Elevated frequency of abnormalities in barn swallows from Chernobyl

Ever since the Chernobyl accident in 1986, that contaminated vast areas in surrounding countries with radiation, abnormalities and birth defects have been reported in human populations. Recently, several studies suggested that the elevated frequency of such abnormalities can be attributed to poverty and stress in affected human populations. Here, we present long-term results for a free-living population of barn swallows, Hirundo rustica, demonstrating the presence of 11 morphological abnormalities in populations around Chernobyl, but much less frequently in an uncontaminated Ukrainian control population and three more distant control populations. The presence of these abnormalities in barn swallows is associated with reduced viability. These findings demonstrate a link between morphological abnormalities and radiation in an animal population that cannot be attributed to poverty and stress. The most parsimonious hypothesis for abnormalities in animal and human populations alike is that the effects are caused by the same underlying cause, viz. radiation derived from the Chernobyl accident.     

Antioxidants, radiation and mutation as revealed by sperm abnormality in barn swallows from Chernobyl

Reduced levels of antioxidants such as carotenoids and vitamins A and E can increase DNA damage caused by free radicals. Exposure to radiation has been proposed to reduce levels of antioxidants that are used for DNA repair and this reduction may be responsible for increased levels of mutation in radioactively contaminated areas. We test this hypothesis using field measures of antioxidants in blood, liver and eggs of the barn swallow Hirundo rustica while relating these to levels of mutation as reflected by the frequency of abnormal sperm. Antioxidant levels in blood, liver and eggs were reduced in Chernobyl, Ukraine, compared with an uncontaminated control area, and levels of antioxidants correlated negatively with levels of background radiation. The frequency of abnormal sperm was almost an order of magnitude higher in Chernobyl than in the control area and was negatively related to antioxidant levels in blood and liver. This is consistent with the hypothesis of a direct link between radiation and individual levels of antioxidants, suggesting that levels of mutation differ among individuals owing to individual differences in the abundance of antioxidants.     

Impaired swimming behaviour and morphology of sperm from barn swallows Hirundo rustica in Chernobyl

We investigated the motility and morphology of live sperm from barn swallows Hirundo rustica breeding in radioactively contaminated areas around Chernobyl and control areas in Ukraine in order to test the hypothesis that swimming behaviour and morphology of sperm was impaired by radioactive contamination. We obtained sperm samples from 98% of sampled birds, thus avoiding sampling bias due to the fraction of males not producing sperm samples. Analyses of within- and between-sample repeatability revealed significant and intermediate to large estimates for all sperm parameters. There were significant differences between the Chernobyl area and the control area for two of 11 sperm behaviour parameters, and significant interactions between area and year for six of these parameters. The proportion of sperm with abnormal morphology was elevated in barn swallows from Chernobyl. A principal component (PC) analysis revealed four significant axes that explained 88% of the variance in sperm behaviour parameters. One of these principal components differed between areas, and three components showed significant year by area interactions. PC2 representing the frequency of slow sperm increased with increasing radiation in one year, but not another. PC3 representing sperm with high linearity, small amplitude of lateral head displacement and low track velocity decreased with increasing background radiation level. PC4 reflecting a large proportion of static sperm with high beat cross frequency increased with increasing background radiation level. Sperm behaviour as reflected by principal components was predictable among years from information on level of radiation, and it was predictable among sites in different years. These results are consistent with the hypothesis that sperm behaviour and morphology have been affected by radiation due to the Chernobyl accident.     

Uninformative exaggeration of male sexual ornaments in barn swallows

Models of sexual selection suggest that mate-choice preferences are favored because differences between males in their degree of ornamental exaggeration convey useful information about the direct or indirect benefits they have to offer [1-5]. Such arguments assume that variation in male ornament size can be attributed to variation in the degree of sexually selected exaggeration. We provide the first test of this assumption by conducting tail-length experiments in male barn swallows. Over the last twenty years, a large amount of work has shown that female barn swallows are influenced by male tail length when choosing a mate [6-12]. Recent experiments have shown that a combination of natural and sexual selection results in the elongated tail streamer--a tail that is on average across the population about 12 mm (approximately 10%) longer than the aerodynamic optimum [13, 14]. We show that the aerodynamically optimal tail length varies significantly between males, whereas the extent of streamer elongation beyond the optimum does not. Similarly, the aerodynamically optimal tail length significantly predicts observed tail length and conveys information about flight performance, whereas the extent of sexually selected exaggeration of streamer length does not. Therefore, contrary to handicap models of sexual selection, the sexually selected exaggeration of this trait provides females with little information about any aspect of mate quality     

