Timothy M. Waring and Zachary T. Wood, Long-term gene–culture coevolution and the human evolutionary transition, Proceedings of the Royal Society B, Vol. 288 No. 1952, 09 June 2021: https://doi.org/10.1098/rspb.2021.0538
Abstract: It has been suggested that the human species may be undergoing an evolutionary transition in individuality (ETI). But there is disagreement about how to apply the ETI framework to our species, and whether culture is implicated as either cause or consequence. Long-term gene–culture coevolution (GCC) is also poorly understood. Some have argued that culture steers human evolution, while others proposed that genes hold culture on a leash. We review the literature and evidence on long-term GCC in humans and find a set of common themes. First, culture appears to hold greater adaptive potential than genetic inheritance and is probably driving human evolution. The evolutionary impact of culture occurs mainly through culturally organized groups, which have come to dominate human affairs in recent millennia. Second, the role of culture appears to be growing, increasingly bypassing genetic evolution and weakening genetic adaptive potential. Taken together, these findings suggest that human long-term GCC is characterized by an evolutionary transition in inheritance (from genes to culture) which entails a transition in individuality (from genetic individual to cultural group). Thus, research on GCC should focus on the possibility of an ongoing transition in the human inheritance system.
The human species may be undergoing an evolutionary transition in individuality (ETI) [1–6]. The evolutionary transitions framework explains how new levels of biological organization (such as multicellularity, or eusociality) emerge from subsidiary units (such as cells or individuals) through the formation of cooperative groups [6–10]. First proposed by Maynard Smith & Szathmáry , evolutionary transitions are thought to unfold via a shift in the dominant level of selection from competitive individuals to well-integrated functional groups [8,11]. These transitions exhibit a common set of patterns, including new divisions of labour, the loss of full individual autonomy and reproductive control, and the rise of new routes of information transmission [6,7,10]. Humans exhibit many patterns thought to be characteristic of an ETI, including the scale of our cooperation with non-kin, the prominence of human language and our complex, full-time division of labour. Consequently, it has been repeatedly hypothesized that human evolution is in some way characterized by an evolutionary transition [1–6]. However, there is little consensus on how to apply an evolutionary transition framework to humans. Here, we review research and evidence on the human ETI to clarify the roles of culture and genes in a human evolutionary transition.
One line of research applies the ETI framework to humans by focusing solely on biological and genetic evidence. We might call such a transition a ‘genetic ETI’. Research in this theme commonly concludes that humans have begun, but not completed, such an evolutionary transition [2,5,6], having evolved some characteristics of superorganisms but not others. For example, while humans are highly interdependent, sharing resources in large cooperative groups, we also remain highly autonomous and capable of individual reproduction. Stearns  reasons that factors such as migration (which reduces genetic differentiation between groups) and trade (which increases interdependence between groups) are likely to undermine the force of genetic group selection necessary to complete a transition. Szathmáry  concludes that human ‘group structure is too transitory to allow for a major transition in evolution in a purely biological sense’. Kesebir  also argues that, given the fluidity of human groups and our capacity to hold multiple group identities, the superorganism concept is an inappropriate description of human evolutionary status. Viewed from this perspective, aspects of human society, social organization and social cognition may impede a human genetic ETI.
