Host space, not energy or symbiont size, constrains feather mite abundance across passerine bird species.

Comprehending symbiont abundance among host species is a major ecological endeavour, and the metabolic theory of ecology has been proposed to understand what constrains symbiont populations. We parameterized metabolic theory equations to investigate how bird species' body size and the body size of their feather mites relate to mite abundance according to four potential energy (uropygial gland size) and space constraints (wing area, total length of barbs and number of feather barbs). Predictions were compared with the empirical scaling of feather mite abundance across 106 passerine bird species (26,604 individual birds sampled), using phylogenetic modelling and quantile regression. Feather mite abundance was strongly constrained by host space (number of feather barbs) but not by energy. Moreover, feather mite species' body size was unrelated to the body size of their host species. We discuss the implications of our results for our understanding of the bird-feather mite system and for symbiont abundance in general.

To Flee or Not to Flee: How Age, Reproductive Phase, and Mate Presence Affect White Stork Flight Decisions.

Recognizing, assessing, and responding to threats is critical for survival in the wild. Birds, especially in their role as parents, must decide whether to flee or delay flight when threatened. This study examines how age, reproductive stage, and the presence of a mate influence flight initiation distance (FID) and nest recess duration in white storks. Analyzing the data with a generalized additive mixed model (GAMM), we found significant correlations between FID and age, reproductive stage, and presence of a mate. These results suggest that the trade-off between current and future reproduction shifts during critical breeding periods, such as incubation and nestling care. To increase breeding success, White Storks appear willing to take risks and extend their stay in the nest when offspring are most valuable and vulnerable. In the presence of a mate, individuals leave the nest earlier, suggesting possible sexual conflict over parental care. The duration of nest abandonment is consistent with FID, except for age. These results illustrate how parental age, brood value, vulnerability, and sexual dynamics influence white stork flight decisions in complex ways. Understanding these dynamics enriches our knowledge of bird behavior and adaptations to environmental challenges and highlights the complexity of parental decision making.

A chromosome-level reference genome and pangenome for barn swallow population genomics.

Insights into the evolution of non-model organisms are limited by the lack of reference genomes of high accuracy, completeness, and contiguity. Here, we present a chromosome-level, karyotype-validated reference genome and pangenome for the barn swallow (Hirundo rustica). We complement these resources with a reference-free multialignment of the reference genome with other bird genomes and with the most comprehensive catalog of genetic markers for the barn swallow. We identify potentially conserved and accelerated genes using the multialignment and estimate genome-wide linkage disequilibrium using the catalog. We use the pangenome to infer core and accessory genes and to detect variants using it as a reference. Overall, these resources will foster population genomics studies in the barn swallow, enable detection of candidate genes in comparative genomics studies, and help reduce bias toward a single reference genome.

Annual egg productivity predicts female-biased mortality in avian species.

Among avian species, the differential cost entailed by either sex in competition for mates has been regarded as the main evolutionary influence on sex differences in mortality rates. However, empirical evidence suggests that sex-biased adult mortality is mainly related to differential energy investment in gamete production, with a greater annual mass devoted to egg production leading to higher female mortality. We explicitly tested the generality of this pattern in a comparative framework. Annual egg production can be relatively large in some species (up to 200% of female body mass) and annual mortality is generally biased toward females. We showed that greater annual egg productivity resulted in higher mortality rates of females relative to males. Mating system was secondarily important, with species in which males were more involved in mating competition having more equal mortality rates between the sexes. However, both traits explained only a limited fraction of the interspecific variation in female-biased mortality. Other traits, such as sexual size dimorphism and parental care, had much weaker influences on female-biased mortality. Our results suggest that both annual mass devoted to gamete production by females and mating system contribute to the evolution of the fundamental life-history trade-off between reproduction and survival in avian taxa.

Interpretation of gut microbiota data in the 'eye of the beholder': A commentary and re-evaluation of data from 'Impacts of radiation exposure on the bacterial and fungal microbiome of small mammals in the Chernobyl Exclusion Zone'.

