Sperm competition favors increased investment in post-copulatory sexual traits (e.g., long sperm) while reducing parental investment. The relationship between the two investments, however, remains unclear, although it affects the direction and speed of the evolution of each trait. Here, using the Asian barn swallow Hirundo rustica gutturalis, we examined the relationship between total sperm length (i.e., a post-copulatory sexual trait in birds) and male incubation participation (i.e., a paternal investment). This study system provides a unique opportunity to test the relationship, because male incubation has evolved as a derived trait and has not yet been fixed in the populations. After controlling for potential confounding factors (i.e., body condition and pre-copulatory sexual traits), we found that the probability of male participation in incubation increased with the total sperm length. Given that long sperm would secure within-pair paternity, incubation investment by males with long sperm would be adaptive in these sparse populations, rather than pursuing unlikely opportunities for extrapair mating at the expense of participation in incubation. The observed pattern was contrary to the negatively correlated evolution between the total sperm size and male participation in incubation in the family Hirundinidae, indicating that the direction of the relationship between post-copulatory sexual traits and paternal investment can be different from the general pattern of the clade depending on the ecological and evolutionary settings.

Feather coloration changes over time, but the underlying mechanisms remain poorly understood. In this study, using the reddish throat feathers of the barn swallow, Hirundo rustica, a well-known sexually selected trait, we examined whether within-season feather color change reflected the change of the major pigment, pheomelanin. As predicted, the reddish feathers faded over time, as their coloration became significantly less red with increasing intervals from the initial capture date to recapture date. Likewise, the pheomelanin content of these feathers significantly decreased with increasing intervals between captures. Neither feather color change nor pheomelanin content change depended on study year, sex, or initial capture date. However, feather color change, but not pheomelanin content change, depended on body condition at the initial capture. This condition-dependent feather color change, together with the condition-independent pheomelanin loss, indicates that seasonal change of the major pigment is insufficient to explain the observed patterns of feather color change. Future study should pay attention to additional colorants that may impact the signal honesty of animal coloration.

Differential migration strategies favour different sets of characteristics, including sexually selected ornamentation. Such phenotypic variation is particularly evident in a population with partial migration, where migrants and nonmigrants co-exist. Partial migration provides insights into the link among migration, local environment, and ornamentation, although empirical studies remain scarce. Here, we studied the plumage traits of barn swallows (Hirundo rustica) in southern Japan, where both winterings and migrants breed sympatrically. We further examined this relationship with multiple isotopes (δ2H, δ13C, δ15N, and δ34S), which provides insight into their moulting habitat. Among males, winterings and migrants differed in their morphological traits: wintering males had shorter wings, which suggests the high demand for flight apparatus in migratory birds. Moreover, wintering males had larger white tail spots and less colourful throat patches than migratory males, indicating ornament divergence between them. Wintering males had a significantly smaller isotopic space when examining the combinations of δ34S with the other isotopes compared to migratory males, which indicates a differential geographic range between them, perhaps because of the limited variation in the distance to the sea in wintering males. As in males, wintering females had a significantly smaller isotopic space than migrant females, but there were few morphological differences between migratory and wintering females. Instead, some morphological traits were related to isotope values in females. These results indicate sex-specific linkage among migration, local environment, and ornamentation.

Pigmentary coloration is widespread in animals. Its evolutionary and ecological features are often attributed to the property of predominant pigments; therefore, most research has focused on predominant pigments such as carotenoids in carotenoid-based coloration. However, coloration results from predominant pigments and many other minority pigments, and the importance of the latter is overlooked. Here, we focused on porphyrin, an "uncommon" pigment found in bird feathers, and investigated its importance in the context of feather color changes in the barn swallow Hirundo rustica. We found that the "pheomelanin-based coloration" of the barn swallow faded after the irradiation of UV light, and this effect was particularly strong in the feathers of young swallows (nestlings and fledglings, here). We also found that it is not the predominant pigment, pheomelanin, but protoporphyrin IX pigment that showed the same pattern of depigmentation after the irradiation of UV light, particularly in the feathers of young swallows. In fact, the abovementioned age-dependent feather color change was statistically explained by the amount of porphyrin in the feathers. The current study demonstrates that a minority pigment, porphyrin, explains within-season dynamic color change, an ecological feature of feather coloration. The porphyrin-mediated rapid color change would benefit young birds, in which feather coloration affects the parental food allocation during a few weeks before independence, but not later. Future studies should not ignore these minor but essential pigments and their evolutionary and ecological functions.

