Adaptive sex differences in growth of pre-ovulation oocytes in a passerine bird

Maternal modification of offspring sex in birds has strong fitness consequences, however the mechanisms by which female birds can bias sex of their progeny in close concordance with the environment of breeding are not known. In recently established populations of house finches (Carpodacus mexicanus), breeding females lay a sex-biased sequence of eggs when ambient temperature causes early onset of incubation. We studied the mechanisms behind close association of incubation and sex-determination strategies in this species and discovered that pre-ovulation oocytes that produce males and females differed strongly in the temporal patterns of proliferation and growth. In turn, sex-specific exposure of oocytes to maternal secretion of prolactin and androgens produced distinct accumulation of maternal steroids in oocyte yolks in relation to oocyte proliferation order. These findings suggest that sex difference in oocyte growth and egg-laying sequence is an adaptive outcome of hormonal constraints imposed by the overlap of early incubation and oogenesis in this population, and that the close integration of maternal incubation, oocytes' sex-determination and growth might be under control of the same hormonal mechanism. We further document that population establishment and the evolution of these maternal strategies is facilitated by their strong effects on female and offspring fitness in a recently established part of the species range.     

Hormone levels predict individual differences in reproductive success in a passerine bird

Hormones mediate major physiological and behavioural components of the reproductive phenotype of individuals. To understand basic evolutionary processes in the hormonal regulation of reproductive traits, we need to know whether, and during which reproductive phases, individual variation in hormone concentrations relates to fitness in natural populations. We related circulating concentrations of prolactin and corticosterone to parental behaviour and reproductive success during both the pre-breeding and the chick-rearing stages in both individuals of pairs of free-living house sparrows, Passer domesticus. Prolactin and baseline corticosterone concentrations in pre-breeding females, and prolactin concentrations in pre-breeding males, predicted total number of fledglings. When the strong effect of lay date on total fledgling number was corrected for, only pre-breeding baseline corticosterone, but not prolactin, was negatively correlated with the reproductive success of females. During the breeding season, nestling provisioning rates of both sexes were negatively correlated with stress-induced corticosterone levels. Lastly, individuals of both sexes with low baseline corticosterone before and high baseline corticosterone during breeding raised the most offspring, suggesting that either the plasticity of this trait contributes to reproductive success or that high parental effort leads to increased hormone concentrations. Thus hormone concentrations both before and during breeding, as well as their seasonal dynamics, predict reproductive success, suggesting that individual variation in absolute concentrations and in plasticity is functionally significant, and, if heritable, may be a target of selection.     

An experimental test of predator–parasite interaction in a passerine bird

Experimental studies incorporating multiple trophic levels are scarce but of increasing interest for understanding ecological communities. Here we investigated interactive effects of perceived predation risk and parasite pressure on life‐history traits in a hole‐nesting bird, and the effects of predation risk on parasite success. In a 3 × 2 experimental design we increased perceived predation risk for breeding great tits Parus major via simulations of either nest‐predators (woodpeckers) or post‐fledging predators (sparrowhawks) close to nests, and used a non‐predatory species (song thrush) as a control. Concurrently, half of the nests in each treatment were either infested with ectoparasites, or kept parasite‐free. Regarding the predation risk – parasite interaction, exposure to nest‐predators tended to lower wing and sternum growth rates of nestlings in the absence, but not the presence, of parasites. In the presence of parasites, exposure to a post‐fledging, but not to a nest‐predator, led to significantly reduced wing growth. Mass and tarsus length were not affected by predator exposure, but ectoparasites had slight positive effects on mass gain. In the last third of the nestling period, overall nestling size was significantly smaller when exposed to a post‐fledging predator than to a nest‐predator, but neither differed from the control. Parental feeding rates were not affected by the treatments, but parents became less selective towards food items under either predation risk. Hen‐flea population sizes (adult or larvae) in nests were not affected by predation risk treatment of hosts. In summary, we found some evidence for an interactive effect of predation risk and parasite pressure on nestling growth. The complexity of the interaction, combined with certain inconsistencies of the effects and potential statistical artifacts, prevent however a straightforward interpretation of the results. The insights from the study are useful for designing additional experiments to further investigate the complexity of predator–parasite interactions in wild populations.     

Context-dependent vocal mimicry in a passerine bird

How do birds select the sounds they mimic, and in what contexts do they use vocal mimicry? Some birds show a preference for mimicking other species' alarm notes, especially in situations when they appear to be alarmed. Yet no study has demonstrated that birds change the call types they mimic with changing contexts. We found that greater racket-tailed drongos (Dicrurus paradiseus) in the rainforest of Sri Lanka mimic the calls of predators and the alarm-associated calls of other species more often than would be expected from the frequency of these sounds in the acoustic environment. Drongos include this alarm-associated mimicry in their own alarm vocalizations, while incorporating other species' songs and contact calls in their own songs. Drongos show an additional level of context specificity by mimicking other species' ground predator-specific call types when mobbing. We suggest that drongos learn other species' calls and their contexts while interacting with these species in mixed flocks. The drongos' behaviour demonstrates that alarm-associated calls can have learned components, and that birds can learn the appropriate usage of calls that encode different types of information.     

