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Impacts évolutifs de l'urbanisation chez la mésange charbonnière : du phénotype aux (épi)génomes
Abstract and Figures
L’urbanisation est un phénomène mondial convertissant des milieux naturels en milieux artificialisés. Les zones urbaines constituent un nouvel environnement majoritairement façonné par l’homme avec des conditions environnementales inédites pouvant directement impacter les espèces vivant en milieu urbain ainsi que leurs trajectoires évolutives. A l’heure actuelle, les processus évolutifs associés au milieu urbain sont peu connus bien qu’ils déterminent l’histoire passée, présente et future des espèces concernées. Ainsi, l’objectif de cette thèse est d’étudier l’impact de la vie urbaine sur les espèces sauvages et de comprendre si et comment les espèces s’adaptent à ce nouvel environnement. A travers l’étude de populations de mésanges charbonnières (Parus major) urbaine et forestière du sud de la France (Montpellier) ce travail explore dans un premier temps les différences phénotypiques associées au milieu urbain et met en évidence l’existence d’un phénotype urbain caractérisé par une taille réduite, des pontes précoces et réduites, un comportement plus exploratoire et plus agressif ainsi qu’une réponse accrue au stress. Dans un second temps, des analyses de sélection indiquent que ces différences phénotypiques ne résultent pas de nouvelles pressions de sélection associées au milieu urbain et ne sont pas adaptatives. Dans un troisième temps, une approche (épi)génomique dans trois villes (Montpellier, Barcelone et Varsovie) révèle l’existence de traces de sélection dans les génomes ainsi que de régions différentiellement méthylées en milieu urbain, mais peu de parallélisme entre villes. Parmi ces marqueurs (épi)génomiques, nombreux se révèlent associés à des gènes ayant des fonctions impliquées notamment dans le système nerveux, l’immunité, les processus hormonaux ainsi que le comportement, suggérant le potentiel rôle majeur de ces fonctions dans l’adaptation face aux conditions urbaines. Enfin, après avoir proposé une feuille de route pour tout écologue voulant étudier l’adaptation au milieu urbain, ce travail souligne certains points importants à aborder et approfondir dans le domaine, pour construire une compréhension plus vaste et détaillée de l’évolution biologique en milieu urbain.
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Urban environments pose different selective pressures than natural ones, leading to changes in animal behavior, physiology, and morphology. Understanding how animals respond to urbanization could inform the management of urban habitats. Non-avian reptiles have important roles in ecosystems worldwide, yet their responses to urbanization have not been as comprehensively studied as those of mammals and birds. However, unlike mammals and birds, most reptiles cannot easily move away from disturbances, making the selective pressure to adapt to urban environments especially strong. In recent years, there has been a surge in research on the responses of lizards to urbanization, yet no formal synthesis has determined what makes an urban lizard, in other words, which phenotypic traits are most likely to change with urbanization and in which direction? Here, we present a qualitative synthesis of the literature and a quantitative phylogenetic meta-analysis comparing phenotypic traits between urban and non-urban lizard populations. The most robust finding from our analysis is that urban lizards are larger than their non-urban counterparts. This result remained consistent between sexes and taxonomic groups. Hence, lizards that pass through the urban filter have access to better resources, more time for foraging, and/or there is selection on attaining a larger body size. Other results included an increase in the diameters of perches used and longer limb and digit lengths, although this may be a result of increased body size. Urban lizards were not bolder, more active or exploratory, and did not differ in immune responses than non-urban populations. Overall, studies are biased to a few geographic regions and taxa. More than 70% of all data came from three species of anoles in the family Dactyloidae, making it difficult to generalize patterns to other clades. Thus, more studies are needed across multiple taxa and habitats to produce meaningful predictions that could help inform conservation and management of urban ecological communities.
Introduction
Rapid environmental change driven by urbanisation offers a unique insight into the adaptive potential of urban‐dwelling organisms. Urban‐driven phenotypic differentiation is increasingly often demonstrated, but the impact of urbanisation (here modelled as the percentage of impervious surface (ISA) around each nestbox) on offspring developmental rates and subsequent survival remains poorly understood. Furthermore, the role of selection on urban‐driven phenotypical divergence was rarely investigated to date.
