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Although anthropology was the first academic discipline to investigate cultural change, many other disciplines have made noteworthy contributions to understanding what influences the adoption of new behaviors. Drawing on a broad, interdisciplinary literature covering both humans and nonhumans, we examine ( a) which features of behavioral traits make them more transmissible, ( b) which individual characteristics of inventors promote copying of their inventions, ( c) which characteristics of individuals make them more prone to adopting new behaviors, ( d) which characteristics of dyadic relationships promote cultural transmission, ( e) which properties of groups (e.g., network structures) promote transmission of traits, and ( f) which characteristics of groups promote retention, rather than extinction, of cultural traits. One of anthropology's strengths is its readiness to adopt and improve theories and methods from other disciplines, integrating them into a more holistic approach; hence, we identify approaches that might be particularly useful to biological and cultural anthropologists, and knowledge gaps that should be filled.

Mate copying (MC), a type of non-independent mate choice, is a behaviour observed in many vertebrate and few invertebrate species. It occurs when an individual’s sexual preference gets socially inclined toward those of its conspecifics. Theoretical models and experimental studies of MC have been limited to choice between two options (or morphs). In this study we model the evolution of morphology in a population under varying extents of mate copying. Multiple morphs and multiple observations are considered and a generalisable model is presented. We quantify the level of copying needed to achieve pseudo-stable equilibria in the presence of multiple morphs. Moving closer to realistic scenarios we support our theoretical development with simulations and discuss relevance for empirical model systems.

Although conformity as a major driver for human cultural evolution is a well-accepted and intensely studied phenomenon, its importance for non-human animal culture has been largely overlooked until recently. This limited for decades the possibility of studying the roots of human culture. Here, we provide a historical review of the study of conformity in both humans and non-human animals. We identify gaps in knowledge and propose an evolutionary route towards the sophisticated cultural processes that characterize humanity. A landmark in the study of conformity is Solomon Asch's famous experiment on humans in 1955. By contrast, interest in conformity among evolutionary biologists has only become salient since the turn of the new millennium. A striking result of our review is that, although studies of conformity have examined many biological contexts, only one looked at mate choice. This is surprising because mate choice is probably the only context in which conformity has self-reinforcing advantages across generations. Within a metapopulation, i.e. a group of subpopulations connected by dispersing individuals, dispersers able to conform to the local preference for a given type of mate have a strong and multigenerational fitness advantage. This is because once females within one subpopulation locally show a bias for one type of males, immigrant females who do not conform to the local trend have sons, grandsons, etc. of the non-preferred phenotype, which negatively and cumulatively affects fitness over generations in a process reminiscent of the Fisher runaway process. This led us to suggest a sex-driven origin of conformity, indicating a possible evolutionary route towards animal and human culture that is rooted in the basic, and thus ancient, social constraints acting on mating preferences within a metapopulation. In a generic model, we show that dispersal among subpopulations within a metapopulation can effectively maintain independent Fisher runaway processes within subpopulations, while favouring the evolution of social learning and conformity at the metapopulation scale; both being essential for the evolution of long-lasting local traditions. The proposed evolutionary route to social learning and conformity casts surprising light on one of the major processes that much later participated in making us human. We further highlight several research avenues to define the spectrum of conformity better, and to account for its complexity. Future studies of conformity should incorporate experimental manipulation of group majority. We also encourage the study of potential links between conformity and mate copying, animal aggregations, and collective actions. Moreover, validation of the sex-driven origin of conformity will rest on the capacity of human and evolutionary sciences to investigate jointly the origin of social learning and conformity. This constitutes a stimulating common agenda and militates for a rapprochement between these two currently largely independent research areas.

High levels of within-population behavioural variation can have drastic demographic consequences, thus changing the evolutionary fate of populations. A major source of within-population heterogeneity is personality. Nonetheless, it is still relatively rarely accounted for in social learning studies that constitute the most basic process of cultural transmission. Here, we performed in female mosquitofish ( Gambusia holbrooki ) a social learning experiment in the context of mate choice, a situation called mate copying (MC), and for which there is strong evidence that it can lead to the emergence of persistent traditions of preferring a given male phenotype. When accounting for the global tendency of females to prefer larger males but ignoring differences in personality, we detected no evidence for MC. However, when accounting for the bold–shy dichotomy, we found that bold females did not show any evidence for MC, while shy females showed significant amounts of MC. This illustrates how the presence of variation in personality can hamper our capacity to detect MC. We conclude that MC may be more widespread than we thought because many studies ignored the presence of within-population heterogeneities.

