Social learning of novel route preferences in adult humans

Non-human animals can acquire novel route preferences by following knowledgeable individuals. Such socially learned route preferences can be stably maintained over multiple transmission episodes, sometimes forming long-lived traditions. In humans, preferences for familiar routes or heavily used worn trails over unfamiliar ones have been described in various contexts. However, social learning of route preferences has not been experimentally demonstrated in humans. Here, we demonstrate that social learning and tradition influence route choice. We led adult male and female participants into a room by one of two routes. Participants followed the demonstrated route choices, and later remembered and preferred this choice even when determinably suboptimal (i.e. longer and not preferred by control participants) or when the choice was indicated as arbitrary (the demonstrator took one route to retrieve a poster that had ostensibly fallen). Moreover, route preferences were stably maintained over multiple transmission episodes. We suggest that simple social learning processes, often neglected in human and primate research, can result in long-lived route preferences that may influence a range of additional behaviour patterns.     

The context of social learning: association patterns in a captive flock of brown-headed cowbirds

Much work on social learning has involved behaviour transmission between pairs of individuals, but recently the need to examine the social context in which learning occurs has been recognized. Previous studies using small numbers of animals have shown social influence on the behavioural development of juvenile male brown-headed cowbirds, Molothrus ater. Here we looked at the larger social context that forms the framework for such influence in more natural settings. We allowed a captive group of over 70 cowbirds, comprising adult and juvenile males and females, to associate freely in a large complex of connected aviaries. Highly organized social assortment emerged in the group, with individuals associating with others based on similarity in age and sex. Juvenile males that associated more with adult males had higher courtship success. Juvenile males that associated more with females sang less over the year. These results indicate that the social context of social learning for juvenile males is not just random association with all other birds in the social group, but is a selective and structured pattern of interaction. Differences in navigating this social structure correlated with courtship success and vocalization, behaviour known to be affected by social learning. Studies such as this, using large groups with free assortment of individuals, are the first step towards understanding the effects of the larger social context surrounding social learning.     

果蝇求偶行为的影响因素及其分子基础

果蝇Drosophila melanogaster Meigen是进行行为遗传学研究的极好材料。果蝇的雄性求偶行为已经被作为行为遗传学研究的模式。文章简要介绍近年来在遗传和分子水平上对果蝇性信息素和求偶行为的研究进展,尤其是突变体在果蝇行为遗传学研究中的应用。通过对果蝇求偶行为的分析,分别介绍果蝇的性信息素及视觉、听觉、嗅觉和味觉相关基因在果蝇求偶和交配行为过程中的作用。     

Communication in the courtship of a madagascan hissing cockroach. I. Normal courtship

The hissing Madagascar cockroach, Gromphadorhina portentosa, has a prolonged and complex courtship involving signals in several sensory modalities. Courtship was described for 13 pairs of cockroaches and the frequencies and sequencing of 16 behavioural units were analysed. Particular attention was paid to the function and interactions of acoustic, chemical and tactile components. The results indicate that posturing and sound production by males, and antennation by both males and females, are important in courtship. They also suggest that courtship in G. portentosa, rather than depending on a rigid sequence of behaviour determined by a series of discrete releasers, is quite flexible, using ‘behavioural monologues’ by both sexes as a means of achieving transitions from one stage of courtship to the next.     

Females lay fewer eggs for males with greater courtship success in a lekking Drosophila

The evolutionary basis for female mate choice in lek mating systems has been a common subject of research in animal behaviour. Because males apparently provide only gametes to females in lekking species, most research has focused on possible indirect (genetic) benefits that females might gain by discriminating among males. Despite the emphasis on indirect benefits, it has been recognized that females in non-resource-based systems such as leks could potentially gain direct benefits via mate choice if males varied in fertilization abilities, for example. Previous evidence has shown that females of a lekking Hawaiian Drosophila, D. grimshawi, vary in fecundity when mated to certain males, and that females possess preferences for vigorously courting males. This study tests the hypothesis that D. grimshawi females gain direct benefits by preferentially mating with more sexually vigorous males. Male courtship vigour (performance of wing and head-under-wing displays) and the consequences of female choice on offspring production were evaluated separately using different females. Unexpectedly, matings involving more vigorously courting males resulted in fewer offspring being produced. Reduced offspring number resulted because females laid fewer eggs when mating with males having greater courtship success. These results are discussed in light of sexual conflict and possible multiple mating by females. Females also demonstrated considerable variation in mating behaviour and behavioural variation was correlated with mating benefits. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Effects of male courtship and gonadal steroids on pair formation, egg-laying, and serum LH in Canvasback ducks (Aythya valisineria)

