International Lectures on Nature and Human Ecology

Kevin Laland
Waddington's influence on some recent developments in the evolutionary sciences

Waddington believed that the Neo-Darwinism of his day was incomplete. The exploitive system and the epigenetic system were two "major factors" that Waddington believed had been left out of evolutionary accounts, but that (he felt) played important evolutionary roles. Waddington's writings on the exploitive system were the perhaps the single most important influence on the development of niche construction theory in the 1980s, which followed Waddington's lead in portraying organisms' choice and modification of environments (now known as 'niche construction') as an important, but historically neglected, evolutionary process. Niche construction theory has since blossomed into a substantive literature, associated with a number of significant empirical and theoretical findings, perhaps most notably concerning 'ecological inheritance' (the ecological legacy of environments, and hence selection pressures, modified through ancestral niche construction) which has been found to strongly influence evolutionary and ecological dynamics, and is now widely recognized as an important component in expanded conceptions of inheritance. However, while niche construction theory is widely endorsed across multiple academic fields, niche construction is not yet accepted as an evolutionary process within evolutionary genetics.

This difference reflects two distinct ways in which niche construction is currently being understood: a traditional interpretation in which niche construction is reduced to 'genetically specified' aspects of phenotypes (or adaptations), and where niche construction is treated as a product, but not a process, of evolution, and an alternative reading, in which niche construction is recognized as a process that directs evolution through nonrandom modification of environments. The former position peripheralizes niche construction, in part because it does not fit with historical conceptions of an evolutionary process within evolutionary biology. Niche construction is not the only evolutionary factor peripheralized by the dominant conceptual framework, and a similar analysis applies equally to phenomena such as 'developmental plasticity' and 'developmental bias', which resonate with Waddington's epigenetic system and systems biology perspective, respectively. 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 of the early 20th 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, ecology and the human sciences is increasingly being questioned.

I briefly reviewed some of these arguments, again focusing on literatures (developmental bias, developmental plasticity) with implications for evolution that 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 interpretation, which I equated with 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, reciprocal portrayals of causation, and organismal causes of variation, fitness and inheritance. One factor that may influence whether a given researcher embraces the traditional or alternative reading of these literature concerns whether they regard the processes of development as 'programmed' by genes, or more open ended ('constructive'). I sketched the structure, core assumptions and novel predictions of the EES, which are designed to be deployed constructively to stimulate and advance research in the evolutionary sciences. I concluded by suggesting that Waddington's evolutionary ideas are alive and well, influencing how many thousands of researchers spanning numerous academic fields conduct their research, and can be regarded as of growing influence. However, these ideas have yet to shape evolutionary genetics.

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