Many empirical studies have focused on highly ornamented species to identify ecological factors that maintain the ornamentation or favour its exaggeration. By contrast, although reduction or loss of ornamentation appears to be widespread, species with reduced/lost ornamentation and its relationship with ecological factors are rarely focused on. Here, based on data collected over 4 years, we studied outermost tail feather length, i.e. a well-known sexual ornamentation in this clade, in relation to roosting location in the Pacific Swallow Hirundo tahitica during winter. In contrast to congeners, this species has inconspicuous tail ornamentation, i.e. very shallowly forked tails with vestigial streamers, providing a rare opportunity to study the ecological factors driving reduced ornamentation. We found that Pacific Swallows mainly roost in old nests under bridges over rivers, which resemble their original roosting sites, but some roost in much warmer sites, i.e. old nests under the eaves of houses above the ground. Individuals roosting under the eaves of houses had significantly longer outermost (but not central) tail feathers than those roosting under bridges. Individuals roosting under the eaves of houses were heavier and showed lower physiological stress, and thus might better endure the maintenance cost, favouring ornament elaboration. Because we controlled for the effects of sex and age, these factors would not confound the observed pattern. Reduced ornamentation, as found in Pacific Swallows roosting under their original roosting sites, could become elaborated in benign environments (i.e. under eaves, here), stressing the importance of balance between the costs and benefits of ornamentation.

Pigment-based coloration is prevalent in animals, but its expression greatly varies across species, populations, and even among individuals in the same populations. Some animals are highly pigmented and thus have conspicuous coloration, whereas others are modestly pigmented and thus have drab coloration. A possible explanation for the variety in pigmentation is a resource-based tradeoff, in which resources invested in pigmentation are unavailable for other functional traits, and thus animals that need to invest in the latter have limited resources to invest in pigmentation. Resource-based tradeoff is plausible in theory, but direct tests are scarce, partially because of many components of pigment-based coloration (i.e., multiple pigments, integument microstructure, and stains) that affect coloration, preventing the use of coloration as an index of pigmentation. Here, using the barn swallow, Hirundo rustica, we examined the relationship between pheomelanin pigmentation in reddish throat patch (a precopulatory sexual trait) and total sperm length (a postcopulatory sexual trait), with particular attention to glutathione as the common resource. We predicted that pheomelanin, which is the predominant pigment in the reddish throat patch, should be negatively related to total sperm length, and that both sexual traits should be further negatively related to the amount of glutathione. As predicted, we found a negative relationship between pheomelanin pigmentation and total sperm length. However, the amount of glutathione in the blood showed no detectable relationship to them. The tradeoff between pheomelanin pigmentation and sperm size, as inferred from the current and previous results, might not be a simple glutathione-based tradeoff.

Many empirical studies have focused on highly-ornamented species to identify ecological factors that maintain the ornamentation or favour its exaggeration. By contrast, although reduction or loss of ornamentation appears to be widespread, species with reduced/lost ornamentation and its relationship with ecological factors are rarely focused on. Here, based on data collected over four years, we studied outermost tail feather length, i.e. a well-known sexual ornamentation in this clade, in relation to roosting location in the Pacific swallow Hirundo tahitica during winter. In contrast to congeners, this species has inconspicuous tail ornamentation, i.e. very shallowly forked tails with vestigial streamers, providing a rare opportunity to study the ecological factors driving reduced ornamentation. We found that Pacific swallows mainly roost in old nests under bridges over rivers, which resemble their original roosting sites, but some roost in old nests under the eaves of houses above the ground. Individuals roosting under the eaves of houses had significantly longer outermost (but not central) tail feathers than those roosting under bridges. Individuals roosting under the eaves of houses were heavier and showed lower physiological stress, and thus might better endure the maintenance cost, favouring ornament elaboration. Because we controlled for the effects of sex and age, these factors would not confound the observed pattern. Reduced ornamentation, as found in Pacific swallows roosting under their original roosting sites, could become elaborated in benign environments (i.e., under eaves, here), stressing the importance of balance between the costs and benefits of ornamentation.

Plumage ornaments, such as colourful feathers and deeply forked tails, are classic examples of sexually selected ornaments, and are shown to be related to ecological factors on an evolutionary time scale. In contrast, although colourful bare skin could also be a visual ornament, few studies have examined the evolutionary relationship between colourful bare skin and ecological factors and its interrelationship with plumage ornaments. Using a phylogenetic comparative approach, we studied leg (and foot) coloration in relation to ecological factors, particularly in habitat type (montane or not), and to well-known sexually selected traits, deeply forked tails and reddish plumage coloration, in the subfamily Hirundininae. We showed that mountain species had redder legs than others. Although we also found that social breeders had redder legs than others, the relationship between habitat type and leg coloration remained significant even after controlling for this relationship. In contrast, tail fork depth and reddish plumage coloration were not significantly related to habitat type. Because leg coloration and these plumage ornaments were not significantly interrelated, they likely evolved partially independently. We also found that mountain species had longer nestling periods than others, indicating higher parental investment in montane area in these monogamous birds. Because bare skin coloration is a dynamic honest signal of the current body condition and parental care ability, birds might utilise this information for successful breeding, particularly in environments where extensive parental care is required.

