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Our understanding of bird song, a model system for animal communication and the neurobiology of learning, depends critically on making reliable, validated comparisons between the complex multidimensional syllables that are used in songs. However, most assessments of song similarity are based on human inspection of spectrograms, or computational methods developed from human intuitions. Using a novel automated operant conditioning system, we collected a large corpus of zebra finches' (Taeniopygia guttata) decisions about song syllable similarity. We use this dataset to compare and externally validate similarity algorithms in widely-used publicly available software (Raven, Sound Analysis Pro, Luscinia). Although these methods all perform better than chance, they do not closely emulate the avian assessments. We then introduce a novel deep learning method that can produce perceptual similarity judgements trained on such avian decisions. We find that this new method outperforms the established methods in accuracy and more closely approaches the avian assessments. Inconsistent (hence ambiguous) decisions are a common occurrence in animal behavioural data; we show that a modification of the deep learning training that accommodates these leads to the strongest performance. We argue this approach is the best way to validate methods to compare song similarity, that our dataset can be used to validate novel methods, and that the general approach can easily be extended to other species., Competing Interests: I have read the journal’s policy and the authors of this manuscript have the following competing interests: DS is currently serving on the editorial board of PLOS Computational Biology., (Copyright: © 2024 Zandberg et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

We vary greatly in our perception of risk, not just because of differences between risks themselves, but also because of individual, contextual and cultural differences too. To better understand and predict responses to risk, we need to (a) integrate these components, combining approaches from different psychological disciplines and (b) also consider risk tolerance - how individuals trade-off between risks and benefits. We therefore developed an ICONS (individual, contextual, cognitive, social) framework; using it across two empirical studies (n = 4228) to examine how individuals perceive and respond to the quotidian risks associated with consumer products. Three dimensions underlined risk perceptions: benefits, dread and individual responsibility. Risk tolerance was typically predicted by interactions between individual (demographic, cultural worldview, personality) and contextual (product type/category, harm information) factors. In turn, perceived dread, benefits and individual differences shaped how likely participants were to communicate risk information. Our results demonstrate for the first time how the interaction between individual, cognitive (risk tolerance, intensity), contextual, and social (risk communication) factors is key to understanding and predicting risk perceptions. Together, our findings help explain why societal responses to risks are often difficult to predict and have implications for the spread, and amplification, of risk information., (© 2024. The Author(s).)

In studies of cumulative cultural evolution in non-human animals, the focus is most often on incremental changes that increase the efficacy of an existing form of socially learned behaviour, such as the refinement of migratory pathways. In this paper, we compare the songs of different species to describe patterns of evolution in the acoustic structure of bird songs, and explore the question of what building blocks might underlie cumulative cultural evolution of bird song using a comparative approach. We suggest that three steps occurred: first, imitation of independent sounds, or notes, via social learning; second, the formation of categories of note types; and third, assembling note types into sequences with defined structures. Simple sequences can then be repeated to form simple songs or concatenated with other sequences to form segmented songs, increasing complexity. Variant forms of both the notes and the sequencing rules may then arise due to copy errors and innovation. Some variants may become established in the population because of learning biases or selection, increasing signal efficiency, or because of cultural drift. Cumulative cultural evolution of bird songs thus arises from cognitive processes such as vocal imitation, categorization during memorization and learning biases applied to basic acoustic building blocks. This article is part of a discussion meeting issue 'The emergence of collective knowledge and cumulative culture in animals, humans and machines'.

Humpback whale song is an extraordinary example of vocal cultural behaviour. In northern populations, the complex songs show long-lasting traditions that slowly evolve, while in the South Pacific, periodic revolutions occur when songs are adopted from neighbouring populations and rapidly spread. In this species, vocal learning cannot be studied in the laboratory, learning is instead inferred from the songs' complexity and patterns of transmission. Here, we used individual-based cultural evolutionary simulations of the entire Southern and Northern Hemisphere humpback whale populations to formalize this process of inference. We modelled processes of song mutation and patterns of contact among populations and compared our model with patterns of song theme sharing measured in South Pacific populations. Low levels of mutation in combination with rare population interactions were sufficient to closely fit the pattern of diversity in the South Pacific, including the distinctive pattern of west-to-east revolutions. Interestingly, the same learning parameters that gave rise to revolutions in the Southern Hemisphere simulations gave rise to evolutionary patterns of cultural evolution in the Northern Hemisphere populations. Our study demonstrates how cultural evolutionary approaches can be used to make inferences about the learning processes underlying cultural transmission and how they might generate emergent population-level processes. This article is part of the theme issue 'Vocal learning in animals and humans'.

