Offspring sexual dimorphism and sex-allocation in relation to parental age and paternal ornamentation in the barn swallow

We analysed the morphology of nestling barn swallows (Hirundo rustica) in relation to their sex, and laying and hatching order. In addition, we studied sex-allocation in relation to parentage, parental age and expression of a secondary sexual character of fathers. Molecular sexing was conducted using the sex chromosome-linked avian CHD1 gene. Sex of the offspring was not associated with laying or hatching order. None of nine morphological, serological and immunological variables varied in relation to offspring sex. Sexual dimorphism did not vary in relation to parental age and expression of a paternal secondary sexual character. The proportion of sons declined with brood size. Individual males and females had a similar proportion of sons during consecutive breeding years. The proportion of sons of individual females declined with age, but increased with the expression of a secondary sexual character of their current mate. The generalized lack of variation in sexual dimorphism among nestlings may suggest that barn swallows do not differentially invest in sons vs. daughters. Alternatively, male offspring may require different parental effort compared to their female siblings in order to attain the same morphological state. The lack of variation in offspring sexual dimorphism with paternal ornamentation suggests no adjustment of overall parental effort in relation to reproductive value of the two sexes. However, male-biased sex ratio among offspring of highly ornamented males may represent an adaptive sex-allocation strategy because the expression of male ornaments is heritable and highly ornamented males are at a sexual selection advantage.     

Immune response covaries with corticosterone plasma levels under experimentally stressful conditions in nestling barn swallows (Hirundo rustica)

Traits related to fitness are often pleiotropically linked orotherwise constrained in their expression. Organisms thereforetrade between fitness components such as number and viabilityof their offspring. The physiological mechanisms mediating suchtrade-offs, however, have been poorly investigated. We manipulatedbrood size and satiation of nestling barn swallows, Hirundorustica, to simulate the effect of two kinds of natural stresses,i.e., long-term intense competition in a large brood and acutefood deprivation, and we measured their effect on body condition,T cell–mediated immune response, and corticosterone, themain hormone mediating the adrenocortical stress-response. Broodenlargement increased corticosterone levels compared with thosefor brood reduction, and brood enlargement depressed immuneresponse, body mass, and condition. Corticosterone levels markedlyincreased after food deprivation. Immune response negativelycovaried with corticosterone levels measured after long-termstress. Hence, living in a crowded nest and with food deprivationelicited a stress response mediated by corticosterone, and depressedan important component of offspring fitness such as T cell–mediatedimmunity. The negative covariation between circulating corticosteroneand immunity suggests that the trade-off between offspring numberand quality is mediated by variation in plasma levels of corticosterone,which has immunosuppressive effects.     

Extrapair paternity in relation to sexual ornamentation, arrival date, and condition in a migratory bird

We tested the novel hypothesis that arrival date in migratorybirds represents a reliable indicator of male quality that canbe used by females as a cue in extrapair mating decisions. Secondarysexual characters are often condition-dependent, and competitionfor early arrival leads to condition-dependent migration. Hence,both secondary sexual characters and arrival date are predictedto be condition-dependent indicators of male phenotypic quality.We studied the relationship between expression of a secondarysexual character, arrival date, and condition, respectively,and extrapair paternity in a Spanish population of barn swallows,Hirundo rustica. By using microsatellite markers to determinepaternity, we showed that 17.8% of all offspring (N = 674) and32.4% of all broods (N = 170) were due to extrapair paternity.Quasi-parasitism (in which the male nest owner fathered theoffspring, but the eggs were laid by another female) occurredin 2.6% of all nestlings and 2.9% of all broods. Individualswere consistent in the frequency of extrapair paternity amongfirst, second, and third broods. Males with long outermost tailfeathers, arriving early and in prime body condition, had littleextrapair paternity in their nests. This was also the case whencontrolling for the confounding effects of male age. Partialcorrelation analysis was used to investigate the direct andindirect effects of tail length, arrival date, and body conditionon extrapair paternity. Body condition accounted for most ofthe variance in extrapair paternity, whereas tail length andarrival date accounted for a smaller proportion of the variance.Body condition was strongly correlated with tail length andarrival date. However, because females cannot directly assesscondition or arrival date (males arrive before females), femalesmay obtain an indirect measure of condition and migration abilityfrom tail length and other phenotypic traits of males. Thissuggests that extrapair paternity depends on the effects ofcondition, through its indirect effects on arrival date, taillength, and other variables.     