International audience; The zebrafish Danio rerio is an important model organism, but little is known about its mating preferences and how these are influenced by personality traits like boldness. In this study, we tested two strains of zebrafish and addressed whether females used social information to build a mating preference, a behavior called mate copying, and whether this social learning was affected by boldness. Thus, we provided positive social information for small males to test whether female zebrafish changed their mate preference after observing a pair of a small and a large male with a demonstrator female next to the small one. After that, we tested the observer female in a test maze to evaluate boldness. We found no significant evidence for mate copying as females did not change their preference for the small male after witnessing the large male alone and the small male interacting with another female and chose consistently larger males in a control without opportunity to copy. Whether the female was defined as shy or bold had no effect on mate copying. We conclude that mate copying is probably inexistent or only relatively weak in this species.

The social environment offers fish complex information about the quality, performance, personality and other cues of potential mates and competitors simultaneously. It is likely, therefore, that the environmental information regarding the context of mate choice is perceived and processed differently in species and sexes in respect to lateralisation. The present study comparatively assessed visual lateralisation behaviour in response to different social or sexual stimuli in three closely related poeciliid species (P. latipinna, P. mexicana, P. formosa) in comparison to a more distantly related species (P. reticulata). Individuals were presented with four different social or sexual stimuli that were tested against a control stimulus; (a) a conspecific male, (b) a conspecific female, (c) a heterosexual conspecific pair, (d) three conspecific females (shoal). In order to approach a target stimulus, focal fish had to perform detours to the right or left of a vertically straight-shaped barrier. The three closely related poeciliid species, P. latipinna, P. mexicana, P. formosa, appeared to have a general tendency to turn right (i.e., left-eye preference), whereas the more distantly related P. reticulata males and females showed an overall bias to the left (i.e., right-eye preference) in response to various social-sexual incitements. Moreover, body size seemed to significantly influence especially the males' detour behaviour, with smaller males acting in opposition to their larger conspecifics in response to certain social stimuli. In this case, smaller and larger Poecilia spp. males responded in the same way as smaller and larger males of the other three poeciliid species. Therefore, results possibly point to differences in the degree of general social behaviour between closely and more distantly related species and mating motivation amongst larger and smaller individuals when placed in a novel social environment. Hence, present results possibly suggest a sex-specific functional lateralisation for the analysis of visual information and seem to support the closer ancestral relationships between the Poecilia spp. tested in this study and the more distantly related guppies in terms of their left-right lateralisation. Generally, present results suggest that functional asymmetries in behaviour could be widespread among vertebrates, thus supporting the hypothesis of an early evolution of lateralisation in brain and behaviour.

We are grateful to the Templeton World Charity Foundation, Inc. for funding this work and to the Diverse Intelligences research community for valuable conversations around these themes. S. Nöbel acknowledges IAST funding from the French National Research Agency (ANR) under the Investissements d’Avenir program, grant ANR-17-EUR-0010 and support by the Laboratoires d’Excellence TULIP (ANR-10-LABX-41). EA and MS acknowledge support from the US Army Research Office (W911NF‐17‐1‐0017 to EA). Innovation—the combination of invention and social learning—can empower species to invade new niches via cultural adaptation. Social learning has typically been regarded as the fundamental driver for the emergence of traditions and thus culture. Consequently, invention has been relatively understudied outside the human lineage—despite being the source of new traditions. This neglect leaves basic questions unanswered: what factors promote the creation of new ideas and practices? What affects their spread or loss? We critically review the existing literature, focusing on four levels of investigation: traits (what sorts of behaviours are easiest to invent?), individuals (what factors make some individuals more likely to be inventors?), ecological contexts (what aspects of the environment make invention or transmission more likely?), and populations (what features of relationships and societies promote the rise and spread of new inventions?). We aim to inspire new research by highlighting theoretical and empirical gaps in the study of innovation, focusing primarily on inventions in non-humans. Understanding the role of invention and innovation in the history of life requires a well-developed theoretical framework (which embraces cognitive processes) and a taxonomically broad, cross-species dataset that explicitly investigates inventions and their transmission. We outline such an agenda here. This article is part of the theme issue ‘Foundations of cultural evolution’. Publisher PDF

Mate-copying is a form of social learning in which witnessing sexual interactions between conspecifics biases an observer female's future mate-choice. We show in the fruit fly that females of either the Curly-wing (Cy) or the wild-type (WT) phenotype, after observing another female preferring to copulate with a fitness-lowering Cy male over a WT male, increased their preference for the usually nonpreferred Cy phenotype. Thus, mate-copying also exists for costly variants in invertebrates.

