The evolution of social learning rules: Payoff-biased and frequency-dependent biased transmission

Humans and other animals do not use social learning indiscriminately, rather, natural selection has favoured the evolution of social learning rules that make selective use of social learning to acquire relevant information in a changing environment. We present a gene-culture coevolutionary analysis of a small selection of such rules (unbiased social learning, payoff-biased social learning and frequency-dependent biased social learning, including conformism and anti-conformism) in a population of asocial learners where the environment is subject to a constant probability of change to a novel state. We define conditions under which each rule evolves to a genetically polymorphic equilibrium. We find that payoff-biased social learning may evolve under high levels of environmental variation if the fitness benefit associated with the acquired behaviour is either high or low but not of intermediate value. In contrast, both conformist and anti-conformist biases can become fixed when environment variation is low, whereupon the mean fitness in the population is higher than for a population of asocial learners. Our examination of the population dynamics reveals stable limit cycles under conformist and anti-conformist biases and some highly complex dynamics including chaos. Anti-conformists can out-compete conformists when conditions favour a low equilibrium frequency of the learned behaviour. We conclude that evolution, punctuated by the repeated successful invasion of different social learning rules, should continuously favour a reduction in the equilibrium frequency of asocial learning, and propose that, among competing social learning rules, the dominant rule will be the one that can persist with the lowest frequency of asocial learning.     

The evolution of vocabulary

Human language is unique among the communication systems of the natural world. The vocabulary of human language is unique in being both culturally transmitted and symbolic. In this paper I present an investigation into the factors involved in the evolution of such vocabulary systems. I investigate both the cultural evolution of vocabulary systems and the biological evolution of learning rules for vocabulary acquisition. Firstly, vocabularies are shown to evolve on a cultural time-scale so as to fit the expectations of learners-a population's vocabulary adapts to the biases of the learners in that population. A learning bias in favour of one-to-one mappings between meanings and words leads to the cultural evolution of communicatively optimal vocabulary systems, even in the absence of any explicit pressure for communication. Furthermore, the pressure to conform to the biases of learners is shown to outweigh natural selection acting on cultural transmission. Human language learners appear to bring a one-to-one bias to the acquisition of vocabulary systems. The functionality of human vocabulary may therefore be a consequence of the biases of human language learners. Secondly, the evolutionary stability of genetically transmitted vocabulary learning biases is investigated using both static and dynamic models. A one-to-one learning bias, which leads to the cultural evolution of optimal communication, is shown to be evolutionarily stable. However, the evolution de novo of this bias is complicated by the cumulative nature of the cultural evolution of vocabulary systems. This suggests that the biases of human language learners may not have evolved specifically and exclusively for the acquisition of communicatively functional vocabulary.     

Interactions of genetic and cultural evolution: Models and examples

This paper proposes models and examples of five principal modes of interaction between genes and culture in human evolution. Because genes and culture ultimately interact in the minds of individuals, the models are focused on individual level processes of constrained microevolution. The central hypotheses are (1) that cultural evolution as well as genetic evolution commonly proceeds by the differential transmission of alternative instructions among individuals, (2) that genetic and cultural processes directly interact through mutual influence on each other's differentials of transmission in a population, (3) that the cultural process is often self-selecting by its own criteria, and (4) that these criteria generally operate to enhance rather than oppose human adaptation. Evolutionary change at higher levels, which is particularly important in sociocultural evolution, is interpreted as restructuring the nature and extent of the variability available at the individual level. To clarify the conceptual differences of the models and hopefully to stimulate related analyses in other areas, I discuss selected examples of each of these interactions. I conclude with some remarks on the relative importance of the models to human ecology and evolution.     

