The extended evolutionary synthesis (EES) is a 21st century version of evolutionary theory according to which developmental processes, including memory and learning, play a crucial role in heredity and evolution alongside processes of Darwinian selection. The role of the activities of organisms and the development-led evolution of their behaviors and cognition are central to the EES explanatory framework.

History

The EES is conceptually continuous with the biological approach of a group of biologists called the organicists, who in the 1930s stressed the evolutionary primacy of the nonrandom developmental responses of the organism to internal and external challenges (Peterson, 2016). In its modern form, the EES emerged as a result of empirical discoveries and theoretical and conceptual models and syntheses that became consolidated into a coherent system of evolutionary theorizing in the first two decades of the 21st century (Jablonka & Lamb, 2020). It is an extension as well as a challenge to the neo-Darwinian view of evolution called the modern synthesis that dominated evolutionary thinking since the mid-20th century (Mayr & Provine, 1980) and is still represented in evolution textbooks. The modern synthesis asserts that adaptive evolution is exclusively due to gradual natural selection acting on heritable variability; this variability is assumed to originate solely through accidental genetic changes that arise without reference to their advantages or disadvantages (Charlesworth et al., 2017; Mayr & Provine, 1980).

According to the EES, evolutionary change is initiated through the generation of nonrandom phenotypic variants that can be directly inherited or affect their own inheritance indirectly through selection and niche construction (Jablonka & Lamb, 2014; Lala et al., 2024; Laland et al., 2015) [see Niche Construction]. Hence, genes are considered as followers, not leaders, in evolution (Waddington, 1975; West-Eberhard, 2003). Moreover, by stressing the heritability of many developmentally acquired phenotypic variations, there is a return to the previously discredited neo-Lamarckian idea that environmentally induced, acquired responses can be inherited and therefore affect evolutionary change (Gissis & Jablonka, 2011).

Core concepts

Developmental plasticity, an extended notion of heredity, a focus on agency, and an extended notion of selection are central to the EES framework.

Developmental plasticity

Developmental plasticity—the ability of an organism with a particular genetic constitution to modify its structure, function, and behavior in response to environmental challenges—is considered a primitive of life (there can be no sustainable life without plasticity; West-Eberhard, 2003). Furthermore, plasticity has itself evolved, so there is no general and unstructured plasticity; different species have different developmental affordances and biases that affect their evolutionary trajectories in a taxon-specific manner (Lala et al., 2024; Müller & Newman, 2003). Animals’ behavioral plasticity is both a consequence and a driver of their cognitive evolution, which is tailored to their ecological and social niches.

Evolvability, the capacity to generate adaptive diversity, is often continuous with and dependent on phenotypic plasticity. During the early evolution of animal morphology, generative physicochemical processes, as well as the cybernetic dynamics of gene regulatory networks, imposed specific constraints and opened up specific affordances that can explain directional and saltational evolutionary changes in basic animal form and function (Newman, 2012). Plasticity in the form of neural learning has played a central role in animal and human evolution. It was suggested that the evolution of associative learning spurred the Cambrian explosion 540 million years ago, when almost all animal phyla appeared (Ginsburg & Jablonka, 2019). A more recent and well-studied example of evolution driven by selection for behavior is domestication; selection by humans for docile behavior in animals led to the evolution of multiple behavioral and morphological changes such as those seen in the domestic dog. Another example of behavior-driven evolution is the evolution of symbolic language, which was at least partially driven by cultural changes in pre-symbolic human communication in early human societies (Jablonka & Lamb, 2014; Lala et al., 2024).

Extended heredity

The EES highlights the developmental aspects of heredity. Soft inheritance—that is, the inheritance of developmentally acquired (induced, learned, constructed) variations that depend on the nonrandom and often functional responses of the organisms to the conditions of life—is assumed to be ubiquitous and play an important role in evolution. Heritable developmental variations can occur at the epigenetic, behavioral, and symbolic levels (Bonduriansky & Day, 2018; Jablonka & Lamb, 2014, 2020) [see Cultural Evolution]. Heredity is therefore not confined to the function-blind copying and transmission of random variation in DNA (even at the DNA levels, some variations are developmentally regulated).

There are many mechanisms that lead to the generation and transmission of persistent and heritable developmental variations. Such mechanisms are called epigenetic mechanisms. At the cellular level, they lead to the generation of several types of acquired variations in gene expression that involve variations in DNA methylation patterns, in chromatin modifications, in profiles of regulatory RNAs, in self-sustaining loops, and in three-dimensional protein conformations (Jablonka & Lamb, 2014, 2020). Novel, function-relevant acquired epigenetic variations are generated during development, and through developmental reconstruction, they are transmitted to subsequent generations. Social learning such as that observed in mammals, birds, and human symbol-based transmission are additional important routes of transfer of behaviors and behavioral aptitudes between generations in social nonhuman animals and humans, respectively (Jablonka & Lamb, 2014; Lala et al., 2024) [see Social Learning].

There are also other, partially external sources of transmissible variations: symbionts (e.g., microbes) that have significant phenotypic effects are transferred within and between lineages, and material and informational resources can be transmitted between generations through niche construction. The different modes and systems of inheritance interact; the developmental architecture biases the direction of selection, changes in animal behavior may guide selection, and epigenetic variations can bias DNA mutations as well as affect their selection (Jablonka & Lamb, 2020).

