The Inheritance of Process: A Dynamical Systems Approach

Abstract

A central unresolved problem of evolutionary biology concerns the way in which evolution at the genotypic level relates to the evolution of phenotypes. This genotype-phenotype map involves developmental and physiological processes, which are complex and not well understood. These processes co-determine the rate and direction of adaptive change by shaping the distribution of phenotypic variability on which selection can act. In this study, we argue-expanding on earlier ideas by Goodwin, Oster, and Alberch-that an explicit treatment of this map in terms of dynamical systems theory can provide an integrated understanding of evolution and development. We describe a conceptual framework, which demonstrates how development determines the probability of possible phenotypic transitions-and hence the evolvability of a biological system. We use a simple conceptual model to illustrate how the regulatory dynamics of the genotype-phenotype map can be passed on from generation to generation, and how heredity itself can be treated as a dynamic process. Our model yields explanations for punctuated evolutionary dynamics, the difference between micro- and macroevolution, and for the role of the environment in major phenotypic transitions. We propose a quantitative research program in evolutionary developmental systems biology-combining experimental methods with mathematical modeling-which aims at elaborating our conceptual framework by applying it to a wide range of evolving developmental systems. This requires a large and sustained effort, which we believe is justified by the significant potential benefits of an extended evolutionary theory that uses dynamic molecular genetic data to reintegrate development and evolution.

Reverse-Engineering Post-Transcriptional Regulation of Gap Genes in Drosophila melanogaster

“…For example, delays can greatly increase the time it takes for the system to reach its steady stage [79], [80]. This may be functionally important for gap gene patterning, where the expression domains in the posterior half of the embryo have to be kept moving anteriorly until the onset of gastrulation (and the subsequent disappearance of gap expression), while gap domains in the central part of the embryo remain stable and reach their steady states much earlier [25], [59].…”

The ontology of organisms: Mechanistic modules or patterned processes?

“…Importantly then, in any particular developmental system, these relations are determined by, and are therefore ontologically dependent upon, the character of its constitutive GRN which encodes a specific set of available protein-protein and gene-protein interactions, their directionality (constituting upstream and downstream expression control), and their interaction modalities (activation, repression, etc. ) This is evidenced by the fact that mutational changes in both the protein-coding and cis-regulatory regions of a system"s genome are capable of substantially modifying its dynamical landscape: these alterations effect both the topology (the number, kind, and relative placement of attractors and their associated basins) and the geometry (the position, shape and/or size of attractors and their associated basins) of that landscape (Kim & Wang 2007;Jaeger et al 2012;Verd et al 2014). Thus, the regulatory structure of a particular genome which determines the specific elevation mapping, and thus the higher-order dynamics of any particular developmental system is, in the end, mechanistically explicable: the regulatory logic governing the stability of its states is one whose content is cashed-out by the familiar and well-studied causal role of transcription factors at cis-regulatory regions -a role which has been quite naturally explicated via a mechanistic ontology.…”

A Philosophical Perspective on Evolutionary Systems Biology

“…Here, we are not particularly interested in that debate as it stands; far more compelling is the question of how EvoDevo itself can be understood in light of ESB. Some very promising results have been achieved along those lines already, with—for example—the development of a conceptual framework that has the scope for understanding phenotypic variability both quantitatively and dynamically (Jaeger et al 2012). One of the articles in this collection will delve more deeply into epistemic questions about EvoDevo and dynamic mechanistic models (Jaeger et al 2015, this issue—see below).…”