Song correlates with social context,testosterone and body condition in male barn swallows

Bird song, like many other male secondary sexual characters, may have evolved as intra- or inter-sexual signals of male phenotypic quality. The hypotheses that song rate and song features reflect androgen levels and body condition, qualities useful in male–male competition, and that they are also influenced by social context, was tested for the first time in the present correlational study. The relationships between song rate and 14 variables describing song structure, respectively, and absolute plasma testosterone levels, body mass, body condition, number of neighbouring males and distances between nest sites in male barn swallows,Hirundo rustica, were analysed. Song rate was not correlated with any of the song features nor with male or social context characteristics. By contrast, a harsh song syllable, the ‘rattle’, was positively related to plasma testosterone levels, and its peak amplitude frequency varied inversely with male body mass and condition. In addition, eight features of song varied according to the social environment of each male. In particular, males sang longer and more varied songs when they had few or no neighbours, whereas males in highly competitive contexts uttered short songs, interrupted them more frequently, and emphasized the rattle. Neighbouring males also sang more similar songs than distant males, and this resulted in matched countersinging. The quality of song output therefore reflects aspects of male competitive potential, and relationships between song structure and social context suggest that some features, such as the rattle, might have originally evolved to serve in male–male interactions; a female preference may have further promoted song evolution leading to complex syllable repertoires.     

Sexual selection in the monogamous barn swallow (Hirundo rustica). II. Mechanisms of sexual selection

Mechanisms of sexual selection in the monogamous, sexually dimorphic barn swallow (Hirundo rustica) were studied during a seven-year period. First, the sex ratio of reproducing adults was male-biased, and mated males had significantly longer tail ornaments than unmated males. Secondly, some of the unmated individuals later committed infanticide and became mated with the mother of the killed brood. Fathers of killed broods had significantly shorter tails than other males, and there was a tendency for infanticidal males to have longer tail ornaments than other unmated males. Thirdly, long-tailed male barn swallows were more successful in acquiring extra-pair copulations than other males, and females involved in extra-pair copulations, as compared to females not involved in such copulations, had mates with shorter tail ornaments. Fourthly, male barn swallows having long tails as compared to short-tailed males acquired mates in better body condition. Females mated to long-tailed males reproduced earlier, laid more eggs and were more likely to have two clutches than were females mated to short-tailed males. Finally, females mated to long-tailed males put more effort into reproduction than did other females, as evidenced by their relatively larger contribution to feeding of offspring. Thus, at least five different components of sexual selection affected male reproductive success. Selection arising from differential success during extra-pair copulations, differential reproductive success and differential male reproductive effort thus accounted for most of the selection on tail ornaments in male barn swallows.     

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.     

Strophe Length in Spontaneous Songs Predicts Male Response to Playback in the Hoopoe Upupa epops

Hoopoe (Upupa epops, Coraciformes) males produce a very simple song during the breeding season in order to attract females and repel intruders. Strophes vary in length (i.e. number of elements) both within and between males, and previous studies have shown that this song cue is positively correlated with male condition and breeding success. In the present study we tested whether strophe length of males influences male behaviour during intra‐sexual contests, in a colour‐ringed population in southeast Spain. Paired males were presented with a recorded song with long strophes during the pre‐laying period, while they were near their mates, in order to provoke male mate‐defence behaviour. Most males responded to the playback, but the strategy of defence adopted depended on their own strophe length in spontaneous songs recorded before the experiments. While singing responses were common to most of the males, only those using long strophes adopted the most risky strategy of approaching the loudspeaker. However, the males that approached produced abnormal songs during playback, that were shorter and with fewer strophes than those of males that did not approach, and used shorter strophes in comparison with spontaneous songs before the experiment. These differences in quality of the song produced in response to the playback suggest that long‐strophe males were basing their response mainly on attacking rather than singing, while short‐strophe males tried to resolve the contest at a distance by means of their song. These results show that strophe length reflects some component of the competitive ability of males (either physical strength or aggressiveness) in the hoopoe, which together with previous results regarding its role for female choice, show that it is a sexual signal with dual function.     

