or if some males attract highly fecund females. Alternatively, sexual selection might result from promiscuous copulations outside the pair bond, although several recent studies have cast doubt on this possibility, in particular by showing that variance in apparent male reproductive success (number of social young) differs little from variance in actual male reproductive success (number of young sired). Our results from a long-term study of the socially monogamous splendid fairy-wren (Malurus splendens) demonstrate that such comparisons are misleading and do not adequately assess the effects of extra-pair paternity (EPP). By partitioning the opportunity for selection and calculating Bateman gradients, we show that EPP has a strong effect on male annual and lifetime fitness, whereas other proposed mechanisms of sexual selection do not. Thus, EPP drives sexual selection in this, and possibly other, socially monogamous species.     

Mutation and sexual selection: a test using barn swallows from Chernobyl

Abstract Secondary sexual characters have been hypothesized to be particularly susceptible to the deleterious effects of mutation because the expression of such characters is usually influenced by many more metabolic pathways than are ordinary morphological characters. We tested this hypothesis using the elevated mutation rates in the barn swallow ( Hirundo rustica ) of the Chernobyl region of Ukraine as a model system. A great deal is known about the relative importance of different characters for male mating success in this species. The importance of phenotypic characters for male mating success was quantified based on a long-term study of a Danish breeding population, by expressing phenotypic differences between mated and unmated males as the difference between log-transformed mean values. For field samples from Ukraine we likewise expressed the difference in male phenotype between individuals living in a relatively uncontaminated area and individuals from the Chernobyl region as the difference between log-transformed mean values. The standardized difference in male phenotype between the two regions in Ukraine for the 41 different characters was strongly positively correlated with the standardized difference in male phenotype between mated and unmated males from Denmark. The standardized difference in male phenotype between the two regions in Ukraine was significantly positively associated with sexual size dimorphism. However, the standardized difference in male phenotype between mated and unmated males was a much better predictor of standardized difference in male phenotype between the two regions in Ukraine than was the standardized difference in sexual size dimorphism, expressed as the difference between log-transformed mean values for males and females. These findings are consistent with the hypothesis that traits most important for sexual selection are particularly susceptible to the effects of deleterious mutations.