Methods and Results
Data on nestling development and body mass were analysed in a gradient of urbanisation set in Warsaw, Poland, in two passerine species: great tits (Parus major ) and blue tits (Cyanistes caeruleus ). Increasing levels of impervious surface area (ISA) delayed the age of fastest growth in blue tits. Also, nestling body mass was negatively affected by increasing ISA 5 and 10 days after hatching in great tits, and 10 and 15 days in blue tits, respectively. High levels of ISA also increased nestling mortality 5 and 10 days after hatching in both species. An analysis of selection differentials performed for two levels of urbanisation (low and high ISA) revealed a positive association between mass at day 2 and survival at fledging.
Discussion
This study confirms the considerable negative impact of imperviousness –a proxy for urbanisation level‐ on offspring development, body mass and survival, and highlights increased selection on avian mass at hatching in a high ISA environment.
The altered ecological and environmental conditions in towns and cities strongly affect demographic traits of urban animal populations, for example avian reproductive success is often reduced. Previous work suggests that this is partly driven by low insect availability during the breeding season, but robust experimental evidence that supports this food limitation hypothesis is not yet available.
We tested core predictions of the food limitation hypothesis using a controlled experiment that provided supplementary insect food (nutritionally enhanced mealworms supplied daily to meet 40%–50% of each supplemented brood's food requirements) to great tit nestlings in urban and forest habitats.
We measured parental provisioning rates and estimated the amount of supplementary food consumed by control and experimental nestlings, and assessed their body size and survival rates.
Provisioning rates were similar across habitats and control and supplemented broods, but supplemented (and not control) broods consumed large quantities of supplementary food. As predicted by the food limitation hypothesis we found that nestlings in (a) urban control broods had smaller body size and nestling survival rates than those in forest control broods; (b) forest supplemented and control broods had similar body size and survival rates; (c) urban supplemented nestlings had larger body size and survival rates than those in urban control broods; and crucially (d) urban supplemented broods had similar body size and survival rates to nestlings in forest control broods.
Our results provide rare experimental support for the strong negative effects of food limitation during the nestling rearing period on urban birds' breeding success. Furthermore, the fact that supplementary food almost completely eliminated habitat differences in survival rate and nestling body size suggest that urban stressors other than food shortage contributed relatively little to the reduced avian breeding success. Finally, given the impacts of the amount of supplementary food that we provided and taking clutch size differences into account, our results suggest that urban insect populations in our study system would need to be increased by a factor of at least 2.5 for urban and forest great tits to have similar reproductive success.
The world is urbanising rapidly, and it is predicted that by 2050, 66% of the global human population will be living in urban areas. Urbanisation is characterised by land-use changes such as increased residential housing, business development and transport infrastructure, resulting in habitat loss and fragmentation. Over the past two decades, interest has grown in how urbanisation influences fundamental aspects of avian biology such as life-history strategies, survival, breeding performance, behaviour and individual health. Here, we review current knowledge on how urbanisation influences the nesting biology of birds, which determines important fitness-associated processes such as nest predation and community assembly. We identify three major research areas: (i) nest sites of birds in urban areas, (ii) the composition of their nests, and (iii) how these aspects of their nesting biology influence their persistence (and therefore conservation efforts) in urban areas. We show that birds inhabiting urban areas nest in a wide variety of locations, some beneficial through exploitation of otherwise relatively empty avian ecological niches, but others detrimental when birds breed in ecological traps. We describe urban-associated changes in nesting materials such as plastic and cigarette butts, and discuss several functional hypotheses that propose the adaptive value and potential costs of this new nesting strategy. Urban areas provide a relatively new habitat in which to conserve birds, and we show that nestboxes and other artificial nest sites can be used successfully to conserve some, but not all, bird species. Finally, we identify those subject areas that warrant further research attention in the hope of advancing our understanding of the nesting biology of birds in urban areas.