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     

Attraction of Hoopoe Upupa epops females and males by means of song playback in the field: influence of strophe length

Experimental Hoopoe Upupa epops songs prepared with synthetic sound to differ in strophe length were used to test whether Hoopoe females prefer long strophes. The songs were broadcast simultaneously in the field from two loudspeakers situated 100 m apart, in early spring, when females actively search for mates. The playbacks attracted a total of 87 individuals, both males and females, with a maximum of five individuals (three males and two females) per trial. A female was considered to have been attracted by the song broadcast from a loudspeaker when she approached unaccompanied by a male, and when there was no male nearby. A total of 15 females chose one of the songs and significantly more were attracted by the one with long strophes. These results suggest that in the Hoopoe, male song attracts females, and that strophe length is a sexually selected song cue. There were no differences in the number or kind of males (classified according to strophe length) attracted by each playback. Frequently the experiment attracted more than one male simultaneously. These aggregations cannot be explained as territorial responses, and their significance is discussed together with that of natural spontaneous groupings of displaying males. Apparently males aggregate where they expect to find females.     

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.     

Sexual ornamentation and immunocompetence in the barn swallow

The handicap hypothesis of honest signaling suggests that secondarysexual characters reliably reflect phenotypic or genotypic qualityof signalers. This hypothesis is based on the assumptions thatsignals are costly to produce and/or maintain and the cost ofa given level of signaling is higher for low quality than forhigh quality signalers. We tested these assumptions in a fieldexperiment in which the size of a secondary sexual character[tail length in male barn swallows (Hirundo rustica)] was experimentallymanipulated. Males were randomly assigned to tail elongation,tail shortening, or two control treatments (tail manipulation,or just capture, ringing, and handling). Male barn swallowswere challenged with an injection of sheep red blood cells,and blood was sampled on the day of first capture and after3 to 4 weeks for determination of concentrations of gamma-globulins.Tail-elongated males did not increase levels of gamma-globulinswhile males of the other three groups demonstrated increases.Analyses of variation in gamma-globulins within treatment groupsrevealed a positive correlation between gamma-globulins andoriginal tail length among males with elongated tails. Theseresults suggest that tail length imposes an immu-nocompetencecost on males, and that males with naturally long tails aredifferentially better able to cope with this cost.     

Aerodynamic costs of long tails in male barn swallows Hirundo rustica and the evolution of sexual size dimorphism

Exaggerated tail feathers of birds constitute a standard exampleof evolution of extravagant characters due to sexual selection.Such secondary sexual traits are assumed to be costly to produceand maintain, and they usually are accompanied by morphologicaladaptations that tend to reduce their costs. The aerodynamiccosts for male barn swallows Hirundo rustica of having longtails were quantified using aerodynamics theory applied to morphologicaldata from seven European populations. Latitudinal differencesin tail length were positively correlated with differences inflight costs predicted by aerodynamics theory. A positive relationshipbetween aerodynamic costs of long tails and the degree of sexualsize dimorphism was found among populations. Latitudinal differencesin foraging costs may result in tail length being relativelysimilar in males and females in southern populations, whereasthe low foraging costs for males in northern populations mayallow them to cope with higher aerodynamic costs, giving riseto large sexual size dimorphism. Enlargement of wingspan inmales can alleviate but not eliminate the costs of tail exaggeration,and therefore differences in aerodynamic costs of male ornamentswere maintained among populations. Sexual size dimorphism in thebarn swallow arises as a consequence of latitudinal differencesin the advantages of sexual selection for males and the costsof long tails for males and females.     

Dominant male song performance reflects current immune state in a cooperatively breeding songbird

Conspicuous displays are thought to have evolved as signals of individual “quality”, though precisely what they encode remains a focus of debate. While high quality signals may be produced by high quality individuals due to “good genes” or favourable early‐life conditions, whether current immune state also impacts signalling performance remains poorly understood, particularly in social species. Here, we experimentally demonstrate that male song performance is impaired by immune system activation in the cooperatively breeding white‐browed sparrow weaver (Plocepasser mahali). We experimentally activated the immune system of free‐living dominant males via subcutaneous injection of phytohemagglutinin (PHA) and contrasted its effects with those of a control (phosphate buffered saline) injection. PHA‐challenged males showed significant reductions in both the duration and the rate of their song performance, relative to controls, and this could not be readily attributed to effects of the challenge on body mass, as no such effects were detected. Furthermore, male song performance prior to immune‐challenge predicted the scale of the inflammatory response to the challenge. Our findings suggest that song performance characteristics are impacted by current immune state. This link between current state and signal performance might therefore contribute to enforcing the honesty of signal performance characteristics. Impacts of current state on signaling may be of particular importance in social species, where subordinates may benefit from an ability to identify and subsequently challenge same‐sex dominants in a weakened state.     