The effects of social stimuli on the reproductive physiology of female birds have been widely studied. This study examined the endocrine and behavioural responses of female Canvasbacks ( Aythya valisineria ) to changes in the behavioural and endocrine states of the male, as signalled by his courtship displays. Male Canvasbacks exposed to female conspecifics exhibited a variety of courtship displays which increased significantly with testosterone administration. However, the testosterone-increased courtship displays of males did not increase female receptivity or serum LH, or stimulate reproductive development or egg-laying in unpaired females placed with them. Females confined in cubicles within a pen that held breeding pairs and a free-swimming flock had higher serum LH levels and laid more eggs than did females in cubicles in another pen without breeding pairs or a free-swimming flock. This suggests that social factors, such as vocalizations from a flock and breeding pairs, may increase serum LH and egg-laying in unpaired females. Oestradiol implants in female Canvasbacks did not elevate receptivity to courting drakes, nor did they stimulate pair formation, nesting activity, or egg-laying behaviour. Testosterone implants in drakes and oestradiol implants in females decreased serum LH in each group. These results show that increasing the amount of courtship is not adequate to stimulate pairing behaviour or increases in reproductive hormones. Thus, our results suggest that female receptivity to male courtship may be a key determinant of pair formation and consequent synchronization of the behaviour patterns between members of a pair of wild birds. Our results may further suggest a dissociation between effects of courtship and pair formation in wild Canvasbacks.     

Not in their genes: Phenotypic flexibility, behavioural traditions and cultural evolution in wild bonnet macaques

Phenotypic flexibility, or the within-genotype, context-dependent, variation in behaviour expressed by single reproductively mature individuals during their lifetimes, often impart a selective advantage to organisms and profoundly influence their survival and reproduction. Another phenomenon apparently not under direct genetic control is behavioural inheritance whereby higher animals are able to acquire information from the behaviour of others by social learning, and, through their own modified behaviour, transmit such information between individuals and across generations. Behavioural information transfer of this nature thus represents another form of inheritance that operates in many animals in tandem with the more basic genetic system. This paper examines the impact that phenotypic flexibility, behavioural inheritance and socially transmitted cultural traditions may have in shaping the structure and dynamics of a primate society — that of the bonnet macaque (Macaca radiata), a primate species endemic to peninsular India. Three principal issues are considered: the role of phenotypic flexibility in shaping social behaviour, the occurrence of individual behavioural traits leading to the establishment of social traditions, and the appearance of cultural evolution amidst such social traditions. Although more prolonged observations are required, these initial findings suggest that phenotypic plasticity, behavioural inheritance and cultural traditions may be much more widespread among primates than have previously been assumed but may have escaped attention due to a preoccupation with genetic inheritance in zoological thinking. This paper is dedicated with admiration and gratitude to the late Dr Raja Ramanna, a man who held all primates in great esteem.     

From fish to fashion: experimental and theoretical insights into the evolution of culture

Recent years have witnessed a re-evaluation of the cognitive capabilities of fishes, including with respect to social learning. Indeed, some of the best experimental evidence for animal traditions can be found in fishes. Laboratory experimental studies reveal that many fishes acquire dietary, food site and mating preferences, predator recognition and avoidance behaviour, and learn pathways, through copying other fishes. Concentrating on foraging behaviour, we will present the findings of laboratory experiments that reveal social learning, behavioural innovation, the diffusion of novel behaviour through populations and traditional use of food sites. Further studies reveal surprisingly complex social learning strategies deployed by sticklebacks. We will go on to place these observations of fish in a phylogenetic context, describing in which respects the learning and traditionality of fish are similar to, and differ from, that observed in other animals. We end by drawing on theoretical insights to suggest processes that may have played important roles in the evolution of the human cultural capability.     

