Vocal functional flexibility: what it is and why it matters

Evolving pragmatics

Language has been considered by many to be uniquely human. Numerous theories for how it evolved have been proposed but rarely tested. The articles in this theme issue consider the extent to which aspects of language, such as vocal learning, phonology, syntax, semantics, intentionality, cognition and neurobiological adaptations, are shared with other animals. By adopting a comparative approach, insights into the mechanisms and origins of human language can be gained. While points of agreement exist among the authors, conflicting viewpoints are expressed on several issues, such as the presence of proto-syntax in animal communication, the neural basis of the Merge operation, and the neurogenetic changes necessary for vocal learning. Future comparative research in animal communication has the potential to teach us even more about the evolution, neurobiology and cognitive basis of human language. This article is part of the theme issue 'What can animal communication teach us about human language?'

Estimating vocal repertoire size is like collecting coupons: a theoretical framework with heterogeneity in signal abundance.

Playbacks are one of the most useful experimental tools in animal communication research. Playbacks of substrate vibrations present special challenges, but conducting high-fidelity vibrational playbacks is not difficult and depends less on the specific equipment used than on avoiding some common pitfalls. We review the major issues, describing both the problems and a range of solutions. Our focus is on playback through living plants, but most of the issues apply to playback through other substrates as well. The major challenge for playback through any substrate is that the vibrational signal is almost always changed by the playback equipment and the substrate, so that the signal received by the focal animal is different from the one intended by the experimenter. The general solution to this problem is to measure the changes imposed by the playback system and to pre-filter the playback signal to compensate for them. A second challenge is to ensure that the focal animal receives a signal at the appropriate amplitude. Achieving the proper amplitude is a straightforward process. However, amplitude is substrate dependent (e.g., on a plant, amplitude is inversely proportional to stem diameter), and the experimenter should choose a realistic amplitude for the substrate. Other issues include choices of playback device, natural versus artificial substrates, single versus multiple substrate exemplars, and playback in laboratory versus field. Our goal in this chapter is to give experimenters, especially those just starting out, the knowledge and confidence needed to conduct high-quality vibrational playbacks.

Animal signals are inherently complex phenotypes with many interacting parts combining to elicit responses from receivers. The pattern of interrelationships between signal components reflects the extent to which each component is expressed, and responds to selection, either in concert with or independently of others. Furthermore, many species have complex repertoires consisting of multiple signal types used in different contexts, and common morphological and physiological constraints may result in interrelationships extending across the multiple signals in species’ repertoires. The evolutionary significance of interrelationships between signal traits can be explored within the framework of phenotypic integration, which offers a suite of quantitative techniques to characterize complex phenotypes. In particular, these techniques allow for the assessment of modularity and integration, which describe, respectively, the extent to which sets of traits covary either independently or jointly. Although signal and repertoire complexity are thought to be major drivers of diversification and social evolution, few studies have explicitly measured the phenotypic integration of signals to investigate the evolution of diverse communication systems. We applied methods from phenotypic integration studies to quantify integration in the two primary vocalization types (advertisement and aggressive calls) in the treefrogs Hyla versicolor, Hyla cinerea, and Dendropsophus ebraccatus. We recorded male calls and calculated standardized phenotypic variance–covariance (P) matrices for characteristics within and across call types. We found significant integration across call types, but the strength of integration varied by species and corresponded with the acoustic similarity of the call types within each species. H. versicolor had the most modular advertisement and aggressive calls and the least acoustically similar call types. Additionally, P was robust to changing social competition levels in H. versicolor. Our findings suggest new directions in animal communication research in which the complex relationships among the traits of multiple signals are a key consideration for understanding signal evolution.

