Social learning and human mate preferences: a potential mechanism for generating and maintaining between-population diversity in attraction

Inspired by studies demonstrating mate-choice copying effects in non-human species, recent studies of attractiveness judgements suggest that social learning also influences human preferences. In the first part of our article, we review evidence for social learning effects on preferences in humans and other animals. In the second part, we present new empirical evidence that social learning not only influences the attractiveness of specific individuals, but can also generalize to judgements of previously unseen individuals possessing similar physical traits. The different conditions represent different populations and, once a preference arises in a population, social learning can lead to the spread of preferences within that population. In the final part of our article, we discuss the theoretical basis for, and possible impact of, biases in social learning whereby individuals may preferentially copy the choices of those with high status or better access to critical information about potential mates. Such biases could mean that the choices of a select few individuals carry the greatest weight, rapidly generating agreement in preferences within a population. Collectively, these issues suggest that social learning mechanisms encourage the spread of preferences for certain traits once they arise within a population and so may explain certain cross-cultural differences.     

Sound facilitates visual learning

Numerous studies show that practice can result in performance improvements on low-level visual perceptual tasks [1-5]. However, such learning is characteristically difficult and slow, requiring many days of training [6-8]. Here, we show that a multisensory audiovisual training procedure facilitates visual learning and results in significantly faster learning than unisensory visual training. We trained one group of subjects with an audiovisual motion-detection task and a second group with a visual motion-detection task, and compared performance on trials containing only visual signals across ten days of training. Whereas observers in both groups showed improvements of visual sensitivity with training, subjects trained with multisensory stimuli showed significantly more learning both within and across training sessions. These benefits of multisensory training are particularly surprising given that the learning of visual motion stimuli is generally thought to be mediated by low-level visual brain areas [6, 9, 10]. Although crossmodal interactions are ubiquitous in human perceptual processing [11-13], the contribution of crossmodal information to perceptual learning has not been studied previously. Our results show that multisensory interactions can be exploited to yield more efficient learning of sensory information and suggest that multisensory training programs would be most effective for the acquisition of new skills.     

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.     

Gaze following in human infants depends on communicative signals

Humans are extremely sensitive to ostensive signals, like eye contact or having their name called, that indicate someone's communicative intention toward them [1-3]. Infants also pay attention to these signals [4-6], but it is unknown whether they appreciate their significance in the initiation of communicative acts. In two experiments, we employed video presentation of an actor turning toward one of two objects and recorded infants' gaze-following behavior [7-13] with eye-tracking techniques [11, 12]. We found that 6-month-old infants followed the adult's gaze (a potential communicative-referential signal) toward an object only when such an act is preceded by ostensive cues such as direct gaze (experiment 1) and infant-directed speech (experiment 2). Such a link between the presence of ostensive signals and gaze following suggests that this behavior serves a functional role in assisting infants to effectively respond to referential communication directed to them. Whereas gaze following in many nonhuman species supports social information gathering [14-18], in humans it initially appears to reflect the expectation of a more active, communicative role from the information source.     

Behavioural evidence for polarisation vision in stomatopods reveals a potential channel for communication.

Polarisation sensitivity (PS) - the ability to detect the orientation of polarised light - occurs in a wide variety of invertebrates [1] [2] and vertebrates [3] [4] [5], many of which are marine species [1]. Of these, the crustacea are particularly well documented in terms of their structural [6] and neural [7] [8] adaptations for PS. The few behavioural studies conducted on crustaceans demonstrate orientation to, or local navigation with, polarised sky patterns [9]. Aside from this, the function of PS in crustaceans, and indeed in most animals, remains obscure. Where PS can be shown to allow perception of polarised light as a 'special sensory quality' [1], separate from intensity or colour, it has been termed polarisation vision (PV). Here, within the remarkable visual system of the stomatopod crustaceans (mantis shrimps) [10], we provide the first demonstration of PV in the crustacea and the first convincing evidence for learning the orientation of polarised light in any animal. Using new polarimetric [11] and photographic methods to examine stomatopods, we found striking patterns of polarisation on their antennae and telson, suggesting that one function of PV in stomatopods may be communication [12]. PV may also be used for tasks such as navigation [5] [9] [13], location of reflective water surfaces [14] and contrast enhancement [1] [15] [16] [17] [18]. It is possible that the stomatopod PV system also contributes to some of these functions.     

Observed heterospecific clutch size can affect offspring investment decisions

Optimal investment in offspring is important in maximizing lifetime reproductive success. Yet, very little is known how animals gather and integrate information about environmental factors to fine tune investment. Observing the decisions and success of other individuals, particularly when those individuals initiate breeding earlier, may provide a way for animals to quickly arrive at better breeding investment decisions. Here we show, with a field experiment using artificial nests appearing similar to resident tit nests with completed clutches, that a migratory bird can use the observed high and low clutch size of a resident competing bird species to increase and decrease clutch size and egg mass, accordingly. Our results demonstrate that songbirds can discriminate between high and low quantity of heterospecific eggs, and that social information can have long-term physiological consequences affecting reproductive strategies. Such behaviour may help animals to better adapt to changing environments and lead to convergent traits with competitors.     

