Thomas C. Scott-Phillips

Evolutionary Theory and the Ultimate–Proximate Distinction in the Human Behavioral Sciences

To properly understand behavior, we must obtain both ultimate and proximate explanations. Put briefly, ultimate explanations are concerned with why a behavior exists, and proximate explanations are concerned with how it works. These two types of explanation are complementary and the distinction is critical to evolutionary explanation. We are concerned that they have become conflated in some areas of the evolutionary literature on human behavior. This article brings attention to these issues. We focus on three specific areas: the evolution of cooperation, transmitted culture, and epigenetics. We do this to avoid confusion and wasted effort—dangers that are particularly acute in interdisciplinary research. Throughout this article, we suggest ways in which misunderstanding may be avoided in the future.

Language evolution in the laboratory

The historical origins of natural language cannot be observed directly. We can, however, study systems that support language and we can also develop models that explore the plausibility of different hypotheses about how language emerged. More recently, evolutionary linguists have begun to conduct language evolution experiments in the laboratory, where the emergence of new languages used by human participants can be observed directly. This enables researchers to study both the cognitive capacities necessary for language and the ways in which languages themselves emerge. One theme that runs through this work is how individual-level behaviours result in population-level linguistic phenomena. A central challenge for the future will be to explore how different forms of information transmission affect this process.

Signalling signalhood and the emergence of communication

A unique hallmark of human language is that it uses signals that are both learnt and symbolic. The emergence of such signals was therefore a defining event in human cognitive evolution, yet very little is known about how such a process occurs. Previous work provides some insights on how meaning can become attached to form, but a more foundational issue is presently unaddressed. How does a signal signal its own signalhood? That is, how do humans even know that communicative behaviour is indeed communicative in nature? We introduce an experimental game that has been designed to tackle this problem. We find that it is commonly resolved with a bootstrapping process, and that this process influences the final form of the communication system. Furthermore, sufficient common ground is observed to be integral to the recognition of signalhood, and the emergence of dialogue is observed to be the key step in the development of a system that can be employed to achieve shared goals.

THE NICHE CONSTRUCTION PERSPECTIVE: A CRITICAL APPRAISAL

Niche construction refers to the activities of organisms that bring about changes in their environments, many of which are evolutionarily and ecologically consequential. Advocates of niche construction theory (NCT) believe that standard evolutionary theory fails to recognize the full importance of niche construction, and consequently propose a novel view of evolution, in which niche construction and its legacy over time (ecological inheritance) are described as evolutionary processes, equivalent in importance to natural selection. Here, we subject NCT to critical evaluation, in the form of a collaboration between one prominent advocate of NCT, and a team of skeptics. We discuss whether niche construction is an evolutionary process, whether NCT obscures or clarifies how natural selection leads to organismal adaptation, and whether niche construction and natural selection are of equivalent explanatory importance. We also consider whether the literature that promotes NCT overstates the significance of niche construction, whether it is internally coherent, and whether it accurately portrays standard evolutionary theory. Our disagreements reflect a wider dispute within evolutionary theory over whether the neo‐Darwinian synthesis is in need of reformulation, as well as different usages of some key terms (e.g., evolutionary process).

Combinatorial quorum sensing allows bacteria to resolve their social and physical environment

Significance Many bacterial species engage in a form of cell–cell communication known as quorum sensing (QS). Despite great progress in unravelling the molecular mechanisms of QS, controversy remains over its functional role. There is disagreement over whether QS surveys bacterial cell density or rather environmental properties like diffusion or flow, and moreover there is no consensus on why many bacteria use multiple signal molecules. We develop and test a new conceptual framework for bacterial cell–cell communication, demonstrating that bacteria can simultaneously infer both their social (density) and physical (mass-transfer) environment, given combinatorial (nonadditive) responses to multiple signals with distinct half-lives. Our results also show that combinatorial communication is not restricted solely to primates and is computationally achievable in single-celled organisms. Quorum sensing (QS) is a cell–cell communication system that controls gene expression in many bacterial species, mediated by diffusible signal molecules. Although the intracellular regulatory mechanisms of QS are often well-understood, the functional roles of QS remain controversial. In particular, the use of multiple signals by many bacterial species poses a serious challenge to current functional theories. Here, we address this challenge by showing that bacteria can use multiple QS signals to infer both their social (density) and physical (mass-transfer) environment. Analytical and evolutionary simulation models show that the detection of, and response to, complex social/physical contrasts requires multiple signals with distinct half-lives and combinatorial (nonadditive) responses to signal concentrations. We test these predictions using the opportunistic pathogen Pseudomonas aeruginosa and demonstrate significant differences in signal decay between its two primary signal molecules, as well as diverse combinatorial responses to dual-signal inputs. QS is associated with the control of secreted factors, and we show that secretome genes are preferentially controlled by synergistic “AND-gate” responses to multiple signal inputs, ensuring the effective expression of secreted factors in high-density and low mass-transfer environments. Our results support a new functional hypothesis for the use of multiple signals and, more generally, show that bacteria are capable of combinatorial communication.