Evaluating sound similarity is a fundamental building block in acoustic perception and computational analysis. Traditional data-driven analyses of perceptual similarity are based on heuristics or simplified linear models, and are thus limited. Deep learning embeddings, often using triplet networks, have been useful in many fields. However, such networks are usually trained using large class-labelled datasets. Such labels are not always feasible to acquire. We explore data-driven neural embeddings for sound event representation when class labels are absent, instead utilising proxies of perceptual similarity judgements. Ultimately, our target is to create a perceptual embedding space that reflects animals' perception of sound. We create deep perceptual embeddings for bird sounds using triplet models. In order to deal with the challenging nature of triplet loss training with the lack of class-labelled data, we utilise multidimensional scaling (MDS) pretraining, attention pooling, and a triplet mining scheme. We also evaluate the advantage of triplet learning compared to learning a neural embedding from a model trained on MDS alone. Using computational proxies of similarity judgements, we demonstrate the feasibility of the method to develop perceptual models for a wide range of data based on behavioural judgements, helping us understand how animals perceive sounds.

Inbreeding is often avoided in natural populations by passive processes such as sex-biased dispersal. But, in many social animals, opposite-sexed adult relatives are spatially clustered, generating a risk of incest and hence selection for active inbreeding avoidance. Here we show that, in long-tailed tits ( Aegithalos caudatus ), a cooperative breeder that risks inbreeding by living alongside opposite-sex relatives, inbreeding carries fitness costs and is avoided by active kin discrimination during mate choice. First, we identified a positive association between heterozygosity and fitness, indicating that inbreeding is costly. We then compared relatedness within breeding pairs to that expected under multiple mate-choice models, finding that pair relatedness is consistent with avoidance of first-order kin as partners. Finally, we show that the similarity of vocal cues offers a plausible mechanism for discrimination against first-order kin during mate choice. Long-tailed tits are known to discriminate between the calls of close kin and nonkin, and they favor first-order kin in cooperative contexts, so we conclude that long-tailed tits use the same kin discrimination rule to avoid inbreeding as they do to direct help toward kin., Competing Interests: The authors declare no competing interest.

Most cooperative breeders live in discrete family groups, but in a minority, breeding populations comprise extended social networks of conspecifics that vary in relatedness. Selection for effective kin recognition may be expected for more related individuals in such kin neighbourhoods to maximize indirect fitness. Using a long-term social pedigree, molecular genetics, field observations and acoustic analyses, we examine how vocal similarity affects helping decisions in the long-tailed tit Aegithalos caudatus . Long-tailed tits are cooperative breeders in which help is typically redirected by males that have failed in their own breeding attempts towards the offspring of male relatives living within kin neighbourhoods. We identify a positive correlation between call similarity and kinship, suggesting that vocal cues offer a plausible mechanism for kin discrimination. Furthermore, we show that failed breeders choose to help males with calls more similar to their own. However, although helpers fine-tune their provisioning rates according to how closely related they are to recipients, their effort was not correlated with their vocal similarity to helped breeders. We conclude that although vocalizations are an important part of the recognition system of long-tailed tits, discrimination is likely to be based on prior association and may involve a combination of vocal and non-vocal cues. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

The use of information provided by others is a common short-cut adopted to inform decision-making. However, instead of indiscriminately copying others, animals are often selective in what, when and whom they copy. How do they decide which 'social learning strategy' to use? Previous research indicates that stress hormone exposure in early life may be important: while juvenile zebra finches copied their parents' behaviour when solving novel foraging tasks, those exposed to elevated levels of corticosterone (CORT) during development copied only unrelated adults. Here, we tested whether this switch in social learning strategy generalizes to vocal learning. In zebra finches, juvenile males often copy their father's song; would CORT-treated juveniles in free-flying aviaries switch to copying songs of other males? We found that CORT-treated juveniles copied their father's song less accurately as compared to control juveniles. We hypothesized that this could be due to having weaker social foraging associations with their fathers, and found that sons that spent less time foraging with their fathers produced less similar songs. Our findings are in line with a novel hypothesis linking early-life stress and social learning: early-life CORT exposure may affect social learning indirectly as a result of the way it shapes social affiliations.This article is part of the theme issue 'Causes and consequences of individual differences in cognitive abilities'., (© 2018 The Authors.)

Cultural traditions have been observed in a wide variety of animal species. It remains unclear, however, what is required for social learning to give rise to stable traditions: what level of precision and what learning strategies are required. We address these questions by fitting models of cultural evolution to learned bird song. We recorded 615 swamp sparrow (Melospiza georgiana) song repertoires, and compared syllable frequency distributions to the output of individual-based simulations. We find that syllables are learned with an estimated error rate of 1.85% and with a conformist bias in learning. This bias is consistent with a simple mechanism of overproduction and selective attrition. Finally, we estimate that syllable types could frequently persist for more than 500 years. Our results demonstrate conformist bias in natural animal behaviour and show that this, along with moderately precise learning, may support traditions whose stability rivals those of humans.

