Introduction to the Special Issue: Development, Evolution, and Movements toward Resynthesis

In much of pre-Darwinian evolutionary thought, individual development took center stage as the primary driver of evolutionary changes in organized complexity. Natural selection, though recognized as conceptually important for understanding evolution, assumed a principally negative role in such changes, serving, in a sieve-like manner, to evolutionarily eliminate certain organized variants, never to construct any (Gould, 2002; Ho, 2010; Sober, 1984; Webster & Goodwin, 1982). With the arrival of Darwin’s (1859/1991) Origin of Species, this conceptual landscape qualitatively changed. One of Darwin’s most significant contributions to evolutionary theory involved reconceptualizing natural selection as a “creative force of evolutionary change,” conferring upon the process a heavily privileged positive role in the construction of all organized complexity in phenotypic form and function (Gould, 2002, p. 139; Ho, 2010; Sober, 1984). In the decades that followed, mainstream evolutionary theory gradually solidified its Newtonian, mechanistic focus on natural selection and progressively stripped individual development of any significant formative status in the origins of organized complexity. Explanations for evolutionary change instead began to steadily crystalize around a central process of cross-generational shaping, whereby selective pressures from the external environment impose order – within populations and across evolutionary time – on unorganized, directionless variability, thereby slowly establishing increasing complexity of form and function (Depew & Weber, 1995; Gould, 2002; Russell, 1916).

Though severely marginalized, support for the critical role of individual development in evolutionary change was not completely obliterated in this landscape and continued to surface among formalist, orthogenetic critics of an exclusive focus on natural selection, such as Mivart, Bateson, Garstang, and de Beer (Gottlieb, 1992; Gould, 2002). That, however, changed with the rise and consolidation of neo-Darwinism, or the “Modern Synthesis,” a paradigm that arose from the merger of Mendelian genetics and Darwin’s theory of natural selection. The Modern Synthesis effectively eliminated individual development from the evolutionary picture by promoting natural selection as the principal driving force behind evolutionary change and by attributing to genetics alone both inheritance and the generation of evolutionarily meaningful phenotypic variance. And because of neo-Darwinism’s dominance over evolutionary thought, 20th-century biologists and psychologists increasingly came to regard development as having little to no relevance for evolution, despite some noteworthy exceptions in the work of Waddington (1953, 1961) and Piaget (1978), among others.

Beginning in the late 1970s, a new contingent of calls arose within evolutionary theorizing urging reexamination of the explanatory significance of development and developmental theory in understanding evolutionary change (e.g., Alberch, 1982; Bonner, 1982; Gottlieb, 1987; Gould, 1977; Oyama, 1985). Such calls prompted a flurry of proposals across biology and psychology designed to reinstate developmental processes as an integral part of the evolutionary process (e.g., Amundson, 2005; Gottlieb, 1992; Jablonka & Lamb, 2005; Lickliter, 2008; Robert, 2004; Sansom & Brandon, 2007; Stotz, 2014; West-Eberhard, 2003). Many of these proposals remained committed to the idea of natural selection as a central creative force in the emergence of organized complexity but sought to overhaul the extreme marginalization of development promulgated by the Modern Synthesis (e.g., Pigliucci, 2007; Pigliucci & Müller, 2010; see Walsh, 2015, for discussion). Other proposals, however, called for a fundamental overhaul of the very conceptualization of natural selection as a “creative force” in the evolutionary process (e.g., Ho & Saunders, 1979; Johnson & Gottlieb, 1990; Sober, 1984; Webster & Goodwin, 1982).

Recent findings from the study of evolutionary developmental biology, niche construction, and developmental plasticity have not only reasserted the importance of individual development for evolutionary change but have also begun to seriously challenge key assumptions of neo-Darwinian and even Darwinian evolutionary theory (Jablonka & Lamb, 2020; Laland et al., 2014, 2015; Odling-Smee et al., 2003; Uller & Laland, 2019). Calls have become increasingly prominent for an “Extended Evolutionary Synthesis” that rejects conceptualizing organisms as evolving to fit environments (and environmental “problems”) that preexist those organisms, in favor of conceptualizing organisms and environments as co-constructing each other, involving simultaneous evolution of organism and world (both physical and socio-cultural). Treatments of organisms as active constructors of their own environments, co-directing their own development and evolution through their active commerce with the world and therefore serving as both causes and products of selective pressures (e.g., Lewontin, 2000), have reached new levels of mainstream consideration.

The purpose of this special issue of Human Development is to critically examine the theoretical and empirical impetus behind the movement toward an Extended Evolutionary Synthesis as well as the implications of reintroducing individual development into evolutionary theory for how we conceptualize both evolutionary and developmental processes. We seek, in other words, to systematically explore the implications of recent challenges to orthodox evolutionary theory for our understanding of development, evolution, and development-evolution relations. To highlight points of conceptual convergence and divergence across the special issue’s five major articles, we asked each of this issue’s authors to consider the following questions:

• How do developmental processes play a role in evolutionary change?

• How do evolutionary processes play a role in developmental change?