The function of female ornamentation in (inter)sexual selection is attracting increasing attention, but empirical field studies are mostly based on indirect measures such as mating patterns; direct evidence of male mate preference on female ornamentation while controlling for confounding factors is needed. Here, we performed model presentation experiments to study male mate preference in the barn swallow Hirundo rustica, a model species of sexual selection. Although female tails are shorter than male tails in the barn swallow, they are still long and indicate female quality, possibly due to the differential costs of ornamentation. Although many correlational and experimental studies of live females have focused on long tails in female barn swallows over the last three decades, direct behavioral tests of male mate preference are lacking. In our sequential model presentation experiment, in which we repeated the trials with the same males, we found that males significantly reduced the number of pairing displays when presented with tail-elongated female models compared to controls. The interaction between treatment and male tail length was far from significant. The observed pattern is inconsistent with the prevailing view that female ornamentation is maintained via male preference for more ornamented females; rather, it is consistent with the sexual mimicry hypothesis, in which females can avoid sexual and social harassment by mimicking males.

Evolutionary drivers of the gain and loss of ornamentation are often unclear even for classic ornamentation such as swallows' tails, because macroevolutionary analysis, which is needed to clarify the factors responsible for the transition, is rarely conducted. Some behavioural experiments support the hypothesis that sexual selection is responsible for the evolution of "forked" tails, while others support the hypothesis that foraging on large prey favours the evolution of forked tails. However, empirical tests of these hypotheses used already-ornamented species and macroevolutionary studies of forked/forkless tails, which is critical for inferring the evolutionary forces driving the transition between the presence and absence of ornamentation, are still lacking. Here, using a clade of swallows and martins (Aves: Hirundininae), we examined the evolutionary transition between forkless and forked tails in relation to measures of foraging mode and sexual selection. We found replicated evolution of forkless tails from forked tails, all in clades with sexually monomorphic plumage. Furthermore, we detected correlated evolution of tail shape (i.e., forkless/forked) and extrapair mating opportunity, measured as incubation type which is tightly linked to extrapair paternity both within and among species. A transition from forked to forkless tails was less likely to occur than the reverse transition when extrapair mating opportunities were readily available, but not when extrapair mating opportunities were limited. In contrast, the tail shape was more likely to evolve independently with prey size (i.e., small/large) and social foraging behaviour (i.e., social/solitary foraging). These findings indicate that the intensity of sexual selection, rather than foraging mode, explains the evolutionary transition between the presence and absence of tail ornamentation, questioning the widespread perspective that capturing large prey is an evolutionary force driving and maintaining forked tails.

AbstractThe function of female ornamentation in the context of (inter)sexual selection attracts keen attention these days, but empirical field studies are mostly based on indirect measures such as mating patterns; direct evidence of male mate preference on female ornamentation while controlling for confounding factors is needed. Here we performed model presentation experiments to study male mate preference in the barn swallowHirundo rustica, a model species of sexual selection. Female barn swallows have somewhat shorter tails than males, but their tails are still long and costly. Although many correlational and experimental studies of live females have focused on long tails in female barn swallows over the last three decades, direct behavioral tests of male mate preference are lacking. By using a sequential model presentation experiment, in which we repeated the trials with the same males, we found that males significantly reduced the number of pairing displays when they were presented with tail-elongated female models compared to control female models. Interaction between treatment and male tail length was far from significant. The observed pattern is inconsistent with the prevailing view that costly female ornamentation is maintained via male preference for more ornamented females. Rather, the observed pattern is consistent with the sexual mimicry hypothesis, in which females can avoid sexual (and social) harassment by mimicking males.

Many sexual selection studies focus on conspicuous ornaments, such as long tails, but neglect to investigate inconspicuous traits. Here, we studied a well-known sexual selection mechanism, the Darwin–Fisher mechanism (i.e., breeding date selection), in relation to tarsus length in male barn swallows Hirundo rustica , a model species for sexual selection. When controlling for body size, we found that males with shorter tarsi started breeding earlier than those with longer tarsi. The current study indicates a selective advantage of short-legged males, explaining the reversed sexual dimorphism in tarsus length in this short-legged species.