Digit ratios, secondary sexual characters and condition in barn swallows Hirundo rustica

The second and fourth digit length ratio (2D:4D) is sexuallydimorphic in many vertebrates. This ratio has been suggestedto provide an estimate of steroid levels encountered duringprenatal development, which may have organizational consequencesfor physiology and behavior of adults. However, recent studiesshowed that the relation between digit ratio and steroids seemsinconsistent and may vary among species and populations. Wetested the hypothesis that digit ratios would be correlatedwith the expression of secondary sexual characters, using thebarn swallow (Hirundo rustica) as a model system. This was doneby testing whether variation in 2D:4D ratio was correlated withtail length and features of song, which are important secondarysexual characters positively correlated with circulating steroidconcentration in adult birds. Furthermore, we examined the predictionthat male and female digit ratios would correlate with bodymass in an antagonistic way. There was no significant sexualdimorphism in digit ratio, which may be due to low levels ofsexual selection in this population. Adult right 2D:4D ratiowas negatively linked to tail length but not to male song output.Moreover, right 2D:4D ratio was negatively correlated with bodymass in male and positively in females. These results are consistentwith high digit ratios reflecting low levels of testosteronein this bird species.     

Telomere shortening is associated with corticosterone stress response in adult barn swallows

When vertebrates face stressful events, the hypothalamic–pituitary–adrenal (HPA) axis is activated, generating a rapid increase in circulating glucocorticoid (GC) stress hormones followed by a return to baseline levels. However, repeated activation of HPA axis may lead to increase in oxidative stress. One target of oxidative stress is telomeres, nucleoprotein complexes at the end of chromosomes that shorten at each cell division. The susceptibility of telomeres to oxidizing molecules has led to the hypothesis that increased GC levels boost telomere shortening, but studies on this link are scanty. We studied if, in barn swallows Hirundo rustica, changes in adult erythrocyte telomere length between 2 consecutive breeding seasons are related to corticosterone (CORT) (the main avian GC) stress response induced by a standard capture-restraint protocol. Within-individual telomere length did not significantly change between consecutive breeding seasons. Second-year individuals showed the highest increase in circulating CORT concentrations following restraint. Moreover, we found a decline in female stress response along the breeding season. In addition, telomere shortening covaried with the stress response: a delayed activation of the negative feedback loop terminating the stress response was associated with greater telomere attrition. Hence, among-individual variation in stress response may affect telomere dynamics.     

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.     

Humoral immune response in relation to senescence, sex and sexual ornamentation in the barn swallow (Hirundo rustica)

Performance of animals may decline with age. The effects of senescence, however, may differ between the sexes because of differences in physiology and behaviour. Acquired immunity provides hosts with efficient mechanisms of anti-parasite defence, but the effect of senescence on immunocompetence has never been studied in natural populations. In the barn swallow (Hirundo rustica), primary antibody response to an antigen during one breeding season declined with age in females, while secondary response during the following breeding season declined with age in both sexes. Parasite-mediated sexual selection theory posits that male secondary sexual characters reveal resistance to parasites. Males with large tail ornaments had stronger primary response, retained larger antibody levels until the following year, but did not differ in secondary response compared with short-tailed males, as predicted if ornamentation reflects resistance to parasites. This is the first study showing that immunocompetence declines with age in any vertebrate under natural conditions.     

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     

Plumage coloration, not length or symmetry of tail-streamers, is a sexually selected trait in North American barn swallows

Sexual adornments often vary markedly across a species' range,which presumably is owing to differences in local environmentalconditions and the associated selection pressures, such as naturalversus sexual selection or the relative signaling value of differentornamental traits. However, there are only a few reported examplesin which the information content of mating signals varies geographically,and even fewer in which a set of secondary sexual traits servesdifferent signaling functions in different populations. Classicstudies of sexual selection in the European barn swallow (Hirundorustica rustica) demonstrate that elongate tail-streamers provideseveral reproductive advantages to males and females and areused as reliable signals of mate quality. Here, we show thattail-streamers do not appear to confer these same benefits ina population of barn swallows from North America (Hirundo rusticaerythrogaster). Instead, ventral plumage coloration, which ismore exaggerated in North American swallows compared with theirEuropean counterparts, predicts patterns of assortative matingand annual reproductive success in H. r. erythrogaster. Theseobservations support the idea that ornamental traits can servedifferent functions among animal populations and suggest thatgeographic variation in different sexual signals may facilitatepopulation divergence, which may ultimately lead to speciation.     