In many sexually reproducing species, individuals can gather information about potential mates by observing their mating success. This behavioral pattern, that we call mate-copying, was reported in the fruit fly Drosophila melanogaster where females choosing between 2 males of contrasting phenotypes can build a preference for males of the phenotype they previously saw being chosen by a demonstrator female. As sex ratio is known to affect mate choice, our goal was to test whether mate-copying is also affected by encountered sex ratios. Thus, we created a gradient of sex ratio during demonstrations of mate-copying experiments by changing the number of females observing from a central arena 6 simultaneous demonstrations unfolding in 6 peripheral compartments of a hexagonal device. We also tested whether the sex ratio experienced by females during demonstrations affected their choosiness (male courtship duration and double courtship rate) in subsequent mate-choice tests. Experimental male:female sex ratio during demonstrations did not affect mate-copying indices, but positively affected the proportion of both males courting the female during mate-choice tests, as well as male courtship duration, the latter potentially explaining the former relationship. As expected, the sex ratio affected female choosiness positively, and Drosophila females seem to have evolved a mate-copying ability independently of sex ratio, and a capacity to adapt their choosiness to male availability. This suggests that, as in many animal species, individuals, especially females, can adapt their mate choice depending on the current sex ratio.

National audience

National audience; Thornquist and Crickmore claim that systematic experimental error may explain the results of Danchin and colleagues. Their claim rests on mistakes in their analyses, for which we provide corrections. We reassert that conformity in fruitflies predicts long-lasting mate-preference traditions.

Despite theoretical justification for the evolution of animal culture, empirical evidence for it beyond mammals and birds remains scant, and we still know little about the process of cultural inheritance. In this study, we propose a mechanism-driven definition of animal culture and test it in the fruitfly. We found that fruitflies have five cognitive capacities that enable them to transmit mating preferences culturally across generations, potentially fostering persistent traditions (the main marker of culture) in mating preference. A transmission chain experiment validates a model of the emergence of local traditions, indicating that such social transmission may lead initially neutral traits to become adaptive, hence strongly selecting for copying and conformity. Although this situation was suggested decades ago, it previously had little empirical support.

Mate-copying is a form of social learning in which the mate-choice decision of an individual (often a female) is influenced by the mate-choice of conspecifics. Drosophila melanogaster females are known to perform such social learning, and in particular, to mate-copy after a single observation of one conspecific female mating with a male of one phenotype, while the other male phenotype is rejected. Here, we show that this form of social learning is dependent on serotonin and dopamine. Using a pharmacological approach, we reduced dopamine or serotonin synthesis in adult virgin females with 3-iodotyrosine (3-IY) and DL-para-chlorophenylalanine (PCPA), respectively, and then tested their mate-copying performance. We found that, while control females without drug treatment copied the choice of the demonstrator, drug-treated females with reduced dopamine or serotonin chose randomly. To ensure the specificity of the drugs, the direct precursors of the neurotransmitters, either the dopamine precursor L-3,4-dihydroxyphenylalanine (L-DOPA) or the serotonin precursor 5-L-hydroxytryptophan (5-HTP) were given together with the drug, (respectively 3-IY and PCPA) resulting in a full rescue of the mate-copying defects. This indicates that dopamine and serotonin are both required for mate-copying. These results give a first insight into the mechanistic pathway underlying this form of social learning in D. melanogaster.

In many sexually reproducing species, individuals can gather information about potential mates by observing their mating success. This behavioral pattern, that we call mate-copying, was reported in the fruit fly Drosophila melanogaster where females choosing between 2 males of contrasting phenotypes can build a preference for males of the phenotype they previously saw being chosen by a demonstrator female. As sex ratio is known to affect mate choice, our goal was to test whether mate-copying is also affected by encountered sex ratios. Thus, we created a gradient of sex ratio during demonstrations of mate-copying experiments by changing the number of females observing from a central arena 6 simultaneous demonstrations unfolding in 6 peripheral compartments of a hexagonal device. We also tested whether the sex ratio experienced by females during demonstrations affected their choosiness (male courtship duration and double courtship rate) in subsequent mate-choice tests. Experimental male:female sex ratio during demonstrations did not affect mate-copying indices, but positively affected the proportion of both males courting the female during mate-choice tests, as well as male courtship duration, the latter potentially explaining the former relationship. As expected, the sex ratio affected female choosiness positively, and Drosophila females seem to have evolved a mate-copying ability independently of sex ratio, and a capacity to adapt their choosiness to male availability. This suggests that, as in many animal species, individuals, especially females, can adapt their mate choice depending on the current sex ratio.