Humans copy rapidly increasing choices in a multiarmed bandit problem

Conformist social learning, the tendency to acquire the most common trait in a group, allows individuals to rapidly acquire established beneficial traits from a multitude of options. However, conformist strategies hinder acquisition of novel advantageous behavior patterns, because such innovations are by definition uncommon. This raises the possibility that proxy cues of the success of novel traits may be utilized to identify and acquire advantageous innovations and disregard failing options. We show that humans use changes in trait frequency over time as such a cue in an economic game. Participants played a three-alternative forced choice game (i.e., a multi-armed bandit), using social information to attempt to locate a high reward that could change location. Participants viewed temporal changes in how many players chose each option in two successive rounds. Participants supplemented conformist strategies with a “copy-increasing-traits” strategy. That is, regardless of the traits absolute population frequencies, participants' choices were guided by changes in trait frequencies. Thus, humans can detect advantageous innovations by monitoring how many individuals adopt these over time, adopting traits increasing in frequency, and abandoning traits decreasing in frequency. Copying rapidly increasing traits allows identification and acquisition of advantageous innovations, and is thus potentially key in facilitating their early diffusion and cultural evolution.     

Culture and geographic variation in orangutan behavior

Although geographic variation in an organism's traits is often seen as a consequence of selection on locally adaptive genotypes accompanied by canalized development [1], developmental plasticity may also play a role [2, 3], especially in behavior [4]. Behavioral plasticity includes both individual learning and social learning of local innovations ("culture"). Cultural plasticity is the undisputed and dominant explanation for geographic variation in human behavior. It has recently also been suggested to hold for various primates and birds [5], but this proposition has been met with widespread skepticism [6-8]. Here, we analyze parallel long-term studies documenting extensive geographic variation in behavioral ecology, social organization, and putative culture of orangutans [9] (genus Pongo). We show that genetic differences among orangutan populations explain only very little of the geographic variation in behavior, whereas environmental differences explain much more, highlighting the importance of developmental plasticity. Moreover, variation in putative cultural variants is explained by neither genetic nor environmental differences, corroborating the cultural interpretation. Thus, individual and cultural plasticity provide a plausible pathway toward local adaptation in long-lived organisms such as great apes and formed the evolutionary foundation upon which human culture was built.     

Explaining social learning of food preferences without aversions: an evolutionary simulation model of Norway rats

Norway rats (Rattus norvegicus) transmit preferences for novel foods socially by smelling each other's breath. However, rats fail to learn aversions, acquiring a preference even if the rat whose breath they smell has been poisoned. Rats can distinguish between sick and healthy conspecifics and social learning of both preferences and aversions is present in other species - hence it is unclear why rats cannot learn aversions socially. We constructed an evolutionary simulation in which a population of rats foraged from a central location, exploiting food sites that could contain edible or toxic foodstuffs. We examined the relationship between toxin lethality and selection for individual versus social learning and discrimination between sick and healthy conspecifics in order to allow learning of both preferences and aversions. At low lethality levels individual learning was selected for and at intermediate levels we found social learning of both preferences and aversions. Finally, given high lethality levels the simulated rats would employ social learning but failed to learn aversions, matching the behaviour of real rats. We argue that Norway rats do not learn aversions socially because their environment may contain only highly lethal toxins which make interaction with a sick conspecific an extremely rare event.     

Sensorimotor learning configures the human mirror system

Cells in the "mirror system" fire not only when an individual performs an action but also when one observes the same action performed by another agent [1-4]. The mirror system, found in premotor and parietal cortices of human and monkey brains, is thought to provide the foundation for social understanding and to enable the development of theory of mind and language [5-9]. However, it is unclear how mirror neurons acquire their mirror properties -- how they derive the information necessary to match observed with executed actions [10]. We address this by showing that it is possible to manipulate the selectivity of the human mirror system, and thereby make it operate as a countermirror system, by giving participants training to perform one action while observing another. Before this training, participants showed event-related muscle-specific responses to transcranial magnetic stimulation over motor cortex during observation of little- and index-finger movements [11-13]. After training, this normal mirror effect was reversed. These results indicate that the mirror properties of the mirror system are neither wholly innate [14] nor fixed once acquired; instead they develop through sensorimotor learning [15, 16]. Our findings indicate that the human mirror system is, to some extent, both a product and a process of social interaction.     

