Effects of urban-induced mutations on ecology, evolution and health.

Increasing evidence suggests that urbanization is associated with higher mutation rates, which can affect the health and evolution of organisms that inhabit cities. Elevated pollution levels in urban areas can induce DNA damage, leading to de novo mutations. Studies on mutations induced by urban pollution are most prevalent in humans and microorganisms, whereas studies of non-human eukaryotes are rare, even though increased mutation rates have the potential to affect organisms and their populations in contemporary time. Our Perspective explores how higher mutation rates in urban environments could impact the fitness, ecology and evolution of populations. Most mutations will be neutral or deleterious, and higher mutation rates associated with elevated pollution in urban populations can increase the risk of cancer in humans and potentially other species. We highlight the potential for urban-driven increased deleterious mutational loads in some organisms, which could lead to a decline in population growth of a wide diversity of organisms. Although beneficial mutations are expected to be rare, we argue that higher mutation rates in urban areas could influence adaptive evolution, especially in organisms with short generation times. Finally, we explore avenues for future research to better understand the effects of urban-induced mutations on the fitness, ecology and evolution of city-dwelling organisms.

The plastic homes of hermit crabs in the Anthropocene.

Plastic is the most pervasive element of marine waste, with harmful impact on wildlife. By using iEcology (i.e., internet Ecology, use of online data sources as a new tool in ecological research), we report on the emergence of a novel behaviour in hermit crabs related to the use of plastic or other anthropogenic materials as protective shells. We analysed images posted on social media to identify 386 individuals with artificial shells - mainly plastic caps (85 %). We report that 10 of the world's 16 terrestrial hermit crabs use artificial shells, a behaviour observed on all of the Earth's tropical coasts. Four non-exclusive mechanisms may drive individual choice for artificial shells: sexual signaling, lightness of artificial shells, odour cues, and camouflage in a polluted environment. Further research is needed to determine the impact of this behaviour on hermit crab evolutionary trajectories.

Extra-pair paternity, breeding density, and synchrony in natural cavities versus nestboxes in two passerine birds.

Most of what is known about extra-pair paternity in hole-nesting birds derives from studies using artificial nesting sites, such as nestboxes. However, it has rarely been investigated whether inference drawn from breeding events taking place in nestboxes matches what would be observed under natural conditions, that is, in natural cavities. We here report on a variation in promiscuity in blue tits and great tits nesting in natural cavities and nestboxes in an urban forest in Warsaw, Poland. Specifically, we tested whether local breeding density, local breeding synchrony, and extra-pair paternity (inferred from SNP data generated with a high-throughput genotyping by sequencing method) differed between birds nesting in natural cavities and nestboxes. In both blue tits and great tits, the frequency of extra-pair paternity was similar between the two cavity types. In blue tits, we observed shorter nearest neighbor distance, higher neighbor density, and higher synchronous neighbor density (i.e., density of fertile females) in nestboxes relative to natural cavities. No such pattern was found in great tits. Moreover, we detected a positive relationship between the proportion of extra-pair offspring in the nest and neighbor density around the nest in blue tits. Our results revealed that the provisioning of nestboxes did not change rates of extra-pair paternity, suggesting that conclusions drawn from nestbox studies might adequately represent the natural variation in extra-pair matings in some species or sites. However, the observed differences in spatiotemporal components of breeding dynamics highlight the fact that these parameters should be carefully considered when comparing mating behavior across studies and/or sites.

Breeding in the pandemic: short-term lockdown restrictions in a European capital city did not alter the life-history traits of two urban adapters.

Humans are transforming natural habitats into managed urban green areas and impervious surfaces at an unprecedented pace. Yet the effects of human presence per se on animal life-history traits are rarely tested. This is particularly true in cities, where human presence is often indissociable from urbanisation itself. The onset of the SARS-CoV-2 outbreak, along with the resulting lockdown restrictions, offered a unique, "natural experiment" to investigate wildlife responses to a sudden reduction in human activity. We analysed four years of avian breeding data collected in a European capital city to test whether lockdown measures altered nestbox occupancy and life-history traits in terms of egg laying date, incubation duration and clutch size in two urban adapters: great tits (Parus major) and blue tits (Cyanistes caeruleus). Lockdown measures, which modulated human presence, did not influence any of the life-history traits investigated. In contrast, the interaction between year and tree cover, a distinct ecological attribute of the urban space, was positively associated with clutch size, a key avian life-history and reproductive trait. This highlights the importance of inter-year variation and habitat quality over human activity on urban wildlife reproduction. We discuss our results in the light of other urban wildlife studies carried out during the pandemic, inviting the scientific community to carefully interpret all lockdown-associated shifts in biological traits. Supplementary Information: The online version contains supplementary material available at 10.1007/s11252-022-01309-5.

