Age‐dependent relationships between coloration and reproduction in a species exhibiting delayed plumage maturation in females

Males of many bird species exhibit delayed plumage maturation (DPM), a condition in which young individuals display an immature plumage. Several adaptive hypotheses have been suggested for the signaling utility of DPM in males. Tree swallows Tachycineta bicolor, however, are one of the few bird species to exhibit DPM in females, but not in males. Few studies have focused on the age‐dependent signaling function of female plumage traits due to the uncommon nature of DPM in females. Therefore, we used reflectance spectrometry and scanning electron microscopy of sub‐adult (melanin‐based brown) and adult (iridescent‐blue structural) female tree swallows to characterize plumage coloration. Next, we asked whether variation in plumage coloration in females reflects condition and reproductive performance between and within age classes. We found that older females were in better body condition and laid eggs earlier in the season compared to young females; however, average egg mass and reproductive success (number of offspring fledged and offspring condition) did not differ between age classes. There were significant relationships indicating that young females with more‐ornamented (darker brown melanin) plumage laid smaller eggs, but hatched eggs earlier in the season leading to nestlings in better condition compared to less‐ornamented young females. Older females that were more ornamented (brighter, greater blue chroma, and lower hues in iridescent plumage) laid heavier eggs, but ornamentation was negatively associated with immune function, health, and reproductive success. Together, these data suggest that female ornamentation reflects reproductive performance and that there are complicated relationships between plumage coloration, condition, and reproductive performance that ultimately influence reproductive success.     

Coloration,Paternity, and Assortative Mating in Western Bluebirds

Coloration in birds can act as an important sexual signal in males, yet in many species, both sexes display bright colors. Social selection may account for this pattern, with more brightly colored individuals pairing together on the best territories. Mutual mate choice may also explain this, as males investing a great deal of parental care in the offspring should be choosy about their social mates. It is less clear whether this pattern of mate choice can apply to extra‐pair partners as well. We examined western bluebirds (Sialia mexicana) to determine whether more colorful individuals tended to pair with one another, both in social pairs and between females and their extra‐pair partners. Both male and female western bluebirds display both UV‐blue structural plumage and a melanin‐based chestnut breast patch, although females are duller than males. Social pairs mated assortatively with regard to UV‐blue brightness, but not chestnut coloration. There was no evidence that extra‐pair partners mated assortatively, but males with brighter UV‐blue coloration had fewer extra‐pair offspring in their nests. Older males were more successful at siring extra‐pair offspring, despite displaying no differences in coloration compared to younger males. Coloration did not play a role in determining extra‐pair male success. These results suggest that coloration plays a role in the formation of social pairs, but not mate choice for extra‐pair partners.     

Reproductive correlates of plumage coloration of female Mountain Bluebirds

Many studies have shown that the plumage coloration of male birds can act as an honest signal of quality, indicating benefits that a female could gain from pairing with a specific male. In some species, females also display ornamental plumage, but less is known about the function and potential adaptive significance of female coloration because most research has focused on male coloration. Male Mountain Bluebirds (Sialia currucoides) display full body, ultraviolet (UV)‐blue plumage, whereas female plumage is more subdued, with blue color focused on the rump, wing, and tail. During the 2011 and 2012 breeding seasons (May–July) near Kamloops, BC, Canada, we examined coloration of the rump and tail of female Mountain Bluebirds to determine if their plumage could act as an indicator of direct reproductive benefits (e.g., enhanced parental care or reproductive success) to potential mates. We found no relationship between female plumage coloration and either provisioning rate or fledging success. However, female coloration varied with age, with after‐second‐year (ASY) females having brighter, more UV‐blue tail feathers than second‐year (SY) females. In addition, ASY females with brighter, more UV‐blue tails had larger clutches. We also observed positive assortative mating by tarsus length. Because previous work with other species suggests that female body size may be a good predictor of breeding success, males could potentially benefit from pairing with larger females. However, reproductive success did not vary with female size in our study. Although our evidence that structural plumage coloration of female Mountain Bluebirds is a signal of direct reproductive benefits for males (e.g., higher reproductive success) is limited, our results (i.e., ASY females with brighter tails than SY females, and ASY females with brighter tails having larger clutches) do suggest the potential for sexual selection to act on female coloration.     

