Sex roles in birds: Phylogenetic analyses of the influence of climate, life histories and social environment.

Sex roles describe sex differences in courtship, mate competition, social pair-bonds and parental care. A key challenge is to identify associations among the components and the drivers of sex roles. Here, we investigate sex roles using data from over 1800 bird species. We found extensive variation and lability in proxies of sex roles, indicating remarkably independent evolution among sex role components. Climate and life history showed weak associations with sex roles. However, adult sex ratio is associated with sexual dimorphism, mating system and parental care, suggesting that social environment is central to explaining variation in sex roles among birds. Our results suggest that sex differences in reproductive behaviour are the result of diverse and idiosyncratic responses to selection. Further understanding of sex roles requires studies at the population level to test how local responses to ecology, life histories and mating opportunities drive processes that shape sex role variation among higher taxa.

Isopropyl Amino Acid Esters Ionic Liquids as Vehicles for Non-Steroidal Anti-Inflammatory Drugs in Potential Topical Drug Delivery Systems with Antimicrobial Activity.

New derivatives of non-steroidal anti-inflammatory drugs were synthesized via conjugation with L-amino acid isopropyl esters. The characteristics of the physicochemical properties of the obtained pharmaceutically active ionic liquids were determined. It has been shown how the incorporation of various L-amino acid esters as an ion pair affects the properties of the parent drug. Moreover, the antimicrobial activity of the obtained compounds was evaluated. The proposed structural modifications of commonly used drugs indicate great potential for use in topical and transdermal preparations.

Territorial behaviour of buzzards versus random matrix spacing distributions.

A deeper understanding of the processes underlying the distribution of animals in space is crucial for both basic and applied ecology. The Common buzzard (Buteo buteo) is a highly aggressive, territorial bird of prey that interacts strongly with its intra- and interspecific competitors. We propose and use random matrix theory to quantify the strength and range of repulsion as a function of the buzzard population density, thus providing a novel approach to model density dependence. As an indicator of territorial behaviour, we perform a large-scale analysis of the distribution of buzzard nests in an area of 300 square kilometres around the Teutoburger Wald, Germany, as gathered over a period of 20 years. The nearest and next-to-nearest neighbour spacing distribution between nests is compared to the two-dimensional Poisson distribution, originating from uncorrelated random variables, to the complex eigenvalues of random matrices, which are strongly correlated, and to a two-dimensional Coulomb gas interpolating between these two. A one-parameter fit to a time-moving average reveals a significant increase of repulsion between neighbouring nests, as a function of the observed increase in absolute population density over the monitored period of time, thereby proving an unexpected yet simple model for density-dependent spacing of predator territories. A similar effect is obtained for next-to-nearest neighbours, albeit with weaker repulsion, indicating a short-range interaction. Our results show that random matrix theory might be useful in the context of population ecology.

Developmental conditions promote individual differentiation of endocrine axes and behavior in a tropical pinniped.

Between-individual variation in behavior can emerge through complex interactions between state-related mechanisms, which include internal physiological constraints or feedback derived from the external environment. State-related conditions can be especially influential during early life, when parental effort and exposure to social stress may canalize consistent differences in offspring hormonal profiles and foster specific behavioral strategies. Here, we unravel how relevant state variables, including sex, somatic condition, local population density, and maternal traits, contribute to within-cohort differences in stress, sex, and thyroid hormone axes in dependent Galapagos sea lions with the primary goal of understanding downstream effects on boldness, docility, habitat use, and activity. Pups within denser natal sites had higher levels of cortisol and thyroid T4, a prohormone and proxy for metabolic reserves, likely as an adaptive physiological response after exposure to increased numbers of conspecific interactions. Furthermore, considering maternal effects, mothers in better body condition produced pups with higher testosterone yet downregulated basal cortisol and thyroid T4. This hormonal profile was correlated with increased boldness toward novel objects and attenuated stress responsiveness during capture. Intriguingly, pups with increased thyroid T3, the biologically active form, maintained faster somatic growth and were observed to have increased activity and extensively explored surrounding habitats. Collectively, these findings provide comprehensive evidence for several links to hormone-mediated behavioral strategies, highlighted by variation in socio-environmental and maternally derived input during a foundational life stage.