Testosterone control of male courtship in birds

A sequence of behaviours which we call courtship initiates reproduction in a large number of species. In vertebrates, as a component of male sexual behaviour courtship is strongly influenced by testicular androgen. Here I will review some salient issues about the regulation of courtship by testosterone in birds. The first section will briefly summarize the first 100 years of research on this topic. The specific role of testosterone or its oestrogenic metabolites in the control of different components of courtship will be the subject of the second section. Then, I will discuss how behavioural patterns can be recruited into courtship and modified in their structure by testosterone action. In the following section, the role of sexual selection and female choice in shaping the link between testosterone and courtship will be addressed. The problematic nature of the quantitative relationships between testosterone and behaviour will be topic of the fifth section. Finally, I will discuss how courtship traits that are activated by testosterone can be apparently independent of hormone blood concentrations. These issues will be examined in an evolutionary perspective, in an attempt to understand how natural and sexual selection have shaped the links between the hormone and the behaviour.     

Social learning in animals: comparative analysis of different forms and levels

Social learning as one of the key concepts of cognitive ecology includes different forms of behavioural displays from relatively simple, such as "social release" and "stimulus enhancement" up to "teaching" and "cultural transmission" in animal communities. Rapid development of this fields resulted in some contradictions in methods and terminology. In this review different forms and levels of social learning are analyzed. Ecological aspects of social learning are connected with diet shaping, fear of predators and mate choice. The first aspect is the most studied but still discussible. Social learning being an intricate component of feeding behaviour matches with innate behaviour, imprinting as well as early associative learning. Investigation of cognitive aspects of social learning going back to Thorndike's crucial question "Do apes ape?" are now developing into series of questions including even: "Do ants ape?". Elaboration of universal methods of comparative studying of social learning such as "artificial fruit" and "two ways/one outcome" has essentially enlightened these questions and made comparative analysis possible. Large continuum of displays of cognitive skills in social learning has been revealed in non-primate species. One of the discussible issues in the role of social learning is distribution of innovations. Many authors have investigated this intriguing aspect of animal behaviour in different ways, such as long field observations as well as laboratory experiments based on "artificial innovators" that is specimens specially taught by experimentalists. Many impressive results were obtained; in particular it turned out in contradiction with some mathematical models that individuals in groups are rather different in their psychophysiological predisposition to innovative behaviour. Role of teaching in such different forms of behaviour as shaping of species-specific behavioural patterns and spread of innovations is considered. Although the majority of animals in wild populations are not good teachers and pupils, some cultural aspects of behaviour were recently revealed, mostly in primates. At the same time some classical results concerning cultural transmission of new patterns (for example, bottle-opening in tits) were experimentally revised. Many problems still remain unsolved, in particular, how spread of innovations may favour prosperity of populations; to what degree behavioural peculiarities of local groups may be determined by processes of social learning; which internal and external factors and under what circumstances invest into social learning in natural environment.     

Behavioural variation in 172 small-scale societies indicates that social learning is the main mode of human adaptation

The behavioural variation among human societies is vast and unmatched in the animal world. It is unclear whether this variation is due to variation in the ecological environment or to differences in cultural traditions. Underlying this debate is a more fundamental question: is the richness of humans’ behavioural repertoire due to non-cultural mechanisms, such as causal reasoning, inventiveness, reaction norms, trial-and-error learning and evoked culture, or is it due to the population-level dynamics of cultural transmission? Here, we measure the relative contribution of environment and cultural history in explaining the behavioural variation of 172 Native American tribes at the time of European contact. We find that the effect of cultural history is typically larger than that of environment. Behaviours also persist over millennia within cultural lineages. This indicates that human behaviour is not predominantly determined by single-generation adaptive responses, contra theories that emphasize non-cultural mechanisms as determinants of human behaviour. Rather, the main mode of human adaptation is social learning mechanisms that operate over multiple generations.     