Cultural niche construction in a metapopulation

Cultural niche construction is the process by which certain evolving cultural traits form a cultural niche that affects the evolution of other genetic and cultural traits [Laland, K., et al., 2001. Cultural niche construction and human evolution. J. Evol. Biol. 14, 22-33; Ihara, Y., Feldman, M., 2004. Cultural niche construction and the evolution of small family size. Theor. Popul. Biol. 65, 105-111]. In this study we focus on cultural niche construction in a metapopulation (a population of populations), where the frequency of one cultural trait (e.g. the level of education) determines the transmission rate of a second trait (e.g. the adoption of fertility reduction preferences) within and between populations. We formulate the Metapopulation Cultural Niche Construction (MPCNC) model by defining the cultural niche induced by the first trait as the construction of a social interaction network on which the second trait may percolate. Analysis of the model reveals dynamics that are markedly different from those observed in a single population, allowing, for example, different (or even opposing) dynamics in each population. In particular, this model can account for the puzzling phenomenon reported in previous studies [Bongaarts, J., Watkins, S., 1996. Social interactions and contemporary fertility transitions. Popul. Dev. Rev. 22 (4), 639-682] that the onset of the demographic transition in different countries occurred at ever lower levels of development.     

Roosts as information centres: social learning of food preferences in bats

The short-tailed fruit bat, Carollia perspicillata, lives in groups in tree hollows and caves. To investigate whether these roosts might serve as information centres, we tested whether individuals' preferences for novel foods could be enhanced through social learning at the roost. We also determined whether socially learned preferences for novel foods were reversed through interaction with other roost mates by simulating changes in available food resources such as those associated with variations in timing of fruit production in different plant species. Bats exhibited socially induced preferences that were readily reversible. We suggest that for frugivorous bats, roosts can serve as centres for information exchange about novel and familiar, ephemeral foods without requiring conspecific recruitment to these resources.     

Evolution of social learning does not explain the origin of human cumulative culture

Because culture requires transmission of information between individuals, thinking about the origin of culture has mainly focused on the genetic evolution of abilities for social learning. Current theory considers how social learning affects the adaptiveness of a single cultural trait, yet human culture consists of the accumulation of very many traits. Here we introduce a new modeling strategy that tracks the adaptive value of many cultural traits, showing that genetic evolution favors only limited social learning owing to the accumulation of maladaptive as well as adaptive culture. We further show that culture can be adaptive, and refined social learning can evolve, if individuals can identify and discard maladaptive culture. This suggests that the evolution of such "adaptive filtering" mechanisms may have been crucial for the birth of human culture.     

A general model for multiphase texture segmentation and its applications to retinal image analysis

In this paper we propose a general variational segmentation model for multiphase texture segmentation based on fuzzy region competition principle. An important strength of the proposed framework is that different region terms (e.g. mutual information Kim et al. (2005) [1], local histogram Ni et al. (2009) [2] models for texture-based segmentation, and piecewise constant intensity model Chan and Vese (2001) [3] for intensity-based segmentation) can be included as appropriate to the problem. Constraints of different phases are considered by introducing Lagrangian multipliers into the energy functional, and a fast numerical solution is achieved by employing the fast dual projection algorithm Chambolle (2004) [4]. The proposed model has been applied to synthetic and natural images in order to make comparisons with other competing models in literature. Our results demonstrate superiority in dealing with multiphase texture segmentation problems. To demonstrate its usefulness in biomedical applications we have applied the new model to two retinal image segmentation problems: segmentation of capillary non-perfusion regions in fluorescein angiogram and segmentation of cellular layers of the retina in optical coherence tomography, and evaluated against the gold standard set by experts. The generalized overlap analysis shows good agreement for both applications. As a generic segmentation technique our new model has the potential to be extended for wider applications.     

Mid-Mesozoic flea-like ectoparasites of feathered or haired vertebrates

Parasite-host associations among insects and mammals or birds are well attended by neontological studies [1]. An Eocene bird louse compression fossil [2, 3] and several flea specimens from Eocene and Oligocene ambers [4-8], reported to date, are exceptionally similar to living louse and flea taxa. But the origin, morphology, and early evolution of parasites and their associations with hosts are poorly known [9, 10] due to sparse records of putative ectoparasites with uncertain classification in the Mesozoic, most lacking mouthpart information and other critical details of the head morphology [11-15]. Here we present two primitive flea-like species assigned to the Pseudopulicidae Gao, Shih et Ren familia nova (fam. nov.), Pseudopulex jurassicus Gao, Shih et Ren genus novum et species nova (gen. et sp. nov) from the Middle Jurassic [16] and P. magnus Gao, Shih et Ren sp. nov. from the Early Cretaceous in China [17]. They exhibit many features of ectoparasitic insects. Large body size and long serrated stylets for piercing tough and thick skin or hides of hosts suggest that these primitive ectoparasites might have lived on and sucked the blood of relatively large hosts, such as contemporaneous feathered dinosaurs and/or pterosaurs or medium-sized mammals (found in the Early Cretaceous, but not the Middle Jurassic).     