Individuality counts: A new comprehensive approach to foraging strategies of a tropical marine predator.

Foraging strategies are of great ecological interest, as they have a strong impact on the fitness of an individual and can affect its ability to cope with a changing environment. Recent studies on foraging strategies show a higher complexity than previously thought due to intraspecific variability. To reliably identify foraging strategies and describe the different foraging niches they allow individual animals to realize, high-resolution multivariate approaches which consider individual variation are required. Here we dive into the foraging strategies of Galápagos sea lions (Zalophus wollebaeki), a tropical predator confronted with substantial annual variation in sea surface temperature. This affects prey abundance, and El Niño events, expected to become more frequent and severe with climate change, are known to have dramatic effects on sea lions. This study used high-resolution measures of depth, GPS position and acceleration collected from 39 lactating sea lion females to analyze their foraging strategies at an unprecedented level of detail using a novel combination of automated broken stick algorithm, hierarchical cluster analysis and individually fitted multivariate hidden Markov models. We found three distinct foraging strategies (pelagic, benthic, and night divers), which differed in their horizontal, vertical and temporal distribution, most likely corresponding to different prey species, and allowed us to formulate hypotheses with regard to adaptive values under different environmental scenarios. We demonstrate the advantages of our multivariate approach and inclusion of individual variation to reliably gain a deeper understanding of the adaptive value and ecological relevance of foraging strategies of marine predators in dynamic environments.

Early sexual dimorphism in the developing gut microbiome of northern elephant seals.

The gut microbiome is an integral part of a species' ecology, but we know little about how host characteristics impact its development in wild populations. Here, we explored the role of such intrinsic factors in shaping the gut microbiome of northern elephant seals (Mirounga angustirostris) during a critical developmental window of 6 weeks after weaning, when the pups stay ashore without feeding. We found substantial sex differences in the early-life gut microbiome, even though males and females could not yet be distinguished morphologically. Sex and age both explained around 15% of the variation in gut microbial beta diversity, while microbial communities sampled from the same individual showed high levels of similarity across time, explaining another 40% of the variation. Only a small proportion of the variation in beta diversity was explained by health status, assessed by full blood counts, but clinically healthy individuals had a greater microbial alpha diversity than their clinically abnormal peers. Across the post-weaning period, the northern elephant seal gut microbiome was highly dynamic. We found evidence for several colonization and extinction events as well as a decline in Bacteroides and an increase in Prevotella, a pattern that has previously been associated with the transition from nursing to solid food. Lastly, we show that genetic relatedness was correlated with gut microbiome similarity in males but not females, again reflecting early sex differences. Our study represents a naturally diet-controlled and longitudinal investigation of how intrinsic factors shape the early gut microbiome in a species with extreme sex differences in morphology and life history.

Zebra finches bi-directionally selected for personality differ in repeatability of corticosterone and testosterone.

Consistent between-individual differences in behaviour have been documented across the animal kingdom. Such variation between individuals has been shown to be the basis for selection and to act as a pacemaker for evolutionary change. Recently, equivocal evidence suggests that such consistent between-individual variation is also present in hormones. This observation has sparked interest in understanding the mechanisms shaping individual differences, temporal consistency and heritability of hormonal phenotypes and to understand, if and to what extent hormonal mechanisms are involved in mediating consistent variation in behaviour between individuals. Here, we used zebra finches of the fourth generation of bi-directionally selected lines for three independent behaviours: aggression, exploration and fearlessness. We investigated how these behaviours responded to artificial selection and tested their repeatability. We further tested for repeatability of corticosterone and testosterone across and within lines. Moreover, we are presenting the decomposed variance components for within-individual variance (i.e. flexibility) and between-individual variance (i.e. more or less pronounced differences between individuals) and investigate their contribution to repeatability estimates. Both hormones as well as the exploration and fearlessness but not aggressiveness, were repeatable. However, variance components and hence repeatability differed between lines and were often lower than in unselected control animals, mainly because of a reduction in between-individual variance. Our data show that artificial selection (including active selection and genetic drift) can affect the mean and variance of traits. We stress the importance for understanding how variable a trait is both between and within individuals to assess the selective value of a trait.