Moving past the challenges and misconceptions in urban adaptation research.

Although the field of urban evolutionary ecology has recently expanded, much progress has been made in identifying adaptations that arise as a result of selective pressures within these unique environments. However, as studies within urban environments have rapidly increased, researchers have recognized that there are challenges and opportunities in characterizing urban adaptation. Some of these challenges are a consequence of increased direct and indirect human influence, which compounds long-recognized issues with research on adaptive evolution more generally. In this perspective, we discuss several common research challenges to urban adaptation related to (1) methodological approaches, (2) trait-environment relationships and the natural history of organisms, (3) agents and targets of selection, and (4) habitat heterogeneity. Ignoring these challenges may lead to misconceptions and further impede our ability to draw conclusions regarding evolutionary and ecological processes in urban environments. Our goal is to first shed light on the conceptual challenges of conducting urban adaptation research to help avoid the propagation of these misconceptions. We further summarize potential strategies to move forward productively to construct a more comprehensive picture of urban adaptation, and discuss how urban environments also offer unique opportunities and applications for adaptation research.

Preserving avian blood and DNA sampled in the wild: A survey of personal experiences.

Collecting and storing biological material from wild animals in a way that does not deteriorate DNA quality for subsequent analyses is instrumental for research in ecology and evolution. Our aims were to gather reports on the effectiveness of methods commonly used by researchers for the field collection and long-term storage of blood samples and DNA extracts from wild birds. Personal experiences were collected with an online survey targeted specifically at researchers sampling wild birds. Many researchers experienced problems with blood sample storage but not with DNA extract storage. Storage issues generated problems with obtaining adequate DNA quality and sufficient DNA quantity for the targeted molecular analyses but were not related to season of blood sampling, access to equipment, transporting samples, temperature, and method of blood storage. Final DNA quality and quantity were also not affected by storage time before DNA extraction or the methods used to extract DNA. We discuss practical aspects of field collection and storage and provide some general recommendations, with a list of pros and cons of different preservation methods of avian blood samples and DNA extracts.

A global horizon scan for urban evolutionary ecology.

Research on the evolutionary ecology of urban areas reveals how human-induced evolutionary changes affect biodiversity and essential ecosystem services. In a rapidly urbanizing world imposing many selective pressures, a time-sensitive goal is to identify the emergent issues and research priorities that affect the ecology and evolution of species within cities. Here, we report the results of a horizon scan of research questions in urban evolutionary ecology submitted by 100 interdisciplinary scholars. We identified 30 top questions organized into six themes that highlight priorities for future research. These research questions will require methodological advances and interdisciplinary collaborations, with continued revision as the field of urban evolutionary ecology expands with the rapid growth of cities.

Coping with novelty across an urban mosaic: Provisioning latency increases closer to roads and is associated with species-specific reproductive success in two urban adapters.

Most research on urban avian ecology has focused on population- and community-level phenomena, whereas fewer studies have examined how urbanization affects individual behavioral responses to a sudden and novel stimulus, and how those translate to fitness. We measured between-individual variation in provisioning latency in two urban adapters - great tits and blue tits - in response to an infrared camera installed in the nestbox, encountered when offspring in the nest were at the peak of food demand (9-10-days old). For each nestbox, we quantified urbanization as intensity in human activity, distance to road and proportion of impervious surface area. In both species, provisioning latency increased closer to roads. Moreover, increased provisioning latency when exposed to a novel object was associated with higher reproductive success in great tits whose nestboxes were surrounded by high amounts of impervious surface. In contrast, increased provisioning latency was consistently associated with lower reproductive success in blue tits. Our results suggest that provisioning latency changes in relation to the environment surrounding the nest, and may be context- and species-specific when exposed to a novel stimulus, such as a novel object in the nest. To better understand the role of initial behavioral responses towards novelty across an individual's lifetime and, ultimately, its impact on fitness in the urban mosaic, further research explicitly testing different behavioral responses across the entire breeding cycle in wild model systems is needed.

