Ecological conditions during winter predict arrival date at the breeding quarters in a trans-Saharan migratory bird

We studied variation in arrival date to the breeding colonies in Italy of a trans‐Saharan migratory bird, the barn swallow Hirundo rustica, in relation to variation in ecological conditions, as reflected by the normalized difference vegetation index (NDVI), in the winter quarters. Arrival date of old but not young individuals captured during consecutive breeding seasons was earlier after winters with favourable conditions. Change in arrival date in relation to change in NDVI was similar in the two sexes. Change in arrival date significantly and positively predicted change in breeding date. As a result of increased frequency of second broods determined by earlier arrival, the number of fledged offspring per season was larger after African winters with good in comparison to poor ecological conditions for barn swallows. This is the first study demonstrating phenotypic plasticity in migration phenology of a long‐distance migratory bird in relation to ecological conditions during wintering.     

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.     

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.     

Protandry and sexual dimorphism in trans-Saharan migratory birds

Earlier arrival to reproductive sites of males relative to females(protandry) is widespread among migratory organisms. Diversemechanisms have been proposed that may select for protandry,including competition for limiting resources (e.g., territories)or mates. In species with large variation in male reproductivesuccess, such as polygamous species and those with intense spermcompetition, early arriving males may accrue a fitness advantagebecause they acquire more mates or have larger chances of paternity.Comparative studies of birds have shown that sexual size dimorphism(SSD) is positively associated with the level of polygyny, whereasintense sperm competition is associated with sexual dichromatism(SD). Positive correlations between protandry and SSD or SDcan therefore be expected to exist across avian species. Becauselarge males are predicted to be better able to cope with adverseecological conditions early in the breeding season, selectionfor protandry, in turn, may have a correlated response on SSDamong migratory species breeding in boreal latitudes. Althoughprevious studies of birds have analyzed the association betweenSSD and protandry, none has analyzed SD in relation to protandry.Here we analyze the association between protandry during springmigration, SSD, and SD in 21 trans-Saharan monogamous migratorybird species. The difference in median migration dates betweenfemales and males, reflecting protandry, was positively associatedwith SD but not with SSD. Because dichromatism is positivelyrelated to sperm competition across species, present resultsare consistent with predictions derived from sexual selectionhypotheses for the evolution of protandry mediated by spermcompetition.     

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.     

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.     

An analysis of continent-wide patterns of sexual selection in a passerine bird

Patterns of selection are widely believed to differ geographically, causing adaptation to local environmental conditions. However, few studies have investigated patterns of phenotypic selection across large spatial scales. We quantified the intensity of selection on morphology in a monogamous passerine bird, the barn swallow Hirundo rustica, using 6495 adults from 22 populations distributed across Europe and North Africa. According to the classical Darwin-Fisher mechanism of sexual selection in monogamous species, two important components of fitness due to sexual selection are the advantages that the most attractive males acquire by starting to breed early and their high annual fecundity. We estimated directional selection differentials on tail length (a secondary sexual character) and directional selection gradients after controlling for correlated selection on wing length and tarsus length with respect to these two fitness components. Phenotype and fitness components differed significantly among populations for which estimates were available for more than a single year. Likewise, selection differentials and selection gradients differed significantly among populations for tail length, but not for the other two characters. Sexual selection differentials differed significantly from zero across populations for tail length, particularly in males. Controlling statistically for the effects of age reduced the intensity of selection by 60 to 81%, although corrected and uncorrected estimates were strongly positively correlated. Selection differentials and gradients for tail length were positively correlated between the sexes among populations for selection acting on breeding date, but not for fecundity selection. The intensity of selection with respect to breeding date and fecundity were significantly correlated for tail length across populations. Sexual size dimorphism in tail length was significantly correlated with selection differentials with respect to breeding date for tail length in male barn swallows across populations. These findings suggest that patterns of sexual selection are consistent across large geographical scales, but also that they vary among populations. In addition, geographical patterns of phenotypic selection predict current patterns of phenotypic variation among populations, suggesting that consistent patterns of selection have been present for considerable amounts of time.     