Evidence that exposure to environmental pollutants can alter the gut microbiota composition of wildlife includes studies of rodents exposed to radionuclides. Antwis et al. (2021) used amplicon sequencing to characterise the gut microbiota of four species of rodent (Myodes glareolus, Apodemus agrarius, A. flavicollis and A. sylvaticus) inhabiting the Chernobyl Exclusion Zone (CEZ) to examine possible changes in gut bacteria (microbiota) and gut fungi (mycobiota) associated with exposure to radionuclides and whether the sample type (from caecum or faeces) affected the analysis. The conclusions derived from the analyses of gut mycobiota are based on data that represent a mixture of ingested fungi (e.g. edible macrofungi, polypores, lichens and ectomycorrhizae) and gut mycobiota (e.g. microfungi and yeasts), which mask the patterns of inter- and intraspecific variation in the authentic gut mycobiota. Implying that 'faecal samples are not an accurate indicator of gut composition' creates an unnecessary controversy about faecal sampling because the comparison of samples from the caecum and faeces confounds many other possible drivers (including different animals from different locations, sampled in different years) of variation in gut microbiota. It is relevant also that Antwis et al.'s (2021) data lack statistical power to detect an effect of exposure to radionuclides on the gut microbiota because (1) all of their samples of Apodemus mice had experienced a medium or high total absorbed dose rate and (2) they did not collect samples of bank voles (M. glareolus) from replicate contaminated and uncontaminated locations. Discussion of Antwis et al.'s (2021) analysis, especially the claims presented in the Abstract, is important to prevent controversy about the outcome of research on the biological impacts of wildlife inhabiting the CEZ.

Sparrows use a medicinal herb to defend against parasites and increase offspring condition.

The incorporation of aromatic plants into nests by birds is suspected to constitute an example of preventative medicine use, whereby the phytochemical compounds within plants reduce infestation by parasites and increase offspring condition [1,2]. In China, russet sparrows (Passer cinnamomeus) incorporate wormwood (Artemisia verlotorum) leaves into their nests around the same time that local people hang wormwood from their doors as a traditional custom during the Dragon Boat Festival. The belief that this behaviour confers protection against ill health [3] is supported by the description of anti-parasite compounds in wormwood [4]. It has been suggested that the incorporation of fresh wormwood leaves into nests may serve a similar function for sparrows. Here we show that sparrows choose nest location and resupply established nests with fresh wormwood leaves using olfactory cues, that nests containing wormwood leaves have lower ectoparasite loads, and that nests with more wormwood leaves produce heavier chicks. Our results indicate that sparrows use wormwood as a preventative medicine to control ectoparasites and improve the body mass of their offspring.

Anther-smut fungi from more contaminated sites in Chernobyl show lower infection ability and lower viability following experimental irradiation.

The long-term contamination that followed the nuclear disaster at Chernobyl provides a case study for the effects of chronic ionizing radiation on living organisms and on their ability to tolerate or evolve resistance to such radiation. Previously, we studied the fertility and viability of early developmental stages of a castrating plant pathogen, the anther-smut fungus Microbotryum lychnidis-dioicae, isolated from field sites varying over 700-fold in degree of radioactive contamination. Neither the budding rate of haploid spores following meiosis nor the karyotype structure varied with increasing radiation levels at sampling sites. Here, we assessed the ability of the same M. lychnidis-dioicae strains to perform their whole life cycle, up to the production of symptoms in the plants, that is, the development of anthers full of fungal spores; we also assessed their viability under experimental radiation. Fungal strains from more contaminated sites had no lower spore numbers in anthers or viability, but infected host plants less well, indicating lower overall fitness due to radioactivity exposure. These findings improve our understanding of the previous field data, in which the anther-smut disease prevalence on Silene latifolia plants caused by M. lychnidis-dioicae was lower at more contaminated sites. Although the fungus showed relatively high resistance to experimental radiation, we found no evidence that increased resistance to radiation has evolved in populations from contaminated sites. Fungal strains from more contaminated sites even tolerated or repaired damage from a brief acute exposure to γ radiation less well than those from non- or less contaminated sites. Our results more generally concur with previous studies in showing that the fitness of living organisms is affected by radiation after nuclear disasters, but that they do not rapidly evolve higher tolerance.

Sex in the city: sexual selection and urban colonization in passerines.