Sex-specific early survival drives adult sex ratio bias in snowy plovers and impacts mating system and population growth.

Adult sex ratio (ASR) is a central concept in population biology and a key factor in sexual selection, but why do most demographic models ignore sex biases? Vital rates often vary between the sexes and across life history, but their relative contributions to ASR variation remain poorly understood-an essential step to evaluate sex ratio theories in the wild and inform conservation. Here, we combine structured two-sex population models with individual-based mark-recapture data from an intensively monitored polygamous population of snowy plovers. We show that a strongly male-biased ASR (0.63) is primarily driven by sex-specific survival of juveniles rather than adults or dependent offspring. This finding provides empirical support for theories of unbiased sex allocation when sex differences in survival arise after the period of parental investment. Importantly, a conventional model ignoring sex biases significantly overestimated population viability. We suggest that sex-specific population models are essential to understand the population dynamics of sexual organisms: reproduction and population growth are most sensitive to perturbations in survival of the limiting sex. Overall, our study suggests that sex-biased early survival may contribute toward mating system evolution and population persistence, with implications for both sexual selection theory and biodiversity conservation.

Extremely low Plasmodium prevalence in wild plovers and coursers from Cape Verde and Madagascar.

BACKGROUND: Relatively little is known about the prevalence of blood parasites in shorebirds, especially those breeding in the tropics. The prevalence of blood parasites of the genera Plasmodium, Haemoproteus and Leucocytozoon was assessed in blood samples from Kentish plovers and cream-coloured coursers in Cape Verde, and samples of Kittlitz's plovers, Madagascar plovers and white-fronted plovers in Madagascar. RESULTS: Only two of these samples were positive for Plasmodium: a Kittlitz's plover was infected by a generalist lineage of Plasmodium that has already been reported in Europe and Africa, while in a white-fronted plover direct sequencing revealed a previously un-described Plasmodium lineage. CONCLUSION: Potential explanations for the low prevalence of blood parasites include the scarcity of vectors in habitats used by these bird species and their resistance to parasitic infections.

Phosphorus in recycling fertilizers - analytical challenges.

The importance of secondary raw materials for phosphorus (P) fertilizer production is expected to increase in the future due to resource depletion, supply risks, and heavy metal contamination of fossil phosphate resources. Municipal wastewater is a promising source for P recovery. In Germany for instance, it contains almost 50% of the total amount of P that is currently applied as mineral fertilizer. Several procedures have been developed to recover and re-use P resulting in a growing number of recycling fertilizers that are currently not regulated in terms of fertilizer efficiency. We tested various materials and matrices for their total P content, solubility of P in neutral ammonium citrate (Pnac) and water, and performed robustness tests to check if existing analytical methods are suitable for those new materials. Digestion with inverse aqua regia was best suited to determine the total P content. Pnac sample preparation and analyses were feasible for all matrices. However, we found significant time and temperature dependencies, especially for materials containing organic matter. Furthermore, several materials didn't reach equilibrium during the extractions. Thus, strict compliance of the test conditions is strongly recommended to achieve comparable results.

Neurobiology of knowledge and misperception of lyrics.

We conducted two functional magnetic resonance imaging (fMRI) experiments to investigate the neural underpinnings of knowledge and misperception of lyrics. In fMRI experiment 1, a linear relationship between familiarity with lyrics and activation was found in left-hemispheric speech-related as well as bilateral striatal areas which is in line with previous research on generation of lyrics. In fMRI experiment 2, we employed so called Mondegreens and Soramimi to induce misperceptions of lyrics revealing a bilateral network including middle temporal and inferior frontal areas as well as anterior cingulate cortex (ACC) and mediodorsal thalamus. ACC activation also correlated with the extent to which misperceptions were judged as amusing corroborating previous neuroimaging results on the role of this area in mediating the pleasant experience of chills during music perception. Finally, we examined the areas engaged during misperception of lyrics using diffusion-weighted imaging (DWI) to determine their structural connectivity. These combined fMRI/DWI results could serve as a neurobiological model for future studies on other types of misunderstanding which are events with potentially strong impact on our social life.

Intraguild predation leads to cascading effects on habitat choice, behaviour and reproductive performance.