Rapid evolutionary change in a secondary sexual character linked to climatic change

The ability of organisms to respond evolutionarily to rapid climatic change is poorly known. Secondary sexual characters show the potential for rapid evolutionary change, as evidenced by strong divergence among species and high evolvability. Here we show that the length of the outermost tail feathers of males of the socially monogamous barn swallow Hirundo rustica, feathers that provide a mating advantage to males, has increased by more than 1 standard deviation during the period from 1984 to 2003. Barn swallows from the Danish population studied here migrate through the Iberian Peninsula to South Africa in fall, and return along the same route in spring. Environmental conditions on the spring staging grounds in Algeria, as indexed by the Normalized Difference Vegetation Index, predicted tail length and change in tail length across generations. However, conditions in the winter quarters and at the breeding grounds did not predict change in tail length. Environmental conditions in Algeria in spring showed a temporal deterioration during the study period, associated with a reduction in annual survival rate of male barn swallows. Phenotypic plasticity in tail length of males, estimated as the increase in tail length from the age of 1 to 2 years, decreased during the course of the study. Estimates of directional selection differentials for male tail length with respect to mating success, breeding date, fecundity, survival and total selection showed temporal variation, with the intensity of breeding date selection, survival selection and total selection declining during the study. Response to selection as estimated from the product of heritability and total selection was very similar to the observed temporal change in tail length. These findings provide evidence of rapid micro-evolutionary change in a secondary sexual character during a very short time period, which is associated with a rapid change in environmental conditions.     

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.     

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     

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.     

Sexual selection in the barn swallow (Hirundo rustica). V. Geographic variation in ornament size

Models of sexual selection in a cline predict the patterns of clinal variation in female mate preference and male secondary sexual characters. These predictions were tested for the nominate subspecies of the barn swallow Hirundo rustica which demonstrates clinal variation in morphology, with several characters in both sexes showing increasing size at higher latitudes. Sexual size dimorphism in the length of the tail ornament and the short, central tail feathers increase with increasing latitude while size dimorphism in other morphological characters is independent of latitude. The main reason for the two divergent patterns of sexual size dimorphism appears to be the higher foraging cost of having a long tail ornamental at low latitudes. The control of development decreases with increasing latitude as demonstrated by an increasing latitudinal cline in fluctuating asymmetry of tail length. Phenotypic variance in tail length increases with latitude in males, but not in females, as shown by the coefficients of variation. Clinal variation in morphology is not due to natural selection associated with a latitudinal increase in the distance between breeding and wintering areas. The geographic patterns of morphological variation suggest that the tail character has diverged geographically as a result of a sexual process of reliable signalling.     

Geographical and seasonal variation in the intensity of sexual selection in the barn swallow Hirundo rustica: a meta‐analysis

Sexual selection arises from competition among individuals for access to mates, resulting in the evolution of conspicuous sexually selected traits, especially when inter‐sexual competition is mediated by mate choice. Different sexual selection regimes may occur among populations/subspecies within the same species. This is particularly the case when mate choice is based on multiple sexually selected traits. However, empirical evidence supporting this hypothesis at the among‐populations level is scarce. We conducted a meta‐analysis of the intensity of sexual selection on the largest database to date for a single species, the barn swallow (Hirundo rustica), relying on quantitative estimates of sexual selection. The intensity of sexual selection was expressed as the strength (effect size) of the relationships between six plumage ornaments (tail length, tail asymmetry, size of white spots on tail, ventral plumage colour, throat plumage colour and throat patch size) and several fitness proxies related to reproduction, parental care, offspring quality, arrival date from spring migration, and survival. The data were gathered for four geographically separated subspecies (H. r. rustica, H. r. erythrogaster, H. r. gutturalis, H. r. transitiva). The overall mean effect size (Z_r = 0.214; 95% confidence interval = 0.175–0.254; N = 329) was of intermediate magnitude, with intensity of sexual selection being stronger in males than in females. Effect sizes varied during the breeding cycle, being larger before egg deposition, when competition for access to mates reaches its maximum (i.e. in the promiscuous part of the breeding cycle), and decreasing thereafter. In addition, effect sizes from experiments were not significantly larger than those from correlative studies. Finally, sexual selection on different sexually dimorphic traits varied among subspecies. This last result suggests that morphological divergence among populations has partly arisen from divergent sexual selection, which may eventually lead to speciation.     

