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.

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.

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.

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.

Lower prevalence but similar fitness in a parasitic fungus at higher radiation levels near Chernobyl.

Nuclear disasters at Chernobyl and Fukushima provide examples of effects of acute ionizing radiation on mutations that can affect the fitness and distribution of species. Here, we investigated the prevalence of Microbotryum lychnidis-dioicae, a pollinator-transmitted fungal pathogen of plants causing anther-smut disease in Chernobyl, its viability, fertility and karyotype variation, and the accumulation of nonsynonymous mutations in its genome. We collected diseased flowers of Silene latifolia from locations ranging by more than two orders of magnitude in background radiation, from 0.05 to 21.03 µGy/h. Disease prevalence decreased significantly with increasing radiation level, possibly due to lower pollinator abundance and altered pollinator behaviour. Viability and fertility, measured as the budding rate of haploid sporidia following meiosis from the diploid teliospores, did not vary with increasing radiation levels and neither did karyotype overall structure and level of chromosomal size heterozygosity. We sequenced the genomes of twelve samples from Chernobyl and of four samples collected from uncontaminated areas and analysed alignments of 6068 predicted genes, corresponding to 1.04 × 10(7)  base pairs. We found no dose-dependent differences in substitution rates (neither dN, dS, nor dN/dS). Thus, we found no significant evidence of increased deleterious mutation rates at higher levels of background radiation in this plant pathogen. We even found lower levels of nonsynonymous substitution rates in contaminated areas compared to control regions, suggesting that purifying selection was stronger in contaminated than uncontaminated areas. We briefly discuss the possibilities for a mechanistic basis of radio resistance in this nonmelanized fungus.

Climatic conditions cause complex patterns of covariation between demographic traits in a long-lived raptor.

Environmental variation can induce life-history changes that can last over a large part of the lifetime of an organism. If multiple demographic traits are affected, expected changes in climate may influence environmental covariances among traits in a complex manner. Thus, examining the consequences of environmental fluctuations requires that individual information at multiple life stages is available, which is particularly challenging in long-lived species. Here, we analyse how variation in climatic conditions occurring in the year of hatching of female goshawks Accipiter gentilis (L.) affects age-specific variation in demographic traits and lifetime reproductive success (LRS). LRS decreased with increasing temperature in April in the year of hatching, due to lower breeding frequency and shorter reproductive life span. In contrast, the probability for a female to successfully breed was higher in years with a warm April, but lower LRS of the offspring in these years generated a negative covariance among fecundity rates among generations. The mechanism by which climatic conditions generated cohort effects was likely through influencing the quality of the breeding segment of the population in a given year, as the proportion of pigeons in the diet during the breeding period was positively related to annual and LRS, and the diet of adult females that hatched in warm years contained fewer pigeons. Climatic conditions experienced during different stages of individual life histories caused complex patterns of environmental covariance among demographic traits even across generations. Such environmental covariances may either buffer or amplify impacts of climate change on population growth, emphasizing the importance of considering demographic changes during the complete life history of individuals when predicting the effect of climatic change on population dynamics of long-lived species.

Do malaria parasites manipulate the escape behaviour of their avian hosts? An experimental study.

Escape behaviour is the behaviour that birds and other animals display when already caught by a predator. An individual exhibiting higher intensity of such anti-predator behaviour could have greater probabilities of escape from predators. Parasites are known to affect different aspects of host behaviour to increase their own fitness. Vector-transmitted parasites such as malaria parasites should gain by manipulating their hosts to enhance the probability of transmission. Several studies have shown that malaria parasites can manipulate their vectors leading to increased transmission success. However, little is known about whether malaria parasites can manipulate escape behaviour of their avian hosts thereby increasing the spread of the parasite. Here we used an experimental approach to explore if Plasmodium relictum can manipulate the escape behaviour of one of its most common avian hosts, the house sparrow Passer domesticus. We experimentally tested whether malaria parasites manipulate the escape behaviour of their avian host. We showed a decrease in the intensity of biting and tonic immobility after removal of infection with anti-malaria medication compared to pre-experimental behaviour. These outcomes suggest that infected sparrows performed more intense escape behaviour, which would increase the likelihood of individuals escaping from predators, but also benefit the parasite by increasing its transmission opportunities.

Changes in breeding phenology and population size of birds.

Although the phenology of numerous organisms has advanced significantly in response to recent climate change, the life-history and population consequences of earlier reproduction remain poorly understood. We analysed extensive data on temporal change in laying date and clutch size of birds from Europe and North America to test whether these changes were related to recent trends in population size. Across studies, laying date advanced significantly, while clutch size did not change. However, within populations, changes in laying date and clutch size were positively correlated, implying that species which advanced their laying date the most were also those that increased their clutch size the most. Greater advances in laying date were associated with species that had multiple broods per season, lived in nonagricultural habitats and were herbivorous or predatory. The duration of the breeding season increased for multibrooded species and decreased for single-brooded species. Changes in laying date and clutch size were not related to changes in population size (for resident or migratory species). This suggests that, across a wide variety of species, mismatches in the timing of egg laying or numbers of offspring have had relatively little influence on population size compared with other aspects of phenology and life history.

