Does urbanisation lead to parallel demographic shifts across the world in a cosmopolitan plant?

Urbanisation is occurring globally, leading to dramatic environmental changes that are altering the ecology and evolution of species. In particular, the expansion of human infrastructure and the loss and fragmentation of natural habitats in cities is predicted to increase genetic drift and reduce gene flow by reducing the size and connectivity of populations. Alternatively, the ‘urban facilitation model’ suggests that some species will have greater gene flow into and within cities leading to higher diversity and lower differentiation in urban populations. These alternative hypotheses have not been contrasted across multiple cities. Here, we used the genomic data from the GLobal Urban Evolution project (GLUE), to study the effects of urbanisation on non‐adaptive evolutionary processes of white clover (Trifolium repens) at a global scale. We found that white clover populations presented high genetic diversity and no evidence of reduced Ne linked to urbanisation. On the contrary, we found that urban populations were less likely to experience a recent decrease in effective population size than rural ones. In addition, we found little genetic structure among populations both globally and between urban and rural populations, which showed extensive gene flow between habitats. Interestingly, white clover displayed overall higher gene flow within urban areas than within rural habitats. Our study provides the largest comprehensive test of the demographic effects of urbanisation. Our results contrast with the common perception that heavily altered and fragmented urban environments will reduce the effective population size and genetic diversity of populations and contribute to their isolation

Electronic Supplementary Materials from Urban versus forest ecotypes are not explained by divergent reproductive selection

Increasing urbanization offers a unique opportunity to study adaptive responses to rapid environmental change. Numerous studies have demonstrated phenotypic divergence between urban and rural organisms. However, comparing the direction and magnitude of natural selection between these environments has rarely been attempted. Using seven years of monitoring of nest-box breeding of great tits (<i>Parus major</i>) in the city of Montpellier and in a nearby oak forest, we find phenotypic divergence in four morphological and two life-history traits between urban and forest birds. We then measure reproductive selection on these traits, and compare selection between the habitats. Urban birds had significantly smaller morphological features than their rural counterparts, with a shorter tarsus, lower body mass, and smaller wing and tail lengths relative to their overall body size. While urban female tarsus length was under stabilizing selection, and forest males show positive selection for tarsus length and negative selection for body mass, selection gradients were significantly divergent between habitats only for body mass. Urban great tits also had earlier laying dates and smaller clutches. Surprisingly, we found selection for earlier laying date in the forest but not in the city. Conversely, we detected no linear selection on clutch size in the forest, but positive selection on clutch size in the urban habitat. Overall, these results do not support the hypothesis that contemporary reproductive selection explains differences in morphology and life history between urban- and forest-breeding great tits. We discuss how further experimental approaches will help confirm whether the observed divergence is maladaptive while identifying the environmental drivers behind it

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 nonpara

An avian urban morphotype: how the city environment shapes great tit morphology at different life stages

International audienceUrbanization is a worldwide phenomenon associated with tremendous modifications of natural habitats. Understanding how city dwelling species are affected by those changes is becoming a pressing issue. We presently lack fine scale spatio-temporal studies investigating the impact of urbanization across different life stages and along urbanization gradients. Based on 8 years of monitoring of urban and forest great tits (Parus major), we investigated how city life shapes morphological characteristics at different life stages in the city versus the forest, and within the urban habitat (along naturalness and pedestrian frequency gradients). We found that urban nestlings were significantly smaller than forest ones, but not in lower body condition. Urban breeders showed reduced tarsus, wing and tail lengths compared to forest birds. Within the city, variation in nestling tarsus length and body condition along the naturalness gradient highly depended on the year, with no consistent pattern. For breeders, tarsus length and body condition were positively correlated to the naturalness gradient, although only in 2019 for tarsus, and only in older individuals for body condition. Finally, we found that males had smaller wing lengths in more urbanized parts of the city. These results suggest that urbanization affects morphology early on in development, influencing many morphological attributes. While the mechanisms underlying the urban morphotype remain to be determined, we discuss the potential origins for the documented differences between forest and urban morphotypes, and argue that they most probably result from urban environmental constraints linked to food availability

Epigenetics and the city: non‐parallel DNA methylation modifications across pairs of urban‐rural 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 non-parallel 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 non-parallel mechanisms of rapid adaptation in novel environments such as urbanized areas

Testing for parallel genomic and epigenomic footprints of adaptation to urban life in a passerine bird

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.eparallel) or involves mostly non-parallel molecular processes among cities, we analysed three distinct pairs of city and forest Great tit populations across Europe. Results 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 the modulation gene expression. Both genomic and epigenomic outliers were found in genomic regions enriched for genes with biological functions related to nervous system, immunity, behaviour, 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 non-parallel mechanisms of rapid adaptation in new environments such as urbanized areas