Phenotypic quality and molt in the barn swallow, Hirundo rustica

Phenotypic quality may determine the development and expressionof secondary sexual characters. We studied the relationshipbetween molt and several measures of phenotypic quality in thesexually size-dimorphic barn swallow (Hirundo rustica) in itswinter quarters in Namibia. Males were in a more advanced stageof molt than females and juveniles, and the speed of molt asdetermined from the residual of the regression of the size ofthe gap in wings caused by missing and growing feathers on wingmolt score (residual wing raggedness) was also higher in malesthan in females and juveniles. Male barn swallows with longand symmetric tail feathers had a more advanced stage of moltand molted at a higher speed than males with short and asymmetrictails. Long-tailed females had a delayed molt, and females withasymmetric tails had less advanced molt and lower rates of feathergrowth than females with symmetric tails. Molt of secondariesin juveniles also appeared to be less advanced if they had longtails. Adult barn swallows molted their tail feathers in anirregular sequence with the longest, outermost tail featherusually replaced before the second or the third outermost feathers.Good body condition was positively associated with a high moltscore for some feather tracts and a rapid wing molt in adultfemales and tail molt in juveniles. Mallophaga were only weaklynegatively associated with primary and secondary molt scorein adult females and speed of wing molt in adult males. In conclusion,phenotypic quality of adult male barn swallows as reflectedby the expression of their secondary sexual character duringthe previous molt reliably reflected stage and speed of currentmolt.     

Paternity and multiple signaling: effects of a secondary sexual character and song on paternity in the barn swallow

ABSTRACT Multiple signals may evolve because they provide independent information on the condition of a signaler. Females should pay attention to male characters relative to their reliability as signals of male attractiveness or quality. Since behavioral traits are flexible and, therefore, subject to strong environmental influences, females should weigh stable morphological signals higher in their choice of mates for genetic benefits than flexible behavioral traits, for example, by paying particular attention to phenotypically plastic traits when produced in combination with an exaggerated morphological signal. Consistent with this prediction, female barn swallows Hirundo rustica, which are known to prefer males with the longest tail feathers (a secondary sexual character), also preferred males with extreme expressions of a behavioral trait (song rate), as determined from patterns of paternity assessed by microsatellites. However, a statistical interaction between tail length and song rate implied that song rate was relatively unimportant for males with a short tail but more important for longtailed males. Since song rate is a flexible behavioral trait, females appear to have responded to this flexibility by devaluing the importance of song rate in assessment of unattractive sires.     

No evidence for adjustment of sex allocation in relation to paternal ornamentation and paternity in barn swallows

Sex allocation theory predicts that parents should adjust investment in sons and daughters according to relative fitness of differently sexed offspring. In species with female preference for highly ornamented males, one advantage potentially accruing to parents from investing more in sons of the most ornamented males is that male offspring will inherit characters ensuring sexual attractiveness or high-quality genes, if ornaments honestly reveal male genetic quality. Furthermore, in species where extra-pair fertilizations occur, offspring sired by an extra-pair male are expected to more frequently be male than those of the legitimate male if the latter is of lower quality than the extra-pair male. We investigated adjustment of sex ratio of offspring in relation to ornamentation of the extra-pair and the social mate of females by direct manipulation of tails of male barn swallows Hirundo rustica . Molecular sexing of the offspring was performed using the W chromosome-linked avian chromo-helicase-DNA-binding protein (CHD) gene while paternity assessment was conducted by typing of hypervariable microsatellite loci. Extra-pair offspring sex ratio was not affected by ornamentation of their biological fathers relative to the experimental ornamentation of the parental male. Experimental ornamentation of the parental males did not affect the sex ratio of nestlings in their broods. Female barn swallows might be unable to bias offspring sex ratio at hatching according to the quality of the biological father. Alternatively, fitness benefits in terms of sexual attractiveness of sons might be balanced by the cost of compensating for little parental care provided by highly ornamented parental males, if sons are more costly to rear than daughters, or the advantage of producing more daughters, if males with large ornaments contribute differentially more to the viability of daughters than sons.     