Variation in the hematocrit of a passerine bird across life stages is mainly of environmental origin

The heritability of the hematocrit in adult, breeding pied flycatchers Ficedula hypoleuca is examined in a southern European population across seven years to see the consistency, or lack thereof, of patterns found with the trait at fledgling age where no significant heritability could be detected. While the across-years repeatability of the trait in adult, breeding birds was low but significant, heritabilities based on adult parent-adult offspring regressions controlling for assortative mating and full-sibling comparisons did not differ significantly from zero. Neither were heritability estimates affected by selection on fledgling hematocrit, as it was unrelated to local recruitment. There was no relationship between fledgling and adult hematocrit, suggesting that both behave as phenotypically plastic, different traits. This is the first study testing for the heritability of a physiological trait in birds with data from adult, free-ranging individuals.     

Antioxidant defenses predict long-term survival in a passerine bird

Background

Normal and pathological processes entail the production of oxidative substances that can damage biological molecules and harm physiological functions. Organisms have evolved complex mechanisms of antioxidant defense, and any imbalance between oxidative challenge and antioxidant protection can depress fitness components and accelerate senescence. While the role of oxidative stress in pathogenesis and aging has been studied intensively in humans and model animal species under laboratory conditions, there is a dearth of knowledge on its role in shaping life-histories of animals under natural selection regimes. Yet, given the pervasive nature and likely fitness consequences of oxidative damage, it can be expected that the need to secure efficient antioxidant protection is powerful in molding the evolutionary ecology of animals. Here, we test whether overall antioxidant defense varies with age and predicts long-term survival, using a wild population of a migratory passerine bird, the barn swallow (Hirundo rustica), as a model.

Methodology/Principal Findings

Plasma antioxidant capacity (AOC) of breeding individuals was measured using standard protocols and annual survival was monitored over five years (2006–2010) on a large sample of selection episodes. AOC did not covary with age in longitudinal analyses after discounting the effect of selection. AOC positively predicted annual survival independently of sex. Individuals were highly consistent in their relative levels of AOC, implying the existence of additive genetic variance and/or environmental (including early maternal) components consistently acting through their lives.

Conclusions

Using longitudinal data we showed that high levels of antioxidant protection positively predict long-term survival in a wild animal population. Present results are therefore novel in disclosing a role for antioxidant protection in determining survival under natural conditions, strongly demanding for more longitudinal eco-physiological studies of life-histories in relation to oxidative stress in wild populations.     

Exploring the genetics of aging in a wild passerine bird

Senescence is the decline in survival and reproduction as an organism ages and is known to occur in collared flycatchers Ficedula albicollis. We consider annual fitness (the estimated genetic contribution that an individual makes to next year's gene pool) as a measure of age-specific fitness. We apply a restricted maximum likelihood linear mixed-model approach on 25 years of data on 3,844 male and 4,992 female collared flycatchers. Annual fitness had a significant additive genetic component (h2 of about 4%). Annual fitness declined at later ages in both sexes. Using a random regression animal model, we show that the observed age-related phenotypic changes in annual fitness were not present on the additive genetic level, contrary to predictions of genetic hypotheses of senescence. Our study suggests that patterns of aging in the wild need to be interpreted with caution in terms of underlying genetics because they may be largely determined by environmental processes.     

Egg rejection in a passerine bird: size does matter

Avian brood parasites reduce the reproductive success of their hosts, selecting for the evolution of egg discrimination by the host, and potentially creating a coevolutionary arms race between host and parasite. Host egg discrimination ability is crucial in determining whether the arms race results in extinction (of the parasite on a particular host) or stable coevolutionary equilibrium of the host-parasite pair. I examined egg discrimination behaviour in the yellow-browed leaf warbler, Phylloscopus humei, a presumed former host of parasitic cuckoos, to show how discrimination ability has become very strong. Field experiments using model eggs demonstrate that rejection decisions are based on the relative size of eggs in the clutch. Individuals do not learn the particular size of their own eggs, but will accept both large and small eggs as long as all eggs in the clutch are of similar size. Host rejection decisions are continuously modified based on assessment of variation in egg sizes currently in the clutch, making it a difficult strategy for a cuckoo to defeat. Copyright 2000 The Association for the Study of Animal Behaviour.     

