Host dispersal shapes the population structure of a tick-borne bacterial pathogen

Birds are hosts for several zoonotic pathogens. Because of their high mobility, especially of longdistance migrants, birds can disperse these pathogens, affecting their distribution and phylogeography. We focused on Borrelia burgdorferi sensu lato, which includes the causative agents of Lyme borreliosis, as an example for tick-borne pathogens, to address the role of birds as propagation hosts of zoonotic agents at a large geographical scale. We collected ticks from passerine birds in 11 European countries. B. burgdorferi s.l. prevalence in Ixodes spp. was 37% and increased with latitude. The fieldfare Turdus pilaris and the blackbird T. merula carried ticks with the highest Borrelia prevalence (92 and 58%, respectively), whereas robin Erithacus rubecula ticks were the least infected (3.8%). Borrelia garinii was the most prevalent genospecies (61%), followed by B. valaisiana (24%), B. afzelii (9%), B. turdi (5%) and B. lusitaniae (0.5%). A novel Borrelia genospecies "Candidatus Borrelia aligera" was also detected. Multilocus sequence typing (MLST) analysis of B. garinii isolates together with the global collection of B. garinii genotypes obtained from the Borrelia MLST public database revealed that: (a) there was little overlap among genotypes from different continents, (b) there was no geographical structuring within Europe, and (c) there was no evident association pattern detectable among B. garinii genotypes from ticks feeding on birds, questing ticks or human isolates. These findings strengthen the hypothesis that the population structure and evolutionary biology of tick-borne pathogens are shaped by their host associations and the movement patterns of these hosts.Peer reviewe

Fitness consequences of physiological responses to environmental variation in wild great tits

Environments change continuously. Fluctuations in temperature, rainfall, and food availability, can be predictable on the long term, but unpredictable within short time frames. Additionally, fluctuations in the environment can now occur unpredictably and with increasing frequency and duration because of human activities. Changes in an organism’s environment can be challenging because they destabilize its homeostatic processes. Understanding how organisms respond to these homeostatic disturbances, and if and how they can cope with them has become critically important and urgently needed in the light of climate change and increasing human disturbance. Physiological signals serve to integrate environmental and genomic information, and transmit that information within the organism to mediate a phenotypic response. Physiological traits, which refer to aspects of organism functioning, like nutrition, metabolism, thermal relationships, endocrine responses, and changes in immune parameters are important mechanisms to cope with fluctuating environments. If these traits directly affect an organism’s fitness and have transgenerational effects that also affect the phenotype and survival of its offspring, then they are potentially important drivers for evolutionary processes in response to rapidly changing environments. The general aim of my thesis was to determine the fitness consequences of physiological responses to environmental variation. For this, I studied how the physiological response of parents to environmental conditions relates to patterns of reproductive investment, reproductive success and offspring fitness in a wild population of great tits (Parus major). I first studied how the physiological response of parents to environmental conditions relates to their reproductive success (chapter 2). I tested the hypothesis that physiological traits covary and predict fitness primarily under challenging environmental conditions. I used data on six physiological traits (i.e., glucocorticoids: baseline and stress-induced concentrations, oxidative status: pro-oxidants, dietary and enzymatic antioxidant concentrations, and body condition) and fitness proxies (i.e., fledgling number and mass) collected over two breeding seasons that significantly differed in environmental conditions. Chapter 2 shows that physiological traits do not covary but they predict, in a sex-specific way, reproductive success when environmental conditions are challenging. In the year with low ambient temperature and high cumulated rainfall, females in a better oxidative condition produced more and heavier fledglings, while males with high body condition fledged more offspring. In males, but not in females, high baseline and low stress-induced glucocorticoid concentrations were also positively and negatively related to high fledgling mass. Chapter 2 suggests that glucocorticoids, oxidative state and body condition might be important mediators to successfully cope with challenging environmental circumstances. The way in which mothers cope with environmental changes can affect their reproductive investment, by altering the resources mothers pass on to their developing embryos. In egg laying species, females deposit hormones, nutrients and immune components into their eggs. In birds, the patterns of yolk deposition of these components along the laying sequence vary across and within species, but the processes that shape female yolk deposition are not yet fully understood. In chapter 3, I used a statistical approach based on repeated measures to study female yolk deposition along the laying sequence at both the population and among-female levels. I used data on the concentrations of 11 yolk components including steroid hormones, antioxidants, and fatty acids, which I determined in the eggs of 11 entire clutches collected during one breeding season. Chapter 3 shows that variation in yolk deposition at a population level is underpinned by different individual patterns, and that these individual patterns may be shaped by both genetic and environmental components. It also confirms that the method of analyzing the fourth egg from a nest is a suitable way to estimate clutch-level yolk composition in studies of wild populations. Further, chapter 3 shows that mothers concomitantly secret steroid hormones, antioxidants and fatty acids into their egg yolks, suggesting that maternal substances work interactively within an egg to influence the phenotype of the offspring. In chapter 4, I built on the knowledge obtained in the previous chapter to test for interactive effects of yolk components on offspring phenotypic traits (i.e., oxidative state and body condition) and fitness proxies (i.e., hatchling number, fledgling number, mass and tarsus). I used data on concentrations of 31 yolk components measured in the fourth egg from 69 nests collected over two breeding seasons. Chapter 4 shows that offspring phenotypes relate to the interactions among the yolk components that females deposit into their eggs. This chapter also provides the first evidence for a relationship between yolk fatty acids and hatchling and fledgling number in a wild population; thus, suggesting that these yolk components, which are strongly influenced by the quantity and quality of the food consumed by mothers during egg laying, can greatly influence an individual’s fitness. In summary, chapter 3 and 4 show that the way mothers cope with environmental changes affects the resources they transfer to their eggs, which interact to shape phenotypic and fitness traits in the offspring. With this thesis I thus contributed empirically to the study of how changes in physiological traits due to environmental variation relate to fitness and phenotypic responses. My thesis shows that birds from a free-living population can successfully cope with unpredictable environmental disturbances during the breeding season, such as low temperatures and high cumulated rainfall, and suggests that glucocorticoids, oxidative state and body condition are important mediators to do so. However, female reproductive success might be negatively affected via transgenerational effects on offspring fitness if fluctuations in environmental conditions cause a decrease in food supply, and therefore a decrease in essential yolk components transferred by the mothers into the eggs. Overall, my thesis shows that the interactions between parents and offspring fitness are an important point to include in studies aiming to understand if and how organisms cope with environmental changes.publishe

