Continent-wide genomic signatures of adaptation to urbanisation in a songbird across Europe

Abstract

Urbanisation is increasing worldwide, and there is now ample evidence of phenotypic changes in wild organisms in response to this novel environment. Yet, the genetic changes and genomic architecture underlying these adaptations are poorly understood. Here, we genotype 192 great tits (
Parus major
) from nine European cities, each paired with an adjacent rural site, to address this major knowledge gap in our understanding of wildlife urban adaptation. We find that a combination of polygenic allele frequency shifts and recurrent selective sweeps are associated with the adaptation of great tits to urban environments. While haplotypes under selection are rarely shared across urban populations, selective sweeps occur within the same genes, mostly linked to neural function and development. Collectively, we show that urban adaptation in a widespread songbird occurs through unique and shared selective sweeps in a core-set of behaviour-linked genes.

Topics

No keywords indexed for this article. Browse by subject →

References

104

[1]

Hendry, A. P., Gotanda, K. M. & Svensson, E. I. Human influences on evolution, and the ecological and societal consequences. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372, 20160028 (2017). 10.1098/rstb.2016.0028

[2]

Johnson, M. T. J. & Munshi-South, J. Evolution of life in urban environments. Science 358, eaam8327 (2017). 10.1126/science.aam8327

[3]

Mueller, J. C., Partecke, J., Hatchwell, B. J., Gaston, K. J. & Evans, K. L. Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds. Mol. Ecol. 22, 3629–3637 (2013). 10.1111/mec.12288

[4]

Harris, S. E. & Munshi-South, J. Signatures of positive selection and local adaptation to urbanization in white-footed mice (Peromyscus leucopus). Mol. Ecol. 26, 6336–6350 (2017). 10.1111/mec.14369

[5]

Rivkin, L. R. et al. A roadmap for urban evolutionary ecology. Evol. Appl. 12, 384–398 (2019). 10.1111/eva.12734

[6]

Alberti, M. et al. Global urban signatures of phenotypic change in animal and plant populations. Proc. Natl Acad. Sci. USA 114, 8951–8956 (2017). 10.1073/pnas.1606034114

[7]

Møller, A. P. & Ibáñez-Álamo, J. D. Escape behaviour of birds provides evidence of predation being involved in urbanization. Anim. Behav. 84, 341–348 (2012). 10.1016/j.anbehav.2012.04.030

[8]

Audet, J.-N., Ducatez, S. & Lefebvre, L. The town bird and the country bird: problem solving and immunocompetence vary with urbanization. Behav. Ecol. 27, 637–644 (2016). 10.1093/beheco/arv201

[9]

Carrete, M. & Tella, J. L. Behavioral correlations associated with fear of humans differ between rural and urban burrowing owls. Front. Ecol. Evol. 5, 54 (2017). 10.3389/fevo.2017.00054

[10]

Winchell, K. M., Reynolds, R. G., Prado‐Irwin, S. R., Puente‐Rolón, A. R. & Revell, L. J. Phenotypic shifts in urban areas in the tropical lizard Anolis cristatellus. Evolution 70, 1009–1022 (2016). 10.1111/evo.12925

[11]

Winchell, K. M., Maayan, I., Fredette, J. R. & Revell, L. J. Linking locomotor performance to morphological shifts in urban lizards. Proc. R. Soc. B Biol. Sci. 285, 20180229 (2018). 10.1098/rspb.2018.0229

[12]

Kern, E. M. A. & Langerhans, R. B. Urbanization drives contemporary evolution in stream fish. Glob. Change Biol. 24, 3791–3803 (2018). 10.1111/gcb.14115

[13]

Parsons, K. J. et al. Skull morphology diverges between urban and rural populations of red foxes mirroring patterns of domestication and macroevolution. Proc. R. Soc. B Biol. Sci. 287, 20200763 (2020). 10.1098/rspb.2020.0763

[14]

Reid, N. M. et al. The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish. Science 354, 1305–1308 (2016). 10.1126/science.aah4993

[15]

Campbell-Staton, S. C. et al. Parallel selection on thermal physiology facilitates repeated adaptation of city lizards to urban heat islands. Nat. Ecol. Evol. 4, 652–658 (2020). 10.1038/s41559-020-1131-8

[16]

Bosse, M. et al. Recent natural selection causes adaptive evolution of an avian polygenic trait. Science 358, 365–368 (2017). 10.1126/science.aal3298

[17]

Hendry, A. P., Farrugia, T. J. & Kinnison, M. T. Human influences on rates of phenotypic change in wild animal populations. Mol. Ecol. 17, 20–29 (2008). 10.1111/j.1365-294x.2007.03428.x

[18]

