THE EVOLUTION OF INDIVIDUAL VARIATION IN COMMUNICATION STRATEGIES

Communication is a process in which senders provide information via signals and receivers respond accordingly. This process relies on two coevolving conventions: a “sender code” that determines what kind of signal is to be sent given the sender's state; and a “receiver code” that determines the appropriate responses to different signal types. By means of a simple but generic model, we show that polymorphic sender and receiver strategies emerge naturally during the evolution of communication, and that the number of alternative strategies observed at equilibrium depends on the potential for error in signal production. Our model suggests that alternative communication strategies will evolve whenever senders possess imperfect information about their own quality or state, signals are costly, and genetic mechanisms allow for a correlation between sender and receiver behavior. These findings provide an explanation for recent reports of individual differences in communication strategies, and suggest that the amount of individual variation that can be expected in communication systems depends on the type of information being conveyed. Our model also suggests a link between communication and the evolution of animal personalities, which is that individual differences in the production and interpretation of signals can result in consistent differences in behavior.     

Honest signalling through chemicals by elephants with applications for care and conservation

Chemical signals are difficult to fake because they are often directly associated with phenotype and physiological condition, and hence likely to be honest signals for intraspecific communication. Chemical signals may be modified after release by the sender or by the environment. The proximate and ultimate signal meanings are dependent not only on the condition of the sender, but also on the physiological status of the receiver. Understanding the relationships and linkage among signal modality, signal function and receiver response is an essential first step before using natural signals for animal care and conservation. Our studies on chemical communication in Asian and African elephants combine observational and experimental work in captive and wild settings to further this understanding. Recent discoveries of pheromones in Asian elephants and the biochemistry of these compounds provide strong evidence that such chemical signals are honest indicators of reproductive status. Chemically identifying the signals and verifying their functional context with statistically robust behavioural studies are essential aspects for understanding the communication system. Additionally, the investigative process of discovering, identifying and verifying the function of chemical signals among captive elephants offers safe and stimulating enrichments. The knowledge garnered from such studies has potential conservation benefits for managing wild elephant populations. A firm foundation of scientific information is required for successful behavioural investigations and applied conservation and enrichment components.     

Begging and sibling competition: how should offspring respond to their rivals?

Godfray's influential model of competitive begging predicted that offspring should respond to each other's behavior, displaying more intensely when competing with needier rivals. Empirical tests of this prediction have, however, yielded equivocal results. Here, I develop a series of evolutionarily stable strategy models of begging as a signal of need, which show that this prediction holds only for competitive aspects of display that influence the division of food among the brood. No such response is expected for cooperative begging (which influences the total level of provisioning by the parent), and the models even predict the opposite trend under some circumstances (where the indirect costs of extracting additional resources from the parent are high). These contrasting sets of predictions may help to explain the varying empirical results obtained by studies of sibling interaction. Cooperative (as opposed to competitive) begging is likely to be of greater significance in cases where dominant young can gain direct control of allocation (or enjoy some competitive advantage). Dominants are then predicted to parasitize the efforts of their weaker rivals and reduce their own investment in cooperative signaling while continuing to claim a disproportionately large share of the resources provided by the parent.     

Implications of variation in worker body size for the honey bee recruitment system

Honey bee scouts seek food from flowers, return to the colony, and may perform a dance used to recruit dance followers to the flowers. Variation in body size of workers may result in the communication of misinformation because some information acquired by the scout and signaled to recruits is affected by body size. I tested two predictions of this hypothesis. (1) Recruitment communication takes place between bees of similar size despite the withincolony size distribution. (2) There is an inverse relationship between the size variation of foraging honey bees (Apis mellifera)and the rate at which nectar is returned to the colony. A positive relationship was found between the size of a dancer and that of its dance followers, which together comprise a dance group. There was less variation in size within dance groups than among groups. These two factors effectively lower the difference in size between signal sender and signal receiver and may enhance the flow of accurate size-dependent information. Also, an inverse relationship between size variation and rate of nectar intake was detected in each of six colonies using partial correlation analysis. This may be due to communication of misinformation when size variance is higher. The relationship was statistically significant in two colonies and the combined results were significant. The results of the first study suggest the generally weak relationships found in this second study.     