Intraguild predation (IGP) is a commonly recognized mechanism influencing the community structure of predators, but the complex interactions are notoriously difficult to disentangle. The mesopredator suppression hypothesis predicts that a superpredator may either simultaneously repress two mesopredators, restrain the dominant one and thereby release the subdominant mesopredator, or elicit different responses by both mesopredators. We show the outcome arising from such conditions in a three-level predator assemblage (Eurasian eagle owl Bubo bubo L., northern goshawk Accipiter gentilis L. and common buzzard Buteo buteo L.) studied over 25 years. In the second half of the study period, the eagle owl re-colonized the study area, thereby providing a natural experiment of superpredator introduction. We combined this set-up with detailed GIS analysis of habitat use and a field experiment simulating intrusion by the superpredator into territories of the subdominant mesopredator, the buzzard. Although population trends were positive for all three species in the assemblage, the proportion of failed breeding attempts increased significantly in both mesopredators after the superpredator re-colonized the area. We predicted that superpredator-induced niche shifts in the dominant mesopredator may facilitate mesopredator coexistence in superpredator-free refugia. We found significant changes in nesting habitat choice in goshawk, but not in buzzard. Since competition for enemy-free refugia and the rapid increase in population density may have constrained niche shifts of the subdominant mesopredator, we further predicted behavioural changes in response to the superpredator. The field experiment indeed showed a significant increase in aggressive response of buzzards towards eagle owl territory intrusion over the course of 10 years, probably due to phenotypic plasticity in the response towards superpredation risk. Overall, our results show that intraguild predation can be a powerful force of behavioural change, simultaneously influencing habitat use and aggressiveness in predator communities. These changes might help to buffer mesopredator populations against the negative effects of intraguild predation.

De novo assembly of the dual transcriptomes of a polymorphic raptor species and its malarial parasite.

BACKGROUND: Studies of non-model species are important for understanding the molecular processes underpinning phenotypic variation under natural ecological conditions. The common buzzard (Buteo buteo; Aves: Accipitriformes) is a widespread and common Eurasian raptor with three distinct plumage morphs that differ in several fitness-related traits, including parasite infestation. To provide a genomic resource for plumage polymorphic birds in general and to search for candidate genes relating to fitness, we generated a transcriptome from a single dead buzzard specimen plus easily accessible, minimally invasive samples from live chicks. RESULTS: We not only de novo assembled a near-complete buzzard transcriptome, but also obtained a significant fraction of the transcriptome of its malaria-like parasite, Leucocytozoon buteonis. By identifying melanogenesis-related transcripts that are differentially expressed in light ventral and dark dorsal feathers, but which are also expressed in other regions of the body, we also identified a suite of candidate genes that could be associated with fitness differences among the morphs. These include several immune-related genes, providing a plausible link between melanisation and parasite load. qPCR analysis of a subset of these genes revealed significant differences between ventral and dorsal feathers and an additional effect of morph. CONCLUSION: This new resource provides preliminary insights into genes that could be involved in fitness differences between the buzzard colour morphs, and should facilitate future studies of raptors and their malaria-like parasites.

Apparent vector-mediated parent-to-offspring transmission in an avian malaria-like parasite.

Parasite transmission strategies strongly impact host-parasite co-evolution and virulence. However, studies of vector-borne parasites such as avian malaria have neglected the potential effects of host relatedness on the exchange of parasites. To test whether extended parental care in the presence of vectors increases the probability of transmission from parents to offspring, we used high-throughput sequencing to develop microsatellites for malaria-like Leucocytozoon parasites of a wild raptor population. We show that host siblings carry genetically more similar parasites than unrelated chicks both within and across years. Moreover, chicks of mothers of the same plumage morph carried more similar parasites than nestlings whose mothers were of different morphs, consistent with matrilineal transmission of morph-specific parasite strains. Ours is the first evidence of an association between host relatedness and parasite genetic similarity, consistent with vector-mediated parent-to-offspring transmission. The conditions for such 'quasi-vertical' transmission may be common and could suppress the evolution of pathogen virulence.

Personality over ontogeny in zebra finches: long-term repeatable traits but unstable behavioural syndromes.