Genetic and ecological studies of animals in Chernobyl and Fukushima.

Recent advances in genetic and ecological studies of wild animal populations in Chernobyl and Fukushima have demonstrated significant genetic, physiological, developmental, and fitness effects stemming from exposure to radioactive contaminants. The few genetic studies that have been conducted in Chernobyl generally show elevated rates of genetic damage and mutation rates. All major taxonomic groups investigated (i.e., birds, bees, butterflies, grasshoppers, dragonflies, spiders, mammals) displayed reduced population sizes in highly radioactive parts of the Chernobyl Exclusion Zone. In Fukushima, population censuses of birds, butterflies, and cicadas suggested that abundances were negatively impacted by exposure to radioactive contaminants, while other groups (e.g., dragonflies, grasshoppers, bees, spiders) showed no significant declines, at least during the first summer following the disaster. Insufficient information exists for groups other than insects and birds to assess effects on life history at this time. The differences observed between Fukushima and Chernobyl may reflect the different times of exposure and the significance of multigenerational mutation accumulation in Chernobyl compared to Fukushima. There was considerable variation among taxa in their apparent sensitivity to radiation and this reflects in part life history, physiology, behavior, and evolutionary history. Interestingly, for birds, population declines in Chernobyl can be predicted by historical mitochondrial DNA base-pair substitution rates that may reflect intrinsic DNA repair ability.

Has removal of excess cysteine led to the evolution of pheomelanin? Pheomelanogenesis as an excretory mechanism for cysteine.

Pheomelanogenesis may have evolved as an excretory mechanism to remove excess cysteine, and in humans this might potentially confer a greater ability to avoid disease such as Parkinson's and Alzheimer's disease, in which excess cysteine is a contributory cause.

Patterns of sperm damage in Chernobyl passerine birds suggest a trade-off between sperm length and integrity.

Interspecific variation in sperm size is enigmatic, but generally assumed to reflect species-specific trade-offs in selection pressures. Among passerine birds, sperm length varies sevenfold, and sperm competition risk seems to drive the evolution of longer sperm. However, little is known about factors favouring short sperm or constraining the evolution of longer sperm. Here, we report a comparative analysis of sperm head abnormalities among 11 species of passerine bird in Chernobyl, presumably resulting from chronic irradiation following the 1986 accident. Frequencies of sperm abnormalities varied between 15.7 and 77.3% among species, more than fourfold higher than in uncontaminated areas. Nonetheless, species ranked similarly in sperm abnormalities in unpolluted areas as in Chernobyl, pointing to intrinsic factors underlying variation in sperm damage among species. Scanning electron microscopy of abnormal spermatozoa revealed patterns of acrosome damage consistent with premature acrosome reaction. Sperm length, but not sperm competition risk explained variation in sperm damage among species. This suggests that longer spermatozoa are more susceptible to premature acrosome reaction. Therefore, we hypothesize a trade-off between sperm length and sperm integrity affecting sperm evolution in passerine birds.

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.

Egg phenotype matching by cuckoos in relation to discrimination by hosts and climatic conditions.

Although parasites and their hosts often coexist in a set of environmentally differentiated populations connected by gene flow, few empirical studies have considered a role of environmental variation in shaping correlations between traits of hosts and parasites. Here, we studied for the first time the association between the frequency of adaptive parasitic common cuckoo Cuculus canorus phenotypes in terms of egg matching and level of defences exhibited by its reed warbler Acrocephalus scirpaceus hosts across seven geographically distant populations in Europe. We also explored the influence of spring climatic conditions experienced by cuckoos and hosts on cuckoo-host egg matching. We found that between-population differences in host defences against cuckoos (i.e. rejection rate) covaried with between-population differences in degree of matching. Between-population differences in host egg phenotype were associated with between-population differences in parasitism rate and spring climatic conditions, but not with host level of defences. Between-population differences in cuckoo egg phenotype covaried with between-population differences in host defences and spring climatic conditions. However, differences in host defences still explained differences in mimicry once differences in climatic conditions were controlled, suggesting that selection exerted by host defences must be strong relative to selection imposed by climatic factors on egg phenotypes.

Population regulation by habitat heterogeneity or individual adjustment?

