The extended evolutionary synthesis: its structure, assumptions and predictions

Abstract

Scientific activities take place within the structured sets of ideas and assumptions that define a field and its practices. The conceptual framework of evolutionary biology emerged with the Modern Synthesis in the early twentieth century and has since expanded into a highly successful research program to explore the processes of diversification and adaptation. Nonetheless, the ability of that framework satisfactorily to accommodate the rapid advances in developmental biology, genomics and ecology has been questioned. We review some of these arguments, focusing on literatures (evo-devo, developmental plasticity, inclusive inheritance and niche construction) whose implications for evolution can be interpreted in two ways—one that preserves the internal structure of contemporary evolutionary theory and one that points towards an alternative conceptual framework. The latter, which we label the 'extended evolutionary synthesis' (EES), retains the fundaments of evolutionary theory, but differs in its emphasis on the role of constructive processes in development and evolution, and reciprocal portrayals of causation. In the EES, developmental processes, operating through developmental bias, inclusive inheritance and niche construction, share responsibility for the direction and rate of evolution, the origin of character variation and organism-environment complementarity. We spell out the structure, core assumptions and novel predictions of the EES, and show how it can be deployed to stimulate and advance research in those fields that study or use evolutionary biology.

Keywords: developmental plasticity; evolutionary developmental biology; extended evolutionary synthesis; inclusive inheritance; niche construction; reciprocal causation.

Figure 1.

Contrasting views of development. (a) Programed development. Traditionally, development has been conceptualized as programed, unfolding according to rules and instructions specified within the genome. DNA is ascribed a special causal significance, and all other parts of the developing organism serve as ‘substrate’, or ‘interpretative machinery’ for the expression of genetic information. Evolutionarily relevant phenotypic novelty results solely from genetic mutations, which alter components of the genetic program. Under this perspective, organisms are built from the genome outwards and upwards, with each generation receiving the instruction on how to build a phenotype through the transmission of DNA. (b) Constructive development. By contrast, in the EES, genes and genomes represent one of many resources that contribute to the developing phenotype. Causation flows both upwards from lower levels of biological organization, such as DNA, and from higher levels downwards, such as through tissue- and environment-specific gene regulation. Exploratory and selective processes are important sources of novel and evolutionarily significant phenotypic variation. Rather than containing a ‘program’, the genome represents a component of the developmental system, shaped by evolution to sense and respond to relevant signals and to provide materials upon which cells can draw.

Figure 2.

The structure of the EES. The EES includes as evolutionary causes processes that generate novel variants, bias selection, modify the frequency of heritable variation (including, but not restricted to, genes) and contribute to inheritance. A variety of developmental processes (e.g. epigenetic effects, regulation of gene expression, construction of internal and external developmental environments) contribute to the origin of novel phenotypic variation, which may be viable and adaptive (i.e. ‘facilitated variation’). In addition to accepted evolutionary processes that directly change gene frequencies, the EES recognizes processes that bias the outcome of natural selection, specifically developmental bias and niche construction. All processes that generate phenotypic variation, including developmental plasticity and some forms of inclusive inheritance, are potential sources of bias. A broadened conception of inheritance encompasses genetic, epigenetic and ecological (including cultural) inheritance. Arrows represent causal influences. Processes shown in red are those emphasized by the EES, but not a more traditional perspective. ^¶Mutation pressure refers to the population-level consequences of repeated mutation, here depicted as dashed because mutation is also represented in ‘processes that generate novel variation’. ^‡In the EES, this category of processes will often need to be broadened to encompass processes that modify the frequencies of other heritable resources. ^§Developmental bias and niche construction can also affect other evolutionary processes, such as mutation, drift and gene flow. (Online version in colour.)