The extended avian urban phenotype: anthropogenic solid waste pollution, nest design, and fitness.

Solid waste pollution (garbage discarded by humans, such as plastic, metal, paper) has received increased attention given its importance as a global threat to biodiversity. Recent studies highlight how animals incorporate anthropogenic materials into their life-cycle, for example in avian nest construction. While increasingly monitored in natural areas, the influence of solid waste pollution on wildlife has been seldom explored in the urban habitat. There is limited data on the relationship between anthropogenic solid waste pollution, nest design, and reproductive success in an urban context. We address this knowledge gap (i) by investigating the presence of environmental solid waste pollution in the breeding habitats of great tits Parus major and blue tits Cyanistes caeruleus reproducing in a gradient of urbanisation, and (ii) by quantifying (ii) the contribution of different anthropogenic materials in their nests. We further examine potential drivers of solid waste pollution by inferring three distinct properties of the urban space: environmental solid waste pollution on the ground, human presence, and the intensity of urbanisation (e.g impervious surfaces) in nestbox vicinity. Finally, (iii) we explore the relationship between anthropogenic nest materials and reproductive success. We found that environmental solid waste pollution was positively associated with human presence and urbanisation intensity. There was also a positive relationship between increased human presence and the amount of anthropogenic materials in great tit nests. Interestingly, in both species, anthropogenic nest materials covaried negatively with nest materials of animal origin (fur and feathers). We suggest that fur and feathers - key insulating materials in nest design - may be scarcer in areas with high levels of human presence, and are consequently replaced with anthropogenic nest materials. Finally, we report a negative relationship between anthropogenic nest materials and blue tit reproductive success, suggesting species-specific vulnerability of urban birds to solid waste pollution.

Changes to the gut microbiota of a wild juvenile passerine in a multidimensional urban mosaic.

Urbanisation is a major anthropogenic perturbation presenting novel ecological and evolutionary challenges to wild populations. Symbiotic microorganisms residing in the gastrointestinal tracts (gut) of vertebrates have mutual connections with host physiology and respond quickly to environmental alterations. However, the impact of anthropogenic changes and urbanisation on the gut microbiota remains poorly understood, especially in early development. To address this knowledge gap, we characterised the gut microbiota of juvenile great tits (Parus major) reared in artificial nestboxes and in natural cavities in an urban mosaic, employing two distinct frameworks characterising the urban space. Microbial diversity was influenced by cavity type. Alpha diversity was affected by the amount of impervious surface surrounding the breeding location, and positively correlated with tree cover density. Community composition differed between urban and rural sites: these alterations covaried with sound pollution and distance to the city centre. Overall, the microbial communities reflect and are possibly influenced by the heterogeneous environmental modifications that are typical of the urban space. Strikingly, the choice of framework and environmental variables characterising the urban space can influence the outcomes of such ecological studies. Our results open new perspectives to investigate the impact of microbial symbionts on the adaptive capacity of their hosts.

Epigenetics and the city: Non-parallel DNA methylation modifications across pairs of urban-forest Great tit populations.

Identifying the molecular mechanisms involved in rapid adaptation to novel environments and determining their predictability are central questions in evolutionary biology and pressing issues due to rapid global changes. Complementary to genetic responses to selection, faster epigenetic variations such as modifications of DNA methylation may play a substantial role in rapid adaptation. In the context of rampant urbanization, joint examinations of genomic and epigenomic mechanisms are still lacking. Here, we investigated genomic (SNP) and epigenomic (CpG methylation) responses to urban life in a passerine bird, the Great tit (Parus major). To test whether urban evolution is predictable (i.e. parallel) or involves mostly nonparallel molecular processes among cities, we analysed both SNP and CpG methylation variations across three distinct pairs of city and forest Great tit populations in Europe. Our analyses reveal a polygenic response to urban life, with both many genes putatively under weak divergent selection and multiple differentially methylated regions (DMRs) between forest and city great tits. DMRs mainly overlapped transcription start sites and promotor regions, suggesting their importance in modulating gene expression. Both genomic and epigenomic outliers were found in genomic regions enriched for genes with biological functions related to the nervous system, immunity, or behavioural, hormonal and stress responses. Interestingly, comparisons across the three pairs of city-forest populations suggested little parallelism in both genetic and epigenetic responses. Our results confirm, at both the genetic and epigenetic levels, hypotheses of polygenic and largely nonparallel mechanisms of rapid adaptation in novel environments such as urbanized areas.