Meiotic recombination is a crucial biological process that ensures proper chromosomal pairing and promotes adaptation. In placental mammals, recombination rates vary widely across species, populations, sexes, individuals, and chromosomes. While the placental X chromosome shows remarkable conservation of both gene order and the recombination landscape across deep evolutionary history, it is unknown whether similar levels of autosomal conservation persist despite extensive chromosomal evolution. Here, we reconstructed an ancestral placental mammal karyotype from chromosome-level assemblies, using slow rates of karyotypic evolution, and inferred an ancestral autosomal recombination map. Analysis of phylogenetic branch lengths and PhyloP-based scores of evolutionary constraint reveals that conserved autosomal regions with low recombination rates have evolved under stronger purifying selection, whereas regions with conserved high recombination rates are less constrained and freer to evolve. Ancestral autosomal regions with low recombination rates were enriched for pathways and GO terms related to cellular function, whereas ancestral regions with high recombination rates were enriched for regulation and some immune-related systems. Tracking the fate of these conserved ancestral recombination hotspots and coldspots across 13 mammal lineages with variable rates of karyotype evolution revealed the retention of autosomal AHRs, but the absence of autosomal ALR conservation. Collectively, our findings reveal variable levels of evolutionary constraint at meiotic recombination in relation to karyotypic evolution, providing new insights into how natural selection influences the evolution of chromosomal organization.

Lurking in what used to be referred to as “junk DNA,” and beyond the realm of the well-known non-coding RNAs such as mRNA and tRNA, are non-coding sequences that are transcribed into RNAs with important epigenetic modulatory functions. Now in this special online collection in BioEssays (http://onlinelibrary.wiley.com/journal/10.1002/%28ISSN%291521-1878/homepage/non_coding_rnas_virtual_ issue.htm) we bring together diverse corners of a rapidly expanding field of research. Already it is becoming clear that certain miRNAs modulate the expression of RNAs coding for proteins cell cycle regulators, signalling pathway effectors and transcription factors that determine cell pluripotency, and cell fate, as discussed by Li and He 1. And from these observations it is a small conceptual step to assume that non-coding RNAs are also involved in cancer. Indeed, lncRNAs (long non-coding RNAs) are found highly expressed in solid tumours, and their mechanism of action, in general, appears to rely on their modification of chromatin via recruitment of chromatin remodelling complexes 2. Returning to their shorter cousins, miRNAs, it has been observed that the mammalian X-chromosome contains a disproportionately large number of sequences coding for miRNAs, and several of these have been shown to play roles in immunity and cancer. In a hypothesis piece, Pinheiro et al. 3 raise the possibility that the lesser immune response to infection mounted by males could be a result of males possessing only one X-chromosome. The other side of the coin is that females tend to suffer more autoimmune disease than males because (so it may be hypothesised) they have two X-chromosomes. The precise X-chromosome-encoded non-coding RNAs involved in autoimmunity have yet to be identified, but there is mounting support for the role of miRNAs in general in autoimmune disease. A strong recent candidate is an miRNA proposed to result from processing of a ribonucleoprotein-associated ‘Y RNA’ 4, the RNP of which (Ro RNP) is, itself, the target of the autoimmune response in systemic lupus erythematosus. Beyond the immune system, a speculative article explores the roles of miRNAs in injury of the central nervous system 5: certain miRNAs are already recognised as key modulators of gene expression in processes involved with neuronal differentiation and maturation. But there is emerging evidence that defined miRNAs are consistently up- or down-regulated in ischaemia, traumatic brain injury and spinal cord injury, for example. Some are neurotoxic, whereas others are neuroprotective, hence opening a conceptual avenue to miRNA-based therapeutic intervention. And it is not only in CNS injury that non-coding RNAs play an important role in the brain: the mammalian brain and placenta manifest particularly high expression of imprinted genes, a phenomenon that is orchestrated by regulatory small-RNAs. In a hypothesis article, Labialle and Cavaillé propose that subclasses of these RNAs – recognised as “genomic parasites” – have contributed to the emergence of genomic imprinting by virtue of their occurrence in huge repeat arrays 6. In general, non-coding transcripts, including long non-coding RNA sequences, reside in juxtaposition with gene clusters in imprinted domains of chromosomes. Regulatory non-coding RNAs are generated in a bewildering variety of ways via the processing of precursor transcripts, a newly hypothesised route being the fragmentation of small nucleolar RNAs (snoRNAs) into yet smaller, stable, RNAs 7. But regulatory non-coding RNAs need not only be encoded in the genome that they regulate: evidence is accumulating that external non-coding RNAs are very important for maintaining normal homeostasis. An obvious source is the food that we eat, and recently plant-derived RNAs have, indeed, been found circulating in the blood of the consumers 8. And so, lastly, to the question of where, indeed, non-coding RNAs come from in the first place. It is likely that many miRNAs have arisen in response to the integration of retroviruses into the host genome: small complementary RNA sequences target the viral RNA for degradation or prevent it from being mobilised. Might they, therefore, have a deep evolutionary history in our unicellular ancestors? That is a very controversial claim, as Tarver et al. 9 make clear in an article that puts numerous miRNAs that suggest deep evolutionary origin to the test: most do not meet the criteria for miRNA annotation, suggesting that plants and animals did not acquire their respective miRNAs from a crown ancestor of eukaryotes after all. As for the rest of the non-coding RNA menagerie, it remains very fertile soil for hypothesis. Perhaps this question will be addressed in new articles that will regularly join our special collection in future. Andrew Moore Editor-in-Chief