Impaired swimming behaviour and morphology of sperm from barn swallows Hirundo rustica in Chernobyl

We investigated the motility and morphology of live sperm from barn swallows Hirundo rustica breeding in radioactively contaminated areas around Chernobyl and control areas in Ukraine in order to test the hypothesis that swimming behaviour and morphology of sperm was impaired by radioactive contamination. We obtained sperm samples from 98% of sampled birds, thus avoiding sampling bias due to the fraction of males not producing sperm samples. Analyses of within- and between-sample repeatability revealed significant and intermediate to large estimates for all sperm parameters. There were significant differences between the Chernobyl area and the control area for two of 11 sperm behaviour parameters, and significant interactions between area and year for six of these parameters. The proportion of sperm with abnormal morphology was elevated in barn swallows from Chernobyl. A principal component (PC) analysis revealed four significant axes that explained 88% of the variance in sperm behaviour parameters. One of these principal components differed between areas, and three components showed significant year by area interactions. PC2 representing the frequency of slow sperm increased with increasing radiation in one year, but not another. PC3 representing sperm with high linearity, small amplitude of lateral head displacement and low track velocity decreased with increasing background radiation level. PC4 reflecting a large proportion of static sperm with high beat cross frequency increased with increasing background radiation level. Sperm behaviour as reflected by principal components was predictable among years from information on level of radiation, and it was predictable among sites in different years. These results are consistent with the hypothesis that sperm behaviour and morphology have been affected by radiation due to the Chernobyl accident.     

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.     

Immune response of male barn swallows in relation to parental effort, corticosterone plasma levels, and sexual ornamentation

Life-history theory posits trade-offs between fitness components. Reproduction negatively affects physiology and immune systemfunctioning, and the effect of this form of stress may be mediatedby glucocorticosteroids. We manipulated brood size of barnswallows (Hirundo rustica) to study the effect of stress arisingfrom reproductive effort on corticosterone levels of males.We also measured T-cell—mediated immunocompetence by intradermally injecting birds with phytohemagglutinin, whichis mitogenic to T-lymphocytes. The results confirmed the predictionof a negative effect of parental effort on lymphoproliferativeresponse. We found no covariation between immune response andcorticosterone levels. Males with long tails, an ornament currentlyunder directional sexual selection, had a relatively large T-cell response to the mitogen, consistent with models of parasite-mediated sexual selection predicting higher levels of immune defensein highly ornamented males. In addition, males with large sexualornaments had relatively low corticosterone levels at the endof the parental period. These results can be reconciled withthe hypothesis proposing a trade-off between parental activitiesand adaptive immunity and suggest that highly ornamented malesare less exposed or less susceptible to stress arising fromparental effort.     

The design of complex sexual traits in male barn swallows: associations between signal attributes

Variation in the expression of sexually selected traits among individuals is widely investigated on the premise that these traits evolved to signal male quality. Significant repeatabilities of sexual signals and their associations with condition, mating success, survivorship and age may be the signatures of sexual selection. However, little is known about the relationship between these sexual attributes. Here we studied 28 acoustic and visual traits in the barn swallow, Hirundo rustica, that may potentially function in sexual selection. Based on effect sizes calculated at the between-individual level, we assessed the relationship between repeatability, condition-dependence, attractiveness, age-dependence and viability indicator value of sexual traits using sexual signals as the units of analyses. Those traits that showed high within-year repeatability also showed high between-year repeatability, indicating that between-individual variation is consistent within and among seasons. In addition, age-dependence of traits, probably causing between-year variation, was negatively related to between-year repeatability. Condition-dependence was negatively correlated with effect sizes for the extent to which traits predicted viability. Therefore, traits that are positively related to immediate condition are those that are negatively related to survival, which may be the signature of a trade-off between current and future reproductive success ultimately reflecting signal reliability. No other significant relationship was found between trait attributes. We conclude that multiple sexual signals reflect different aspects of male quality in the barn swallow.     