Autocatalysis in cultural ecology: model ecosystems and the dynamics of biocultural evolution

Using a well-known mathematical model frequently applied in theoretical population dynamics, certain ecological mechanisms are investigated that are inherent in the organic evolution of cultural capacities in man. Culture is argued to involve ecological interactions exhibiting analogies to the interaction of chemical species in autocatalytic biomolecular reactions. In the model, biocultural evolution proceeds by more and more broadening ecological niches and, thus, releasing competitive selection pressure on the populations involved. This, in turn, facilitates the maintenance of polymorphism in these populations as well as the individual acquisition of organic traits through learning and cultural transmission. The result is that the genetic variance in phenotypic expressions decreases at an accelerated rate.     

Primate origins and the evolution of angiosperms

Traditionally, the morphological traits of primates were assumed to be adaptations to an arboreal way of life. However, Cartmill [1972] pointed out that a number of morphological traits characteristic of primates are not found in many other arboreal mammals. He contends that orbital convergence and grasping extremities indicate that the initial divergence of primates involved visual predation on insects in the lower canopy and undergrowth of the tropical forest. However, recent research on nocturnal primates does not support the visually-oriented predation theory. Although insects were most likely important components of the diets of the earliest euprimates, it is argued here that visual predation was not the major impetus for the evolution of the adaptive traits of primates. Recent paleobotanical research has yielded evidence that a major evolutionary event occurred during the Eocene, involving the angiosperms and their dispersal agents. As a result of long-term diffuse coevolutionary interactions with flowering plants, modern primates, bats, and plant-feeding birds all first arose around the Paleocene-Eocene boundary and became the major seed dispersers of modern tropical flora during the Eocene. Thus, it is suggested here that the multitude of resources available on the terminal branches of the newly evolved angiosperm, rain forest trees led to the morphological adaptations of primates of modern aspect.     

Animal personalities and their implications for complex signaling

Animal personalities have been a major focus of behavioral ecology over the past decade. Consistent individual dif ferences in behavior have been found across taxa, and have been shown to influence a range of ecological processes. The role of personalities in sexual selection has been considered, and examples exist that show selection for personality traits with both assortative and disassortative mating patterns between personality types. One overlooked aspect of the personality and sexual se lection literature is the potential for personalitysignaling interactions, specifically with complex signaling. Complex signaling is a diverse topic in itself, and in short, consists of multiple signals within one or more modalities that interact to elicit a receiver response. Research into complex signaling has been thorough, although at times studies discover complex signaling systems that fail to fit into one of the existing hypotheses in the literature. Here, we argue that personalities may interact with complex signal ing, which should be considered by researchers of both personality and sexual selection and communication. We describe several ways in which personalitycomplex signaling interactions could affect both the signaler and receiver, and the way in which they may drive personalityspecific signals as well as receiver preferences. Finally, we discuss how considering personality in com plex signaling studies may inform theory as well as improve the ability of researchers to accurately describe its function.     

Short-term rates of parasite evolution predict the evolution of host diversity

Coevolution with parasites has been implicated as an important factor driving the evolution of host diversity. Studies to date have focussed on gross effects of parasites: how host diversity differs in the presence vs. absence of parasites. But parasite-imposed selection is likely to show rapid variation through time. It is unclear whether short-term fluctuations in the strength of parasite-imposed selection tend to affect host diversity, because increases in host diversity are likely to be constrained by both the supply of genetic variation and ecological processes. We followed replicate populations of coevolving, initially isogenic, bacteria and phages through time, measuring host diversity (with respect to bacterial colony morphologies), host density and rates of parasite evolution. Both host density and time-lagged rates of parasite evolution were good independent predictors of the magnitude of bacterial within- and between-population diversities. Rapid parasite evolution and low host density decreased host within-population diversity, but increased between-population diversity. This study demonstrates that short-term changes in the rate of parasite evolution can predictably drive patterns of host diversity.     