Ecology and agency

The EES offers a developmental view of ecology, focusing on the agency of organisms and their active construction of the niches in which they live and which they leave to their descendants (Odling-Smee et al., 2003). Organisms construct both their external environment (e.g., soil properties constructed by earthworms or the nests built by birds) and their social environment through their social interactions and social learning. Organisms also construct the internal developmental niches of their offspring by ensuring that they acquire their symbionts (e.g., their microbiome). The effects of these external and internal constructions are legacies that are transmitted to their descendants.

The evolutionary effects of symbiosis in both micro- and macroevolution, which are common and can lead to rapid (and sometimes dramatic) evolutionary transformations (Lala et al., 2024; Margulis, 1998), are highlighted by EES proponents. Hybridization, which occurs when distinct species interbreed and create offspring (called hybrids) that are sometimes fertile, and horizontal gene transfer (the transfer of genes between lineages, for example, through infection) are additional processes that are considered evolutionarily important by EES advocates. The patterns and rates of phylogenetic change driven by symbiotic relations, horizontal gene transfer, and hybridization are not overwhelmingly gradual and tree-like, since gene sharing and the merging of lineages can lead to rapid changes and weblike phylogenetic patterns.

Extended selection

Development selection, based on exploration and stabilization mechanisms, is considered an important aspect of developmental plasticity. The EES extends the notion of selection by incorporating processes of intra-organismal selection that are either based on differential replication as in the immune system or on differential persistence that is not replication based. An important example of the latter process is neuronal selection, which underlies memory and learning in animals and has been crucial for the evolution of cognition and consciousness (Changeux, 1997; Edelman, 1993; Ginsburg & Jablonka, 2019) [see The Mind-Body Problem]. The effects of developmental selection in both plants and animals can be directly, as well as indirectly, transmitted to descendants and affect their evolution (Buss, 1987; Jablonka & Lamb, 2014).

In addition to classical Darwinian selection that can occur among any type of reproducing organism, there are modes of selection that can be attributed only to particular types of organism. These include human artificial selection (which involves rational, reflection-based choice) and selection driven by perceived and desired goals that only phenomenally conscious animals can exert. Both desire-driven and rationality-driven selection have important evolutionary effects in animals and humans, respectively, as well as in the species with which they interact.

Evolutionary analysis according to this EES perspective starts at the level of the developmental system under investigation—usually the active, interacting, individual organism. It is assumed that the generation and transmission of the heritably varying traits occurring at this level drive changes at lower levels. A recent, general methodology based on the combination of the minimal number of recursive steps required to generate a complex assembly and the number of copies of such an assembly provides a unifying framework that enables the detection of different types of selection—chemical, ontogenetic, and phylogenetic—bridging the gulf between physics, biology, and psychology (Sharma et al., 2023).

Questions, controversies, and new developments

There is much to discover about epigenetic inheritance mechanisms, developmental biases, and niche construction. For example, it is necessary to systematically survey symbiotic interactions, better understand the molecular mechanisms of the inheritance of epigenetic variations through sex cells, and to construct more integrative models based on EES and systems biology.

Since the EES leads to a synthesis bringing together selection-focused (Darwinian) and development-focused (Lamarckian) evolutionary considerations, it is vehemently opposed by evolutionary biologists adhering to the modern synthesis. The critics claim that soft inheritance is not stable enough to have evolutionary importance and that the other aspects of the EES are not novel (e.g., Charlesworth et al., 2017; Wray et al., 2014). However, the wealth of new discoveries on the ubiquity of soft inheritance and its evolutionary effects (Lala et al., 2024), the progress in uncovering the molecular underpinnings of some epigenetic inheritance processes, the developments in epigenetic medicine, and the theoretical coherence of the different core aspects of the EES (Jablonka & Lamb, 2020; Lala et al., 2024) are supportive of the EES view.

Broader connections

The EES requires the rethinking of basic concepts such as individuality, identity, evolvability, homology, and the relation between ultimate and proximate causation (Jablonka & Lamb, 2020). The EES outlook suggests that current existential challenges, including the future epigenetic effects of climate change and the developmental and evolutionary effects of artificial intelligence technologies on individual and collective psychology, can have far-reaching evolutionary effects. The EES framework also offers a new way of linking the philosophy of biology with the philosophy of mind via studies of the biology and evolution of consciousness (Ginsburg & Jablonka, 2019) and by highlighting the shared dynamic organizational principles of mental and behavioral learning and memory and morphogenetic processes of development (Levin, 2022). The focus on learning and ontogenetic development and the continuity of these processes with evolutionary and historical changes allow the construction of a common language promising to bridge the disciplinary gulf between biology, psychology, the social sciences, and the humanities.

Further reading

• Chiu, L. (2022). Extended evolutionary synthesis. A review of the latest scientific research. John Templeton Foundation.

• Jablonka, E., & Lamb, M. J. (2020). Inheritance systems and the extended evolutionary synthesis. Cambridge University Press.

• Laland, K. N., Uller, T., Feldman, M. W., Sterelny, K., Müller, G. B., Moczek, A., Jablonka, E., & Odling-Smee, J. (2015). The extended evolutionary synthesis: Its structure, assumptions and predictions. Proceedings of the Royal Society B, 282(1813), 20151019. https://doi.org/10.1098/rspb.2015.1019

• Müller, G. B. (2017). Why an extended evolutionary synthesis is necessary. Interface Focus, 7(5), 20170015. https://doi.org/10.1098/rsfs.2017.0015