Jacobs, A. et al. Rapid niche expansion by selection on functional genomic variation after ecosystem recovery. Nat. Ecol. Evol. 3, 77–86 (2019). 10.1038/s41559-018-0742-9

[19]

Pritchard, J. K., Pickrell, J. K. & Coop, G. The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Curr. Biol. 20, R208–R215 (2010). 10.1016/j.cub.2009.11.055

[20]

Thompson, K. A., Renaudin, M. & Johnson, M. T. J. Urbanization drives the evolution of parallel clines in plant populations. Proc. R. Soc. B Biol. Sci. 283, 20162180 (2016). 10.1098/rspb.2016.2180

[21]

Perrier, C. et al. Great tits and the city: distribution of genomic diversity and gene–environment associations along an urbanization gradient. Evolut. Appl. 11, 593–613 (2018). 10.1111/eva.12580

[22]

Mueller, J. C. et al. Genes acting in synapses and neuron projections are early targets of selection during urban colonization. Mol. Ecol. 29, 3403–3412 (2020). 10.1111/mec.15451

[23]

Johnson, M. T. J., Prashad, C. M., Lavoignat, M. & Saini, H. S. Contrasting the effects of natural selection, genetic drift and gene flow on urban evolution in white clover (Trifolium repens). Proc. R. Soc. B Biol. Sci. 285, 20181019 (2018). 10.1098/rspb.2018.1019

[24]

Elmer, K. R. & Meyer, A. Adaptation in the age of ecological genomics: insights from parallelism and convergence. Trends Ecol. Evol. 26, 298–306 (2011). 10.1016/j.tree.2011.02.008

[25]

Miles, L. S., Rivkin, L. R., Johnson, M. T. J., Munshi‐South, J. & Verrelli, B. C. Gene flow and genetic drift in urban environments. Mol. Ecol. 28, 4138–4151 (2019). 10.1111/mec.15221

[26]

Barghi, N., Hermisson, J. & Schlötterer, C. Polygenic adaptation: a unifying framework to understand positive selection. Nat. Rev. Genet. 21, 769–781 (2020). 10.1038/s41576-020-0250-z

[27]

Boyce, M. S. & Perrins, C. M. Optimizing great tit clutch size in a fluctuating environment. Ecology 68, 142–153 (1987). 10.2307/1938814

[28]

Charmantier, A. et al. Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320, 800–803 (2008). 10.1126/science.1157174

[29]

Charmantier, A., Demeyrier, V., Lambrechts, M., Perret, S. & Grégoire, A. Urbanization is associated with divergence in pace-of-life in great tits. Front. Ecol. Evol. 5, 53 (2017). 10.3389/fevo.2017.00053

[30]

Pettifor, R. A., Perrins, C. M. & McCleery, R. H. Individual optimization of clutch size in great tits. Nature 336, 160–162 (1988). 10.1038/336160a0

[31]

Bouwhuis, S., Sheldon, B. C., Verhulst, S. & Charmantier, A. Great tits growing old: selective disappearance and the partitioning of senescence to stages within the breeding cycle. Proc. Biol. Sci. 276, 2769–2777 (2009).

[32]

Krebs, J. R. Territory and breeding density in the great tit, Parus major L. Ecology 52, 2–22 (1971). 10.2307/1934734

[33]

Salmón, P., Nilsson, J. F., Watson, H., Bensch, S. & Isaksson, C. Selective disappearance of great tits with short telomeres in urban areas. Proc. R. Soc. B Biol. Sci. 284, 20171349 (2017). 10.1098/rspb.2017.1349

[34]

Sprau, P., Mouchet, A. & Dingemanse, N. J. Multidimensional environmental predictors of variation in avian forest and city life histories. Behav. Ecol. 28, 59–68 (2017). 10.1093/beheco/arw130

[35]

Senar, J. C. et al. Urban great tits (Parus major) show higher distress calling and pecking rates than rural birds across Europe. Front. Ecol. Evol. 5, 163 (2017). 10.3389/fevo.2017.00163

[36]

Isaksson, C., Sturve, J., Almroth, B. C. & Andersson, S. The impact of urban environment on oxidative damage (TBARS) and antioxidant systems in lungs and liver of great tits, Parus major. Environ. Res. 109, 46–50 (2009). 10.1016/j.envres.2008.10.006

[37]

Caizergues, A. E., Grégoire, A. & Charmantier, A. Urban versus forest ecotypes are not explained by divergent reproductive selection. Proc. R. Soc. B Biol. Sci. 285, 20180261 (2018). 10.1098/rspb.2018.0261

[38]