Information,influence, and the causal-explanatory role of content in understanding receiver responses

Sceptics of informational terminology argue that by attributing content to signals, we fail to address nonhuman animal communication on its own terms. Primarily, we ignore that communication is sender driven: i.e. driven by the intrinsic physical properties of signals, themselves the result of selection pressures acting on signals to influence receivers in ways beneficial for senders. In contrast, information proponents argue that this ignores the degree to which communication is, in fact, receiver driven. The latter argue that an exclusive focus on the intrinsic mechanical properties of signals cannot explain why receivers respond as they do. This is because receivers are not prisoners of sender influence. They possess response flexibility, and so we can only explain why receivers respond to signals as they do by positing that receivers ‘derive information’ from signals. I argue that, while basically true, this response flexibility can take one of two forms depending on the causal-explanatory role of information in understanding the response of the receiver: diachronic, on the one hand; and synchronic, on the other. In species with diachronic response flexibility only, information is derived by receivers from signals in a minimal sense. In such cases, information is an ultimate explanatory construct: one underpinned by historical facts at the population level. Alternatively, in species with synchronic response flexibility, information is derived by receivers from signals in a richer sense. Here, information is a proximate explanatory construct: one underpinned by cognitive-mechanistic facts at the level of the individual organism. Without recognising the different ways information can be derived from signals, and the different causal-explanatory roles (ultimate vs proximate) information can play in understanding alternate kinds of receiver flexibility (diachronic vs synchronic), proponents of information leave themselves open to the charge of anthropomorphising some signalling systems.     

CONSPIRATORIAL WHISPERS AND CONSPICUOUS DISPLAYS: GAMES OF SIGNAL DETECTION

Recent models of signaling have assumed that the expenditure required to ensure detection of a display is negligible and have concentrated instead on the costs that may be necessary to maintain honesty. Such models predict that individuals who share the same interests are likely to communicate using “conspiratorial whispers,” signals that are cheap and inconspicuous. Here, I present a game-theoretical model of signal detection (in a noisy environment, in the presence of potential eavesdroppers), which demonstrates that the idea of conspiratorial whispers is far too simplistic. It is true that in “cooperative” signaling systems (where signalers attempt to elicit responses that are beneficial for receivers), signal cost is not required to maintain honesty. However, some level of expenditure is still needed to ensure that a signal is reliably detected. Moreover, there exists a conflict of interest between signalers and receivers over the division of this expenditure. To predict the stable level of display in such cases, one needs to know how this conflict of interest will be resolved. The model reveals that the outcome may range from a whisper to a conspicuous and costly (though still conspiratorial) display. The more closely related the receiver is to the signaler, the greater the level of signal exaggeration that is expected—the opposite prediction to that of honest signaling models.     

A Direct Brain-to-Brain Interface in Humans

We describe the first direct brain-to-brain interface in humans and present results from experiments involving six different subjects. Our non-invasive interface, demonstrated originally in August 2013, combines electroencephalography (EEG) for recording brain signals with transcranial magnetic stimulation (TMS) for delivering information to the brain. We illustrate our method using a visuomotor task in which two humans must cooperate through direct brain-to-brain communication to achieve a desired goal in a computer game. The brain-to-brain interface detects motor imagery in EEG signals recorded from one subject (the “sender”) and transmits this information over the internet to the motor cortex region of a second subject (the “receiver”). This allows the sender to cause a desired motor response in the receiver (a press on a touchpad) via TMS. We quantify the performance of the brain-to-brain interface in terms of the amount of information transmitted as well as the accuracies attained in (1) decoding the sender’s signals, (2) generating a motor response from the receiver upon stimulation, and (3) achieving the overall goal in the cooperative visuomotor task. Our results provide evidence for a rudimentary form of direct information transmission from one human brain to another using non-invasive means.     

Evolutionary novelty in communication between the sexes

The diversity of signalling traits within and across taxa is vast and striking, prompting us to consider how novelty evolves in the context of animal communication. Sexual selection contributes to diversification, and here we endeavour to understand the initial conditions that facilitate the maintenance or elimination of new sexual signals and receiver features. New sender and receiver variants can occur through mutation, plasticity, hybridization and cultural innovation, and the initial conditions of the sender, the receiver and the environment then dictate whether a novel cue becomes a signal. New features may arise in the sender, the receiver or both simultaneously. We contend that it may be easier than assumed to evolve new sexual signals because sexual signals may be arbitrary, sexual conflict is common and receivers are capable of perceiving much more of the world than just existing sexual signals. Additionally, changes in the signalling environment can approximate both signal and receiver changes through a change in transmission characteristics of a given environment or the use of new environments. The Anthropocene has led to wide-scale disruption of the environment and may thus generate opportunity to directly observe the evolution of new signals to address questions that are beyond the reach of phylogenetic approaches.     