One of the most fascinating questions within the field of sexual selection is why and how females and males choose particular conspecifics as mates. Sexual selection theories provide different explanations for the origin and evolution of ornamental traits and mate preferences for such traits (overview in Andersson 1994; Jennions et al. 2001; Kokko et al. 2003). Genes for the ornamental trait and genes for the concomitant preference can co-evolve as a result of a genetic linkage between those genes as a result of the Fisherian runaway process (Fisher 1930; Lande 1981; Kirkpatrick 1982; Brooks 2000) or as a result of a selection for mates advertising ‘good genes’ (indicator models; Zahavi 1975; Moller & Alatalo 1999). These models generally assume that mate preferences are genetically based (Bakker 1999). Forming mate preferences, however, is a complex process involving not only genetic factors but also non-genetic factors. Increasing evidence suggests that the social environment (Dugatkin 1996a; Westneat et al. 2000) and learning are important factors in forming mate preferences. The mate choice of conspecifics influences the mate choice decisions of an individual, who can alter mate preferences through learning processes. Social learning, and using public information (Danchin et al. 2004; and see Chapter 10) and other kinds of learning, therefore, significantly influence the process of sexual selection. Forms of social learning have now been recognized as meaningful mechanisms for the non-genetic inheritance (i.e. cultural transmission) of mate preferences, leading to cultural evolution of mate preferences. This chapter illustrates how learning is involved in the mate choices of fishes and emphasizes the important roles that different kinds of learning, particularly social learning, play in sexual selection. It focuses on four different kinds of learning: sexual imprinting; learning after reaching maturity; eavesdropping; and mate-choice copying.

SUMMARYWeakly electric fish generate electric fields with an electric organ and perceive them with cutaneous electroreceptors. During active electrolocation,nearby objects are detected by the distortions they cause in the electric field. The electrical properties of objects, their form and their distance,can be analysed and distinguished. Here we focus on Gnathonemus petersii (Günther 1862), an African fish of the family Mormyridae with a characteristic chin appendix, the Schnauzenorgan. Behavioural and anatomical results suggest that the mobile Schnauzenorgan and the nasal region serve special functions in electroreception, and can therefore be considered as electric foveae. We investigated passive pre-receptor mechanisms that shape and enhance the signal carrier. These mechanisms allow the fish to focus the electric field at the tip of its Schnauzenorgan where the density of electroreceptors is highest (tip-effect). Currents are funnelled by the open mouth (funnelling-effect), which leads to a homogenous voltage distribution in the nasal region. Field vectors at the trunk, the nasal region and the Schnauzenorgan are collimated but differ in the angle at which they are directed onto the sensory surface. To investigate the role of those pre-receptor effects on electrolocation, we recorded electric images of objects at the foveal regions. Furthermore, we used a behavioural response(novelty response) to assess the sensitivity of different skin areas to electrolocation stimuli and determined the receptor densities of these regions. Our results imply that both regions – the Schnauzenorgan and the nasal region – can be termed electric fovea but they serve separate functions during active electrolocation.

Background Electric fish navigate and explore their dark and turbid environment with a specialised electric sense. This active electrolocation involves the generation and perception of an electric signal and fish have proven to be useful model systems for the investigation of sensory-motor interactions. A well studied example is the elephantnose fish, Gnathonemus petersii, which has a characteristic and unique elongated chin covered with hundreds of electroreceptor organs. This highly moveable so-called Schnauzenorgan constitutes the main fovea of the active electrosensory system. Here we present first evidence for a sensory-motor loop relating active electrical sensing to active motor exploration of the environment. Results Both anatomical and behavioural evidence have shown that the moveable Schnauzenorgan is crucial for prey localization. Here we show for the first time that a motor response (Schnauzenorgan-response, SOR) can be elicited by novel electrosensory stimuli. The SOR could be triggered with highest reliability by novel electrical stimuli near the Schnauzenorgan and, to a lesser extend, near the head of the animal. The probability of evoking the response depended on the magnitude of the amplitude change of the electric input, with bigger changes eliciting SORs more reliably. Similarly, increasing the distance of the stimulus reduced the response. In this respect the SOR is comparable to the well described novelty response, a transient acceleration of the production rate of electric signals, although the latter occurs at a shorter delay and can also be evoked by non-electrical stimuli. Conclusion Our experiments show a novel motor response that is mediated by the active electric sense of Gnathonemus petersii. This response will allow a detailed analysis of the neural system underlying direct interaction between sensory and motor processes in future experiments.