Social effects on fruit fly courtship song

Courtship behavior in Drosophila has often been described as a classic innate behavioral repertoire, but more recently extensive plasticity has been described. In particular, prior exposure to acoustic signals of con‐ or heterspecific males can change courtship traits in both sexes that are liable to be important in reproductive isolation. However, it is unknown whether male courtship song itself is socially plastic. We examined courtship song plasticity of two species in the Drosophila melanogaster subgroup. Sexual isolation between the species is influenced by two male song traits, the interpulse interval (IPI) and sinesong frequency (SSF). Neither of these showed plasticity when males had prior experience of con‐ and heterospecific social partners. However, males of both species produced longer bursts of song during courtship when they were exposed to social partners (either con‐ or heterospecific) than when they were reared in isolation. D. melanogaster carrying mutations affecting short‐ or medium‐term memory showed a similar response to the social environment, not supporting a role for learning. Our results demonstrate that the amount of song a male produces during courtship is plastic depending on the social environment, which might reflect the advantage of being able to respond to variation in intrasexual competition, but that song structure itself is relatively inflexible, perhaps due to strong selection against hybridization.     

The sterile male technique: Irradiation negatively affects male fertility but not male courtship

The sterile male technique is a common method to assign paternity, widely adopted due to its relative simplicity and low cost. Male sterility is induced by exposure to sub lethal doses of chemosterilants or irradiation, the dosage of which has to be calibrated for every species to provide successful male sterilisation, without affecting male physiology and behaviour. While the physiological effects of sterilisation are usually assessed for each study, the behavioural ones are rarely analysed in detail. Using the orb web spider Argiope keyserlingi as a model we first tested (1) the validity of the thread assay, which simulates male courtship behaviour in a standardised context, as a proxy representing courtship on a female web. We then investigated (2) the effectiveness of male sterilisation via irradiation and (3) its consequences on male courtship behaviour. Our results validate the thread assay and the sterile male technique as legitimate tools for the study of male courtship behaviour and fertilisation success. We show that these techniques are time and cost effective and reduce undesirable variation, thereby creating opportunities to study and understand the mechanisms underlying sexual selection.     

Copulatory courtship and cryptic female choice in red flour beetles Tribolium castaneum

Males of many animal species engage in courtship behaviours during and after copulation that appear to be solely aimed at stimulating the female. It has been suggested that these behaviours have evolved by cryptic female choice, whereby females are thought to impose biases on male postmating paternity success. Males of the red flour beetle Tribolium castaneum rub the lateral edges of the females' elytra with their tarsi during copulation. We manipulated female perception of this behaviour by tarsal ablation in males, thus preventing males from reaching the edge of the female elytra with their manipulated legs, and by subsequently performing a series of double-mating experiments where the copulatory behaviour was quantified. We found a positive relationship between the intensity of the copulatory courtship behaviour and relative fertilization success among unmanipulated males. This pattern, however, was absent in manipulated males, where female perception of male behaviour differed from that actually performed. Thus, female perception of male copulatory courtship behaviour, rather than male behaviour per se, apparently governs the fate of sperm competing over fertilizations within the female, showing that copulatory courtship is under selection by cryptic female choice.     

Pheromonal inhibition of male courtship behaviour in the brown tree snake, Boiga irregularis: a mechanism for the rejection of potential mates