• Canopy chemistry and spectroscopy offer insight into community assembly and ecosystem processes in high-diversity tropical forests, but phylogenetic and environmental factors controlling chemical traits underpinning spectral signatures remain poorly understood. • We measured 21 leaf chemical traits and spectroscopic signatures of 594 canopy individuals on high-fertility Inceptisols and low-fertility Ultisols in a lowland Amazonian forest. The spectranomics approach, which explicitly connects phylogenetic, chemical and spectral patterns in tropical canopies, provided the basis for analysis. • Intracrown and intraspecific variation in chemical traits varied from 1.4 to 36.7% (median 9.3%), depending upon the chemical constituent. Principal components analysis showed that 14 orthogonal combinations were required to explain 95% of the variation among 21 traits, indicating the high dimensionality of canopy chemical signatures among taxa. Inceptisols and lianas were associated with high leaf nutrient concentrations and low concentrations of defense compounds. Independent of soils or plant habit, an average 70% (maximum 89%) of chemical trait variation was explained by taxonomy. At least 10 traits were quantitatively linked to remotely sensed signatures, which provided highly accurate species classification. • The results suggest that taxa found on fertile soils carry chemical portfolios with a deep evolutionary history, whereas taxa found on low-fertility soils have undergone trait evolution at the species level. Spectranomics provides a new connection between remote sensing and community assembly theory in high-diversity tropical canopies.

Comparative phylogenetic analyses based on linguistic data are useful for reconstructing the cultural evolution of recent expansions of humans around the world. It is an exciting time for phylogenetic comparative studies in lowland South America given the emergence of more comprehensive ethnolinguistic datasets. Phylogenetic methods can now be applied to more lowland language families to facilitate the study of pre-historical population expansions and cultural variation. This chapter investigates phylogenetic relationships among the six major lowland South American language families using structural linguistic data. Two cultural traits that are likely to have deep evolutionary histories that extend back to last common ancestors of several large language families include uxorilocal postmarital residence (women continue to live near natal families after marriage) and partible paternity beliefs (conception belief that multiple men can be co-genitors of one child). The Carib-Pano-Tupi-Jê clade is mostly uxorilocal with partible paternity beliefs in thirty-eight of forty-three societies.

Humans and other great apes have evolved rich social and emotional capacities that enable them to navigate their complex social worlds. These include sophisticated ways to produce, perceive, and express affective states, as well as to respond effectively to the states of others. A distinctive feature of human emotional functioning is empathy, the capacity to share and understand others’ states. Far from being uniquely human, empathy has a deep evolutionary history and may be found across diverse animal species in both mammals and birds. This chapter examines some of the continuities between the emotional processes, including empathy of humans and our closest ape relatives. Chimpanzees (Pan troglodytes) and bonobos (P. paniscus) are our closest cousins and show numerous overlaps in their socio-affective and cognitive capacities, social structures, and life histories. Studying their emotional and empathic capacities reveals many overlaps, highlighting a deep evolutionary basis of hominid emotionality.