The evolution of insect/vertebrate associations

The evolution of close vertebrate associations has occurred in seven orders of insects, resulting in a great diversity of interactions which range from commensalism to true parasitism. The evolution of each taxon of vertebrate associates is discussed in turn, some new ideas on the development of certain groups are presented and, on a broader scale, a general model for the evolution of ectoparasitic insects is proposed. It argues that all vertebrate associates have evolved along one of two macroevolutionary pathways which differ only in the sequencing of adaptations facilitating host association and host feeding. These pathways lead to parasite types which differ greatly in their life history and intimacy of host association.
Some microevolutionary processes influencing the diversification of ectoparasites are discussed, in particular the process of insect/vertebrate coevolution and the forms this may take. Host specificity, one consequence of coevolution, is recognised as an important factor influencing the structure of ectoparasite communities, and a hypothesis is presented that competition between ectoparasite species, mediated by host defensive responses, is also important in determining community structure.     

A two level mutation-selection model of cultural evolution and diversity

Cultural evolution is a complex process that can happen at several levels. At the level of individuals in a population, each human bears a set of cultural traits that he or she can transmit to its offspring (vertical transmission) or to other members of his or her society (horizontal transmission). The relative frequency of a cultural trait in a population or society can thus increase or decrease with the relative reproductive success of its bearers (individual’s level) or the relative success of transmission (called the idea’s level). This article presents a mathematical model on the interplay between these two levels. The first aim of this article is to explore when cultural evolution is driven by the idea’s level, when it is driven by the individual’s level and when it is driven by both. These three possibilities are explored in relation to (a) the amount of interchange of cultural traits between individuals, (b) the selective pressure acting on individuals, (c) the rate of production of new cultural traits, (d) the individual’s capacity to remember cultural traits and to the population size. The aim is to explore the conditions in which cultural evolution does not lead to a better adaptation of individuals to the environment. This is to contrast the spread of fitness-enhancing ideas, which make individual bearers better adapted to the environment, to the spread of “selfish” ideas, which spread well simply because they are easy to remember but do not help their individual bearers (and may even hurt them). At the same time this article explores in which conditions the adaptation of individuals is maximal. The second aim is to explore how these factors affect cultural diversity, or the amount of different cultural traits in a population. This study suggests that a larger interchange of cultural traits between populations could lead to cultural evolution not improving the adaptation of individuals to their environment and to a decrease of cultural diversity.     

Experimental models for testing hypotheses about cumulative cultural evolution

The rapid appearance (over evolutionary time) of the cognitive skills and complex inventions of modern humans has been attributed to “cumulative cultural evolution” (CCE), the accumulation of knowledge and skills over generations. To date, researchers have only been able to speculate about the reasons for the apparent absence of this phenomenon in nonhumans, and it has not been possible to test hypotheses regarding the mechanisms underlying it. Here, we show that it is possible to demonstrate CCE under laboratory conditions by simulating generational succession through the repeated removal and replacement of human participants within experimental groups. We created “microsocieties” in which participants were instructed to complete simple tasks using everyday materials. In one of our procedures, participants were instructed to build a paper aeroplane which flew as far as possible, and in the other, they were instructed to construct a tower of spaghetti which was as tall as possible. We show that, in both cases, information accumulates within the groups such that later generations produce designs which are more successful than earlier ones. These methods offer researchers a window to understanding CCE, allowing for experimental manipulation and hypothesis testing.     

Modularity and the units of evolution

Summary While many developmental processes (e. g., gene networks or signaling pathways) are astonishingly conserved during evolution, they may be employed differently in different metazoan taxa or may be used multiply in different contexts of development. This suggests that these processes belong to building blocks or modules, viz., highly integrated parts of the organism, which develop and/or function relatively independent from other parts. Such modules may be relatively easy to dissociate from other modules and, therefore, could also serve as units of evolution. However, in order to further explore the implications of modularity for evolution, the vague notion of “modularity” as well as its relation to concepts like “unit of evolution” need to be more precisely specified. Here, a module is characterized as a certain type of dynamic pattern of couplings among the constituents of a process. It may or may not form a spatially contiguous unit. A unit of selection is defined as a unit of those constituents of a reproducing process/system, which exists in different variants and acts as a non-decomposable unit of fitness and variant reproduction during a particular selection process. The more general notion of a unit of evolution is characterized as a nondecomposable unit of constituents with reciprocal fitness dependence, be it due to fitness epistasis or due to the lack of independent variability. Because such fitness dependence may only be observed for some combinations of variants, several constituents may act as a unit of evolution only with a certain probability (coevolution probability). It is argued, that under certain conditions modules are likely to act as units of evolution with high coevolution probabilities, because there is likely to be a close tie between the pattern of couplings of the constituents of a reproducing system and their interdependent fitness contributions. Moreover and contrary to the traditional dichotomy of genes versus organisms as units of selection, modules tend to be more important in delimiting actual units of selection than either organisms or genes, because they are less easily disrupted by recombination than organisms, while having less contextsensitive fitness values than genes. Finally, it is suggested that the evolution of modularity is self-reinforcing, because the flexibility of intermodular connections facilitates the recombination among modules and their multiple employment in new contexts.     