Quantifying Glucocorticoid Plasticity Using Reaction Norm Approaches : There Still is So Much to Discover!

Hormones are highly responsive internal signals that help organisms adjust their phenotype to fluctuations in environmental and internal conditions. Our knowledge of the causes and consequences of variation in circulating hormone concentrations has improved greatly in the past. However, this knowledge often comes from population-level studies, which generally tend to make the flawed assumption that all individuals respond in the same way to environmental changes. Here, we advocate that we can vastly expand our understanding of the ecology and evolution of hormonal traits once we acknowledge the existence of individual differences by quantifying hormonal plasticity at the individual level, where selection acts. In this review, we use glucocorticoid (GC) hormones as examples of highly plastic endocrine traits that interact intimately with energy metabolism but also with other organismal traits like behavior and physiology. First, we highlight the insights gained by repeatedly assessing an individual's GC concentrations along a gradient of environmental or internal conditions using a “reaction norm approach.” This study design should be followed by a hierarchical statistical partitioning of the total endocrine variance into the among-individual component (individual differences in average hormone concentrations, i.e., in the intercept of the reaction norm) and the residual (within-individual) component. The latter is ideally further partitioned by estimating more precisely hormonal plasticity (i.e., the slope of the reaction norm), which allows to test whether individuals differ in the degree of hormonal change along the gradient. Second, we critically review the published evidence for GC variation, focusing mostly on among- and within-individual levels, finding only a good handful of studies that used repeated-measures designs and random regression statistics to investigate GC plasticity. These studies indicate that individuals can differ in both the intercept and the slope of their GC reaction norm to a known gradient. Third, we suggest rewarding avenues for future work on hormonal reaction norms, for example to uncover potential costs and trade-offs associated with GC plasticity, to test whether GC plasticity varies when an individual's reaction norm is repeatedly assessed along the same gradient, whether reaction norms in GCs covary with those in other traits like behavior and fitness (generating multivariate plasticity), or to quantify GC reaction norms along multiple external and internal gradients that act simultaneously (leading to multidimensional plasticity). Throughout this review, we emphasize the power that reaction norm approaches offer for resolving unanswered questions in ecological and evolutionary endocrinology.publishe

Natural variation in yolk fatty acids, but not androgens, predicts offspring fitness in a wild bird

BackgroundIn egg-laying animals, mothers can influence the developmental environment and thus the phenotype of their offspring by secreting various substances into the egg yolk. In birds, recent studies have demonstrated that different yolk substances can interactively affect offspring phenotype, but the implications of such effects for offspring fitness and phenotype in natural populations have remained unclear. We measured natural variation in the content of 31 yolk components known to shape offspring phenotypes including steroid hormones, antioxidants and fatty acids in eggs of free-living great tits (Parus major) during two breeding seasons. We tested for relationships between yolk component groupings and offspring fitness and phenotypes.ResultsVariation in hatchling and fledgling numbers was primarily explained by yolk fatty acids (including saturated, mono- and polyunsaturated fatty acids) - but not by androgen hormones and carotenoids, components previously considered to be major determinants of offspring phenotype. Fatty acids were also better predictors of variation in nestling oxidative status and size than androgens and carotenoids.ConclusionsOur results suggest that fatty acids are important yolk substances that contribute to shaping offspring fitness and phenotype in free-living populations. Since polyunsaturated fatty acids cannot be produced de novo by the mother, but have to be obtained from the diet, these findings highlight potential mechanisms (e.g., weather, habitat quality, foraging ability) through which environmental variation may shape maternal effects and consequences for offspring. Our study represents an important first step towards unraveling interactive effects of multiple yolk substances on offspring fitness and phenotypes in free-living populations. It provides the basis for future experiments that will establish the pathways by which yolk components, singly and/or interactively, mediate maternal effects in natural populations.publishe

