Repeated genomic signatures of adaptation to urbanisation in a songbird across Europe

Salmón, Pablo; Jacobs, Arne; Ahrén, Dag; Biard, Clotilde; Nj, Dingemanse; Dominoni, Davide M.; Helm, Barbara; Lundberg, Max; Senar, Juan Carlos; Sprau, Philipp; Me, Visser; Isaksson, Caroline

doi:10.1101/2020.05.05.078568

Cited by 11 publications

(19 citation statements)

References 59 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Besides, the gene ontology enrichment analysis, performed on the entire set of genes identified via the outlier genome scan, reinforced these findings since multiple enriched GO terms were associated with the nervous system and stress response as well as hormonal response. These results are informative on the type of traits involved in avian urban adaptation in cities and corroborate previous results from (22, 60, 61) suggesting that natural selection repeatedly acted on neuronal, behavioural and cognitive traits that could contribute to the phenotypic shifts described in urban great tits (i.e. more aggressive and exploratory birds, with higher breath rate: 62, 63 & Caizergues et al in prep )…”

Section: Discussionsupporting

confidence: 89%

“…It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for this this version posted February 10, 2021. ; https://doi.org/10.1101/2021.02.10.430452 doi: bioRxiv preprint to be greater in urban areas than in any other habitat types, including non-urban anthropogenic contexts (18,19). The exploration of the molecular mechanisms implicated in urban-driven phenotypic changes has only begun, with both genetic (20)(21)(22), and epigenetic investigations (23)(24)(25). For instance, DNA methylation variations have been associated in vertebrates with high levels of traffic-related air pollution (e.g.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

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

Grégoire

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

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 (ie parallel) 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.

show abstract

Section: Discussionsupporting

confidence: 89%

Section: Introductionmentioning

confidence: 99%

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

Grégoire

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Clearly, we have only touched on haplotype-based methods to infer adaptation here, and this will be the subject of future work. Environmental association approaches are also highly suited to detecting adaptation in widespread continental species [71,72], and further work will test how variation in the environment has shaped patterns of genomic variation in great tits [73]. This combination of environmental and genomic data in species such as great tits, in which a wealth of ecological and genomic resources are available, is likely to generate interesting insights into the the genetic and phenotypic basis of natural selection.…”

Section: Genomic Landscapes Of Differentiationmentioning

confidence: 99%

The great tit HapMap project: a continental-scale analysis of genomic variation in a songbird

Spurgin

Bosse²,

Albayrak

et al. 2019

Preprint

Self Cite

View full text Add to dashboard Cite

85A major aim of evolutionary biology is to understand why patterns of genomic variation vary among 86 populations and species. Large-scale genomic studies of widespread species are useful for studying how 87 the environment and demographic history shape patterns of genomic divergence, and with the continually 88 decreasing cost of sequencing, such studies are now becoming feasible. Here, we carry out one of the most 89 comprehensive surveys of genomic variation in a wild vertebrate to date; the great tit (Parus major) HapMap 90 project. We screened ca 500,000 SNP markers across 647 individuals from 29 populations, spanning almost 91 the entire geographic range of the European great tit subspecies. We found that genome-wide variation was 92 consistent with a recent colonisation across Europe from a single refugium in the Balkans and/or Turkey, with 93 bottlenecks and reduced genetic diversity in island populations. Differentiation across the genome was highly 94 heterogeneous, with clear "islands of differentiation" even among populations which are ostensibly panmictic. 95These islands of differentiation were consistently found in regions of low recombination, suggesting that 96 background selection can rapidly promote population differentiation among even the most recently colonised 97 populations. We also detected genomic outlier regions that were unique to peripheral great tit populations, 98 most likely as a result of recent directional selection at the range edges of this species. These "unique" 99 outlier regions contained candidate genes for morphology, thermal adaptation and colouration, supporting 100 previous research in this species, and providing avenues for future investigation. Our study suggests that 101 comprehensive screens of genomic variation in wild organisms can provide unique insights into evolution. 102Author summary 103 Studying patterns of genetic variation is a useful way of determining why populations and species differ in 104 nature. Genetic variation is shaped by natural selection, but also by the present and past size of populations, 105 the amount of migration, and by features of the genome, such as variation in recombination rate, of the 106 organism being studied. Teasing apart the effects of these different processes on genomic diversity is difficult, 107 but one way that this can be achieved is by studying genomic variation across the entire range of a species. 108 We performed a continental-scale analysis of genetic variation in the great tit -a widespread songbird that 109 has been the focus of extensive ecological research. We first used genomic data to reconstruct the historical 110 colonisation of great tits across Europe, and showed that during the last ice age, this species was likely 111 restricted to a single region in Eastern Europe, from which they spread across the continent. We then 112 studied how patterns of variation differ along the genome, and show that recombination rate is a key driver 113 of variation among all populations. Importantly, by comparing ma...