Convergent transformation and selection in cultural evolution

In biology, natural selection is the main explanation of adaptations and it is an attractive idea to think that an analogous force could have the same role in cultural evolution. In support of this idea, all the main ingredients for natural selection have been documented in the cultural domain. However, the changes that occur during cultural transmission typically result in convergent transformation, non-random cultural modifications, casting some doubts on the importance of natural selection in the cultural domain. To progress on this issue more empirical research is needed. Here, using nearly half a million experimental trials performed by a group of baboons (Papio papio), we simulate cultural evolution under various conditions of natural selection and do an additional experiment to tease apart the role of convergent transformation and selection. Our results confirm that transformation strongly constrain the variation available to selection and therefore strongly limit its impact on cultural evolution. Surprisingly, in our study, transformation also enhances the effect of selection by stabilising cultural variation. We conclude that, in culture, selection can change the evolutionary trajectory substantially in some cases, but can only act on the variation provided by (typically biased) transformation.     

Essential conditions for evolution of communication within a species

A major obstacle in analyzing the evolution of information exchange and processing is our insufficient understanding of the underlying signaling and decision-making biological mechanisms. For instance, it is unclear why are humans unique in developing such extensive communication abilities. To treat this problem, a method based on the mutual information approach is developed that evaluates the information content of communication between interacting individuals through correlations of their behavior patterns (rather than calculating the information load of exchanged discrete signals, e.g. Shannon entropy). It predicts that correlated interactions of the indirect reciprocity type together with affective behavior and selection rules changing with time are necessary conditions for the emergence of significant information exchange. Population size variations accelerate this development. These results are supported by evidence of demographic bottlenecks, distinguishing human from other species’ (e.g. apes) evolution line. They indicate as well new pathways for evolution of information based phenomena, such as intelligence and complexity.     

A phylogenetic method for detecting positive epistasis in gene sequences and its application to RNA virus evolution

RNA virus genomes are compact, often containing multiple overlapping reading frames and functional secondary structure. Consequently, it is thought that evolutionary interactions between nucleotide sites are commonplace in the genomes of these infectious agents. However, the role of epistasis in natural populations of RNA viruses remains unclear. To investigate the pervasiveness of epistasis in RNA viruses, we used a parsimony-based computational method to identify pairs of co-occurring mutations along phylogenies of 177 RNA virus genes. This analysis revealed widespread evidence for positive epistatic interactions at both synonymous and nonsynonymous nucleotide sites and in both clonal and recombining viruses, with the majority of these interactions spanning very short sequence regions. These findings have important implications for understanding the key aspects of RNA virus evolution, including the dynamics of adaptation. Additionally, many comparative analyses that utilize the phylogenetic relationships among gene sequences assume that mutations represent independent, uncorrelated events. Our results show that this assumption may often be invalid.     