1. The habitat heterogeneity (HHH) and individual adjustment (IAH) hypotheses are commonly proposed to explain a decrease in reproduction rate with increasing population density. Higher numbers of low-quality territories with low reproductive success as density increases lead to a decrease in reproduction under the HHH, while more competition at high density decreases reproduction across all territories under the IAH. 2. We analyse the influence of density and habitat heterogeneity on reproductive success in eight populations of long-lived territorial birds of prey belonging to four species. Sufficient reliability in distinguishing between population-wide, site-specific and individual quality effects on reproduction was granted through the minimal duration of 20 years of all data sets and the ability to control for individual quality in five of them. 3. Density increased in five populations but reproduction did not decrease in these. Territory occupancy as a surrogate of territory quality correlated positively with reproductive success but only significantly so in large data sets with more than 100 territories. 4. Reproductive success was always best explained by measures of territory quality in multivariate models. Direct or delayed (t-1) population density entered very few of the best models. Mixed models controlling for individual quality showed an increasing reproductive performance in older individuals and in those laying earlier, but measures of territory quality were also always retained in the best models. 5. We find strong support for the habitat heterogeneity hypothesis but weak support for the individual adjustment hypothesis. Both individual and site characteristics are crucial for reproductive performance in long-lived birds. Proportional occupancy of territories enables recognition of high-quality territories as preferential conservation targets.

High prevalence of cataracts in birds with pheomelanin-based colouration.

The crystalline lens of the eyes of vertebrates focuses light on the retina. Therefore, maintaining the lens clear is necessary for proper visual function. However, oxidative damage to proteins of the lens leads to opacification and lens dysfunction, termed cataract. Antioxidants thus have a role in avoiding the development of cataracts through their reduction of oxidative stress, and glutathione (GSH), a key intracellular antioxidant, belongs to the primary antioxidant defence mechanism of the lens. Other physiological mechanisms that require GSH may compete with the antioxidant mechanism of the eye. Pheomelanin is a main type of melanin, the most common pigment in vertebrates, and its synthesis consumes GSH. Here, we use data on 81 bird species to test the hypothesis that species producing large amounts of pheomelanin should have diminished capacity to use GSH to protect their eyes and, as a consequence, higher prevalence of cataracts. As predicted, the proportion of pheomelanic plumage was positively associated with the proportion of individuals with cataracts across species, suggesting that production of pheomelanin may have profound fitness consequences, as birds with cataracts have limited ability to perform vital activities. This constitutes the first comparative study of cataracts in wild animals.

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.

Genetic differentiation among sympatric cuckoo host races: males matter.

Generalist parasites regularly evolve host-specific races that each specialize on one particular host species. Many host-specific races originate from geographically structured populations where local adaptations to different host species drive the differentiation of distinct races. However, in sympatric populations where several host races coexist, gene flow could potentially disrupt such host-specific adaptations. Here, we analyse genetic differentiation among three sympatrically breeding host races of the brood-parasitic common cuckoo, Cuculus canorus. In this species, host-specific adaptations are assumed to be controlled by females only, possibly via the female-specific W-chromosome, thereby avoiding that gene flow via males disrupts local adaptations. Although males were more likely to have offspring in two different host species (43% versus 7%), they did not have significantly more descendants being raised outside their putative foster species than females (9% versus 2%). We found significant genetic differentiation for both biparentally inherited microsatellite DNA markers and maternally inherited mitochondrial DNA markers. To our knowledge, this is the first study that finds significant genetic differentiation in biparentally inherited markers among cuckoo host-specific races. Our results imply that males also may contribute to the evolution and maintenance of the different races, and hence that the genes responsible for egg phenotype may be found on autosomal chromosomes rather than the female-specific W-chromosome as previously assumed.

Bird population declines due to radiation exposure at Chernobyl are stronger in species with pheomelanin-based coloration.

Eumelanin and pheomelanin are the most common pigments providing color to the integument of vertebrates. While pheomelanogenesis requires high levels of a key intracellular antioxidant (glutathione, GSH), eumelanogenesis is inhibited by GSH. This implies that species that possess the molecular basis to produce large amounts of pheomelanin might be more limited in coping with environmental conditions that generate oxidative stress than species that produce eumelanin. Exposure to ionizing radiation produces free radicals and depletes antioxidant resources. GSH is particularly susceptible to radiation, so that species with large proportions of pheomelanic integument may be limited by the availability of GSH to combat oxidative stress and may thus suffer more from radiation effects. We tested this hypothesis in 97 species of birds censused in areas with varying levels of radioactive contamination around Chernobyl. After controlling for the effects of carotenoid-based color, body mass and similarity among taxa due to common phylogenetic descent, the proportion of pheomelanic plumage was strongly negatively related to the slope estimates of the relationship between abundance and radiation levels, while no effect of eumelanic color proportion was found. This represents the first report of an effect of the expression of melanin-based coloration on the capacity to resist the effects of ionizing radiation. Population declines were also stronger in species that exhibit carotenoid-based coloration and have large body mass. The magnitude of population declines had a relatively high phylogenetic signal, indicating that certain groups of birds, especially non-corvid passeriforms, are particularly susceptible to suffer from the effects of radioactive contamination due to phylogenetic inertia.