Social transmission of face preferences among humans

Previous studies demonstrating mate choice copying effects among females in non-human species have led many researchers to propose that social transmission of mate preferences may influence sexual selection for male traits. Although it has been suggested that social transmission may also influence mate preferences in humans, there is little empirical support for such effects. Here, we show that observing other women with smiling (i.e. positive) expressions looking at male faces increased women's preferences for those men to a greater extent than did observing women with neutral (i.e. relatively negative) expressions looking at male faces. By contrast, the reverse was true for male participants (i.e. observing women with neutral expressions looking at male faces increased male participant's preferences for those men to a greater extent than did observing women smiling at male faces). This latter finding suggests that within-sex competition promotes negative attitudes among men towards other men who are the target of positive social interest from women. Our findings demonstrate that social transmission of face preferences influences judgments of men's attractiveness, potentially demonstrating a mechanism for social transmission of mate preferences.     

大型食草动物的聚群规则:印度西部热带干旱森林中有蹄类动物局域和区域尺度的多样性格局

竞争能够塑造自然群落并由其给出可用备择模型检验的一般性聚集规则。关于多种动物集合的竞争结构证据至今还非常少见,我们给出了一个备择模型分析用于检验印度西部热带干旱森林中当地5种大型食草类动物(花鹿Axisaxis,印度大蓝羚Boselaphustragocamelus,水鹿Cervusunicolor,印度瞪羚Gazellabennetti,野猪Susscrofa)是否符合一般性集合规则。使用蒙特卡罗模拟分析了动物的生态位重叠和身体大小比率的类似性,结果表明当地这些种的集合不是竞争结构决定的,其内部阶元结构处于亚最适种丰富度。另外2种有蹄类(印度黑羚Antilopecervicapra,四角羚羊Tetracerusquadricornis)属于地域性种库的组成部分,但缺失于这种集合;身体大小组合在地域性物种集合中不是随机的,然而在当地集合中能够通过随机性机会获得。对于观察到的类型,我们认为由于灭绝留下的统计学空缺似乎最能解释现存集合。由于天敌(大型食肉类)能够减少猎物物种的种间竞争,使得这种无规则生态位配置具有成立的可能性。由于对四角羚羊(T.quadricornis)的生物学和保护现状知之甚少,未将该种包括在该聚集中。我认为对这类较少被人类了解的物种其保护问题被忽视了,今后获得这些稀少的地方特有物种的生态学资料是一项紧急课题.     

An eye for detail: selective sexual imprinting in zebra finches

To investigate the idea that sexual imprinting creates incipient reproductive isolation between phenotypically diverging populations, I performed experiments to determine whether colony-reared zebra finches would imprint on details of artificial white crests. In the first experiment, adults in one breeding colony wore white crests with a vertical black stripe, while in another colony adults wore crests having a horizontal black stripe; except for their crests, breeders possessed wild-type plumage and conformation. Offspring of both sexes reared in these colonies developed mate preferences for opposite-sexed birds wearing the crest type with which they were reared; neither sex developed a social preference for crested individuals of the same sex. In a second experiment, females reared by crested parents preferred crested males versus males with red leg bands, while control females (reared in a colony of wild-type, uncrested birds) preferred red-banded males in the same test. Results of a third experiment that used sexually dimorphic crest phenotypes indicate that both sexes of offspring imprinted on maternal crest patterns. Results support the hypothesis that sexual imprinting can facilitate isolation both by engendering a preference for population-typical traits and by prioritizing such an imprinting-based preference over species-typical preferences for other traits used in mate choice. Comparison with results of other recent studies indicates that imprinting tendencies of both sexes vary with the characteristics of traits presented as an imprinting stimuli. Tendency to imprint may vary with the perceived information content (e.g., kin, sex, or population indicator) of parental traits, a process dubbed selective sexual imprinting.     

The logic of fashion cycles

Many cultural traits exhibit volatile dynamics, commonly dubbed fashions or fads. Here we show that realistic fashion-like dynamics emerge spontaneously if individuals can copy others' preferences for cultural traits as well as traits themselves. We demonstrate this dynamics in simple mathematical models of the diffusion, and subsequent abandonment, of a single cultural trait which individuals may or may not prefer. We then simulate the coevolution between many cultural traits and the associated preferences, reproducing power-law frequency distributions of cultural traits (most traits are adopted by few individuals for a short time, and very few by many for a long time), as well as correlations between the rate of increase and the rate of decrease of traits (traits that increase rapidly in popularity are also abandoned quickly and vice versa). We also establish that alternative theories, that fashions result from individuals signaling their social status, or from individuals randomly copying each other, do not satisfactorily reproduce these empirical observations.