Linkage mapping reveals sex-dimorphic map distances in a passerine bird

Linkage maps are lacking for many highly influential model organisms in evolutionary research, including all passerine birds. Consequently, their full potential as research models is severely hampered. Here, we provide a partial linkage map and give novel estimates of sex-specific recombination rates in a passerine bird, the great reed warbler (Acrocephalus arundinaceus). Linkage analysis of genotypic data at 51 autosomal microsatellites and seven markers on the Z-chromosome (one of the sex chromosomes) from an extended pedigree resulted in 12 linkage groups with 2-8 loci. A striking feature of the map was the pronounced sex-dimorphism: males had a substantially lower recombination rate than females, which resulted in a suppressed autosomal map in males (sum of linkage groups: 110.2 cM) compared to females (237.2 cM; female/male map ratio: 2.15). The sex-specific recombination rates will facilitate the building of a denser linkage map and cast light on hypotheses about sex-specific recombination rates.     

Olfactory conditioning experiments in a food-searching passerine bird in semi-natural conditions

Because passerine birds have a very small relative olfactory bulb size, they have been considered to have weak olfactory capacities for decades. Recent investigations however suggest that breeding female blue tits (Parus caeruleus) are sensitive to lavender odour in the reproductive context of building and maintaining the nest. Here, we present results of an olfactory conditioning experiment in blue tits held in semi-natural conditions during the breeding season. We show that captive male blue tits, trained to associate lavender odour with a food reward, are more attracted to an empty feeder box emitting lavender odour than an odourless empty feeder box. Females did not distinguish significantly between empty feeders with and without lavender odour during the test phase, although they responded positively at the end of the training phase. These results suggest that male blue tits can use olfaction in a context not related to nest building. Additional experiments will be required to better understand the observed sex differences in response to the experimental set up, and in what context free-ranging individuals use olfaction.     

Maladaptive habitat selection of a migratory passerine bird in a human-modified landscape

In human-altered environments, organisms may preferentially settle in poor-quality habitats where fitness returns are lower relative to available higher-quality habitats. Such ecological trapping is due to a mismatch between the cues used during habitat selection and the habitat quality. Maladaptive settlement decisions may occur when organisms are time-constrained and have to rapidly evaluate habitat quality based on incomplete knowledge of the resources and conditions that will be available later in the season. During a three-year study, we examined settlement decision-making in the long-distance migratory, open-habitat bird, the Red-backed shrike (Lanius collurio), as a response to recent land-use changes. In Northwest Europe, the shrikes typically breed in open areas under a management regime of extensive farming. In recent decades, Spruce forests have been increasingly managed with large-size cutblocks in even-aged plantations, thereby producing early-successional vegetation areas that are also colonised by the species. Farmland and open areas in forests create mosaics of two different types of habitats that are now occupied by the shrikes. We examined redundant measures of habitat preference (order of settlement after migration and distribution of dominant individuals) and several reproductive performance parameters in both habitat types to investigate whether habitat preference is in line with habitat quality. Territorial males exhibited a clear preference for the recently created open areas in forests with higher-quality males settling in this habitat type earlier. Reproductive performance was, however, higher in farmland, with higher nest success, offspring quantity, and quality compared to open areas in forests. The results showed strong among-year consistency and we can therefore exclude a transient situation. This study demonstrates a case of maladaptive habitat selection in a farmland bird expanding its breeding range to human-created open habitats in plantations. We discuss the reasons that could explain this decision-making and the possible consequences for the population dynamics and persistence.     

Feather micro-organisms and uropygial antimicrobial defences in a colonial passerine bird

1.  The relationship between the composition of communities of micro-organisms and their hosts remains poorly understood. We conducted extensive field studies of feather-degrading bacteria, other cultivable bacteria, and fungi on the plumage of a migratory bird, the barn swallow Hirundo rustica Linnaeus, to understand the association between micro-organisms, host sociality and host antimicrobial defences, as reflected by the size of the uropygial gland.
2.  The abundance of feather-degrading bacteria, but not other cultivable bacteria or fungi, decreased with increasing size of the uropygial gland.
3.  Females had more feather-degrading bacteria than males.
4.  Barn swallows living in larger colonies had more feather-degrading bacteria than less social conspecifics.
5.  These findings suggest that the uropygial gland plays a specific role in regulating the abundance of feather-degrading bacteria that furthermore depends on the social environment of the host.     