Structural coloration and sexual selection in the barn swallow Hirundo rustica

Structural coloration has been hypothesized to play a role insexual selection, and we tested whether this was the case ina field study of the barn swallow Hirundo rustica. The dorsaliridescent plumage of barn swallows has a strong reflectancein the ultraviolet (UV) region, with adult males on averagereflecting 8-9% more than adult females, as revealed by a 2-yearstudy in southwestern Spain. The correlation between structural coloration (described by the reflectance in the UV part of thespectrum, UV chroma and blue chroma) and three other secondarysexual characters significantly associated with male matingsuccess (tail length, tail asymmetry, and red facial coloration)was weak and generally nonsignificant. Nor was there a significantrelationship between color parameters and body condition. Wetested for an association between structural coloration of the dorsal plumage and sexual selection in a number of independenttests. Arrival date of males was not significantly relatedto color; there was no significant relationship between colorationand probability of survival or age; mated males did not havestronger reflectance than unmated males; and the duration ofthe premating period was not significantly related to color.Reproductive success was not significantly correlated withplumage coloration in males, nor was the feeding rate of offspringby brightly colored males higher than that of males with lessbright plumage. Given that sample sizes were large, and the power of statistical tests high, we conclude that current sexualselection on the coloration of the dorsal plumage in the barnswallow is, at best, weak.     

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.     

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.     

Immunoglobulin plasma concentration in relation to egg laying and mate ornamentation of female barn swallows (Hirundo rustica)

In vertebrates, offspring have a relatively inefficient immune system soon after birth. Female birds transmit immunoglobulins to the egg, which can confer protection against parasites to their offspring after hatching, but allocation of immune factors can depend on the reproductive value of the offspring as affected, for example, by the quality of their father. We analyse the variation in immunoglobulin levels of female barn swallows (Hirundo rustica) during the breeding cycle in relation to the expression of a secondary sexual character of their mates. Circulating immunoglobulins peaked on approximately the day before that of laying of their first egg, but postlaying concentration was similar to the concentration well before laying. Immunoglobulin levels per unit volume of plasma were lower for females breeding late compared with those breeding early. Haematocrit of females reached an absolute minimum on the day of laying of the third egg. In males, concentration of immunoglobulins relative to other plasma proteins did not change in relation to the breeding stage. Smaller relative concentrations of immunoglobulins and haematocrit were observed in males breeding late in the season. Immunoglobulin concentration of females was positively correlated with the level of ornamentation of their mates. These results suggest that females alter their immune profile to transmit humoral factors providing immune defence against pathogens to their offspring after hatching. This enhancement of immune protection is larger when the offsprings are of relatively large reproductive value as when sired by high quality males. Alternatively, females with relatively large immunoglobulin concentration preferentially mate with the most ornamented males.     

Rapid change in nest size of a bird related to change in a secondary sexual character

Among bird species in which males contribute to nest building,sexual selection has favored larger nests. I investigated determinantsof nest size in the barn swallow Hirundo rustica and how nestsize changed during the period 1977–2003, when tail length(a male secondary sexual character) increased by more than 1.2standard deviations. Males with short tails contributed moreto nest building than long-tailed males, signaling their futureinvestment in food provisioning of offspring. Pairs of barnswallows were consistent in nest size when build ing new neststhe same or different years, and level of phenotypic plasticityin nest size was small and could not account for temporal patternsin nest size. Offspring resembled their parents with respectto nest size, indicating a significant heritability of nestsize, independent of whether offspring were reared by theirparents or by foster parents, and there was a significant negativegenetic correlation between male tail length and outer nestvolume and amount of nest material. The temporal increase inmale tail length was associated with a decrease in nest size,with the amount of nest material in 2003 on average being lessthan a third of the amount used in 1977. Temporal change innest size could be accounted for by indirect selection on taillength causing change in nest size to match that predicted fromchange in tail length and the genetic correlation between maletail length and nest size.     

The maintenance of phenotypic divergence through sexual selection: An experimental study in barn swallows Hirundo rustica

Previous studies have shown that sexual signals can rapidly diverge among closely related species. However, we lack experimental studies to demonstrate that differences in trait‐associated reproductive performance maintain sexual trait differences between closely related populations, in support for a role of sexual selection in speciation. Populations of Northern Hemisphere distributed barn swallows Hirundo rustica are closely related, yet differ in two plumage‐based traits: ventral color and length of the outermost tail feathers (streamers). Here we provide experimental evidence that manipulations of these traits result in different reproductive consequences in two subspecies of barn swallow: (H. r. erythrogaster in North America and H. r. transitiva in the East Mediterranean). Experimental results in Colorado, USA, demonstrate that males with (1) darkened ventral coloration and (2) shortened streamers gained paternity between two successive reproductive bouts. In contrast, exaggeration of both traits improved reproductive performance within H. r. transitiva in Israel: males with a combination treatment of darkened ventral coloration and elongated streamers gained paternity between two successive reproductive bouts. Collectively, these experimental results fill an important gap in our understanding for how divergent sexual selection maintains phenotype differentiation in closely related populations, an important aspect of the speciation process.     