Non-random pre-transcriptional evolution in HIV-1. A refutation of the foundational conditions for neutral evolution

The complete base sequence of HIV-1 virus and GP120 ENV gene were analyzed to establish their distance to the expected neutral random sequence. An especial methodology was devised to achieve this aim. Analyses included: a) proportion of dinucleotides (signatures); b) homogeneity in the distribution of dinucleotides and bases (isochores) by dividing both segments in ten and three sub-segments, respectively; c) probability of runs of bases and No-bases according to the Bose-Einstein distribution. The analyses showed a huge deviation from the random distribution expected from neutral evolution and neutral-neighbor influence of nucleotide sites. The most significant result is the tremendous lack of CG dinucleotides (p < 10(-50) ), a selective trait of eukaryote and not of single stranded RNA virus genomes. Results not only refute neutral evolution and neutral neighbor influence, but also strongly indicate that any base at any nucleotide site correlates with all the viral genome or sub-segments. These results suggest that evolution of HIV-1 is pan-selective rather than neutral or nearly neutral.     

Cultural selection drives the evolution of human communication systems

Human communication systems evolve culturally, but the evolutionary mechanisms that drive this evolution are not well understood. Against a baseline that communication variants spread in a population following neutral evolutionary dynamics (also known as drift models), we tested the role of two cultural selection models: coordination- and content-biased. We constructed a parametrized mixed probabilistic model of the spread of communicative variants in four 8-person laboratory micro-societies engaged in a simple communication game. We found that selectionist models, working in combination, explain the majority of the empirical data. The best-fitting parameter setting includes an egocentric bias and a content bias, suggesting that participants retained their own previously used communicative variants unless they encountered a superior (content-biased) variant, in which case it was adopted. This novel pattern of results suggests that (i) a theory of the cultural evolution of human communication systems must integrate selectionist models and (ii) human communication systems are functionally adaptive complex systems.     

Voting with your feet: Payoff biased migration and the evolution of group beneficial behavior

Human migration is nonrandom. In small scale societies of the past, and in the modern world, people tend to move to wealthier, safer, and more just societies from poorer, more violent, less just societies. If immigrants are assimilated, such nonrandom migration can increase the occurrence of culturally transmitted beliefs, values, and institutions that cause societies to be attractive to immigrants. Here we describe and analyze a simple model of this process. This model suggests that long run outcomes depend on the relative strength of migration and local adaptation. When local adaption is strong enough to preserve cultural variation among groups, cultural variants that make societies attractive always predominate, but never drive alternative variants to extinction. When migration predominates, outcomes depend both on the relative attractiveness of alternative variants and on the initial sizes of societies that provide and receive immigrants.     

Culture and the evolution of human cooperation

The scale of human cooperation is an evolutionary puzzle. All of the available evidence suggests that the societies of our Pliocene ancestors were like those of other social primates, and this means that human psychology has changed in ways that support larger, more cooperative societies that characterize modern humans. In this paper, we argue that cultural adaptation is a key factor in these changes. Over the last million years or so, people evolved the ability to learn from each other, creating the possibility of cumulative, cultural evolution. Rapid cultural adaptation also leads to persistent differences between local social groups, and then competition between groups leads to the spread of behaviours that enhance their competitive ability. Then, in such culturally evolved cooperative social environments, natural selection within groups favoured genes that gave rise to new, more pro-social motives. Moral systems enforced by systems of sanctions and rewards increased the reproductive success of individuals who functioned well in such environments, and this in turn led to the evolution of other regarding motives like empathy and social emotions like shame.     

Ethics,evolution and culture

Recent work in the fields of evolutionary ethics and moral psychology appears to be converging on a single empirically- and evolutionary-based science of morality or ethics. To date, however, these fields have failed to provide an adequate conceptualisation of how culture affects the content and distribution of moral norms. This is particularly important for a large class of moral norms relating to rapidly changing technological or social environments, such as norms regarding the acceptability of genetically modified organisms. Here we suggest that a science of morality/ethics can benefit from adopting a cultural evolution or gene-culture coevolution approach, which treats culture as a second, separate evolutionary system that acts in parallel to biological/genetic evolution. This cultural evolution approach brings with it a set of established theoretical concepts (e.g. different cultural transmission mechanisms) and empirical methods (e.g. evolutionary game theory) that can significantly improve our understanding of human morality.