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

View ORCID ProfileAude E. Caizergues, View ORCID ProfileJeremy Le Luyer, View ORCID ProfileArnaud Grégoire, View ORCID ProfileMarta Szulkin, View ORCID ProfileJuan-Carlos Señar, View ORCID ProfileAnne Charmantier, View ORCID ProfileCharles Perrier
doi: https://doi.org/10.1101/2021.02.10.430452
Aude E. Caizergues
1CEFE, Univ Montpellier, CNRS, Univ Paul Valéry Montpellier 3, EPHE, IRD, Montpellier, France
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  • For correspondence: audeemiliecaizergues@gmail.com
Jeremy Le Luyer
2Ifremer, UMR EIO 241, Centre du Pacifique, Taravao, Tahiti, Polynésie française, France
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Arnaud Grégoire
1CEFE, Univ Montpellier, CNRS, Univ Paul Valéry Montpellier 3, EPHE, IRD, Montpellier, France
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Marta Szulkin
3Centre of New Technologies, University of Warsaw, S. Banacha 2c, 02-097 Warsaw, Poland
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Juan-Carlos Señar
4Museu de Ciències Naturals de Barcelona, Parc Ciutadella, 08003 Barcelona, Spain
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Anne Charmantier
1CEFE, Univ Montpellier, CNRS, Univ Paul Valéry Montpellier 3, EPHE, IRD, Montpellier, France
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Charles Perrier
5CBGP, INRAe, CIRAD, IRD, Montpellier SupAgro, Univ. Montpellier, Montpellier, France
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Abstract

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.

Significant statement Urbanization drives, all around the globe, tremendous changes in the ecology of species and in individual phenotypes. Molecular bases of phenotypic shifts and of adaptation to urban environments remain under-explored. In particular, the roles of genetic and epigenetic mechanisms, and their parallelism across cities, are still unknown. We searched for genomic (SNP markers) and epigenomic (CpG methylation) differences between urban and forest populations of great tits in three European locations. We identified several and mostly non-parallel molecular marks associated with urbanization. These marks were however associated to similar biological functions related to the nervous system, behaviour and stress response. This study suggests important roles of de novo genetic and epigenetic variation during adaptation to life in the city.

  • adaptation
  • DNA methylation
  • epigenomics
  • genomics
  • urbanization

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted February 10, 2021.
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Testing for parallel genomic and epigenomic footprints of adaptation to urban life in a passerine bird
Aude E. Caizergues, Jeremy Le Luyer, Arnaud Grégoire, Marta Szulkin, Juan-Carlos Señar, Anne Charmantier, Charles Perrier
bioRxiv 2021.02.10.430452; doi: https://doi.org/10.1101/2021.02.10.430452
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Testing for parallel genomic and epigenomic footprints of adaptation to urban life in a passerine bird
Aude E. Caizergues, Jeremy Le Luyer, Arnaud Grégoire, Marta Szulkin, Juan-Carlos Señar, Anne Charmantier, Charles Perrier
bioRxiv 2021.02.10.430452; doi: https://doi.org/10.1101/2021.02.10.430452

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