Spatial distribution of nests constrains the strength of sexual selection in a warbler

In socially monogamous species, extra‐pair paternity may increase the strength of intersexual selection by allowing males with preferred phenotypes to monopolize matings. Several studies have found relationships between male signals and extra‐pair mating, but many others fail to explain variation in extra‐pair mating success. A greater appreciation for the role that ecological contingencies play in structuring behavioural processes may help to reconcile contradictory results. We studied extra‐pair mating in a spatial context in the common yellowthroat (Geothlypis trichas), a territorial wood warbler. Over the course of 6 years, we observed 158 breeding attempts by 99 males, resulting in a total of 369 nests and 520 sampled nestlings. The spatial distribution of territories varied greatly, with males having between 0 and 10 close neighbours and between three and 39 neighbouring nestlings close enough to represent extra‐pair siring opportunities. Both within‐pair and extra‐pair reproductive success increased with breeding density, but the opportunity for sexual selection and strength of selection varied with density. Total variance in reproductive success was highest at low density and was mostly explained by variation in within‐pair success. In contrast, at high density, both within‐pair and extra‐pair successes contributed substantially to variance in reproductive success. The relationships between plumage and extra‐pair mating also varied by density; plumage was under strong sexual selection via extra‐pair mating success at high density, but no selection was detected at low density. Thus, ecological factors that structure social interactions can drive patterns of sexual selection by facilitating or constraining the expression of mating preferences.     

Experimental evidence that extra-pair mating drives asymmetrical introgression of a sexual trait

Theory suggests that traits under positive selection may introgress asymmetrically across a hybrid zone, potentially driven by sexual selection. Two subspecies of the red-backed fairy-wren (Malurus melanocephalus) differ primarily in a sexual signal used in mate choice—red versus orange male back plumage colour—but phylogeographic analyses suggest asymmetrical introgression of red plumage into the genetic background of the orange subspecies. We hypothesized that this asymmetrical introgression may be facilitated by sexual selection if red males have a mating advantage over orange males. We tested this hypothesis with correlational data and a plumage manipulation experiment where we reddened the back plumage of a subset of orange males to mimic males of the red subspecies. There was no correlational evidence of a mating advantage to naturally redder males in this population. Experimentally reddened males sired a similar amount of within-pair young and lost paternity at the same rate as orange males, but they sired significantly more extra-pair young, leading to substantially higher total reproductive success. Thus, we conclude that sexual selection via extra-pair mating is a likely mechanism responsible for the asymmetrical introgression of plumage colour in this system, and is potentially driven by a sensory bias for the red plumage signal.     

Age-related differences in plumage characteristics of male tree swallows Tachycineta bicolor: hue and brightness signal different aspects of individual quality

Age-related differences in plumage characteristics of birds can be the result of differential survival of more ornamented individuals, within-individual changes in plumage attributes with age, or a combination of both. In this study, we investigated age-class related differences in plumage attributes of male tree swallows Tachycineta bicolor by performing both cross-sectional and longitudinal analyses. Male tree swallows in their first breeding season do not display delayed plumage maturation, and possess, like experienced breeders, metallic green to metallic blue iridescent plumage on their dorsal surface. Our results showed that, at the population level, older males were brighter and reflected light maximally at shorter wavelengths (i.e. were more blue). Differences in plumage brightness were most likely caused by changes within individuals as males increased in brightness between the first time they were captured and the subsequent year. Differences in hue, however, were not due to within-individual changes, but rather appear to be the result of greener individuals having lower survival and/or nest site fidelity. Indeed, relatively dull, greener birds had a lower probability of being recaptured the subsequent year. In contrast, we found that if birds captured in their first year as breeding adults were relatively bright, hue was not related to the probability of recapture. These results suggest that plumage attributes in male tree swallows have the potential of being honest signals of quality. Furthermore, plumage brightness and plumage hue might signal different aspects of male quality in this species.     