• What does it mean for the individual dynamics of developmental change to influence the population dynamics of evolutionary change?

• What does it mean for the population dynamics of evolutionary change to influence the individual dynamics of developmental change?

• In what ways do recent empirical and theoretical developments in the biological and developmental sciences challenge orthodox evolutionary theory and its conceptualization in terms of natural selection? Do these recent developments compel a thoroughgoing revision of evolutionary theory?

In the opening contribution to this special issue, Anne Sophie Meincke compellingly argues that a full embrace of an Extended Evolutionary Synthesis demands a fundamental metatheoretical shift in how evolutionary and developmental biologists conceptualize development and evolution. This shift entails wholesale rejection of the “thing” ontology that undergirds the Modern Synthesis—an ontology that conceptualizes change in variational terms, reducible to accidental mutation and the rearrangement of atomic building blocks. Meincke instead argues for evolutionary and developmental theory in biology that draws on a thoroughgoing process ontology, conceptualizing change in genuinely transformative terms by foundationally replacing all appeals to unchanging substrates with the irreducible dynamics of process.

Using the work of Piaget and Waddington as a backdrop, Scott F. Gilbert highlights the instructive, and not merely selective, role that environments play in phenotypic construction. He outlines a series of advances in developmental biology empirically substantiating the impact of “environmental agency” on all facets of developmental construction, from extragenomic factors within to those outside the organism. He also critically evaluates and blurs any hard and fast boundary lines traditionally drawn between developing organisms and their environments by demonstrating that complex organisms are holobionts – that is, integrated assemblages of multi-species ecosystems, the reciprocal relations of which critically inform species-typical morphogenesis and functioning. Gilbert’s blurring of the organism/environment divide carries with it clear implications for reconceptualizing the nature of evolutionary “mechanism.”

Denis M. Walsh’s contribution revolves around Piaget’s contention that organismic adaptive activity critically directs evolutionary change – and around Piaget’s attempts to marshal Waddington’s work on genetic assimilation in the service of reconciling his view to the neo-Darwinian thought of the time. Walsh argues that the Modern Synthesis’ wholesale privileging of genes as both the source of novel variation (through mutation) upon which natural selection acts and of cross-generational inheritance inevitably writes organisms out of the evolutionary picture and promotes a wrongheaded division of genotype as explanation and phenotype as outcome in evolutionary change. Instead, Walsh argues that recent agential conceptions of organisms as enacting (through commerce with the world) both their own adaptive development and species-level evolution provide the necessary reconceptualization of development and evolution to nurture Piaget’s revolutionary ideas.

Longstanding tension exists between conceptualizations of biological and cultural evolution, a tension that Eva Jablonka seeks to remedy and transcend in her contribution by re-conceptualizing evolution and development in dynamic systems terms. Jablonka argues that models inspired by developmental dynamics provide a powerful alternative to the orthodox populational models of evolutionary biology and allow for the study of meaning-making, both at the individual level of development and the trans-generational level of communities and cultures. Dynamic systems models – fashioned in the image of Waddington’s epigenetic landscape metaphor and consisting of reciprocal relations among various intra- and extra-organismic resources – are needed to more comprehensively explain both stability and change, ontogenetically and phylogenetically. Such models undermine strict distinctions between developmental and evolutionary change, which Jablonka illustrates through descriptions of five qualitative models of social landscape stability and change.

Finally, Robert Lickliter and David S. Moore systematically examine how to reconceptualize inheritance in light of modern developments in the study of epigenetics. Adopting a developmental systems perspective, they delve into the multiple developmental resources – both molecular and systemic (or molar) – that are regularly available to developing organisms across generations and critical to stability and change in phenotypic evolution. Lickliter and Moore highlight the continued molecular reductionism evident in most current epigenetics work and argue instead for a systemic epigenetics, based on a broadened, relational unit of analysis: the organism-environment relation. To understand phenotype construction and maintenance at the levels of both development and evolution requires rejection of the orthodox tendency in evolutionary theory to look for and isolate formative influences in the resources themselves, in favor of a process-oriented focus on the dynamics of relations among resources.

Our special issue concludes with the guest editors’ synthetic look at the challenges posed by the Extended Evolutionary Synthesis, not just to neo-Darwinian but to traditional Darwinian Theory. We also examine possibilities for advancing new, development-friendly approaches to evolutionary theory, ones that will transcend the problematic arguments by design which continue to plague developmental and evolutionary thinking in the biological sciences.

No ethical approval was required for preparation of this manuscript, as no human or animal subjects were used.

The authors have no conflicts of interest to declare.

No external funding was received for this manuscript.

David C. Witherington participated in the conceptualization and writing of this paper, authoring both its original draft, and contributing to subsequent rewrites. Robert Lickliter also participated in the conceptualization and writing of this paper, with particular focus on subsequent rewrites. Finally, David S. Moore participated in the conceptualization and writing of this paper, with particular focus on subsequent rewrites.

This manuscript did not include any empirical data; therefore, data availability does not apply for this conceptual paper.