Replicated, urban-driven exposure to metallic trace elements in two passerines.

While there are increasing examples of phenotypic and genotypic differences between urban and non-urban populations of plants and animals, few studies identified the mechanisms explaining those dissimilarities. The characterization of the urban landscape, which can only be achieved by measuring variability in relevant environmental factors within and between cities, is a keystone prerequisite to understand the effects of urbanization on wildlife. Here, we measured variation in bird exposure to metal pollution within 8 replicated urbanization gradients and within 2 flagship bird species in urban evolutionary ecology: the blue tit (Cyanistes caeruleus) and the great tit (Parus major). We report on a highly significant, positive linear relationship between the magnitude of urbanization-inferred as either tree cover, impervious surface cover, or an urbanization score computed from several environmental variables, and copper, zinc and lead concentrations in bird feathers. The reverse relationship was measured in the case of mercury, while cadmium and arsenic did not vary in response to the urbanization level. This result, replicated across multiple cities and two passerine species, strongly suggests that copper, zinc, lead and mercury pollution is likely to trigger the emergence of parallel responses at the phenotypic and/or genotypic level between urban environments worldwide.

Growing in the city: Urban evolutionary ecology of avian growth rates.

INTRODUCTION: Rapid environmental change driven by urbanization offers a unique insight into the adaptive potential of urban-dwelling organisms. Urban-driven phenotypic differentiation is increasingly often demonstrated, but the impact of urbanization (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 phenotypic divergence was rarely investigated to date. METHODS AND RESULTS: Data on nestling development and body mass were analysed in a gradient of urbanization 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. Nestling body mass was also 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 urbanization (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 urbanization level-on offspring development, body mass and survival, and highlights increased selection on avian mass at hatching in a high ISA environment.

Socio-eco-evolutionary dynamics in cities.

Cities are uniquely complex systems regulated by interactions and feedbacks between nature and human society. Characteristics of human society-including culture, economics, technology and politics-underlie social patterns and activity, creating a heterogeneous environment that can influence and be influenced by both ecological and evolutionary processes. Increasing research on urban ecology and evolutionary biology has coincided with growing interest in eco-evolutionary dynamics, which encompasses the interactions and reciprocal feedbacks between evolution and ecology. Research on both urban evolutionary biology and eco-evolutionary dynamics frequently focuses on contemporary evolution of species that have potentially substantial ecological-and even social-significance. Still, little work fully integrates urban evolutionary biology and eco-evolutionary dynamics, and rarely do researchers in either of these fields fully consider the role of human social patterns and processes. Because cities are fundamentally regulated by human activities, are inherently interconnected and are frequently undergoing social and economic transformation, they represent an opportunity for ecologists and evolutionary biologists to study urban "socio-eco-evolutionary dynamics." Through this new framework, we encourage researchers of urban ecology and evolution to fully integrate human social drivers and feedbacks to increase understanding and conservation of ecosystems, their functions and their contributions to people within and outside cities.

The association between stressors and telomeres in non-human vertebrates: a meta-analysis.

Animal response to stressors such as harsh environmental conditions and demanding biological processes requires energy generated through increased mitochondrial activity. This results in the production of reactive oxygen species (ROS). In vitro and some in vivo studies suggest that oxidative damage of DNA caused by ROS is responsible for telomere shortening. Since telomere length is correlated with survival in many vertebrates, telomere loss is hypothesised to trigger cellular ageing and/ or to reflect the harshness of the environment an individual has experienced. To improve our understanding of stress-induced telomere dynamics in non-human vertebrates, we analysed 109 relevant studies in a meta-analytical framework. Overall, the exposure to possible stressors was associated with shorter telomeres or higher telomere shortening rate (average effect size = -0.16 ± 0.03). This relationship was consistent for all phylogenetic classes and for all a priori-selected stressor categories. It was stronger in the case of pathogen infection, competition, reproductive effort and high activity level, which emphasises their importance in explaining intraspecific telomere length variability and, potentially, lifespan variability. Interestingly, the association between stressor exposure and telomeres in one hand, and oxidative stress in the other hand, covaried, suggesting the implication of oxidative stress in telomere dynamics.