Paternity analysis reveals opposing selection pressures on crown coloration in the blue tit (Parus caeruleus)

In socially monogamous species, extra-pair paternity can increase the variance in reproductive success and thereby the potential for sexual selection on male ornaments. We studied whether male secondary sexual ornaments are selected through within- and/or extra-pair reproductive success in the blue tit (Parus caeruleus). Male blue tits display a bright blue crown plumage, which reflects substantially in the ultraviolet (UV) and previously has been indicated to be an important sexual signal. We show that males with a more UV-shifted crown hue were less cuckolded, which probably resulted from female preference for more ornamented mates. By contrast, however, older males and males with a less UV-shifted hue sired more extra-pair young. This probably did not reflect direct female preference, since cuckolders were not less UV-ornamented than the males they cuckolded. Alternatively, a trade-off between UV ornamentation and other traits that enhance extra-pair success could explain this pattern. Our results might reflect two alternative male mating tactics, where more UV-ornamented males maximize within-pair success and less UV-ornamented males maximize extra-pair success. Since crown colour was selected in opposite directions by within-pair and extra-pair paternity, directional selection through extra-pair matings seemed weak, at least in this population and breeding season. Reduced intensity of sexual selection due to alternative mating tactics constitutes a potential mechanism maintaining additive genetic variance of male ornaments.     

Are extra‐pair males different from cuckolded males? A case study and a meta‐analytic examination

Traditional models for female extra‐pair matings assume that females benefit indirectly from extra‐pair mating behaviour. Under these so‐called adaptive models, extra‐pair males are hypothesized to have more compatible genotypes, larger body size, exaggerated ornaments or to be older than cuckolded males. Alternatively, (‘nonadaptive’) models that consider female extra‐pair matings to be a by‐product posit that female extra‐pair mating can be maintained even if there is no benefit to females. This could happen if, for example, males gained fitness benefits from extra‐pair mating, while female and male extra‐pair mating behaviours were genetically correlated. Extra‐pair males are also expected to be older and larger if this improves their ability to convince or coerce females to mate. We investigated whether a female's extra‐pair mates differed from her cuckolded mate in both genetic and phenotypic traits by analysing data from an insular house sparrow population. We found that extra‐pair males were older than cuckolded males, consistent with both models. However, in contrast to the expectations from from adaptive models, extra‐pair and cuckolded males were of similar genetic relatedness, and hence expected compatibility, with the female, and had comparable body size and secondary sexual traits. We also updated previous meta‐analyses examining differences between extra‐pair and cuckolded males. The meta‐analytic results matched results from our house sparrow case study. Although we cannot completely exclude indirect benefits for females, nonadaptive models may better explain female extra‐pair matings. These neglected alternative models deserve more research attention, and this should improve our understanding of the evolution of mating systems.     

The relationship between plumage coloration and aggression in female tree swallows

Intrasexual competition is an important selective force that can favor the evolution of honest signals of fighting ability. Research has focused predominantly on male birds, but many female birds also possess plumage ornaments that could mediate the outcome of competitive interactions. We examined the relationship between blue and white structural coloration and aggression in female tree swallows Tachycineta bicolor. Tree swallows are secondary cavity nesters and females show delayed plumage maturation which may be related to intense competition for nest sites. We compared plumage reflectance of second‐year (SY) and after‐second year (ASY) females, and within‐individual changes in plumage reflectance of ASY females in two successive years. We assessed aggression by placing a caged SY female 2 m from the nest box of an ASY female and quantified the ASY female's response in relation to her own plumage coloration. We found substantial differences in plumage reflectance of SY and ASY females, but found that ASY females became greener with duller white coloration in the second year. This may be due to poor weather that made reproduction particularly costly in the first year of the study and suggests coloration is influenced by condition. We found no relationship between dorsal coloration and aggressiveness. Rather, brighter white females spent more time on their nest box and within 2 m of the intruder than females with dull breasts. Our findings suggest that brighter white ASY females may perceive a SY female as less of a threat or that there may be a trade‐off associated with aggression and parental care that is related to white brightness.     