Female variation in allocation of steroid hormones, antioxidants and fatty acids : a multilevel analysis in a wild passerine bird

The environment where an embryo develops can be influenced by components of maternal origin, which can shape offspring phenotypes and therefore maternal fitness. In birds that produce more than one egg per clutch, females differ in the concentration of components they allocate into the yolk along the laying sequence. However, identification of processes that shape female yolk allocation and thus offspring phenotype still remains a major challenge within evolutionary ecology. A way to increase our understanding is by acknowledging that allocation patterns can differ depending on the level of analysis, such as the population versus the among-female (within-population) level. We employed mixed models to analyze at both levels the variation in allocation along the laying sequence of four steroid hormones, three antioxidants, and four groups of fatty acids present in the egg yolks of wild great tits Parus major. We also quantified repeatabilities for each component to study female consistency. At a population level, the concentrations/proportions of five yolk components varied along the laying sequence, implying that the developmental environment is different for offspring developing in first versus last eggs. Females varied substantially in the mean allocation of components and in their plasticity along the laying sequence. For most components, these two parameters were negatively correlated. Females were also remarkably repeatable in their allocation. Overall, our data emphasize the need to account for female variation in yolk allocation along the laying sequence at multiple levels, as variation at a population level is underpinned by different individual patterns. Our findings also highlight the importance of considering both levels of analysis in future studies investigating the causes and fitness consequences of yolk compounds. Finally, our results on female repeatability confirm that analyzing one egg per nest is a suitable way to address the consequences of yolk resource deposition for the offspring

Host dispersal shapes the population structure of a tick-borne bacterial pathogen

Birds are hosts for several zoonotic pathogens. Because of their high mobility, especially of longdistance migrants, birds can disperse these pathogens, affecting their distribution and phylogeography. We focused on Borrelia burgdorferi sensu lato, which includes the causative agents of Lyme borreliosis, as an example for tick‐borne pathogens, to address the role of birds as propagation hosts of zoonotic agents at a large geographical scale. We collected ticks from passerine birds in 11 European countries. B . burgdorferi s.l. prevalence in Ixodes spp. was 37% and increased with latitude. The fieldfare Turdus pilaris and the blackbird T. merula carried ticks with the highest Borrelia prevalence (92 and 58%, respectively), whereas robin Erithacus rubecula ticks were the least infected (3.8%). Borrelia garinii was the most prevalent genospecies (61%), followed by B. valaisiana (24%), B. afzelii (9%), B. turdi (5%) and B. lusitaniae (0.5%). A novel Borrelia genospecies “Candidatus Borrelia aligera” was also detected. Multilocus sequence typing (MLST ) analysis of B. garinii isolates together with the global collection of B. garinii genotypes obtained from the Borrelia MLST public database revealed that: (a) there was little overlap among genotypes from different continents, (b) there was no geographical structuring within Europe, and (c) there was no evident association pattern detectable among B. garinii genotypes from ticks feeding on birds, questing ticks or human isolates. These findings strengthen the hypothesis that the population structure and evolutionary biology of tick‐borne pathogens are shaped by their host associations and the movement patterns of these hosts

Host dispersal shapes the population structure of a tick‐borne bacterial pathogen

Abstract Birds are hosts for several zoonotic pathogens. Because of their high mobility, especially of longdistance migrants, birds can disperse these pathogens, affecting their distribution and phylogeography. We focused on Borrelia burgdorferi sensu lato, which includes the causative agents of Lyme borreliosis, as an example for tick‐borne pathogens, to address the role of birds as propagation hosts of zoonotic agents at a large geographical scale. We collected ticks from passerine birds in 11 European countries. B. burgdorferi s.l. prevalence in Ixodes spp. was 37% and increased with latitude. The fieldfare Turdus pilaris and the blackbird T. merula carried ticks with the highest Borrelia prevalence (92 and 58%, respectively), whereas robin Erithacus rubecula ticks were the least infected (3.8%). Borrelia garinii was the most prevalent genospecies (61%), followed by B. valaisiana (24%), B. afzelii (9%), B. turdi (5%) and B. lusitaniae (0.5%). A novel Borrelia genospecies “Candidatus Borrelia aligera” was also detected. Multilocus sequence typing (MLST) analysis of B. garinii isolates together with the global collection of B. garinii genotypes obtained from the Borrelia MLST public database revealed that: (a) there was little overlap among genotypes from different continents, (b) there was no geographical structuring within Europe, and (c) there was no evident association pattern detectable among B. garinii genotypes from ticks feeding on birds, questing ticks or human isolates. These findings strengthen the hypothesis that the population structure and evolutionary biology of tick‐borne pathogens are shaped by their host associations and the movement patterns of these hosts