Urbanization leads to a rapid and drastic transformation of habitats, forcing native fauna to manage novel ecological challenges or to move. Sexual selection is a powerful evolutionary force, which is sometimes predicted to enhance the ability of species to adapt to novel environments because it allows females to choose high-quality males, but other times is predicted to reduce the viability of populations because it pushes males beyond naturally selected optima. However, we do not know whether or how sexual selection contributes to the likelihood that animals will establish in urban areas. We use a comparative analysis of passerine birds to test whether traits associated with pre- and post-mating sexual selection predict successful colonization of urban areas. We found that plumage dichromatism was negatively associated with urban tolerance, but found no relationship with sexual size dimorphism or testes mass relative to body mass. While we cannot determine the exact reason why species with high plumage dichromatism occur less in cities, it is likely that urban areas increase the costs of expressing bright coloration due, for instance, to dietary constraints, limited male parental care or increased predation.

Annual variation in predation risk is related to the direction of selection for brain size in the wild.

The direction of predator-mediated selection on brain size is debated. However, the speed and the accuracy of performing a task cannot be simultaneously maximized. Large-brained individuals may be predisposed to accurate but slow decision-making, beneficial under high predation risk, but costly under low risk. This creates the possibility of temporally fluctuating selection on brain size depending on overall predation risk. We test this idea in nesting wild eider females (Somateria mollissima), in which head volume is tightly linked to brain mass (r2 = 0.73). We determined how female relative head volume relates to survival, and characterized the seasonal timing of predation. Previous work suggests that relatively large-brained and small-brained females make slow versus fast nest-site decisions, respectively, and that predation events occur seasonally earlier when predation is severe. Large-brained, late-breeding females may therefore have higher survival during high-predation years, but lower survival during safe years, assuming that predation disproportionately affects late breeders in such years. Relatively large-headed females outsurvived smaller-headed females during dangerous years, whereas the opposite was true in safer years. Predation events occurred relatively later during safe years. Fluctuations in the direction of survival selection on relative brain size may therefore arise due to brain-size dependent breeding phenology.

Pheomelanin synthesis varies with protein food abundance in developing goshawks.

The accumulation of the amino acid cysteine in lysosomes produces toxic substances, which are avoided by a gene (CTNS) coding for a transporter that pumps cystine out of lysosomes. Melanosomes are lysosome-related organelles that synthesize melanins, the most widespread pigments in animals. The synthesis of the orange melanin, termed pheomelanin, depends on cysteine levels because the sulfhydryl group is used to form the pigment. Pheomelanin synthesis may, therefore, be affected by cysteine homeostasis, although this has never been explored in a natural system. As diet is an important source of cysteine, here we indirectly tested for such an effect by searching for an association between food abundance and pheomelanin content of feathers in a wild population of Northern goshawk Accipiter gentilis. As predicted on the basis that CTNS expression may inhibit pheomelanin synthesis and increase with food abundance as previously found in other strictly carnivorous birds, we found that the feather pheomelanin content in nestling goshawks, but not in adults, decreased as the abundance of prey available to them increased. In contrast, variation in the feather content of the non-sulphurated melanin form (eumelanin) was only explained by sex in both nestlings and adults. We also found that the feather pheomelanin content of nestlings was negatively related to that of their mothers, suggesting a relevant environmental influence on pheomelanin synthesis. Overall, our findings suggest that variation in pheomelanin synthesis may be a side effect of the maintenance of cysteine homeostasis. This may help explaining variability in the expression of pigmented phenotypes.

Egg retrieval versus egg rejection in cuckoo hosts.

Before complex nests evolved, birds laid eggs on the ground, and egg retrieval evolved as an adaptation against accidental displacement of eggs outside the nest. Therefore, egg retrieval is an ancient, and likely ancestral, widespread behaviour in birds. However, it has received little attention in studies of avian brood parasitism, perhaps because most parasitism occurs in species with complex nests, a context in which egg retrieval seems irrelevant. However, for cavity-nesting hosts of avian brood parasites, egg retrieval may still play an important role in the coevolutionary interactions between obligate brood parasites and hosts, because egg retrieval can be considered to be antagonistic to egg rejection behaviour in hosts, yet both may involve cognition to recognize eggs. We hypothesized that (1) cavity-nesting hosts should retrieve misplaced eggs from outside the nest cup, (2) brood parasitism has modulated egg retrieval behaviour in cavity-nesting hosts and (3) hosts use the same visual cues for decision-making during egg recognition in both egg retrieval and egg rejection actions. To test these hypotheses, we performed a series of experiments in a cavity-nesting host, the green-backed tit ( Parus monticolus). Foreign eggs with different levels of mimicry were placed within or outside nest cups of hosts to test their responses. We found that host decisions about whether to retrieve or reject an egg both depended on the degree of mimicry. However, hosts sometimes first retrieved poorly mimetic foreign eggs and then rejected them. Alternatively, hosts sometimes failed to retrieve highly mimetic conspecific eggs. We suggest that egg retrieval in hosts is likely to be a result of the interaction between ancient retrieval behaviour and subsequent adaptation against brood parasitism. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

Components of variation in female common cuckoo calls.

