Genome-wide parallelism underlies contemporary adaptation in urban lizards

Author:

Winchell Kristin M.123,Campbell-Staton Shane C.1ORCID,Losos Jonathan B.2,Revell Liam J.34,Verrelli Brian C.5ORCID,Geneva Anthony J.6ORCID

Affiliation:

1. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544

2. Department of Biology, Washington University, St. Louis, MO 63130

3. Department of Biology, University of Massachusetts Boston, Boston, MA 02125

4. Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Concepción, Chile 4090541

5. Center for Biological Data Science, Virginia Commonwealth University, Richmond, VA 23284

6. Department of Biology and Center for Computational and Integrative Biology, Rutgers University–Camden, NJ 08103

Abstract

Urbanization drastically transforms landscapes, resulting in fragmentation, degradation, and the loss of local biodiversity. Yet, urban environments also offer opportunities to observe rapid evolutionary change in wild populations that survive and even thrive in these novel habitats. In many ways, cities represent replicated “natural experiments” in which geographically separated populations adaptively respond to similar selection pressures over rapid evolutionary timescales. Little is known, however, about the genetic basis of adaptive phenotypic differentiation in urban populations nor the extent to which phenotypic parallelism is reflected at the genomic level with signatures of parallel selection. Here, we analyzed the genomic underpinnings of parallel urban-associated phenotypic change inAnolis cristatellus, a small-bodied neotropical lizard found abundantly in both urbanized and forested environments. We show that phenotypic parallelism in response to parallel urban environmental change is underlain by genomic parallelism and identify candidate loci across theAnolisgenome associated with this adaptive morphological divergence. Our findings point to polygenic selection on standing genetic variation as a key process to effectuate rapid morphological adaptation. Identified candidate loci represent several functions associated with skeletomuscular development, morphology, and human disease. Taken together, these results shed light on the genomic basis of complex morphological adaptations, provide insight into the role of contingency and determinism in adaptation to novel environments, and underscore the value of urban environments to address fundamental evolutionary questions.

Funder

National Science Foundation

University of Massachusetts Boston

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

Reference122 articles.

1. Evolution of life in urban environments

2. J. S. Santangelo “Urban environments as a framework to study parallel evolution” in Urban Evolutionary Biology M. Szulkin J. Munshi-South A. Charmantier Eds. (Oxford University Press USA 2020) pp. 36–53.

3. Urban Evolutionary Biology

4. Phenotypic shifts in urban areas in the tropical lizardAnolis cristatellus

5. Human influences on rates of phenotypic change in wild animal populations

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