Population variation and genetic control of pheromone communication systems in moths

The nature of variation in moth pheromone communication systems and its genetic control is critical for the evolution of these systems and for their role in mate-finding and reproductive isolation. Significant additive genetic variance has been demonstrated in female pheromone production in monomorphic populations. However, corresponding variance in male pheromone response with respect to the blend which is most active, appears to be low, as can be expected from the general asymmetry of sexual selection. Pheromone polymorphism and differences in communication systems between closely related species seem to be controlled by a small number of Mendelian genes. The critical biosynthetic steps, which are influenced by the genes controlling pheromone production, can be inferred from our present knowledge of pheromone biosynthesis. A mechanistic understanding of how male response to pheromones is controlled is further away. Failure to demonstrate genes with pleiotropic effects on critical sender and receiver traits, suggests that reciprocal selection on genetically independent sender and receiver loci is the more likely explanation for the generally observed coordination between pheromone production and response in moth populations. Further research on the evolutionary significance of Z-linked pheromone response genes, documented in several species, should be encouraged. Investigations, in the field, of populations that vary in pheromone production and response, and theoretical and empirical studies of the survival of sender and receiver mutants in otherwise monomorphic populations are also important to advance our understanding of how pheromone communication systems evolve.     

Coevolution of Male and Female Response Preferences to Sexual Signals in Music Frogs

Male signaling influences both female choice and male-male competition. Although male signaling characteristics and female preferences have been shown to coevolve in many species, few studies have examined whether male signal characteristics and male receiver responses related to male-male competition also coevolve. The present study tested the hypothesis that male and female signal receiver preferences may coevolve in parallel for frogs in the genus Babina by comparing the acoustic structure of male advertisement calls of four closely related and geographically isolated Babina species. Then we assessed the behavioral responses of both male and female B. daunchina(Emei music frog) to male call playbacks from each of the four species. The results support the hypothesis that male and female signal receiver preferences have coevolved in this species. Specifically, both male and female B. daunchina respond strongly to the heterospecific calls of B. hainanensis, suggesting that preexisting biases exist in both females and males. Both male and female individuals showed a slight response to the calls of B. adenopleura while no response was evoked by the calls of B. lini. The manifestation of similar response profiles in male and female B. daunchina to the calls of the four species support the idea that male and female signal receiver preferences evolved in parallel and that the origin of these receiver biases reflects adaptations dependent on the same neural and cognitive systems in both sexes.     

A teleosemantic approach to information in the brain

The brain is often taken to be a paradigmatic example of a signaling system with semantic and representational properties, in which neurons are senders and receivers of information carried in action potentials. A closer look at this picture shows that it is not as appealing as it might initially seem in explaining the function of the brain. Working from several sender-receiver models within the teleosemantic framework, I will first argue that two requirements must be met for a system to support genuine semantic information: 1. The receiver must be competent—that is, it must be able to extract rewards from its environment on the basis of the signals that it receives. 2. The receiver must have some flexibility of response relative to the signal received. In the second part of the paper, this initial framework will be applied to neural processes, pointing to the surprising conclusion that signaling at the single-neuron level is only weakly semantic at best. Contrary to received views, neurons will have little or no access to semantic information (though their patterns of activity may carry plenty of quantitative, correlational information) about the world outside the organism. Genuine representation of the world requires an organism-level receiver of semantic information, to which any particular set of neurons makes only a small contribution.     

Interaction effects between sender and receiver processes in indirect transmission of Campylobacter jejuni between broilers

ABSTRACT: BACKGROUND: Infectious diseases in plants, animals and humans are often transmitted indirectly between hosts (or between groups of hosts), i.e. via some route through the environment instead of via direct contacts between these hosts. Here we study indirect transmission experimentally, using transmission of Campylobacter jejuni (C. jejuni) between spatially separated broilers as a model system. We distinguish three stages in the process of indirect transmission; (1) an infectious "sender" excretes the agent, after which (2) the agent is transported via some route to a susceptible "receiver", and subsequently (3) the receiver becomes colonised by the agent. The role of the sender and receiver side (stage 1 and stage 3) was studied here by using acidification of the drinking water as a modulation mechanism. RESULTS: In the experiment one control group and three treatment groups were monitored for the presence of C. jejuni by taking daily cloacal swabs. The three treatments consisted of acidification of the drinking water of the inoculated animals (the senders), acidification of the drinking water of the susceptible animals (the receivers) or acidification of the drinking water of both inoculated and susceptible animals. In the control group 12 animals got colonised out of a possible 40, in each treatment groups 3 animals out of a possible 40 were found colonised with C. jejuni. CONCLUSIONS: The results of the experiments show a significant decrease in transmission rate (beta) between the control group and treatments group (p < 0.01 for all groups) but not between different treatments; there is a significant negative interaction effect when both the sender and the receiver group receive acidified drinking water (p = 0.01). This negative interaction effect could be due to selection of bacteria already at the sender side thereby diminishing the effect of acidification at the receiver side.     