Learned bird songs are often characterized by a high degree of variation between individuals and sometimes between populations, while at the same time maintaining species specificity. The evolution of such songs depends on the balance between plasticity and constraints. Captive populations provide an opportunity to examine signal variation and differentiation in detail, so we analyzed adult male zebra finch (Taeniopygia guttata) songs recorded from 13 populations across the world, including one sample of songs from wild-caught males in their native Australia. Cluster analysis suggested some, albeit limited, evidence that zebra finch song units belonged to universal, species-wide categories, linked to restrictions in vocal production and non-song parts of the vocal repertoire. Across populations, songs also showed some syntactical structure, although any song unit could be placed anywhere within the song. On the other hand, there was a statistically significant differentiation between populations, but the effect size was very small, and its communicative significance dubious. Our results suggest that variation in zebra finch songs within a population is largely determined by species-wide constraints rather than population-specific features. Although captive zebra finch populations have been sufficiently isolated to allow them to genetically diverge, there does not appear to have been any divergence in the genetically determined constraints that underlie song learning. Perhaps more surprising is the lack of locally diverged cultural traditions. Zebra finches serve as an example of a system where frequent learning errors may rapidly create within-population diversity, within broad phonological and syntactical constraints, and prevent the formation of long-term cultural traditions that allow populations to diverge.

Adaptive radiations play key roles in the generation of biodiversity and biological novelty, and therefore understanding the factors that drive them remains one of the most important challenges of evolutionary biology. Although both intrinsic innovations and extrinsic ecological opportunities contribute to diversification bursts, few studies have looked at the synergistic effect of such factors. Here we investigate the Teloschistales (Ascomycota), a group of >1,000 lichenized species with variation in species richness and phenotypic traits that hinted at a potential adaptive radiation. We found evidence for a dramatic increase in diversification rate for one of four families within this order--Teloschistaceae--which occurred ∼ 100 Mya (Late Cretaceous) and was associated with a switch from bark to rock and from shady to sun-exposed habitats. This adaptation to sunny habitats is likely to have been enabled by a contemporaneous key novel phenotypic innovation: the production in both vegetative structure (thallus) and fruiting body (apothecia) of anthraquinones, secondary metabolites known to protect against UV light. We found that the two ecological factors (sun exposure and rock substrate) and the phenotypic innovation (anthraquinones in the thallus) were all significant when testing for state-dependent shifts in diversification rates, and together they seem likely to be responsible for the success of the Teloschistaceae, one of the largest lichen-forming fungal lineages. Our results support the idea that adaptive radiations are driven not by a single factor or key innovation, but require a serendipitous combination of both intrinsic biotic and extrinsic abiotic and ecological factors.

Some of the psychological abilities that underlie human speech are shared with other species. One hallmark of speech is that linguistic context affects both how speech sounds are categorized into phonemes, and how different versions of phonemes are produced. We here confirm earlier findings that swamp sparrows categorically perceive the notes that constitute their learned songs and then investigate how categorical boundaries differ according to context. We clustered notes according to their acoustic structure, and found statistical evidence for clustering into 10 population-wide note types. Examining how three related types were perceived, we found, in both discrimination and labeling tests, that an "intermediate" note type is categorized with a "short" type when it occurs at the beginning of a song syllable, but with a "long" type at the end of a syllable. In sum, three produced note-type clusters appear to be underlain by two perceived categories. Thus, in birdsong, as in human speech, categorical perception is context-dependent, and as is the case for human phonology, there is a complex relationship between underlying categorical representations and surface forms. Our results therefore suggest that complex phonology can evolve even in the absence of rich linguistic components, like syntax and semantics.

Cultural transmission can increase the flexibility of behavior, such as bird song. Nevertheless, this flexibility often appears to be constrained, sometimes by preferences for learning certain traits over others, a phenomenon known as "biased" learning or transmission. The sequential colonization of the Atlantic Islands by the chaffinch (Fringilla coelebs) provides a unique model system in which to investigate how the variability of a cultural trait has evolved. We used novel computational methods to analyze chaffinch song from twelve island and continental populations and to infer patterns of evolution in song structure. We found that variability of the subunits within songs ("syllables") differed moderately between populations but was not predicted by whether the population was continental or not. In contrast, we found that the sequencing of syllables within songs ("syntax") was less structured in island than continental populations and in fact decreased significantly after each colonization. Syntactical structure was very clear in the mainland European populations but was almost entirely absent in the most recently colonized island, Gran Canaria. Our results suggest that colonization leads to the progressive loss of a species-specific feature of song, syntactical structure., (Copyright © 2013 Elsevier Ltd. All rights reserved.)

Many models have investigated how the process of speciation may occur in sympatry. In these models, individuals are either asexual or mate choice is determined by very simple rules. Females, for example, may be assumed either to compare their phenotype to that of a potential mate, preferring to mate with similar males (phenotype matching), or to possess preference genes that determine which male phenotype they prefer. These rules often do not reflect the mate-choice rules found in empirical studies. In this paper, we compare these two modes of female choice with various types of sexual imprinting. We examine the efficacy of different mate-choice behavior in causing divergence in male traits under simple deterministic one-locus population genetic models as well as under polygenic, individual-based simulations based on the models of Dieckmann and Doebeli (1999). We find that the inheritance mechanism of mate choice can have a large effect on the ease of sympatric speciation. When females imprint on their mothers, the result of the model is similar to phenotype matching, where speciation can occur fairly easily. When females imprint on their fathers or imprint obliquely, speciation becomes considerably less likely. Finally, when females rely on preference genes, male trait evolution occurs easily, but the correlation between trait and preference can be weak, and interpreting these results as speciation may be suspect.