Evolutionary theory is often viewed as a fusion of Darwinian and Mendelian insights. Notwithstanding the immense progress that these achievements engendered, Richard Lewontin (1983) argues that the legacies of Darwin and Mendel include misleading metaphors that:
are responsible for certain difficulties in biology, difficulties that prevent us from some kinds of further progress and which keep us locked into a rigid framework of thought about the development and evolution of organisms.
Mendel’s view of organisms as the manifestation of autonomous internal ‘factors’ (i.e. genes) with their own laws, germinated into a post-Synthesis metaphor in which ontogeny ‘is seen as an unfolding of a form, already latent in the genes, requiring only an original triggering at fertilization and an environment adequate to allow ‘normal’ development to continue’. We now know that developmental processes are hugely environmentally contingent.
Darwin’s view of organisms as passive objects moulded by the external force of natural selection encouraged a conception of evolution in which ‘the environment “poses the problem”; the organisms posit “solutions”, of which the best is finally “chosen”. The metaphor of selection, inspired by the efficacy of artificial selection, continues to encourage a view of organisms as passive objects upon which external forces act.
Lewontin argues forcefully that these metaphors are misleading. Similar points have been made by Oyama (1985), Griffiths and Gray (2001, 2004), Sultan (2015) and many others.
Lewontin (1983) also took issue with the adaptive landscape metaphor, which is widely used to visualise the fitness of organisms as a function of genetic or phenotypic state. Evolving organisms are general construed as climbing the fitness landscape to a local peak through the action of natural selection. In practice, landscapes are not static. Lewontin pointed out that through their niche construction the organisms themselves alter the landscape, so that moving across a landscape is like walking on a trampoline.
Recently, Tanaka et al (2020) proposed a dual-landscape model of adaptation with natural selection and niche construction, and used it to analyse the dynamics of three cases of microbial evolution.
Lewontin RC. 1983. Gene, organism, and environment. In: Bendall DS, ed. pp. 273-285. Cambridge: Cambridge University Press. This accessible essay introduces the niche construction perspective and critiques conventional evolutionary approaches to adaptation.
Levins R, Lewontin RC. 1985. The Dialectical Biologist. Cambridge: Harvard University Press. Discusses how metaphors concerning selection and development can be misleading.