How Darwinian is cultural evolution

Darwin-inspired population thinking suggests approaching culture as a population of items of different types, whose relative frequencies may change over time. Three nested subtypes of populational models can be distinguished: evolutionary, selectional and replicative. Substantial progress has been made in the study of cultural evolution by modelling it within the selectional frame. This progress has involved idealizing away from phenomena that may be critical to an adequate understanding of culture and cultural evolution, particularly the constructive aspect of the mechanisms of cultural transmission. Taking these aspects into account, we describe cultural evolution in terms of cultural attraction, which is populational and evolutionary, but only selectional under certain circumstances. As such, in order to model cultural evolution, we must not simply adjust existing replicative or selectional models but we should rather generalize them, so that, just as replicator-based selection is one form that Darwinian selection can take, selection itself is one of several different forms that attraction can take. We present an elementary formalization of the idea of cultural attraction.

ON THE CORRECT APPLICATION OF ANIMAL SIGNALLING THEORY TO HUMAN COMMUNICATION

The defining problem of animal signalling theory is how reliable communication systems remain stable. The problem comes into sharp focus when signals take an arbitrary form, as human words do. Many researchers, particularly those in evolutionary linguistics, assume that the handicap principle is the only recognised solution to this paradox, and hence conclude that the process that underpins reliability in humans must be exceptional. However, there are other examples of cheap yet reliable signals in nature, and corresponding processes that may explain such examples. This paper reviews these alternatives and concludes that by far the most likely explanation of the stability of human communication is our ability to assess individual reputation: we hold the threat of social exclusion against those who signal unreliably and hence keep their utterances reliable.

Meaning in animal and human communication

Abstract What is meaning? While traditionally the domain of philosophy and linguistics, this question, and others related to it, is critical for cognitive and comparative approaches to communication. This short essay provides a concise and accessible description of how the term meaning can and should be used, how it relates to ‘intentional communication’, and what would constitute good evidence of meaning in animal communication, in the sense that is relevant for comparisons with human language.

The Social Evolution of Language, and the Language of Social Evolution:

Recent years have witnessed an increased interest in the evolution of the human capacity for language. Such a project is necessarily interdisciplinary. However, that interdisciplinarity brings with it a risk: terms with a technical meaning in their own field are used wrongly or too loosely by those from other backgrounds. Unfortunately, this risk has been realized in the case of language evolution, where many of the terms of social evolution theory (reciprocal altruism, honest signaling, etc.) are incorrectly used in a way that suggests that certain key fundamentals have been misunderstood. In particular the distinction between proximate and ultimate explanations is often lost, with the result that several claims made by those interested in language evolution are epistemically incoherent. However, the correct application of social evolution theory provides simple, clear explanations of why language most likely evolved and how the signals used in language — words — remain cheap yet arbitrary.

Combinatorial Communication in Bacteria: Implications for the Origins of Linguistic Generativity

Combinatorial communication, in which two signals are used together to achieve an effect that is different to the sum of the effects of the component parts, is apparently rare in nature: it is ubiquitous in human language, appears to exist in a simple form in some non-human primates, but has not been demonstrated in other species. This observed distribution has led to the pair of related suggestions, that (i) these differences in the complexity of observed communication systems reflect cognitive differences between species; and (ii) that the combinations we see in non-human primates may be evolutionary pre-cursors of human language. Here we replicate the landmark experiments on combinatorial communication in non-human primates, but in an entirely different species, unrelated to humans, and with no higher cognition: the bacterium Pseudomonas aeruginosa. Using the same general methods as the primate studies, we find the same general pattern of results: the effect of the combined signal differs from the composite effect of the two individual signals. This suggests that advanced cognitive abilities and large brains do not necessarily explain why some species have combinatorial communication systems and others do not. We thus argue that it is premature to conclude that the systems observed in non-human primates are evolutionarily related to language. Our results illustrate the value of an extremely broad approach to comparative research.