Temporal change in mite abundance and its effect on barn swallow reproduction and sexual selection

The tropical fowl mite Ornithonyssus bursa parasitizing barn swallows Hirundo rustica in a Danish population demonstrated a dramatic change in abundance during 1982–2000. Prevalence of mites in nests showed a decrease from 66% in 1987 to a minimum of 1% in 1999. Two parasite manipulation experiments of barn swallow nests in 1988 and 1999 revealed a strong effect of parasites on host reproductive success in the first year (with an average reduction in seasonal reproductive success of 30% when 50 mites were added to nests as compared with controls), but only a weak effect the last year. This pattern was paralleled by a positive relationship between reduction in host reproductive success between egg laying and fledging and mite prevalence during different years of the study period. Mite abundance on adult hosts was negatively related to tail length of males (a secondary sexual character) at the peak of mite abundance in 1988, while that relationship became weaker in the beginning of the 1990s and disappeared at the end of the 1990s. Assortative mating with respect to mite loads in the 1980s also disappeared in the 1990s. Mean tail length of male hosts increased by 1.3 standard deviations during the study period because of changes in phenotype‐dependent patterns of mortality outside the breeding season. This microevolutionary change in mean male phenotype of the host was accompanied by a correlated response in mite abundance. These results are consistent with the hypothesis that the host has become more resistant to the mite during the study period, and that the mite from earlier playing an important role in natural and sexual selection of the host now is of little importance.     

Song and immunological condition in male barn swallows (Hirundo rustica)

Male secondary sexual characters may have evolved as intra-or intersexual signals of male phenotypic or genetic quality.In birds, singing performance may have the function to honestlyreveal health and vigor of individual males. Infectious diseasesand poor body conditions would therefore be expected to negativelyinfluence singing performance. Since bird pathogens are knownto elicit both a humoral and a cell-mediated immune response,it can be predicted that a negative relationship exists betweensinging performance and activity of the immune system. Thisprediction was tested for the first time in this correlationalstudy. The relationships between song rate and features andhematological variables (concentration of leukocytes in peripheralblood, ratio of gamma-globulins to total plasma proteins, bloodcell sedimentation rate, hematocrit) and body condition wereanalyzed in a population of bam swallows (Hirundo rustica).Song rate was negatively correlated with lymphocyte concentrationand with the ratio of gamma-globulins to plasma proteins. Spectrographicanalysis showed that features of song were not significantlycorrelated with hematological variables or body condition. Thelevel of circulating testosterone was not correlated with songrate nor hematological variables. This study is the first toshow a correlation between a bird's singing performance andhematological profile and suggests that song rate of male barnswallows may reflect their health status. Song in this speciesmight thus have evolved because it allows prospecting femalesto assess aspects of phenotypic and/or genetic quality of potentialmates     

Selection on multiple sexual signals in two Central and Eastern European populations of the barn swallow

Variation in intensity and targets of sexual selection on multiple traits has been suggested to play a major role in promoting phenotypic differentiation between populations, although the divergence in selection may depend on year, local conditions or age. In this study, we quantified sexual selection for two putative sexual signals across two Central and East European barn swallow (Hirundo rustica rustica) populations from Czech Republic and Romania over multiple years. We then related these differences in selection to variation in sexual characters among barn swallow populations. Our results show that tail length and ventral coloration vary between populations, sexes, and age classes (first‐time breeders vs. experienced birds). We found that selection on tail length was stronger in first‐time breeders than in experienced birds and in males than in females in the Romanian population, while these differences between age groups and sexes were weak in Czech birds. We suggest that the populational difference in selection on tail length might be related to the differences in breeding conditions. Our results show that ventral coloration is darker (i.e., has lower brightness) in the Romanian than in the Czech population, and in experienced birds and males compared with first‐time breeders and females, respectively. The sexual difference in ventral coloration may suggest sexual selection on this trait, which is supported by the significant directional selection of ventral coloration in first‐time breeding males on laying date. However, after controlling for the confounding effect of wing length and tarsus length, the partial directional selection gradient on this trait turned nonsignificant, suggesting that the advantage of dark ventral coloration in early breeding birds is determined by the correlated traits of body size. These findings show that ventral coloration may be advantageous over the breeding season, but the underlying mechanism of this relationship is not clarified.