A crucial assumption of animal personality research is that behaviour is consistent over time, showing a high repeatability within individuals. This assumption is often made, sometimes tested using short time intervals between behavioural tests, but rarely thoroughly investigated across long time intervals crossing different stages of ontogeny. We performed such a longitudinal test across three life stages in zebra finches (Taeniopygia guttata), representing about 15-20% of their life span in captivity, and found repeatabilities ranging from 0.03 to 0.67. Fearlessness and exploration were the most repeatable traits both within and across life stages. Activity and aggression were repeatable across, but not or only partly within life stages. Boldness was not repeatable. Furthermore, we found no evidence for a consistent behavioural syndrome structure across ontogeny. Our results indicate that the consistency of behavioural traits and their correlations might be overestimated and suggest that life-long stability of animal personality should not simply be assumed.

Complete survey of German sewage sludge ash.

The amount of sewage sludge produced worldwide is expected to further increase due to rising efforts in wastewater treatment. There is a growing concern against its direct use as fertilizer due to contamination of the sludge with heavy metals and organic pollutants. Incinerating the sludge degrades organic compounds almost completely and concentrates heavy metals and phosphorus. However, the sewage sludge ash (SSA) is almost completely disposed of and with it all resources are removed from the economic cycle. Comprehensive knowledge of the composition of SSA is crucial to assess the resource recovery potentials. We conducted a survey of all SSA emerging in Germany and determined the respective mass fractions of 57 elements over a period of one year. The median content of phosphorus was 7.9%, indicating an important recovery potential. Important trace elements were Zn (2.5 g/kg), Mn (1.3 g/kg), and Cu (0.9 g/kg). Mass fractions of technology metals such as V, Cr, Ga, Nb, and rare earths were comparatively low. Considering the possible use of SSA as secondary raw material for fertilizer production it should be noted that its Cd and U content (2.7 mg/kg and 4.9 mg/kg respectively) is significantly lower than that of rock phosphate based mineral fertilizers.

Early-life factors shaping the gut microbiota of Common buzzard nestlings.

BACKGROUND: Exploring the dynamics of gut microbiome colonisation during early-life stages is important for understanding the potential impact of microbes on host development and fitness. Evidence from model organisms suggests a crucial early-life phase when shifts in gut microbiota can lead to immune dysregulation and reduced host condition. However, our understanding of gut microbiota colonisation in long-lived vertebrates, especially during early development, remains limited. We therefore used a wild population of common buzzard nestlings (Buteo buteo) to investigate connections between the early-life gut microbiota colonisation, environmental and host factors. RESULTS: We targeted both bacterial and eukaryotic microbiota using the 16S and 28S rRNA genes. We sampled the individuals during early developmental stages in a longitudinal design. Our data revealed that age significantly affected microbial diversity and composition. Nest environment was a notable predictor of microbiota composition, with particularly eukaryotic communities differing between habitats occupied by the hosts. Nestling condition and infection with the blood parasite Leucocytozoon predicted microbial community composition. CONCLUSION: Our findings emphasise the importance of studying microbiome dynamics to capture changes occurring during ontogeny. They highlight the role of microbial communities in reflecting host health and the importance of the nest environment for the developing nestling microbiome. Overall, this study contributes to understanding the complex interplay between microbial communities, host factors, and environmental variables, and sheds light on the ecological processes governing gut microbial colonisation during early-life stages.

Variation at phenological candidate genes correlates with timing of dispersal and plumage morph in a sedentary bird of prey.

Polymorphic genes involved in the conserved molecular signalling of circadian and circannual clocks may play important roles in governing the timing of breeding and dispersal and thereby affect fitness in vertebrates. However, relatively few studies have explored associations between phenological candidate genes and behaviour, and these are somewhat biased towards particular taxonomic groups such as passerine birds and salmonid fish. Consequently, we assayed microsatellite polymorphisms within the exonic and 3' untranslated regions of the regulatory genes CLOCK, NPAS2, ADCYAP1 and CREB1 in the common buzzard (Buteo buteo), a polymorphic raptor species with three plumage morphs that differ in key life history traits including lifetime reproductive success. In contrast to studies of passerines, CLOCK poly-glutamine (poly-Q) was found to be monomorphic in 976 common buzzard nestlings as well as in three other Buteo species. Moreover, none of the candidate genes were significantly associated with fledging dates, although intermediately melanized females were found to lay earlier on average than light or dark morph individuals, and their offspring carried longer ADCYAP1 alleles. In contrast, all three candidate genes explained significant variation in one or more measures of juvenile buzzard dispersal (resighting probability, timing of dispersal and distance dispersed). Our findings contribute towards a broader body of work on the adaptive significance of CLOCK polymorphism, while also building upon previous studies that have documented links between ADCYAP1 variability and the timing of migration.