Investigations on bird vocalizations have largely focused on males. Female vocalizations are widespread in birds but few studies have investigated female vocal characteristics, particularly in non-Passeriformes. In this study, we use new field recordings from China, and calls available from an online sound library to examine temporal patterns, call consistency and geographical variation in vocalizations of female common cuckoos Cuculus canorous. The peak in vocal activity (both male and female) was in the morning, which contrasts to what would be predicted if the sole function of the female call was to distract the attention of hosts after parasitizing a host's nest in the afternoon. Both male and female common cuckoos were more vocally active in sunny weather, than rainy weather. We also found larger intra-individual variation in female rather than in male calls, which may benefit female cuckoos by increasing stimulation to host species. Peak frequency of female calls decreased with increased latitude, while differences in female call features were not associated with geographic distance. In summary, our findings that female calls are used in the morning, rather than at peak egg laying, yet are highly variable and show little geographic patterns suggest that the function of these female calls may be more variable and intricate than previously thought. However, because research on female vocalizations is underrepresented, future studies are still needed.

Environmental radiation alters the gut microbiome of the bank vole Myodes glareolus.

Gut microbiota composition depends on many factors, although the impact of environmental pollution is largely unknown. We used amplicon sequencing of bacterial 16S rRNA genes to quantify whether anthropogenic radionuclides at Chernobyl (Ukraine) impact the gut microbiome of the bank vole Myodes glareolus. Exposure to elevated levels of environmental radionuclides had no detectable effect on the gut community richness but was associated with an almost two-fold increase in the Firmicutes:Bacteroidetes ratio. Animals inhabiting uncontaminated areas had remarkably similar gut communities irrespective of their proximity to the nuclear power plant. Hence, samples could be classified to high-radiation or low-radiation sites based solely on microbial community with >90% accuracy. Radiation-associated bacteria had distinct inferred functional profiles, including pathways involved in degradation, assimilation and transport of carbohydrates, xenobiotics biodegradation, and DNA repair. Our results suggest that exposure to environmental radionuclides significantly alters vertebrate gut microbiota.

Dispersal capacity explains the evolution of lifespan variability.

The evolutionary explanation for lifespan variation is still based on the antagonistic pleiotropy hypothesis, which has been challenged by several studies. Alternative models assume the existence of genes that favor aging and group benefits at the expense of reductions in individual lifespans. Here we propose a new model without making such assumptions. It considers that limited dispersal can generate, through reduced gene flow, spatial segregation of individual organisms according to lifespan. Individuals from subpopulations with shorter lifespan could thus resist collapse in a growing population better than individuals from subpopulations with longer lifespan, hence reducing lifespan variability within species. As species that disperse less may form more homogeneous subpopulations regarding lifespan, this may lead to a greater capacity to maximize lifespan that generates viable subpopulations, therefore creating negative associations between dispersal capacity and lifespan across species. We tested our model with individual-based simulations and a comparative study using empirical data of maximum lifespan and natal dispersal distance in 26 species of birds, controlling for the effects of genetic variability, body size, and phylogeny. Simulations resulted in maximum lifespans arising from lowest dispersal probabilities, and comparative analyses resulted in a negative association between lifespan and natal dispersal distance, thus consistent with our model. Our findings therefore suggest that the evolution of lifespan variability is the result of the ecological process of dispersal.

Faster Development Covaries with Higher DNA Damage in Grasshoppers (Chorthippus albomarginatus) from Chernobyl.