Some, but not all, animals cope with anthropogenic noise by changing the structure of their acoustic signals, possibly due to two interrelated factors: the design of the acoustic signals and the intrinsic biological state. Here, using the barn swallow (Hirundo rustica) that breed solitarily along streets, we studied male enticement calls and nestling food-begging calls in relation to ambient noise. The former calls are structurally quite similar to the latter, perhaps functioning as a sensory trap to exploit female parental care for nestlings. This provides a unique opportunity to study whether intrinsic biological state (i.e. developmental stage, here), virtually independent of acoustic design, matters in acoustic adaptation to anthropogenic noise. We found that the syllable length of nestling food-begging calls, but not of male enticement calls, decreased with increasing local noise levels within populations. The syllable lengths of the father’s enticement calls and those of the nestling’s food-begging calls were positively related, which explains why male enticement calls as well as nestling food-begging calls had shorter syllables in a noisy urban population compared to those in a quiet rural population. The current findings indicate that the intrinsic biological state of two acoustically similar sounds explains their differential relationships with ambient noise.

Sexual selection favors the evolution of pre-copulatory sexual traits such as ornamentation and post-copulatory sexual traits such as long sperm, but the interrelationships of the two types of sexual traits remain unclear. Here, using Japanese barn swallows, Hirundo rustica gutturalis, and an interspecific analysis of the family Hirundinidae , we examined sperm length in relation to pheomelanin-based plumage coloration. As predicted by the fact that pheomelanogenesis consumes antioxidants, which would be detrimental to develop long sperm, reddish coloration (but not other ornaments) were negatively related to sperm length both within and across species, suggesting an evolutionary tradeoff between these traits.

In our rapidly urbanizing world, species utilizing anthropogenic resources would have positive population trends more than others, although its effect might depend on their ability to cope with environmental change. We tackled this issue using a phylogenetic comparative analysis of hirundines (Aves: Hirundininae). We found that species nesting on buildings, on average, showed more positive population trends than others but, population trends of species nesting on buildings decreased (and even becoming negative) with increasing tail fork depth—an ornament that makes species susceptible to environmental change. Utilizing anthropogenic resources might deteriorate population trends of swallows with deeply forked tails.

Sexual selection can in theory lead to positive and negative effect on population-level fitness and hence population increase/decline in our changing world, but the empirical evidence is scarce. Using a phylogenetic comparative approach, we examined whether and how different sexually selected ornaments affect recent population trends and extinction risk in swallows (Aves: Hirundininae). We found that population trends decreased with increasing depth of male tails, that is a well-known sexually selected trait, and increased with increasing score of reddish plumage coloration, another sexually selected ornament. Similar contrasting patterns were observed for extinction risk. These findings indicate ornament-specific population trends and extinction risk, perhaps due to the differential costs and benefits of ornamentation. Previous studies have mostly focused on the overall effects of sexual selection by combining different kinds of traits, presumed to be sexually selected. However, as predicted by theory, sexual selection would not be a process with the same universal effect on population dynamics as we found here. Divergent ecological consequences would occur through minor differences in sexual selection, which should not be dismissed in future studies.

Empirical studies often support the notion that testosterone inhibits paternal behaviour in animals, although most studies have focused on high, as opposed to low, levels of paternal care. We studied the relationship between plasma testosterone levels and incubation in male Japanese Barn Swallows Hirundo rustica gutturalis, in which some males participate in incubation. Contrary to our prediction, the probability of incubation by males increased with plasma testosterone level. Male incubation behaviour might have emerged as part of nest monitoring behaviour by high-testosterone males in some subspecies that experience high nest predation rates.

The evolution of sexually dimorphic ornamentation should reflect sex differences in a form of parental care, incubation behavior, but empirical support is scarce after controlling for phylogenetic inertia. Here, using phylogenetic comparative methods in swallows and martins (Aves: Hirundinidae), we studied the evolution of sexual dimorphism in tail length in relation to two incubation types, female-only and biparental incubation. We found that species with biparental incubation were more likely to have sexually monomorphic tails compared to species with female-only incubation. Furthermore, an analysis of evolutionary pathways suggested interdependent evolution of biparental incubation and sexual tail dimorphism; transitions to biparental incubation and sexual tail dimorphism were less likely to occur than transitions from that state. This finding is consistent with the hypothesis that selection on male ornamentation matters during the incubation period. We also confirmed that species with biparental incubation had significantly lower rates of extra-pair paternity compared to species with female-only incubation in this clade, providing additional support for the importance of selection on male ornamentation during the incubation period. The current study is one of few phylogenetic comparative studies demonstrating the correlated evolution of biparental incubation and sexual dimorphism in ornamentation.

The original article can be found online.