Plumage brightness and uropygial gland secretions in barn swallows

The uropygial gland has been hypothesized to play a role in sexual signaling through a "make-up" function derived from the effects of secretions from the gland on the appearanee of the plumage and bare parts of the body. Here we show that plumage brightness of dorsal feathers of individual barn swallows Hirundo rustica was greater in mated than in unmated individuals. In addition, plumage brightness in creased with colony size. Furthermore, plumage bright ness was positively correlated with the amount of wax in the uropygial gland, negatively correlated with time of sampling of uropygial wax (perhaps because more wax is present early in the morning after an entire night of wax production without any preening), and negatively correlated with the number of chewing lice that degrade the plumage. Experimentally preventing barn swallows from access to the uropygial gland reduced plumage brightness, showing a causal link between secretions from the uropygial gland and plumage brightness. These findings provide evidence consistent with a role of uropygial secretions in signaling plumage brightness.     

DNA damage in barn swallows (Hirundo rustica) from the Chernobyl region detected by use of the comet assay

We investigated levels of DNA damage in blood cells of barn swallows (Hirundo rustica) inhabiting the Chernobyl region to evaluate whether chronic exposure to low-level radioactive contamination continues to induce genetic damage in free-living populations of animals. Blood samples were obtained from barn swallows collected at sites with different background levels of radiation, including a relatively uncontaminated area. The extent of DNA damage was evaluated using the alkaline (pH = 12.1) comet assay, a robust and sensitive electrophoresis-based technique widely employed in research ranging from biomonitoring to clinical studies. We found that levels of DNA damage, as indexed by the extent of DNA migration, were increased in barn swallows living in areas surrounding Chernobyl when compared to swallows sampled at low-level sites. The results we obtained are consistent with previous findings on this same species, which showed that swallows breeding in areas heavily contaminated with radionuclides have increased mutation rates, higher oxidative stress and incidence of morphological aberrations and tumors. Overall, these results indicate that chronic exposure to radioactive contaminants, even 20 years after the accident at the Chernobyl nuclear power plant, continues to induce DNA damage in cells of free-living animals.     

Testosterone, plumage colouration and extra-pair paternity in male North-American barn swallows

In most monogamous bird species, circulating testosterone concentration in males is elevated around the social female's fertile period. Variation in elevated testosterone concentrations among males may have a considerable impact on fitness. For example, testosterone implants enhance behaviours important for social and extra-pair mate choice. However, little is known about the relationship between natural male testosterone concentration and sexual selection. To investigate this relationship we measured testosterone concentration and sexual signals (ventral plumage colour and tail length), and determined within and extra-pair fertilization success in male North American barn swallows (Hirundo rustica erythrogaster). Dark rusty coloured males had higher testosterone concentrations than drab males. Extra-pair paternity was common (42% and 31% of young in 2009 and 2010, respectively), but neither within- nor extra-pair fertilization success was related to male testosterone concentration. Dark rusty males were less often cuckolded, but did not have higher extra-pair or total fertilization success than drab males. Tail length did not affect within- or extra-pair fertilization success. Our findings suggest that, in North American barn swallows, male testosterone concentration does not play a significant direct role in female mate choice and sexual selection. Possibly plumage colour co-varies with a male behavioural trait, such as aggressiveness, that reduces the chance of cuckoldry. This could also explain why dark males have higher testosterone concentrations than drab males.     

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.     