Great tits and the city: Distribution of genomic diversity and gene-environment associations along an urbanization gradient.

Urbanization is a growing concern challenging the evolutionary potential of wild populations by reducing genetic diversity and imposing new selection regimes affecting many key fitness traits. However, genomic footprints of urbanization have received little attention so far. Using RAD sequencing, we investigated the genomewide effects of urbanization on neutral and adaptive genomic diversity in 140 adult great tits Parus major collected in locations with contrasted urbanization levels (from a natural forest to highly urbanized areas of a city; Montpellier, France). Heterozygosity was slightly lower in the more urbanized sites compared to the more rural ones. Low but significant effect of urbanization on genetic differentiation was found, at the site level but not at the nest level, indicative of the geographic scale of urbanization impact and of the potential for local adaptation despite gene flow. Gene-environment association tests identified numerous SNPs with small association scores to urbanization, distributed across the genome, from which a subset of 97 SNPs explained up to 81% of the variance in urbanization, overall suggesting a polygenic response to selection in the urban environment. These findings open stimulating perspectives for broader applications of high-resolution genomic tools on other cities and larger sample sizes to investigate the consistency of the effects of urbanization on the spatial distribution of genetic diversity and the polygenic nature of gene-urbanization association.

Mediterranean blue tits as a case study of local adaptation.

While the study of the origins of biological diversity across species has provided numerous examples of adaptive divergence, the realization that it can occur at microgeographic scales despite gene flow is recent, and scarcely illustrated. We review here evidence suggesting that the striking phenotypic differentiation in ecologically relevant traits exhibited by blue tits Cyanistes caeruleus in their southern range-edge putatively reflects adaptation to the heterogeneity of the Mediterranean habitats. We first summarize the phenotypic divergence for a series of life history, morphological, behavioural, acoustic and colour ornament traits in blue tit populations of evergreen and deciduous forests. For each divergent trait, we review the evidence obtained from common garden experiments regarding a possible genetic origin of the observed phenotypic differentiation as well as evidence for heterogeneous selection. Second, we argue that most phenotypically differentiated traits display heritable variation, a fundamental requirement for evolution to occur. Third, we discuss nonrandom dispersal, selective barriers and assortative mating as processes that could reinforce local adaptation. Finally, we show how population genomics supports isolation - by - environment across landscapes. Overall, the combination of approaches converges to the conclusion that the strong phenotypic differentiation observed in Mediterranean blue tits is a fascinating case of local adaptation.

Predicting bird phenology from space: satellite-derived vegetation green-up signal uncovers spatial variation in phenological synchrony between birds and their environment.

Population-level studies of how tit species (Parus spp.) track the changing phenology of their caterpillar food source have provided a model system allowing inference into how populations can adjust to changing climates, but are often limited because they implicitly assume all individuals experience similar environments. Ecologists are increasingly using satellite-derived data to quantify aspects of animals' environments, but so far studies examining phenology have generally done so at large spatial scales. Considering the scale at which individuals experience their environment is likely to be key if we are to understand the ecological and evolutionary processes acting on reproductive phenology within populations. Here, we use time series of satellite images, with a resolution of 240 m, to quantify spatial variation in vegetation green-up for a 385-ha mixed-deciduous woodland. Using data spanning 13 years, we demonstrate that annual population-level measures of the timing of peak abundance of winter moth larvae (Operophtera brumata) and the timing of egg laying in great tits (Parus major) and blue tits (Cyanistes caeruleus) is related to satellite-derived spring vegetation phenology. We go on to show that timing of local vegetation green-up significantly explained individual differences in tit reproductive phenology within the population, and that the degree of synchrony between bird and vegetation phenology showed marked spatial variation across the woodland. Areas of high oak tree (Quercus robur) and hazel (Corylus avellana) density showed the strongest match between remote-sensed vegetation phenology and reproductive phenology in both species. Marked within-population variation in the extent to which phenology of different trophic levels match suggests that more attention should be given to small-scale processes when exploring the causes and consequences of phenological matching. We discuss how use of remotely sensed data to study within-population variation could broaden the scale and scope of studies exploring phenological synchrony between organisms and their environment.