A different strain of research suggests that human society may also undergo evolutionary transitions through cultural processes. We might therefore consider a ‘cultural ETI’, in which changes in cultural and social organization are facilitated by cultural evolution, as distinct from a ‘genetic ETI’ in which changes in biological organization are facilitated solely by genetic evolution. In a cultural ETI, the scale of cultural and social organization shifts from single humans, or smaller social units to larger groups composed of many such units via cultural evolution operating without necessarily changing genes. Thus, before a cultural ETI, the predominant levels of control, adaptation and inheritance of cultural traits would be at the subsidiary level (e.g. single humans, families, regional polities), while after a cultural ETI, these would be at the level of the cultural group (e.g. groups, clans, nations). This strain of research focuses on cultural patterns as evidence [1,2,4,6,12]. For more than a century, anthropologists and sociologists have debated whether society represents a novel level of organization (i.e. a ‘superorganic’ entity). Spencer [13,14] saw society as a superorganic, emergent property of interacting individuals, as did Kroeber , who drew on Darwinian principles to explain social change. Recently, cultural evolutionists have argued that human society constitutes a ‘crude superorganism’ , with effective but imperfect mechanisms to achieve unity of action and resolve conflict within a group . Within evolutionary anthropology, a long-term process of cultural selection acting on social groups is considered a primary hypothesis for the emergence of societal features with group-level functionality . Cultural group selection has been proposed as an explanation for large, hierarchical societies [18,19]. Gowdy & Krall [2,20] suggest that the emergence of hierarchical agricultural societies represents a major transition to an ‘ultrasocial’, rather than fully eusocial, state. Powers et al.  argue that society has experienced multiple evolutionary transitions in the emergence of large, complex, cooperative societies facilitated by the human ability to create institutions, which make cooperation individually beneficial and facilitate division of labour. From this perspective, cultural ETIs may occur quite readily, but the implications for genetic and biological organization are unclear and under-developed.
In summary, there is a general consensus that humans exhibit signs of being involved in an evolutionary transition in individuality. But there is significant disagreement about the status and details of a human ETI. Research in biology suggests that culture and social organization may be impeding a genetic ETI, while research in anthropology suggests that multiple cultural ETIs may have occurred, yet they remain somehow disjunct from a genetic ETI. These two approaches to the question of human ETI differ in their evaluation of its status, because they differ in their relevant definitions and nature of evidence. We believe these differences have obscured a deeper understanding of human evolution and highlight our lack of knowledge about how genes and culture are likely to interact in the long term. We therefore organize this review around three emergent themes in human sociobiological research. First, cultural inheritance exhibits greater adaptive capacity and generates more group-level adaptations than genetic inheritance. Second, cultural evolution determines the outcomes of gene–culture coevolution (GCC) more frequently than genetic evolution. Finally, patterns in long-term GCC point to an evolutionary transition in both inheritance and individuality (ETII) from genetic individuals to cultural groups. We argue that this synthesis resolves much of the apparent disagreement and confusion around a possible human ETI.
H/t Tyler Cowen.
I left the following comment at Cowen's Marginal Revolution:
I take Gene Culture Coevolution (GCC) as a given, though the mechanisms are obscure. But no version of it is adequate to account for cultural evolution. Within any version of this general framework (including cultural group selection) it is at the physical individual, a phenotype, that we account for evolutionary benefit. Richard Dawkins had something else in mind when, in The Selfish Gene (1976) he proposed the idea of the meme. He conceived of the meme as a cultural individual that reaps the benefit of evolution. I believe that Dawkins was right in making this proposal.
Alas, Dawkins was clueless about how to develop the idea. For one thing, he didn't know whether this meme should be thought of as something inside the brain, flitting from one brain to another, or whether it was extrasomatic, like the sounds and words of a song. He seems to have settled on locating it in the head, as some kind of homunculus. Dan Dennett certainly conceived it that way and managed to steer the whole conversation in that direction, thus destroying the idea.
I've written a short and informal working paper as a guide to the varieties of thinking about cultural evolution: A quick guide to cultural evolution for humanists. Here is a somewhat longer and more complex and subtle paper in the formal academic literature where I argue for the coordinator – a term I chose to replace "meme", which has been rendered useless for serious discussion – as the extrasomatic genetic component in the evolution of musical culture: “Rhythm Changes” Notes on Some Genetic Elements in Musical Culture. The abstract:
An entity known as Rhythm Changes is analyzed as a genetic entity in musical culture. Because it functions to coordinate the activities of musicians who are playing together it can be called a coordinator. It is a complex coordinator in that it is organized on ﬁve or six levels, each of which contains coordinators that function in other musical contexts. Musicians do not acquire (that is, learn) such a coordinator through “transfer” from one brain to another. Rather, they learn to construct it from publically available performance materials. This particular entity is derived from George Gershwin’s tune “I Got Rhythm” and is the harmonic trajectory of that tune. But it only attained independent musical status after about two decades of performances. Being a coordinator is thus not intrinsic to the entity itself, but is rather a function of how it comes to be used in the musical system. Recent argument suggests that biological genes are like this as well.