Song structure in the Hoopoe (Upupa epops) — Strophe length reflects male condition

Summary The structure of Hoopoe (Upupa epops) song is analysed in a colour ringed population in southern Spain. The song of males in this species is very simple, with a repertoire size of one. The strophes of a male only differ in the number of elements that they include (strophe length), and strophe length is the main song feature differing between males. During the prelaying period each individual used mainly strophes of only two lengths, between 2 and 6 elements per strophe, and mean strophe length of males during this period was highly repeatable. However, some males changed the range of strophe types produced and decreased their mean strophe length after unsuccessful breeding or spending long periods of time singing (unpaired males). These changes show that strophe length is phenotypically plastic, and suggest that singing long strophes is energetically more costly than singing short ones. The significant relationship between strophe length and body condition, and the fact that long strophes were associated with longer previous pauses than short strophes, also suggest that increasing strophe length is costly. All these findings are in accordance with the hypothesis that strophe length reflects male condition in the Hoopoe, although it is not clear what the actual cost of singing long strophes is.

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Struktur des Gesangs des Wiedehopfs (Upupa epops) — Strophenlänge reflektiert Männchen-Qualität

Zusammenfassung Die Struktur des Gesangs des Wiedehopfs wurde in einer farbberingten südspanischen Population untersucht. Der Gesang des Männchens ist sehr einfach und umfaßt nur ein Repertoire. Die Strophen eines Männchens differieren nur in der Anzahl Elemente (Strophenlänge), und die Männchen unterscheiden sich vor allem in der Strophenlänge voneinander. In der Vorbrutphase verwendeten die Männchen meist nur zwei verschieden lange Strophen, bestehend aus 2 und 6 Elementen je Strophe, und die durchschnittliche Strophenlänge war in dieser Phase sehr konstant. Nach Brutverlust oder bei kontinuierlich singenden, ledigen Männchen kam es zu einer Verkürzung der mittleren Strophenlänge. Die Strophenlänge ist phänotypisch plastisch, und lange Strophen zu singen scheint energetisch aufwendiger als kurze Strophen. Der enge Zusammenhang zwischen Strophenlänge und männlicher Konstitution einerseits und die Beobachtung, daß lange Strophen mit langen Pausen korrelieren andererseits, zeigen ebenfalls, daß längere Strophen energetisch aufwendiger sind. Die wirklichen Kosten dafür sind jedoch noch nicht bekannt.

     

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.     

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.     

Song complexity and song structure in the Moustached Warbler Acrocephalus melanopogon

We examined different song parameters leading to a complex song configuration, and song output (production), and their relation in male Moustached Warblers and discuss them with reference to female choice. With more than 120 different syllables per two minutes of song, male Moustached Warblers can be regarded as one of the most complex singers within the genus Acrocephalus . We found significant differences between males for almost all song parameters investigated (repertoire size, switching and repetition rate, song speed and strophe length) but not for time spent singing per 20 minutes. This individual variation probably is an important cue for female mate choice. Male Moustached Warblers achieve song complexity mainly via frequent syllable switching. Song complexity seems to be consistent throughout the song and our results suggest that females could assess the overall song complexity of a singer by examining even very short song bouts. Furthermore, a high proportion of motifs – clusters of syllables with the same sequence – occurs within the song of each male which would also facilitate assessment of song complexity by females. However, repertoire size and strophe length were positively related, thus it remains to be investigated which song feature, if any, females actually use.     

Immune challenge mediates vocal communication in a passerine bird: an experiment

Secondary sexual characters may have evolved in part to signalresistance to parasites. Avian song has been hypothesized tobe involved in this process, but the role of parasites in modulatingacoustic communication systems in birds remains largely unknown,owing to lack of experiments. We studied the relationship betweenparasitism, testosterone, song performance, and mating successin male collared flycatchers (Ficedula albicollis) by experimentallychallenging their immune system with a novel antigen. We predictedthat a challenge of the immune system would reduce song performance,and that this reduction would be conditional on the size ofa visual sexual signal, the forehead patch that was previouslyfound to reflect resistance. An antagonistic linkage betweentestosterone and immune function would predict that a challengeof the immune system should suppress testosterone level. Animmunological treatment by sheep red blood cells (SRBCs) triggereda decrease in body mass, testosterone level, and song rate,but other song traits were not significantly affected by theantigen challenge. Initial testosterone level was associatedwith forehead patch size and all song traits except song rate.SRBC injection caused stronger reduction in song rate amongmales with smaller forehead patches, and the change in songrate was also predictable by song features such as strophe complexityand length. We show that song rate and other song characteristicsmay be important cues in male-male competition and female choice.These results suggest that parasite-mediated sexual selectionhas contributed in shaping a complex acoustic communicationsystem in the collared flycatcher, and that testosterone mayplay an important role in this process. Parasitism may drivea multiple signaling mechanism involving acoustic and visualtraits with different signal function.