Urban landscapes are associated with abiotic and biotic environmental changes that may result in potential stressors for wild vertebrates. Urban exploiters have physiological, morphological, and behavioral adaptations to live in cities. However, there is increasing evidence that urban exploiters themselves can suffer from urban conditions, especially during specific life‐history stages. We looked for a link between the degree of urbanization and the level of developmental stress in an urban exploiter (the house sparrow, Passer domesticus), which has recently been declining in multiple European cities (e.g., London, UK). Specifically, we conducted a large‐scale study and sampled juvenile sparrows in 11 urban and rural sites to evaluate their feather corticosterone (CORT) levels. We found that juvenile feather CORT levels were positively correlated with the degree of urbanization, supporting the idea that developing house sparrows may suffer from urban environmental conditions. However, we did not find any correlation between juvenile feather CORT levels and body size, mass, or body condition. This suggests either that the growth and condition of urban sparrows are not impacted by elevated developmental CORT levels, or that urban sparrows may compensate for developmental constraints once they have left the nest. Although feather CORT levels were not correlated with baseline CORT levels, we found that feather CORT levels were slightly and positively correlated with the CORT stress response in juveniles. This suggests that urban developmental conditions may potentially have long‐lasting effects on stress physiology and stress sensitivity in this urban exploiter.
Rapid urbanization has become an area of crucial concern in conservation owing to the radical changes in habitat structure and loss of species engendered by urban and suburban development. Here, we draw on recent mechanistic ecological studies to argue that, in addition to altered habitat structure, three major processes contribute to the patterns of reduced species diversity and elevated abundance of many species in urban environments. These activities, in turn, lead to changes in animal behavior, morphology and genetics, as well as in selection pressures on animals and plants. Thus, the key to understanding urban patterns is to balance studying processes at the individual level with an integrated examination of environmental forces at the ecosystem scale.
Many ecological and evolutionary processes are affected by urbanization, but cities vary by orders of magnitude in their human population size and areal extent. To quantify and manage urban biodiversity, one must understand both how biodiversity scales with city size, and how ecological, evolutionary, and socioeconomic drivers of biodiversity scale with city size. We show how environmental abiotic and biotic drivers, as well as human cultural and socioeconomic drivers, may act through ecological and evolutionary processes differently, at different scales, to influence patterns in urban biodiversity. Because relationships likely take linear and nonlinear forms, the need to describe the specific scaling relationships is highlighted, including deviations and potential inflection points, where different management strategies may successfully conserve urban biodiversity.
The field of urban ecology has provided many fascinating examples of organisms that display novel biological features in urban environments compared to natural habitats. Quantitative genetics provides a framework that can be used to investigate whether this phenotypic differentiation between urban and natural habitats is adaptive and is the result of heritable changes in response to divergent selection. New generation sequencing tools offer unique opportunities to expand our understanding of the genes and genetic mechanisms implicated in evolution in urban environments. This chapter first reviews quantitative genetics studies investigating the mechanisms of evolution in the city. It then reviews pioneering genomic studies that have shed light on the genes and genetic mechanisms implicated in urban microevolution. The authors discuss how further use of cost-effective high-resolution genomic approaches may improve the comprehension of both genomic and epigenomic mechanisms implicated in such evolution. Finally, the chapter provides an overview of how the integrated use of quantitative genetics, field experiments, and genomics could expand our knowledge of the processes leading to urban evolution.
