Alessandra Costanzo

Viability Is Associated with Melanin-Based Coloration in the Barn Swallow (Hirundo rustica)

Pigmentation of body surface in animals can have multiple determinants and accomplish diverse functions. Eumelanin and pheomelanin are the main animal pigments, being responsible of yellow, brownish-red and black hues, and have partly common biosynthetic pathways. Many populations of vertebrates show individual variation in melanism, putatively with large heritable component. Genes responsible for eu- or pheomelanogenesis have pleiotropic but contrasting effects on life-history traits, explaining the patterns of covariation observed between melanization and physiology (e.g. immunity and stress response), sexual behavior and other characters in diverse taxa. Yet, very few studies in the wild have investigated if eu- and pheomelanization predict major fitness traits like viability or fecundity. In this correlative study, by contrasting adult barn swallows (Hirundo rustica) matched for age, sex, breeding site, and year and date of sampling, we show that males but not females that survived until the next year had paler, relatively more eu- than pheomelanic pigmentation of ventral body feathers. Better performance of individuals that allocate relatively more to eumelanogenesis was expected based on previous evidence on covariation between eumelanic pigmentation and specific traits related to immunity and susceptibility to stress. However, together with the evidence of no covariation between viability and melanization among females, this finding raises the question of the mechanisms that maintain variation in genes for melanogenesis. We discuss the possibility that eu- and pheomelanization are under contrasting viability and sexual selection, as suggested by larger breeding and sperm competition success of darker males from other barn swallow subspecies.

Brownish, small and lousy barn swallows have greater natal dispersal propensity

Natal dispersal contributes to population dynamics and genetic structure. Individuals differ in whether or not they disperse and in the distance they travel from their natal site before settling to breed. Differences in natal dispersal are often associated with variation in other traits. These associations may arise because suites of morphological and behavioural traits are ultimately controlled by the same set of genes. The genes that control melanogenesis in vertebrates pleiotropically influence physiology and behaviour, including boldness and exploration. Because these personality traits predict dispersal, we tested the hypothesis that in the barn swallow, Hirundo rustica , melanic coloration predicts natal dispersal, using a solid matched case–control sampling design and a large sample. We found that males but not females with colour traits that reflect relatively more pheomelanic feather pigmentation were more likely to disperse, consistently with observations on the only other species for which dispersal in relation to plumage melanic coloration has so far been studied. To control for any confounding effects, we also analysed the association of dispersal with morphological traits and parasite infestation. Philopatric individuals were larger than dispersers, whereas dispersal strategy did not differ according to tail length, which is a sexually selected trait. Finally, philopatric females had a smaller infestation of a haematophagous louse fly. The present findings corroborate previous evidence that melanic coloration covaries with a suite of traits. In particular, they show that melanin-based plumage coloration predicts natal dispersal, independently of other factors also influencing dispersal. In addition, our results show that philopatric individuals were larger than dispersers possibly because individuals return to a benign natal place or because large body size confers an advantage in competitive interactions. Finally, they are compatible with the idea of host adaptation to local strains of a parasite with presumably small population size and low dispersing capacity.

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 (Zr = 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.

Sex allocation according to multiple sexually dimorphic traits of both parents in the barn swallow (Hirundo rustica)

Parents should differentially invest in sons or daughters depending on the sex‐specific fitness returns from male and female offspring. In species with sexually selected heritable male characters, highly ornamented fathers should overproduce sons, which will be more sexually attractive than sons of less ornamented fathers. Because of genetic correlations between the sexes, females that express traits which are under selection in males should also overproduce sons. However, sex allocation strategies may consist in reaction norms leading to spatiotemporal variation in the association between offspring sex ratio (SR) and parental phenotype. We analysed offspring SR in barn swallows (Hirundo rustica) over 8 years in relation to two sexually dimorphic traits: tail length and melanin‐based ventral plumage coloration. The proportion of sons increased with maternal plumage darkness and paternal tail length, consistently with sexual dimorphism in these traits. The size of the effect of these parental traits on SR was large compared to other studies of offspring SR in birds. Barn swallows thus manipulate offspring SR to overproduce ‘sexy sons’ and potentially to mitigate the costs of intralocus sexually antagonistic selection. Interannual variation in the relationships between offspring SR and parental traits was observed which may suggest phenotypic plasticity in sex allocation and provides a proximate explanation for inconsistent results of studies of sex allocation in relation to sexual ornamentation in birds.

Clock gene polymorphism and scheduling of migration: a geolocator study of the barn swallow Hirundo rustica

Circannual rhythms often rely on endogenous seasonal photoperiodic timers involving ‘clock’ genes, and Clock gene polymorphism has been associated to variation in phenology in some bird species. In the long-distance migratory barn swallow Hirundo rustica, individuals bearing the rare Clock allele with the largest number of C-terminal polyglutamine repeats found in this species (Q8) show a delayed reproduction and moult later. We explored the association between Clock polymorphism and migration scheduling, as gauged by light-level geolocators, in two barn swallow populations (Switzerland; Po Plain, Italy). Genetic polymorphism was low: 91% of the 64 individuals tracked year-round were Q7/Q7 homozygotes. We compared the phenology of the rare genotypes with the phenotypic distribution of Q7/Q7 homozygotes within each population. In Switzerland, compared to Q7/Q7, two Q6/Q7 males departed earlier from the wintering grounds and arrived earlier to their colony in spring, while a single Q7/Q8 female was delayed for both phenophases. On the other hand, in the Po Plain, three Q6/Q7 individuals had a similar phenology compared to Q7/Q7. The Swiss data are suggestive for a role of genetic polymorphism at a candidate phenological gene in shaping migration traits, and support the idea that Clock polymorphism underlies phenological variation in birds.