Male age and its association with reproductive traits in captive and wild house sparrows

Evolutionary theory predicts that females seek extra‐pair fertilizations from high‐quality males. In socially monogamous bird species, it is often old males that are most successful in extra‐pair fertilizations. Adaptive models of female extra‐pair mate choice suggest that old males may produce offspring of higher genetic quality than young males because they have proven their survivability. However, old males are also more likely to show signs of reproductive senescence, such as reduced sperm quality. To better understand why old males account for a disproportionally large number of extra‐pair offspring and what the consequences of mating with old males are, we compared several sperm traits of both captive and wild house sparrows, Passer domesticus. Sperm morphological traits and cloacal protuberance volume (a proxy for sperm load) of old and young males did not differ substantially. However, old males delivered almost three times more sperm to the female's egg than young males. We discuss the possibility of a post‐copulatory advantage for old over young males and the consequences for females mated with old males.     

Individual Quality and Extra-Pair Paternity in the Blue Tit: Sexy Males Bear the Costs

Adaptive explanations for the evolution of extra-pair paternity (EPP) suggest that females seek extra-pair copulations with high quality males. Still, the link between ornamentation, individual quality, and paternity remains unclear. Moreover, honest signaling is essential when explaining EPP because it is needed for sexual selection to occur; yet, it is understudied in multiple ornaments. Because blue tits (Cyanistes caeruleus) show variable color expression in several plumage patches, we tested: (i) over two seasons, whether males in better condition, more ornamented and less infected by blood parasites gain EPP and have higher reproductive success, and (ii) over three seasons, whether mating patterns affect color change. Males with more saturated yellow feathers, brighter tails, and in better condition had higher reproductive success in one of the seasons. Contrary to expectation, in another season, males that gained EPP were parasitized by blood parasites, suggesting increased vector exposure during extra-pair copulations. Our results for two seasons show that males siring more extra-pair young were older and grew brighter cheek or tail feathers for the following season. Despite the increased mating costs, in socially monogamous avian systems, high quality males incur in EPP without compromising traits that may be under sexual selection.     

Experimentally altering pre‐breeding sex steroids reduces extra‐pair paternity in female tree swallows

Extra‐pair paternity commonly occurs in many socially monogamous animal species, yet the reasons why females mate with males outside the social pair bond remain poorly understood. Because sex steroids mediate aggressive and sexual behaviors that peak prior to egg laying in female birds, we tested whether they also influence the rate of extra‐pair paternity in nests of female tree swallows (Tachycineta bicolor). In one treatment, we experimentally elevated testosterone (T) using implants containing exogenous T, and in another treatment, we blocked the estrogenic and androgenic actions of T using implants containing 1,4,6‐androstatrien‐3,17‐dione in combination with flutamide (ATD+F). Females with empty implants served as controls. Nests of females treated with T and those with ATD+F were less likely to contain extra‐pair offspring and had a lower proportion of extra‐pair offspring, compared to control females. Treating females with T also delayed clutch initiation dates and disrupted incubation behavior, as found in previous studies, but clutch sizes of T females did not differ from controls. Females treated with ATD+F tended to lay larger clutches than control and T‐treated females, which may be due to their clutch sizes not declining with later initiation dates as found in the T and control treatments; however, after controlling for brood size, ATD+F females produced nestlings that were lighter at day 16 than control females. Although the effect of T on extra‐pair paternity that we observed in tree swallows is consistent with previous studies in female birds, our results demonstrate that blocking the estrogenic and/or androgenic actions of T during pre‐breeding also lowers extra‐pair paternity. Overall, our study suggests that extra‐pair paternity in tree swallows is mediated by sex steroids of females.     

Individual variation in sleep behaviour in blue tits Cyanistes caeruleus: assortative mating and associations with fitness‐related traits

Sleep is ubiquitous in animals, but there is great inter‐ and intraspecific variation in the daily amount of sleep that is needed. Chronic sleep curtailment or experimental sleep deprivation are known to impair health and performance of individuals, but not much is known about the fitness consequences of naturally occurring variation in sleep behaviour. Here we test for assortative mating in sleep behaviour and for correlations between sleep phenotypes and reproductive success and survival in a free‐living blue tit population. We found that partners of a social breeding pair were mated assortatively in regard to standardized awakening time, i.e. awakening time relative to that of other birds of the same sex in the population. We found no evidence for assortative mating for other sleep parameters. In female blue tits no sleep parameter that we measured was significantly correlated with lay date or clutch size. Females that had extra‐pair young in their brood did not differ in awakening time, or in any other sleep parameter, compared to females without extra‐pair young. In males, the probability of siring extra‐pair young was related to sleep onset and sleep duration, but not as predicted. Males that began to sleep earlier and slept longer were more likely to sire extra‐pair offspring. None of the sleep parameters were significantly correlated with local survival of first‐year birds. Our results suggest that there is no strong effect of variation in sleep behaviour on fitness in blue tits, at least under natural conditions. Such a relationship might only become evident when natural sleep patterns are experimentally disturbed, or when sleep quality is affected by anthropogenic noise or light pollution.     