In Chernobyl, chronic exposure to radioactive contaminants has a variety of deleterious effects on exposed organisms, including genetic damage and mutation accumulation. However, the potential for such effects to be transmitted to the next generation is poorly understood. We captured lesser marsh grasshoppers (Chorthippus albomarginatus) in the Chernobyl Exclusion Zone from sites varying in levels of environmental radiation by more than three orders of magnitude. We then raised their offspring in a common garden experiment in order to assess the effects of parental exposure to radiation on offspring development and DNA damage. Offspring that reached maturity at a younger age had higher levels of DNA damage. Contrary to our hypothesis, parental exposure to radioactive contamination did not affect DNA damage in their offspring possibly because of intervening adaptation or parental compensatory mechanisms. Our results suggest a trade-off between developmental rate and resistance to DNA damage, whereby offspring developing at faster rates do so at the cost of damaging their DNA. This result is consistent with and extends findings in other species, suggesting that faster growth rates cause increased oxidative damage and stress. We propose that growth rates are subject to stabilizing selection balancing the benefits of fast development and the competing need of buffering its damaging effects to macromolecules and tissues.

Environmental conditions during winter predict age- and sex-specific differences in reproductive success of a trans-Saharan migratory bird.

Previous studies have linked winter habitat with subsequent breeding phenology and physical condition of migratory birds, but few have found delayed effects of winter habitat on subsequent reproductive success. The aim of this study was to test if African winter habitat is related to subsequent reproductive success of house martins (Delichon urbicum) breeding at a colony in Spain. We measured stable isotope (δ2H, δ13C, δ15N) values from feathers moulted in West Africa and used confirmatory path analysis to test if isotopic values of winter-grown feathers were related to reproductive success through the mediation of breeding phenology and body condition. We conducted separate analyses for males, females and age classes (yearlings vs ≥ 2 years old). Experienced males wintering in habitats of higher rainfall (as inferred from lower feather δ2H values) were in better body condition and produced more offspring during the subsequent breeding season. In contrast, we did not find any effect of winter habitat on reproductive success of young males or females. These findings provide evidence consistent with a complex causal link between winter habitat quality and subsequent breeding success of long-distance migratory songbirds.

The role of the mating system and intraspecific brood parasitism in the costs of reproduction in a passerine bird.

Limited resources trigger trade-offs in resource allocation. Reproduction is one of the most demanding activities in terms of energy, and costs related to reproduction can be apparent either as reduced future reproduction or as survival. However, costs are not always detected, because individual heterogeneity in quality and resource acquisition may explain variation in costs among individuals. We conducted a comprehensive study in spotless starlings (Sturnus unicolor) nesting in Central Spain to determine whether costs of reproduction could be detectable in the short and/or long term and whether prenatal or postnatal investment were driving these costs. We took into account the life history of the species, where egg volume is highly repeatable, males are facultatively polygynous, and intraspecific brood parasitism occurs. Females with a high reproductive effort in a breeding event also had a high reproductive effort in the second event of the season. The mating system and maternal age were reliable predictors of breeding success within a breeding event: monogamous and primary females, as well as older mothers, raised more nestlings than secondary females and 1-year-old females, respectively. However, when high-investing females suffered intra-brood parasitism in 1 year, we found a negative correlation between current and future reproduction. These results suggest that, under some circumstances, females are able to skip the short-term costs of reproduction, but when extra effort is added, trade-offs arise. While most studies have focused on different aspects of individual quality on costs, the ecological context seems to represent an important component that should be taken into account.

Capacity of blood plasma is higher in birds breeding in radioactively contaminated areas.

BACKGROUND: Environmental pollution in general, and radioactive contamination in particular, may deeply affect host-parasite relationships and their consequences for the evolution of organisms. The nuclear accident that occurred more than 30 years ago in Chernobyl resulted in significant changes in diversity and richness of microbial communities that could influence characteristics of animal-bacteria interactions, including host immune responses and competitive interference by bacteria. Given the high mortality rate of birds breeding in radioactively contaminated zones, those with stronger defences against infections should experience significant fitness advantages. METHODOLOGY/PRINCIPAL FINDINGS: Here we characterized antimicrobial capacity of barn swallows (Hirundo rustica) from different Ukrainian populations (subject to a gradient of ionizing radiation) against 12 bacterial species. We also quantified constitutive innate immunity, which is the non-specific first barrier of protection of hosts against microbial parasites. We found a positive association between specific antimicrobial capacity of individual hosts and radiation levels in breeding habitats even after controlling for other confounding variables such as sex and age. However, no significant relationship was found between immunocompetence (non-specific response) and background radiation. CONCLUSIONS/SIGNIFICANCE: These results suggest that radiation selects for broad antimicrobial spectra of barn swallows, although not for all bacterial strains. We discuss these results in the framework of host-parasite evolution under extreme environmental conditions.