Immune and Stress Responses Covary with Melanin-Based Coloration in the Barn Swallow

Eumelanin and pheomelanin are the main endogenous pigments in animals and melanin-based coloration has multiple functions. Melanization is associated with major life-history traits, including immune and stress response, possibly because of pleiotropic effects of genes that control melanogenesis. The net effects on pheo- versus eumelanization and other life-history traits may depend on the antagonistic effects of the genes that trigger the biosynthesis of either melanin form. Covariation between melanin-based pigmentation and fitness traits enforced by pleiotropic genes has major evolutionary implications particularly for socio-sexual communication. However, evidence from non-model organisms in the wild is limited to very few species. Here, we tested the hypothesis that melanin-based coloration of barn swallow (Hirundo rustica) throat and belly feathers covaries with acquired immunity and activation of the hypothalamic–pituitary–adrenal (HPA) axis, as gauged by corticosterone plasma levels. Individuals of both sexes with darker brownish belly feathers had weaker humoral immune response, while darker males had higher circulating corticosterone levels only when parental workload was experimentally reduced. Because color of belly feathers depends on both eu- and pheomelanin, and its darkness decreases with an increase in the concentration of eu- relative to pheomelanin, these results are consistent with our expectation that relatively more eu- than pheomelanized individuals have better immune response and smaller activation of the HPA-axis. Covariation of immune and stress response arose for belly but not throat feather color, suggesting that any function of color as a signal of individual quality or of alternative life-history strategies depends on plumage region.

A Trade-Off between Reproduction and Feather Growth in the Barn Swallow (Hirundo rustica)

Physiological trade-offs mediated by limiting energy, resources or time constrain the simultaneous expression of major functions and can lead to the evolution of temporal separation between demanding activities. In birds, plumage renewal is a demanding activity, which accomplishes fundamental functions, such as allowing thermal insulation, aerodynamics and socio-sexual signaling. Feather renewal is a very expensive and disabling process, and molt is often partitioned from breeding and migration. However, trade-offs between feather renewal and breeding have been only sparsely studied. In barn swallows (Hirundo rustica) breeding in Italy and undergoing molt during wintering in sub-Saharan Africa, we studied this trade-off by removing a tail feather from a large sample of individuals and analyzing growth bar width, reflecting feather growth rate, and length of the growing replacement feather in relation to the stage in the breeding cycle at removal and clutch size. Growth bar width of females and length of the growing replacement feather of both sexes were smaller when the original feather had been removed after clutch initiation. Importantly, in females both growth bar width and replacement feather length were negatively predicted by clutch size, and more strongly so for large clutches and when feather removal occurred immediately after clutch completion. Hence, we found strong, coherent evidence for a trade-off between reproduction, and laying effort in particular, and the ability to generate new feathers. These results support the hypothesis that the derived condition of molting during wintering in long-distance migrants is maintained by the costs of overlapping breeding and molt.

Brood size, telomere length, and parent-offspring color signaling in barn swallows

Trade-offs select for optimal allocation of resources among competing functions. Parents are selected to maximize production of viable offspring by balancing between progeny number and “quality.” Telomeres are nucleoproteins, at the ends of eukaryotic chromosomes, that shorten when cells divide. Because shortening below a certain threshold depresses organismal functioning and rate of shortening depends on environmental conditions, telomeres are good candidates as mediators of trade-offs. We altered brood size of barn swallow Hirundo rustica and found that brood enlargement caused a reduction in relative telomere length (RTL). Reliable signals of offspring quality should evolve that mediate adaptive parental care allocation. Because nestlings with darker coloration receive more care, we analyzed the covariation between RTL and coloration and found that RTL increased with plumage darkness, both within and between broods. Hence, we provide unprecedented evidence that signals relevant to parent-offspring communication reflect telomere length and thus offspring reproductive value.

Lifetime reproductive success, selection on lifespan and multiple sexual ornaments in male European barn swallows

Natural and sexual selection arise when individual fitness varies according to focal traits. Extra‐pair paternities (EPPs) can affect the intensity of selection by influencing variance in fitness among individuals. Studies of selection require that individual fitness is estimated using proxies of lifetime reproductive success (LRS). However, estimating LRS is difficult in large, open populations where EPPs cause reallocation of biological paternity. Here, we used extensive field sampling to estimate LRS in a population of barn swallows (Hirundo rustica) to estimate selection on lifespan and ornamental traits of males. We found selection on lifespan mediated both by within‐ and extra‐pair fertilization success and selection on tail length mediated by within‐ but not extra‐pair fertilization success. In addition, we found selection on tail white spots via extra‐pair fertilization success after controlling for selection on other traits. These results were not confounded by factors that hamper studies of LRS, including nonexhaustive sampling of offspring and biased sampling of males. Hence, natural and sexual selection mediated by LRS operates on lifespan, tail length, and size of the tail white spots in barn swallows.

Behavioural stress response and melanin-based plumage colouration in barn swallow nestlings

Consistent and correlated inter-individual differences in behaviours, the so-called ‘personalities’, have been identified in many vertebrates. The ability to respond to stressful events is part of personalities and can have important fitness consequences, as it determines how individuals cope with environmental challenges. As a consequence of pleiotropic effects of genes involved in several functions, inter-individual differences in behavioural responses can be associated with phenotypic traits, like melanin-based plumage colouration in birds. We examined the association between three proxies of the behavioural stress response and breast plumage colouration in barn swallow ( Hirundo rustica ) nestlings. We found that nestling behavioural responses were consistent within individuals and similar among siblings, thus suggesting that these behaviours may contribute to define individual ‘personalities’. However, nestling behavioural stress response was not significantly predicted by variation in breast plumage colouration, indicating that in juveniles of this species melanin-based colouration does not convey to conspecifics reliable information on individual ability to cope with stressful events.