Blue,not UV,plumage color is important in satin bowerbird Ptilonorhynchus violaceus display

Several studies have suggested that peak plumage reflectance in birds matches color preferences used in mate choice. We tested this hypothesis in adult satin bowerbird males that have a short‐wavelength saturated blue‐black plumage with a peak reflectance in the UV. We found that the chroma of the blue (405–480 nm), but not the peak reflecting UV (320–400 nm) portion of the male plumage spectrum was significantly correlated with male mating success. A plot of correlation coefficients between male mating success and plumage saturation showed a well‐defined peak in the blue. This suggests that: 1) blue plumage coloration is more important in mate choice than UV or other colors, and 2) that there is a mismatch between the peak reflectance of the plumage of male satin bowerbirds and the range of plumage wavelengths that are correlated with male mating success. This indicates that it is not safe to infer a role of UV or other colors in mate choice simply because of a peak in plumage reflectance.     

Genetic covariance between components of male reproductive success: within‐pair vs. extra‐pair paternity in song sparrows

The evolutionary trajectories of reproductive systems, including both male and female multiple mating and hence polygyny and polyandry, are expected to depend on the additive genetic variances and covariances in and among components of male reproductive success achieved through different reproductive tactics. However, genetic covariances among key components of male reproductive success have not been estimated in wild populations. We used comprehensive paternity data from socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia) to estimate additive genetic variance and covariance in the total number of offspring a male sired per year outside his social pairings (i.e. his total extra‐pair reproductive success achieved through multiple mating) and his liability to sire offspring produced by his socially paired female (i.e. his success in defending within‐pair paternity). Both components of male fitness showed nonzero additive genetic variance, and the estimated genetic covariance was positive, implying that males with high additive genetic value for extra‐pair reproduction also have high additive genetic propensity to sire their socially paired female's offspring. There was consequently no evidence of a genetic or phenotypic trade‐off between male within‐pair paternity success and extra‐pair reproductive success. Such positive genetic covariance might be expected to facilitate ongoing evolution of polygyny and could also shape the ongoing evolution of polyandry through indirect selection.     

EFFECTS OF SOCIAL AND EXTRA‐PAIR MATING ON SEXUAL SELECTION IN BLUE TITS (CYANISTES CAERULEUS)

The contribution of extra‐pair paternity (EPP) to sexual selection has received considerable attention, particularly in socially monogamous species. However, the importance of EPP remains difficult to assess quantitatively, especially when many extra‐pair young have unknown sires. Here, we combine measurements of the opportunity for selection (I), the opportunity for sexual selection (I_S), and the strength of selection on mating success (Bateman gradient, β_SS) with a novel simulation of random mating tailored to the specific mating system of the blue tit (Cyanistes caeruleus). In a population where social polygyny and EPP are common, the opportunity for sexual selection was significantly stronger and Bateman gradients significantly steeper for resident males than for females. In general, success with the social mate(s) contributed most to variation in male reproductive success. Effects of EPP were small, but significantly higher than expected under random mating. We used sibship analysis to estimate the number of unknown sires in our population. Under the assumption that the unknown sires are nonbreeding males, EPP reduced the variance in and the strength of selection on mating success, a possibility that hitherto has not been considered.     