Environmental mismatch results in emergence of cooperative behavior in a passerine bird

A major problem in the evolution of maternal effects is explaining the origin and persistence of maternally induced phenotypes that lower offspring fitness. Recent work focuses on the relative importance of maternal and offspring selective environments and the mismatch between them. However, an alternative approach is to directly study the origin and performance of offspring phenotypes resulting from mismatch. Here, we capitalize on a detailed understanding of the ecological contexts that provide both the cue and the functional context for expression of maternally induced offspring phenotypes to investigate the consequences of environmental mismatch. In western bluebirds, adaptive integration of offspring dispersal and aggression is induced by maternal competition over nest cavities. When nest cavities are locally abundant, mothers produce nonaggressive offspring that remain in their natal population, and when nest cavities are scarce, mothers produce aggressive dispersers. However, a few offspring neither disperse nor breed locally, instead helping at their parent’s nest, and as a result these offspring have unusually low fitness. Here, we investigate whether females produce helpers to increase their own fitness, or whether helpers result from a mismatch between the cues mothers experience during offspring production and the breeding environment that helpers later encounter. We found that producing helpers does not enhance maternal fitness. Instead, we show that helpers, which were the least aggressive of all returning sons in the population, were most common when population density increased from the time sons were produced to the time of their reproductive maturity, suggesting that the helper phenotype emerges when cues of resource competition during offspring development do not match the actual level of competition that offspring experience. Thus, environmental mismatch might explain the puzzling persistence of maternally induced phenotypes that decrease offspring fitness.     

Pairing context determines condition-dependence of song rate in a monogamous passerine bird

Condition-dependence of male ornaments is thought to provide honest signals on which females can base their sexual choice for genetic quality. Recent studies show that condition-dependence patterns can vary within populations. Although long-term association is thought to promote honest signalling, no study has explored the influence of pairing context on the condition-dependence of male ornaments. In this study, we assessed the influence of natural variation in body condition on song rate in zebra finches (Taeniopygia guttata) in three different situations: during short and long encounters with an unfamiliar female, and within heterosexual mated pairs. We found consistent individual differences in male directed and undirected song rate. Moreover, body condition had a positive effect on song rate in paired males. However, male song rate was not influenced by body condition during short or long encounters with unfamiliar females. Song rate appears to be an unreliable signal of condition to prospective females as even poor-condition birds can cheat and sing at a high rate. By contrast, paired females can reliably use song rate to assess their mate''s body condition, and possibly the genetic quality. We propose that species'' characteristics, such as mating system, should be systematically taken into account to generate relevant hypotheses about the evolution of condition-dependent male ornaments.     

Geographical variation in egg mass and egg content in a passerine bird

Reproductive, phenotypic and life-history traits in many animal and plant taxa show geographic variation, indicating spatial variation in selection regimes. Maternal deposition to avian eggs, such as hormones, antibodies and antioxidants, critically affect development of the offspring, with long-lasting effects on the phenotype and fitness. Little is however known about large-scale geographical patterns of variation in maternal deposition to eggs. We studied geographical variation in egg components of a passerine bird, the pied flycatcher (Ficedula hypoleuca), by collecting samples from 16 populations and measuring egg and yolk mass, albumen lysozyme activity, yolk immunoglobulins, yolk androgens and yolk total carotenoids. We found significant variation among populations in most egg components, but ca. 90% of the variation was among individuals within populations. Population however explained 40% of the variation in carotenoid levels. In contrast to our hypothesis, we found geographical trends only in carotenoids, but not in any of the other egg components. Our results thus suggest high within-population variation and leave little scope for local adaptation and genetic differentiation in deposition of different egg components. The role of these maternally-derived resources in evolutionary change should be further investigated.     

Maternal corticosteroids influence primary offspring sex ratio in a free-ranging passerine bird

When fitness benefits of investment in sons and daughters differ,animals are predicted to manipulate the sex ratio of their offspring.Sex ratio manipulation occurs in many taxa, but the mechanismsunderlying the phenomenon in vertebrates remain largely unknown.Factors favoring skewed sex ratios, such as reduced maternalcondition or food availability, also induce elevated corticosteroids.Recent experimental studies support a causal relationship betweencorticosteroids and sex ratio. Evidence of a natural correlationbetween maternal corticosteroids and offspring sex ratio hasbeen lacking, however. Without such evidence, the importanceof corticosteroids in influencing sex ratios in natural populationswas unknown. We measured baseline corticosteroids in 19 free-rangingfemale white-crowned sparrows (Zonotrichia leucophrys) and thesex ratios of their offspring. Females with high corticosteroidsproduced more daughters than females with low hormone levels.We then conducted a controlled, field-based experiment investigatingthe effects of moderately increased maternal corticosteroidson offspring sex ratios to determine if the observed correlationreflects a causal relationship between maternal corticosteroidsand offspring sex ratio. Hormone-implanted females producedmore female embryos than control females. These findings providethe first evidence of a natural correlation between maternalcorticosteroids and offspring sex ratios in free-ranging birds,and the first experimental evidence of a causal link betweenmoderate increases in corticosteroids and biased primary sexratios.