Interval between clutches, fitness, and climate change

Timing of optimal reproduction can be affected by the presenceof multiple broods, with multi-brooded species breeding earlier(and later) than the optimal timing of breeding as comparedwith single-brooded species that only need to optimize the timingof a single brood. Approximately two-thirds of barn swallowsHirundo rustica produce 2 broods per year, and I tested whetherthe constraints on timing of reproduction were affected by climatechange because climatic amelioration would allow both an earlierstart and a later termination of reproduction. The durationof the interval between first and second clutches and the variancein the duration increased during 1971–2005 when temperatureduring spring, but not summer, increased rapidly. Interclutchinterval was shorter when mean date of breeding was late andalso among late-breeding individuals during individual years.When clutch size and brood size of the first clutch were large,interval until the second brood increased. Pairs with a longinterval produced more fledglings than pairs with a short interval.Pairs with first broods with strong mean T-cell–mediatedimmune responses took shorter time to start their second clutch,whereas mean body mass or tarsus length of first broods werenot significantly related to interclutch interval. Interclutchinterval increased with the size of a secondary sexual character,the length of the outermost tail feathers of adult male barnswallows, but not with tail length of females, or with sizeof several other phenotypic characters in either sex. Thesefindings are consistent with the hypothesis that the durationof the interclutch interval is determined by a combination ofenvironmental conditions, reproductive effort, and sexual selection.     

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.     

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.     

Environmental and geographical constraints on common swift and barn swallow spring arrival patterns throughout the Iberian Peninsula

Aim Still poorly understood, the main migratory pathways for most trans‐Saharan species pass through the Iberian Peninsula, which acts as a gateway to the European–African migratory system. Arrival patterns in this region for the common swift (Apus apus) and barn swallow (Hirundo rustica), of similar morphology and flight capabilities, were described, and the environmental and geographical factors best explaining them were examined, in a search for common ecological constraints on these two migratory species. Location Latitude ranged from 36.02 to 43.68°N, longitude from 9.05°W to 3.17°E, and altitude from 0 to 1595 m a.s.l. for 482 common swift and 812 barn swallow Spanish localities spread widely over the Iberian breeding grounds of the two species. Methods Our data set, covering the years 1960–1990, consisted of 3206 first‐arrival dates for common swifts and 6036 for barn swallows. Forty topographical, climatic, river basin, geographical and spatial variables were used as explanatory variables in general regression models (GRMs). GRMs included polynomial terms up to cubic functions in all variables when they were significant. A backward stepwise selection procedure was applied in all models until only significant terms remained. GRMs were applied in two steps. First, we searched for the best model in each one of the five types of variables (topographical, climatic, river basin, geographical and spatial). To cope with the unavoidable correlation between explanatory variables, the relative importance of each type of variable was assessed by hierarchical variance partitioning. Secondly, we searched for that model able to explain the maximum amount of the observed variability in arrival date. To obtain this model all significant explanatory variables were subjected jointly to a GRM. Spatial variables were then added to this model to take any remaining spatial structure in the data into account. Moran's I autocorrelation coefficient was used to check for spatial autocorrelation. Results Both species arrived earlier in the south‐western Iberian Peninsula, where summers are warmer and drier. From there, both species followed the main southern Iberian river basins towards the north‐east; however, several mountainous regions impede the colonization of eastern Iberia. The best models for each type of variable explained 19–47% of the variability in common swift arrival dates and 14–44% in barn swallow arrival dates. Variance partitioning indicated that climatic and geographical variables best explained variability. The best predictive models built with all variables accounted for 52% of the variability in common swift arrival dates and 50% for the barn swallow. Residuals from both models were not spatially autocorrelated, an indication that all major spatially structured variation had been accounted for. Main conclusions Spring arrival patterns are highly dependent on the geographical configuration of the Iberian Peninsula. This spatial constraint forces both species to converge very closely in their spring migration, because common swifts and barn swallows are subject to a trade‐off between optimum migratory pathways and territories ecologically suitable for breeding.