show abstract

“…Genomic and epigenomic studies offer great potential to understand evolution in cities, yet they remain few and far between (Rivkin et al, 2019;Schell, 2018). While some studies have found genomic signatures of urban adaptation (Harris et al, 2013;Salmón et al, 2020) and consistent differences at the transcriptomic level (Watson et al, 2017), others have found no genetic structure among urban and nonurban congeners (Khimoun et al, 2020). Modifications in DNA methylation have been shown to associate with anthropogenic-linked factors including feeding on anthropogenic-provided food in baboons (Lea et al, 2016), exposure to pollution in humans (Baccarelli et al, 2009), and stress resilience in response to handling in tree swallows (Taff et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Urbanization is associated with modifications in DNA methylation in a small passerine bird

Watson

Powell

Salmón

et al. 2020

Evolutionary Applications

Self Cite

View full text Add to dashboard Cite

Urbanization represents a fierce driver of phenotypic change, yet the molecular mechanisms underlying observed phenotypic patterns are poorly understood. Epigenetic changes are expected to facilitate more rapid adaption to changing or novel environments, such as our towns and cities, compared with slow changes in gene sequence. A comparison of liver and blood tissue from great tits Parus major originating from an urban and a forest site demonstrated that urbanization is associated with variation in genome‐wide patterns of DNA methylation. Combining reduced representation bisulphite sequencing with transcriptome data, we revealed habitat differences in DNA methylation patterns that suggest a regulated and coordinated response to the urban environment. In the liver, genomic sites that were differentially methylated between urban‐ and forest‐dwelling birds were over‐represented in regulatory regions of the genome and more likely to occur in expressed genes. DNA methylation levels were also inversely correlated with gene expression at transcription start sites. Furthermore, differentially methylated CpG sites, in liver, were over‐represented in pathways involved in (i) steroid biosynthesis, (ii) superoxide metabolism, (iii) secondary alcohol metabolism, (iv) chylomicron remodelling, (v) cholesterol transport, (vi) reactive oxygen species (ROS) metabolic process and (vii) epithelial cell proliferation. This corresponds with earlier studies identifying diet and exposure to ROS as two of the main drivers of divergence between organisms in urban and nonurban environments. Conversely, in blood, sites that were differentially methylated between urban‐ and forest‐dwelling birds were under‐represented in regulatory regions, more likely to occur in nonexpressed genes and not over‐represented in specific biological pathways. It remains to be determined whether diverging patterns of DNA methylation represent adaptive evolutionary responses and whether the conclusions can be more widely attributed to urbanization.

show abstract

Repeated genomic signatures of adaptation to urbanisation in a songbird across Europe

Cited by 11 publications

References 59 publications

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

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

The great tit HapMap project: a continental-scale analysis of genomic variation in a songbird

Urbanization is associated with modifications in DNA methylation in a small passerine bird

Contact Info

Product

Resources

About