Substrate-Borne Vibration Mediates Intrasexual Agonism in the New Zealand Cook Strait Giant Weta (<Emphasis Type="Italic">Deinacrida rugosa</Emphasis>)

Substrate-borne vibrational communication is a common mode of information transfer in many invertebrate groups, with vibration serving as both primary and secondary signal channels in Orthopterans. The Cook Strait giant weta, Deinacrida rugosa (Orthoptera: Anostostomatidae), is an endangered New Zealand insect whose communication system has not been previously described. After field observations of intraspecific interactions in D. rugosa provided preliminary evidence for substrate-borne vibrational communication in the species, we sought to identify the following: vibrational signal structure, the mechanism of signal production, whether signal production is a sexually dimorphic trait, whether substrate-borne signals encode information regarding sender size, the primary social context in which vibration is utilized and finally, the function of vibrational signaling in the species. We used laser Doppler vibrometry to show that D. rugosa males produce low frequency (DF?=?37.00?±?1.63 Hz) substrate-borne vibrations through dorso-ventral tremulation. Rarely produced by females, male signals appear to target rivals while both are in the direct physical presence of a female. Tremulatory responses to playbacks were only produced by males in male-male-female trial contexts, and neither sex exhibited walking vibrotaxis to playback signals, indicating that substrate-borne vibrational signals are not likely a component of the courtship repertoire. While we found that vibrational signal structure was not closely related to signaler size, males that initiated male-male signaling bouts held a significant advantage in contests.     

Primate Communication: By Nature Honest, or by Experience Wise?

We review evolutionary views on honesty and deception and their application to studies of nonhuman primate communication. There is evidence that some primate signals are likely to be accurate on the basis of costliness. They appear most often in contexts that include overtly competitive interactions in which unrelated individuals have limited access to information about one another. However, both game theoretic models and most empirical work suggest that costly signals are not often likely to be the basis for honest communication in nonhuman primates. Inexpensive signaling can exist in contexts wherein communication occurs among related animals, something common among many nonhuman primate societies. Another condition in which inexpensive signaling is possible and that is also typical of nonhuman primates, is when sender and receiver both benefit from coordinated interactions. Additionally, when individuals interact repeatedly and can use past interactions to assess the honesty of signals and to modify future response to signals, low-cost signals can evolve. Nonhuman primates appear to deal with the problem of deception via skeptical responding, which can be largely accounted for by learning rules and the fact that they live in stable social groups and can recognize one another and recall past interactions.     

Coevolutionary interactions in a host–parasite system

Interactions between parasitic cuckoos and their hosts represent a classic example of coevolution, where adaptations in the parasite to exploit the host select for defences, which in turn select for new parasite adaptations. Current interactions between the two parties may be at an evolutionary equilibrium or, alternatively, a coevolutionary arms race may be taking place. By taking into account the effect of gene flow in 15 European magpie ( Pica pica ) populations, we studied the coevolutionary interactions with its brood parasite, the great spotted cuckoo ( Clamator glandarius ). Our results suggest that, in Europe, magpies and cuckoos are engaged in an ongoing coevolutionary process because, despite controlling for the large amounts of gene flow among different magpie populations, we still found a positive relationship between host defence (i.e. foreign egg recognition and rejection) and parasite selection pressure.     

Economic models of animal communication

Many models of animal signal evolution fail to incorporate an explicit strategy for receivers prior to the evolution of signals. When reasonable assumptions are made for such strategies, we have shown that there is a minimal accuracy of signal coding that is required before receivers should attend to signals (Bradbury & Vehrencamp 1998, Principles of Animal Communication). Depending upon the relative payoffs of correct and incorrect decisions by receivers, this minimal accuracy can be quite high. Here we use this result to explain why so many signals appear to be traits that provided useful information to receivers before becoming ritualized into signals. Our model also supports one prediction of sensory drive models: that latent preferences may selectively favour some signal precursors over others. However, it imposes a serious constraint on sensory drive by requiring that there be sufficient benefits to a receiver to compensate for the costs of disrupting the optimal receiver strategy used before exploitation. Finally, we discuss the overlap between signal honesty and accuracy and show how senders that completely disagree with receivers about appropriate receiver decisions may still benefit by providing moderately honest and accurate signals. Copyright 2000 The Association for the Study of Animal Behaviour.     

