Roles and future opportunities for genomic architecture in understanding repeated evolution

Riley Kellermeyer; David Alvarez-Ponce; Javier Arsuaga; Frédéric J J Chain; Megan Y Dennis; Mark J Margres; Richard P Meisel; Wynn K Meyer; Tae Seok Moon; Keriayn N Smith; Thomas D Wolfe; Coral Y Zhou; Suzanne McGaugh

doi:10.1093/icb/icaf040

Roles and future opportunities for genomic architecture in understanding repeated evolution

Integr Comp Biol. 2025 May 15:icaf040. doi: 10.1093/icb/icaf040. Online ahead of print.

Authors

Affiliations

¹ Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN, USA.
² Biology Department, University of Nevada, Reno, Reno, NV, USA.
³ Department of Molecular and Cellular Biology and Department of Mathematics, University of California Davis, Davis, CA, USA.
⁴ Department of Biological Sciences, University of Massachusetts Lowell, Lowell MA, USA.
⁵ Department of Biochemistry & Molecular Medicine, Genome Center, MIND Institute, University of California, Davis, Davis, CA, USA.
⁶ Department of Integrative Biology, University of South Florida, Tampa, FL, USA.
⁷ Department of Biology and Biochemistry, University of Houston, Houston, TX, USA.
⁸ Department of Biological Sciences, Lehigh University, Bethlehem, PA, USA.
⁹ Synthetic Biology Group, J. Craig Venter Institute, La Jolla, CA, USA.
¹⁰ School of Data Science and Society, Department of Genetics, School of Medicine, University of North Carolina at Chapel Hill.
¹¹ Department of Molecular Biosciences, University of Kansas, Lawrence Kansas, USA.

PMID: 40372385
DOI: 10.1093/icb/icaf040

Abstract

The trajectory of evolution is impacted by molecular constraints and biases that are difficult to validate experimentally. Repeated evolution of similar traits across the Tree of Life serves as a natural experiment to discern common factors that drive the evolution of these traits. The architecture of genomes in one-dimensional, two-dimensional, and three-dimensional space is emerging as a potential factor that may predict repeated phenotypic evolution. For example, chromatin packaging and the 3D organization of the genome within the nucleus can impose evolutionary constraints by predisposing genomic regions for particular types of mutations, while the evolution of genome sequence can also drive reorganization of chromatin. With the explosion of new library preparation and sequencing technologies that are accessible for non-model species, we envision a great opportunity to understand how genome architecture across phylogenetically disparate species may impact repeated phenotypic evolution. We provide examples of the known and potential avenues of phenotypic convergence at each level of genome architecture and how integration of these data can provide unique insights into the constraints, trajectory, and predictability of evolution.