High functional allelic diversity and copy number in both MHC classes in the common buzzard.

BACKGROUND: The major histocompatibility complex (MHC), which encodes molecules that recognize various pathogens and parasites and initiates the adaptive immune response in vertebrates, is renowned for its exceptional polymorphism and is a model of adaptive gene evolution. In birds, the number of MHC genes and sequence diversity varies greatly among taxa, believed due to evolutionary history and differential selection pressures. Earlier characterization studies and recent comparative studies suggest that non-passerine species have relatively few MHC gene copies compared to passerines. Additionally, comparative studies that have looked at partial MHC sequences have speculated that non-passerines have opposite patterns of selection on MHC class I (MHC-I) and class II (MHC-II) loci than passerines: namely, greater sequence diversity and signals of selection on MHC-II than MHC-I. However, new sequencing technology is revealing much greater MHC variation than previously expected while also facilitating full sequence variant detection directly from genomic data. Our study aims to take advantage of high-throughput sequencing methods to fully characterize both classes and domains of MHC of a non-passerine bird of prey, the common buzzard (Buteo buteo), to test predictions of MHC variation and differential selection on MHC classes. RESULTS: Using genetic, genomic, and transcriptomic high-throughput sequencing data, we established common buzzards have at least three loci that produce functional alleles at both MHC classes. In total, we characterize 91 alleles from 113 common buzzard chicks for MHC-I exon 3 and 41 alleles from 125 chicks for MHC-IIB exon 2. Among these alleles, we found greater sequence polymorphism and stronger diversifying selection at MHC-IIB exon 2 than MHC-I exon 3, suggesting differential selection pressures on MHC classes. However, upon further investigation of the entire peptide-binding groove by including genomic data from MHC-I exon 2 and MHC-IIA exon 2, this turned out to be false. MHC-I exon 2 was as polymorphic as MHC-IIB exon 2 and MHC-IIA exon 2 was essentially invariant. Thus, comparisons between MHC-I and MHC-II that included both domains of the peptide-binding groove showed no differences in polymorphism nor diversifying selection between the classes. Nevertheless, selection analysis indicates balancing selection has been acting on common buzzard MHC and phylogenetic inference revealed that trans-species polymorphism is present between common buzzards and species separated for over 33 million years for class I and class II. CONCLUSIONS: We characterize and confirm the functionality of unexpectedly high copy number and allelic diversity in both MHC classes of a bird of prey. While balancing selection is acting on both classes, there is no evidence of differential selection pressure on MHC classes in common buzzards and this result may hold more generally once more data for understudied MHC exons becomes available.

Sex roles and sex ratios in animals.

In species with separate sexes, females and males often differ in their morphology, physiology and behaviour. Such sex-specific traits are functionally linked to variation in reproductive competition, mate choice and parental care, which have all been linked to sex roles. At the 150th anniversary of Darwin's theory on sexual selection, the question of why patterns of sex roles vary within and across species remains a key topic in behavioural and evolutionary ecology. New theoretical, experimental and comparative evidence suggests that variation in the adult sex ratio (ASR) is a key driver of variation in sex roles. Here, we first define and discuss the historical emergence of the sex role concept, including recent criticisms and rebuttals. Second, we review the various sex ratios with a focus on ASR, and explore its theoretical links to sex roles. Third, we explore the causes, and especially the consequences, of biased ASRs, focusing on the results of correlational and experimental studies of the effect of ASR variation on mate choice, sexual conflict, parental care and mating systems, social behaviour, hormone physiology and fitness. We present evidence that animals in diverse societies are sensitive to variation in local ASR, even on short timescales, and propose explanations for conflicting results. We conclude with an overview of open questions in this field integrating demography, life history and behaviour.