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

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.

Meaning in great ape communication: summarising the debate.

Does non-human great ape communication have meaning in the same way as human words (and some other human behaviours)? I recently argued that the answer to this question is most likely to be in the negative (Scott-Phillips in Anim Cogn 18(3):801-805, 2015a). Here, I (1) briefly respond to criticism of this view; (2) describe exactly what sort of empirical study could settle the matter; and (3) discuss what the best working hypotheses should be, in the absence of definitive empirical studies.

Meaning in animal and human communication.

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 mutual relevance of teaching and cultural attraction.

As Kline envisages, there is an important relationship between cultural attraction and teaching. The very function of teaching is to make the content taught an attractor. Teaching, moreover, typically fulfills its function by exploiting a variety of factors of cultural attraction that help make its content learnable and teachable.

Group-level traits can be studied with standard evolutionary theory.

Smaldino's target article draws on and seeks to add to a literature that has partially rejected orthodox, gene-centric evolutionary theory. However, orthodox theory has much to say about group-level traits. The target article does not reference or refute these views, and provides no explicit arguments for this narrow approach. In this commentary we: (i) give two examples of topics that the target article might and probably should have discussed (cultural epidemiology and the psychology of individual differences); and (ii) argue that the orthodox approach has much more to say about the emergence of group-level traits than the target article recognises, or gives credit for.

How do communication systems emerge?

Communication involves a pair of behaviours--a signal and a response--that are functionally interdependent. Consequently, the emergence of communication involves a chicken-and-egg problem: if signals and responses are dependent on one another, then how does such a relationship emerge in the first place? The empirical literature suggests two solutions to this problem: ritualization and sensory manipulation; and instances of ritualization appear to be more common. However, it is not clear from a theoretical perspective why this should be the case, nor if there are any other routes to communication. Here, we develop an analytical model to examine how communication can emerge. We show that: (i) a state of non-interaction is evolutionarily stable, and so communication will not necessarily emerge even when it is in both parties' interest; (ii) the conditions for sensory manipulation are more stringent than for ritualization, and hence ritualization is likely to be more common; and (iii) communication can arise by a third route, when the intention to communicate can itself be communicated, but this may be limited to humans. More generally, our results demonstrate the utility of a functional approach to communication.

Pragmatics and the aims of language evolution.

Pragmatics has historically played a relatively peripheral role in language evolution research. This is a profound mistake. Here I describe how a pragmatic perspective can inform language evolution in the most fundamental way: by making clear what the natural objects of study are, and hence what the aims of the field should be.

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.

Simulating the real origins of communication.

How communication systems emerge is a topic of relevance to several academic disciplines. Numerous existing models, both mathematical and computational, study this emergence. However, with few exceptions, these models all build some form of communication into their initial specification. Consequently, what these models study is how communication systems transition from one form to another, and not how communication itself emerges in the first place. Here we present a new computational model of the emergence of communication which, unlike previous models, does not pre-specify the existence of communication. We conduct two experiments using this model, in order to derive general statements about how communication systems emerge. The two main routes to communication that we identify correspond with findings from the empirical literature on the evolution of animal signals. We use this finding to explain when and why we should expect communication to emerge in nature. We also compare our model to experimental research on the origins of human communication systems, and hence show that humans are an important exception to the general trends we observe. We argue that this is because humans, and probably only humans, are able to 'signal signalhood', i.e. to express communicative intentions.

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.

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).

Why is combinatorial communication rare in the natural world, and why is language an exception to this trend?

In a combinatorial communication system, some signals consist of the combinations of other signals. Such systems are more efficient than equivalent, non-combinatorial systems, yet despite this they are rare in nature. Why? Previous explanations have focused on the adaptive limits of combinatorial communication, or on its purported cognitive difficulties, but neither of these explains the full distribution of combinatorial communication in the natural world. Here, we present a nonlinear dynamical model of the emergence of combinatorial communication that, unlike previous models, considers how initially non-communicative behaviour evolves to take on a communicative function. We derive three basic principles about the emergence of combinatorial communication. We hence show that the interdependence of signals and responses places significant constraints on the historical pathways by which combinatorial signals might emerge, to the extent that anything other than the most simple form of combinatorial communication is extremely unlikely. We also argue that these constraints can be bypassed if individuals have the socio-cognitive capacity to engage in ostensive communication. Humans, but probably no other species, have this ability. This may explain why language, which is massively combinatorial, is such an extreme exception to nature's general trend for non-combinatorial communication.

Three-year-olds hide their communicative intentions in appropriate contexts.

Human cooperative communication involves both an informative intention that the recipient understands the content of the signal and also a (Gricean) communicative intention that the recipient recognizes that the speaker has an informative intention. The degree to which children understand this 2-layered nature of communication is the subject of some debate. One phenomenon that would seem to constitute clear evidence of such understanding is hidden authorship, in which informative acts are produced but with the communicative intent behind them intentionally hidden. In this study, 3- and 5-year-old children were told that an adult was seeking a toy but wanted to find it on her own. Children of both ages often did something to make the toy easier for the adult to see while at the same time concealing their actions in some way. This suggests that by the age of 3, children are able to separate the multiple layers of intentionality involved in human cooperative communication.

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.

The evolution of relevance.

With human language, the same utterance can have different meanings in different contexts. Nevertheless, listeners almost invariably converge upon the correct intended meaning. The classic Gricean explanation of how this is achieved posits the existence of four maxims of conversation, which speakers are assumed to follow. Armed with this knowledge, listeners are able to interpret utterances in a contextually sensible way. This account enjoys wide acceptance, but it has not gone unchallenged. Specifically, Relevance Theory offers an explicitly cognitive account of utterance interpretation that presents a radical challenge to the neo-Gricean paradigm. Evolutionary considerations are one way in which we can choose between competing theories. A simple game-theoretic model of the evolution of communication is presented, and it is used to derive a number of basic qualities that will be satisfied by all evolved communication systems. These qualities are observed to precisely predict the foundational principles of Relevance Theory. The model thus provides biological support for that enterprise in general, and for the plausibility of the cognitive mechanisms that it describes in particular.

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.