Gregarious foraging in barn swallows after the breeding season

Aerial vertebrate foragers, e.g. insectivorous bats, martins and swallows, often show gregarious behavior such as colonial breeding, communal roosting and aggregating behavior during foraging. Studies of gregariousness in aerial foragers have mostly focused on colonial breeding or communal roosting, and only a few intensive studies have dealt with gregariousness during foraging. Here, we report on large and stable aggregations of barn swallows, Hirundo rustica, observed during daytime after the breeding season in Japan. Relatively large aggregations of 20 or more birds were located around poultry, pig and cattle farms and mounds of manure. The aggregations were stable in size both within-days and between-days. Their activities consisted only of repeated cycles of foraging and resting around the farms where their prey, the large black soldier fly Hermetia illuceus (>10 mm) and other medium (5–10 mm) flies, was dense. Distributions of swallows around the farms overlapped with the distributions of prey, and the size of the aggregations significantly correlated with the abundance of prey.     

Parasitism, host immune function, and sexual selection

Parasite-mediated sexual selection may arise as a consequence of 1) females avoiding mates with directly transmitted parasites, 2) females choosing less-parasitized males that provide parental care of superior quality, or 3) females choosing males with few parasites in order to obtain genes for parasite resistance in their offspring. Studies of specific host-parasite systems and comparative analyses have revealed both supportive and conflicting evidence for these hypotheses. A meta-analysis of the available evidence revealed a negative relationship between parasite load and the expression of male secondary sexual characters. Experimental studies yielded more strongly negative relationships than observations did, and the relationships were more strongly negative for ectoparasites than for endoparasites. There was no significant difference in the magnitude of the negative effect for species with and without male parental care, or between behavioral and morphological secondary sexual characters. There was a significant difference between studies based on host immune function and those based on parasite loads, with stronger effects for measures of immune function, suggesting that the many negative results from previous analyses of parasite-mediated sexual selection may be explained because relatively benign parasites were studied. The multivariate analyses demonstrating strong effect sizes of immune function in relation to the expression of secondary sexual characters, and for species with male parental care as compared to those without, suggest that parasite resistance may be a general determinant of parasite-mediated sexual selection.     

Ecological and phenological covariates of offspring sex ratio in barn swallows

Non-random sex allocation in relation to parental, ecological and phenological factors has been investigated in several correlational studies of birds, mostly based on few breeding seasons and relatively small sample sizes, which have led to different results. We investigated sex ratio of nestling barn swallows (Hirundo rustica) in relation to adult sex ratio, laying date, clutch size, colony size and meteorological conditions in a sample of 553 broods (>2200 nestlings) during 10 years. At the population level, nestling sex ratio varied among years and deviated from parity in two years. Sex ratio among adults did not predict offspring sex ratio in the current or the following year. At the within-family level, the proportion of sons increased with laying date in large clutches, did not vary among clutches of intermediate size, and tended to decline with laying date in small clutches. Large colonies harbored more sons. The proportion of males increased with temperature during laying whereas the effects of temperature during the pre- or post-laying periods and that of rainfall were non-significant. These patterns of variation of offspring sex ratio did not differ between years. Thus, we identified several potential causal sources of variation in barn swallow offspring sex ratio, including temporal, phenological and ecological factors. The observation of an association of offspring sex with temperature during laying is novel for birds and may be mediated by effects on maternal steroid hormones profile. The ecological and evolutionary implications of present findings are discussed in the light of adaptive sex allocation theory.     

Female mate choice based on territory quality in barn swallows

Female mate choice based on territory quality is difficult to study because territories often contain many resources, which are difficult to quantify. Here, using the barn swallow (Hirundo rustica gutturalis) breeding at an outdoor breeding site in Japan, where each male defends only a small territory containing old nests, we studied whether females choose social mates based on territory quality. Since the territories of this species contain few other resources, territory quality can easily be assessed by quantifying old nests in the territory. We made the following four observations: (1) male swallows displayed old nests in their territories to females; (2) the old nests used for the first clutch were less broken than the other old nests within the same territory; (3) territory quality, defined by the number of old nests weighted by the intactness of each old nest, predicted the productivity of the territory; and (4) males with better territories paired with females earlier, and hence bred earlier, than those with inferior territories. The relationships remained significant even after controlling for male morphological traits. Based on these results, we can infer that female swallows choose their mates based, in part, on territory quality.