Extra‐group mating increases inbreeding risk in a cooperatively breeding bird

In many cooperatively breeding species, females mate extra‐group, the adaptive value of which remains poorly understood. One hypothesis posits that females employ extra‐group mating to access mates whose genotypes are more dissimilar to their own than their social mates, so as to increase offspring heterozygosity. We test this hypothesis using life history and genetic data from 36 cooperatively breeding white‐browed sparrow weaver (Plocepasser mahali) groups. Contrary to prediction, a dominant female's relatedness to her social mate did not drive extra‐group mating decisions and, moreover, extra‐group mating females were significantly more related to their extra‐group sires than their social mates. Instead, dominant females were substantially more likely to mate extra‐group when paired to a dominant male of low heterozygosity, and their extra‐group mates (typically dominants themselves) were significantly more heterozygous than the males they cuckolded. The combined effects of mating with extra‐group males of closer relatedness, but higher heterozygosity resulted in extra‐group‐sired offspring that were no more heterozygous than their within‐group‐sired half‐siblings. Our findings are consistent with a role for male–male competition in driving extra‐group mating and suggest that the local kin structure typical of cooperative breeders could counter potential benefits to females of mating extra‐group by exposing them to a risk of inbreeding.     

Increased extra‐pair paternity in broods of aging males and enhanced recruitment of extra‐pair young in a migratory bird

Despite keen interest in extra‐pair mating in birds, its adaptive significance remains unresolved. Here, we use a multi‐year dataset to test whether traits of a female's social mate influence her propensity to produce extra‐pair offspring in a population of house wrens, and whether producing extra‐pair young has consequences for a female's fitness through effects on offspring survival. Females were most likely to produce extra‐pair offspring when paired with old males and when paired with males on poor‐quality territories, although this latter effect was marginally nonsignificant. Among offspring, the cutaneous immunity of within‐pair young decreased as the age of their sires increased, but cutaneous immunity of extra‐pair young was not affected by the age of their extra‐pair sires or by the age of the males rearing them. Extra‐pair offspring were more likely than within‐pair offspring to return as breeding adults to the local population, with extra‐pair sons being more likely to return as a breeder for multiple years. Our findings support the hypothesis that females produce extra‐pair offspring to enhance their inclusive fitness beyond what they are capable of given the male with which they are socially paired.     

Fitness benefits of polyandry for experienced females

Females often mate with several different males, which may promote sperm competition and increase offspring viability. However, the potential benefits of polyandry remain controversial, particularly in birds where recent reviews have suggested that females gain few genetic benefits from extra‐pair mating. In tree swallows (Tachycineta bicolor), we found that females with prior breeding experience had more sires per brood when paired to genetically similar social mates, and, among experienced females, broods with more sires had higher hatching success. Individual females breeding in two consecutive years also produced broods with more sires when they were more genetically similar to their mate. Thus, experienced females were able to avoid the costs of mating with a genetically similar social mate and realize fitness benefits from mating with a relatively large number of males. This is one of the first studies to show that female breeding experience influences polyandry and female fitness in a natural population of vertebrates. Our results suggest that the benefits of polyandry may only be clear when considering both the number of mates females acquire and their ability to modify the outcome of sexual conflict.     

Paternity costs from polyandry compensated by increased fecundity in the hide beetle

Polyandry-induced sperm competition is assumed to impose costson males through reduced per capita paternity success. In contrast,studies focusing on the consequences of polyandry for femalesreport increased oviposition rates and fertility. For thesespecies, there is potential for the increased female fecundityassociated with polyandry to offset the costs to males of sharedpaternity. We tested this hypothesis by comparing the proportionand number of offspring sired by males mated with monandrousand polyandrous females in the hide beetle, Dermestes maculates,both for males mating with different females and for males rematingwith the same female. In 4 mating treatments, monandrous femalesmated either once or twice with the same male and polyandrousfemales mated either twice with 2 different males or thricewith 2 males (where 1 male mated twice). Polyandrous and twice-matingmonandrous females displayed greater fecundity and fertilitythan singly mating monandrous females. Moreover, males rematedto the same female had greater paternity regardless of whetherthat female mated with another male. In both polyandrous treatments,male mating order did not affect paternity success. Finally,although the proportion of eggs sired decreased if a male matedwith a polyandrous female, multiply mating females or femalesthat remated with a previous mate laid significantly more eggsand thus the actual number of eggs sired was comparable. Thus,males do not necessarily accrue a net fitness loss when matingwith polyandrous females. This may explain the absence of anyobvious defensive paternity-protection traits in hide beetlesand other species.