Drift on holey landscapes as a dominant evolutionary process

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 120; no. 52
• Main Authors: Dochtermann, Ned A, Klock, Brady, Roff, Derek A, Royaute, Raphael
• Format: Paper Journal Article
• Language: English
• Published: Cold Spring Harbor Cold Spring Harbor Laboratory Press 23.02.2023; National Academy of Sciences
• Subjects: Animal genetics; Biodiversity; Evolution; Genetics; Integration; Life history; Life Sciences; Phenotypes; Populations and Evolution; Quantitative genetics; Phenotypic integration; G matrix; Adaptive landscape
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1101/2021.10.22.465488

Phenotypes typically display integration, i.e. correlations between traits. For quantitative traits--like many behaviors, physiological processes, and life-history traits--patterns of integration are often assumed to have been shaped by the combination of linear, non-linear, and correlated selection, with trait correlations representative of optimal combinations and reflective of the adaptive landscapes that have shaped a population. Unfortunately, this assumption has rarely been critically tested, in part due to a lack of clear alternatives. Here we show that trait integration across 6 phyla and 60 species (including both Plantae and Animalia) is consistent with evolution across high dimensional "holey landscapes" rather than classical models of selection. This suggests that the leading conceptualizations and modeling of the evolution of trait integration fail to capture how phenotypes are shaped and that traits are integrated in a manner contrary to predictions of dominant evolutionary theory.Competing Interest StatementThe authors have declared no competing interest.Footnotes* Revisions for clarity and adding some supporting references (particularly vis-a-vis Pareto optimization and values of p describing the holey landscapes).* https://github.com/DochtermannLab/Wright_vs_Holey