Research in urban evolution requires that the features of cities are accurately captured for input into evolutionary models. Until recently, the evolutionary effects of cities have often been addressed using single sites, dichotomous urban–rural contrasts or, to a lesser extent, using urban gradients. However, urbanization does not produce a homogenous spatial continuum: cities are highly heterogeneous environments, with sharp and often non-linear environmental changes related to the amount of impervious surface, green vegetation, air pollution, light, noise, or contrasted temperature profiles. The comprehensive quantification of urban heterogeneity in space and time is essential for exploring the origins of organismal variation and adaptation in cities, and to best identify the strength and directionality of selective pressures and neutral processes occurring in populations of urban organisms. This chapter reviews frameworks that can be used to describe and quantify urbanization—these include classical ecological frameworks, the understudied temporal dimension of urban evolutionary biology, and the concept of replicated insight into urban-driven evolutionary processes. The chapter further discusses how axes of variation capturing the urban environment can be quantified with univariate and multivariate approaches, and presents quantitative results on how urbanization is captured in published studies of urban evolution. Finally, it discusses study design and statistical approaches of interest when testing for urban evolution: these include the question of model selection and variable fitting, spatial autocorrelation, and appropriate scale use in studies of urban evolution.
Articles E cologists have long debated what factors control the trophic (feeding) structure and function of ecosystems. This is more than just a matter of determining "who eats whom"; ecologists have pondered whether there are fundamental rules for determining (a) how many trophic levels an ecosystem can support, (b) how much primary production is consumed by herbivores, and (c) whether resources from the bottom of the food chain, or consumers from the top, control biomass, abundance, and species diversity in food webs. These questions are not only fundamental to ecology but essential for conservation and management. For example, the loss of a top predator in a food web that is largely controlled by top-down forces may drastically alter biodiversity and ecosystem function (e.g., nutrient cycling), whereas the same loss may have little effect in a resource-controlled (i.e., bottom-up) food web. To answer these questions, ecologists have expended an enormous effort to understand the relative importance of pre-dation or parasitism (and, to a lesser extent, mutualism) and competition for resources in trophic organization. Three basic models of control of trophic structure have emerged from this endeavor. The first of these, the energetic model of food webs, holds that energy supply (from the bottom of food webs), in concert with the relative efficiencies of consumers, limits the number of trophic levels and the relative biomass of each level in natural ecosystems (Lindeman 1942). The second model, commonly known as the "green world" hypothesis (Hairston et al. 1960), states that predators and parasites exert top-down control on herbivore populations. According to this model, herbivores do not generally compete with each other, and plant resources are not limiting because herbivore population densities remain low as a result of top-down control. The third model (Menge and Sutherland 1987) hypothesizes that the relative effects of predation on species diversity vary as a function of environmental stress (e.g., exposure, desiccation, extreme temperatures) and productivity. Specifically, the Menge-Sutherland model suggests that pre-dation should be more important at low and intermediate levels of stress, because high stress limits the abundance of predators more than it limits herbivore competitors. Competition for resources should be more important at high levels of stress (and low levels of productivity). Various modifications and elaborations of these three basic models of food webs and trophic structure have proliferated in the past several decades (Oksanen et al. 1981, Power 1992). Empirical tests of the food web models, and modifications thereof, have been conducted mostly in non-human-dominated ecosystems ranging from marine environments to freshwater lakes and streams, tundra, deserts, forests, and grasslands, each test often producing a different answer (Con-nell 1983, Schoener 1983, Sih et al. 1985). Empirical tests and the development of theory for food web dynamics have historically involved human-dominated ecosystems, such as agroecosystems (Rosenheim 1998), or recovering agricul-Stanley H. Human activities dramatically change the abundance, diversity, and composition of species. However, little is known about how the most intense human activity, urbanization, alters food webs and trophic structure in biological communities. Studies of the Phoenix area, situated amid the Sonoran Desert, reveal some surprising alterations in the control of trophic dynamics. Species composition is radically altered, and resource subsidies increase and stabilize productivity. Changes in productivity dampen seasonal and yearly fluctuations in species diversity, elevate abundances, and alter feeding behaviors of some key urban species. In urban systems-in contrast to the trophic systems in outlying deserts, which are dominated by limiting resources-predation by birds becomes the dominant force controlling arthropods on plants. Reduced predation risk elevates the abundance of urban birds and alters their foraging behavior such that they exert increased top-down effects on arthropods. Shifts in control of food web dynamics are probably common in urban ecosystems, and are influenced by complex human social processes and feedbacks.