Chasing long-range evolutionary couplings in the AlphaFold era

Coevolution between protein residues is normally interpreted as direct contact. However, the evolutionary record of a protein sequence contains rich information that may include long-range functional couplings, couplings that report on homo-oligomeric states or even conformational changes. Due to the complexity of the sequence space and the lack of structural information on various members of a protein family, it has been difficult to effectively mine the additional information encoded in a multiple sequence alignment (MSA). Here, taking advantage of the recent release of the AlphaFold (AF) database we attempt to identify coevolutionary couplings that cannot be explained simply by spatial proximity. We propose a simple computational method that performs direct coupling analysis on a MSA and searches for couplings that are not satisfied in any of the AF models of members of the identified protein family. Application of this method on 2012 protein families suggests that ~12% of the total identified coevolving residue pairs are spatially distant and more likely to be disordered than their contacting counterparts. We expect that this analysis will help improve the quality of coevolutionary distance restraints used for structure determination and will be useful in identifying potentially functional/allosteric cross-talk between distant residues.     

Contract theory for the evolution of cooperation: The right incentives attract the right partners

Partner choice is a critical stage of many biological interactions, from mating to cooperation. When the quality of the potential partners is unknown, one way to choose is to rely on signaling: costly signals can reveal the quality of the sender and allow the receiver to choose. In some cases, however, signaling (or an active choice based on signals) is not possible, for example in the initiation of the symbiosis between the squid Euprymna scolopes and the bioluminescent bacterium Vibrio fischeri. How is partner choice possible in this and other similar cases? I show that in a game with asymmetric information without signaling, imposing a deliberate cost for establishing the interaction allows the non-informed individual to attract the right partner if the cost induces only high quality individuals to accept the interaction. Furthermore, imposing different costs and rewards may induce the informed individuals to screen themselves according to their types, and therefore allow the non-informed individual to establish an association with the correct partners in the absence of signaling.     

Facilitating play through communication: significance of teeth exposure in the gorilla play face

Primate facial expressions (FEs) likely play an important role in primate society: through facial signals, individuals can potentially send and receive information and may benefit from coordinating their behavior accordingly. Many primates use a relaxed open mouth (ROM) facial display or “play face” (PF) during play behavior, where the mouth is open but teeth are covered. In addition to this conventional PF, however, Western Lowland gorillas (Gorilla gorilla gorilla) also use a full PF where the upper teeth are exposed. As the teeth are similarly exposed in the bared-teeth expression (which is a signal of appeasement, submission and/or affiliation), the full PF may be a blend of the PF and bared-teeth face, and have a different signal function to the PF alone. Focal animal sampling of captive Western Lowland gorillas (N=10) showed that the full PF was more often observed in intense rather than gentle play, and intense play bouts that featured the full PF were longer than those that featured only the PF. Both expressions were associated with an increase in affinitive behavior between sender and receiver postplay, but only the full PF was associated with an increase higher than that of play alone. Overall, the findings suggest that the full PF has an additional role in coordinating and maintaining play, possibly though reducing uncertainty in the receiver and confirming that play is only play.     

Uncovering signal transduction networks from high-throughput data by integer linear programming

Signal transduction is an important process that transmits signals from the outside of a cell to the inside to mediate sophisticated biological responses. Effective computational models to unravel such a process by taking advantage of high-throughput genomic and proteomic data are needed to understand the essential mechanisms underlying the signaling pathways. In this article, we propose a novel method for uncovering signal transduction networks (STNs) by integrating protein interaction with gene expression data. Specifically, we formulate STN identification problem as an integer linear programming (ILP) model, which can be actually solved by a relaxed linear programming algorithm and is flexible for handling various prior information without any restriction on the network structures. The numerical results on yeast MAPK signaling pathways demonstrate that the proposed ILP model is able to uncover STNs or pathways in an efficient and accurate manner. In particular, the prediction results are found to be in high agreement with current biological knowledge and available information in literature. In addition, the proposed model is simple to be interpreted and easy to be implemented even for a large-scale system.