Evolutionary Developmental Biology (Evo-Devo): Past, Present, and Future

Abstract

Evolutionary developmental biology (evo-devo) is that part of biology concerned with how changes in embryonic development during single generations relate to the evolutionary changes that occur between generations. Charles Darwin argued for the importance of development (embryology) in understanding evolution. After the discovery in 1900 of Mendel's research on genetics, however, any relationship between development and evolution was either regarded as unimportant for understanding the process(es) of evolution or as a black box into which it was hard to see. Research over the past two decades has opened that black box, revealing how studies in evo-devo highlight the mechanisms that link genes (the genotype) with structures (the phenotype). This is vitally important because genes do not make structures. Developmental processes make structures using road maps provided by genes, but using many other signals as well-physical forces such as mechanical stimulation, temperature of the environment, and interaction with chemical products produced by other species-often species in entirely different kingdoms as in interactions between bacteria and squid or between leaves and larvae (Greene Science 243:643-666, 1989). Not only do genes not make structures (the phenotype), but new properties and mechanisms emerge during embryonic development: genes are regulated differentially in different cells and places; aggregations of similar cells provide the cellular resources (modules) from which tissues and organs arise; modules and populations of differently differentiated cells interact to set development along particular tracks; and organisms interact with their environment and create their niche in that environment. Such interactions are often termed "epigenetic," meaning that they direct gene activity using mechanisms that are not encoded in the DNA of the genes. This paper reviews the origins of evo-devo, how the field has changed over the past 30 years, evaluates the recognition of the importance for development and evolution of mechanisms that are not encoded in DNA, and evaluates what the future might bring for evo-devo. Although impossible to know, history tells us that we might expect more of the same; expansion of evo-devo into other areas of biology (ecology, physiology, behavior); absorption of evo-devo by evolution or a unification of biology in which evo-devo plays a major role.

The significance and scope of evolutionary developmental biology: a vision for the 21st century

“…Although having antecedents prior to Darwin (see Gould 1977;Friedman and Diggle 2011), evo-devo was made possible in large part by the emerging power of molecular biology to contrast gene sequences, and subsequently gene functions, across taxa (e.g., Ohno 1970;King and Wilson 1975;Jacob 1977;Bonner 1981). Since its emergence as a distinct discipline with dedicated journals and professional societies (Raff 2000), evo-devo has undergone dramatic transformations, and has now grown into a multifaceted discipline that has opened up novel and synthetic ways to address fundamental, long-standing questions across areas of biology, as well as illuminated patterns and processes in biology that other disciplines were unable to see (Hall 2012;Olson 2012). Just as the Modern Synthesis was able to unify many aspects of biology in the mid-20th century, evo-devo is now positioned to transform and unify diverse aspects of biology, one of the primary scientific challenges of the 21st century.…”

Craniofacial skeletal response to encephalization: How do we know what we think we know?

“…Though it is commonly said that phenotypic variation is the product of complex interactions between genotype and environment (Figure 7a), mechanisms and processes that integrate genetic instructions and environmental factors to produce organized structure are not well understood. Following others (Carroll, 2008; Hall, 2012), we propose that developmental interactions among factors at all levels contain the information needed to explain the production of phenomes from genomes. Contemporary developmental analyses have focused on genetics to reveal molecular mechanisms underlying phenotypic change but have fallen short in determining how phenotypes are produced because genes do not make structures—developmental processes make structures (Hall, 2012) through the organization and function of cells using instructions provided by genes.…”

“…Following others (Carroll, 2008; Hall, 2012), we propose that developmental interactions among factors at all levels contain the information needed to explain the production of phenomes from genomes. Contemporary developmental analyses have focused on genetics to reveal molecular mechanisms underlying phenotypic change but have fallen short in determining how phenotypes are produced because genes do not make structures—developmental processes make structures (Hall, 2012) through the organization and function of cells using instructions provided by genes. How cells utilize those instructions and integrate environmental factors, such as mechanical forces generated by cell proliferation and tissue growth, remains a central question of biology.…”

Grand challenges in evolutionary developmental biology

“…To be sure, precise predictions about the future of evo-devo are impossible (Hall, 2012), but the possibility, and in consequence the responsibility, is to an extent in our hands to steer the boat toward intellectually rewarding paths. We are already witnessing our discipline expanding its scope by exploring its boundaries toward other disciplines, ecology in particular (eco-evodevo, e.g., Hall, 2003;Gilbert and Epel, 2008; also evo-devo vs. niche construction, e.g., Laland et al, 2008), but also ethology (e.g., Bertossa, 2011) and the sciences of language (e.g., Hoang et al, 2011;Hall, 2013). Future advances in all these directions are welcome, but I expect that much more progress will come from the impact that evo-devo will eventually have on the foundations and the research agendas of its parent disciplines.…”