Pheromones play a central role in coordinating the events leading up to copulation in snakes. We report here a novel pheromone system in the brown tree snake in which females release a pheromone that inhibits male courtship behaviour. In a previous study, we made observations of female brown tree snakes releasing cloacal secretions (CS) during courtship that appeared to cause courting males to cease courtship. All snakes have glands that release CS through ducts located along the cloacal orifice. Although CS have been studied for many years, their function in the mediation of snake behaviour has not been experimentally well determined. We examined the role of CS in the reproductive behaviour of male and female brown tree snakes. We conducted four experiments to test the effect of both male and female CS on brown tree snake behaviour under two behavioural contexts, courtship and male-male ritualized combat. Within each experiment, we compared the effects of CS to a control. Female CS caused a decrease in the time that males spent courting females and a decrease in the intensity of courtship compared with the control treatment. Male CS did not, however, affect the time that males spent displaying courtship or the intensity of that courtship. Neither male nor female CS had significant effects on male ritualized combat behaviour, including time that males spent in combat or the intensity of combat behaviours displayed. Furthermore, neither female nor male CS had an effect on female courtship versus controls. The inhibition of brown tree snake reproductive behaviours is specific to female CS inhibiting male courtship behaviour. This pheromone acts in concert with the female sex pheromone to regulate the events leading to copulation.Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Learning decreases heterospecific courtship and mating in fruit flies

Recent theory and data suggest that adaptive use of learning in the context of sexual behaviour could contribute to assortative mating. Experiments examining this issue indicated that male Drosophila persimilis that experienced courtship and rejection by heterospecific females exhibited significantly lower levels of heterospecific courtship and mating compared with those of inexperienced males. These results indicate that experience in the context of sexual behaviour in fruit flies could reduce gene flow between diverging populations, which may contribute to incipient speciation.     

Behavioural isolation between two closely related Hawaiian Drosophila species: the role of courtship

Behavioural isolation plays a critical role in several recent models of speciation. A detailed understanding of the process of speciation requires analysis of taxonomic groups that have not completed reproductive isolation. We studied D. silvestris and D. heteroneura because they are still in the process of divergence: behavioural isolation between them is incomplete, and neither postzygotic nor ecological isolation has been detected. Behavioural isolation is due to the failure of courtships between male D. silvestris and female D. heteroneura: there is no postzygotic isolation from either parental species. The F1 hybrids are as successful in courtship with parental individuals as same-species pairs, which suggests that the hybrids resemble male D. heteroneura or female D. silvestris in some behaviour patterns that are crucial to mating success. We searched for this crucial resemblance by examining courtship between F1 hybrids and the parental adults. We found that successful F1 males are somewhat more similar than unsuccessful F1 males to D. heteroneura males, but nevertheless they were intermediate between males of the two species. We also found that in both species the presence of female wings is necessary for courtship to proceed to copulation. These results reinforce an earlier report that behavioural isolation between these species is largely attributable to the decision as to whether to court at all, rather than to the details of courtship. Copyright 2000 The Association for the Study of Animal Behaviour.     

Artificially generated cultural variation between two groups of captive monkeys, Colobus guereza kikuyuensis

The majority of studies of social learning in primates have tested subjects in isolation and investigated the effects of learning over very short periods of time. We aimed to test for social learning in two social groups of colobus monkeys, Colobus guereza kikuyuensis. Subjects were shown video footage of familiar monkeys either pushing or pulling a plastic flap to obtain a food reward, while they were given simultaneous access to the same apparatus. Action frequencies showed a significant difference between the two groups, with the pull group performing a higher proportion of pulls to pushes, compared with the push group. Copying persisted even in later sessions during which the demonstration footage was not being shown. We conclude that we successfully generated two contrasting behavioural traditions in these groups of monkeys. We do not know how long this contrast in behaviour would have persisted had we been able to continue testing for an even longer period of time, but further studies using similar designs and even longer test periods would have the power to confirm whether stable behavioural variation can be sustained between groups of monkeys, supported by social transmission.     

Social learning in insects--from miniature brains to consensus building

Communication and learning from each other are part of the success of insect societies. Here, we review a spectrum of social information usage in insects--from inadvertently provided cues to signals shaped by selection specifically for information transfer. We pinpoint the sensory modalities involved and, in some cases, quantify the adaptive benefits. Well substantiated cases of social learning among the insects include learning about predation threat and floral rewards, the transfer of route information using a symbolic 'language' (the honeybee dance) and the rapid spread of chemosensory preferences through honeybee colonies via classical conditioning procedures. More controversial examples include the acquisition of motor memories by observation, teaching in ants and behavioural traditions in honeybees. In many cases, simple mechanistic explanations can de identified for such complex behaviour patterns.