Kim, J. M. et al. A high-density SNP chip for genotyping great tit (Parus major) populations and its application to studying the genetic architecture of exploration behaviour. Mol. Ecol. Resour. 18, 877–891 (2018). 10.1111/1755-0998.12778

[39]

Laine, V. N. et al. Evolutionary signals of selection on cognition from the great tit genome and methylome. Nat. Commun. 7, 1–9 (2016). 10.1038/ncomms10474

[40]

Lemoine, M. et al. Low but contrasting neutral genetic differentiation shaped by winter temperature in European great tits. Biol. J. Linn. Soc. 118, 668–685 (2016). 10.1111/bij.12745

[41]

Spurgin, L. G. et al. The great tit HapMap project: a continental-scale analysis of genomic variation in a songbird. Preprint at bioRxiv https://doi.org/10.1101/561399 (2020). 10.1101/561399

[42]

Evans, K. L. et al. Independent colonization of multiple urban centres by a formerly forest specialist bird species. Proc. R. Soc. B Biol. Sci. 276, 2403–2410 (2009). 10.1098/rspb.2008.1712

[43]

Forester, B. R., Lasky, J. R., Wagner, H. H. & Urban, D. L. Comparing methods for detecting multilocus adaptation with multivariate genotype–environment associations. Mol. Ecol. 27, 2215–2233 (2018). 10.1111/mec.14584

[44]

Bolnick, D. I., Barrett, R. D., Oke, K. B., Rennison, D. J. & Stuart, Y. E. (Non) parallel evolution. Annu. Rev. Ecol. Evol. Syst. 49, 303–330 (2018). 10.1146/annurev-ecolsys-110617-062240

[45]

Harpak, A. et al. Genetic adaptation in New York City rats. Genome Biol. Evol. 13, evaa247 (2021). 10.1093/gbe/evaa247

[46]

Szpiech, Z. A., Novak, T. E., Bailey, N. P. & Stevison, L. S. High-altitude adaptation in rhesus macaques. Preprint at bioRxiv https://doi.org/10.1101/2020.05.19.104380 (2020). 10.1101/2020.05.19.104380

[47]

Burri, R. Interpreting differentiation landscapes in the light of long-term linked selection. Evol. Lett. 1, 118–131 (2017). 10.1002/evl3.14

[48]

Tang, K., Thornton, K. R. & Stoneking, M. A new approach for using genome scans to detect recent positive selection in the human genome. PLoS Biol. 5, e171 (2007). 10.1371/journal.pbio.0050171

[49]

Thompson, K. A., Osmond, M. M. & Schluter, D. Parallel genetic evolution and speciation from standing variation. Evol. Lett. 3, 129–141 (2019). 10.1002/evl3.106

[50]

Etten, M. V., Lee, K. M., Chang, S.-M. & Baucom, R. S. Parallel and nonparallel genomic responses contribute to herbicide resistance in Ipomoea purpurea, a common agricultural weed. PLoS Genet. 16, e1008593 (2020). 10.1371/journal.pgen.1008593

Showing 50 of 104 references

Cited By

68

Signatures of selective sweeps in urban and rural white clover populations

James S Santangelo, Marc T J Johnson · 2025

Evolution

Adaptation in the Alleyways: Candidate Genes Under Potential Selection in Urban Coyotes

Samantha E S Kreling, Summer E Vance · 2024

Genome Biology and Evolution

Adaptation to urban environments

Sarah E. Diamond, Eric G. Prileson · 2022

Current Opinion in Insect Science

Metrics

68

Citations

104

References

Details

Published: May 20, 2021
Vol/Issue: 12(1)
License: View

Authors

Department of Biology Microbial Ecology Group Lund University Ecology Building SE‐223 62 Lund Sweden; Bioinformatics Infrastructures for Life Sciences (BILS) Department of Biology Lund University Ecology Building SE‐223 62 Lund Sweden

Behavioural Ecology, Faculty of Biology Ludwig‐Maximilians University of Munich Planegg‐Martinsried Germany

Division of Systems Biology of Signal Transduction, German Cancer Research Center (DKFZ), DKFZ-ZMBH Alliance, Heidelberg, Germany

Department of Animal Ecology Netherlands Institute of Ecology (NIOO‐KNAW) Wageningen 6700 AB The Netherlands

C

Caroline Isaksson

Funding

Vetenskapsrådet Award: C0361301

Ministry of Economics and Competiveness

Cite This Article

Pablo Salmón, Arne Jacobs, Dag Ahrén, et al. (2021). Continent-wide genomic signatures of adaptation to urbanisation in a songbird across Europe. Nature Communications, 12(1). https://doi.org/10.1038/s41467-021-23027-w

Continent-wide genomic signatures of adaptation to urbanisation in a songbird across Europe

You May Also Like