Ehud Lamm

Recent and not so recent advances in our molecular understanding of the genome make the once prevalent view of the genome as a passive container of genetic information (i.e., genes) untenable, and emphasize the importance of the internal organization and re-organization dynamics of the genome for both development and evolution. While this conclusion is by now well accepted, the construction of a comprehensive conceptual framework for studying the genome as a dynamic system, capable of self-organization and adaptive behavior is still underway. This work deals with the effect of such a conceptual shift on evolutionary thought. Specifically, I try to articulate the conceptual commitments and obligations of views that privilege explanatorily or causally the genome, its dynamics and mechanisms, over genes. I refer to this class of views as belonging to ‘the genome perspective’.

Organisms inherit various kinds of developmental information and cues from their parents. The study of inheritance systems is aimed at identifying and classifying the various mechanisms and processes of heredity, the types of hereditary information that is passed on by each, the functional interaction between the different systems, and the evolutionary consequences of these properties. We present the discussion of inheritance systems in the context of several debates. First, between proponents of monism about heredity (gene-centric views), holism about heredity (Developmental Systems Theory), and those stressing the role of multiple systems of inheritance. Second, between those analyzing inheritance solely in terms of replication and transmission, and views that stress the multi-generation reproduction of phenotypic traits. A third debate is concerned with different criteria that have been proposed for identifying and delimiting inheritance systems. A fourth controversy revolves around the significance of the “Lamarckian” aspects of some of the inheritance systems that have been identified, such as epigenetic inheritance and behavioral inheritance, that allow the transmission of environmentally induced characters (i.e., “soft inheritance”).

This paper applies the conceptual toolkit of Evolutionary Developmental Biology (evo‐devo) to the evolution of the genome and the role of the genome in organism development. This challenges both the Modern Evolutionary Synthesis, the dominant view in evolutionary theory for much of the 20th century, and the typically unreflective analysis of heredity by evo‐devo. First, the history of the marginalization of applying system‐thinking to the genome is described. Next, the suggested framework is presented. Finally, its application to the evolution of genome modularity, the evolution of induced mutations, the junk DNA versus ENCODE debate, the role of drift in genome evolution, and the relationship between genome dynamics and symbiosis with microorganisms are briefly discussed.