This essay explores ways in which a notion of “weak nature” drawn from certain strains of recent philosophy (especially works by Adrian Johnston and Leonard Lawlor) might be mobilized in critical engagements with contemporary and historical writings on music and sound. To thematize nature’s weakness in this context means to understand ecological phenomena as rooted in contingency, transience, non-identity, and non-presence. Through readings of texts by Timothy Morton, Charles O. Nussbaum, Gary Tomlinson, and G. W. F. Hegel, this essay shows how philosophical thought on music often works to deny or foreclose nature’s weakness, rooting accounts of musical experience or music history (including music’s deep evolutionary history) in visions of nature as consistent, gapless, and present. This same inquiry, however, suggests that musical thought that gives fuller rein to nature’s inconsistency can do greater justice to the spectra of difference that range across the many phenomena of musicking.

Plant nucleotide-binding leucine-rich repeat (NLR) immune receptors generally exhibit hallmarks of rapid evolution, even at the intraspecific level. We used iterative sequence similarity searches coupled with phylogenetic analyses to reconstruct the evolutionary history of HOPZ-ACTIVATED RESISTANCE1 (ZAR1), an atypically conserved NLR that traces its origin to early flowering plant lineages ∼220 to 150 million yrs ago (Jurassic period). We discovered 120 ZAR1 orthologs in 88 species, including the monocot Colocasia esculenta, the magnoliid Cinnamomum micranthum, and most eudicots, notably the Ranunculales species Aquilegia coerulea, which is outside the core eudicots. Ortholog sequence analyses revealed highly conserved features of ZAR1, including regions for pathogen effector recognition and cell death activation. We functionally reconstructed the cell death activity of ZAR1 and its partner receptor-like cytoplasmic kinase (RLCK) from distantly related plant species, experimentally validating the hypothesis that ZAR1 evolved to partner with RLCKs early in its evolution. In addition, ZAR1 acquired novel molecular features. In cassava (Manihot esculenta) and cotton (Gossypium spp.), ZAR1 carries a C-terminal thioredoxin-like domain, and in several taxa, ZAR1 duplicated into 2 paralog families, which underwent distinct evolutionary paths. ZAR1 stands out among angiosperm NLR genes for having experienced relatively limited duplication and expansion throughout its deep evolutionary history. Nonetheless, ZAR1 also gave rise to noncanonical NLRs with integrated domains and degenerated molecular features.

Human hunter-gatherer groups were commonly thought to be broadly egalitarian, with increasingly formal hierarchical social structures hypothesized to spread following the introduction of agriculture. However, this view is being challenged by mounting evidence for social hierarchies in several foraging populations. Nonetheless, the processes by which such hierarchies emerge, and whether human hierarchies are homologous with non-human systems of dominance, remains unclear. Here we examine the role of prestige, the tendency to freely confer status and influence on skilled or esteemed individuals and a proposed component of human-unique cultural psychology, in generating unequal patterns of social influence. Through a combination of cultural evolutionary modelling, human experimentation, and evolutionary simulations, we find that human prestige psychology generates highly unequal influence hierarchies, and that the “prestige sensitivity” we measure empirically in human participants closely matches the predictions of our evolutionary simulations, suggesting it is an evolved psychological adaptation. Nonetheless, unlike non-human dominance hierarchies, the processes involved are non-coercive, being driven by individuals freely seeking high quality information. We thus conclude that social hierarchies plausibly have a deep evolutionary history in our lineage, with prestige enabling hierarchies to be mutually beneficial as opposed to coercive.

Patterns of urinary cortisol levels during ontogeny appear population specific rather than species specific in wild chimpanzees and bonobos

The article aims to provide a general framework for assessing and categorizing the cognitive systems of human and non-human animals. Our approach stems from biosemiotic, ethological, and phenomenological investigations into the relations of organisms to one another and to their environment. Building on the analyses of Merleau-Ponty and Portmann, organismal bodies and surfaces are distinguished as the base for sign production and interpretation. Following the concept of modelling systems by Sebeok, we develop a concentric model of human and non-human animal cognition that posits three intertwined spheres: corporeity, social communication, and culture. The model explicitly works with the pluralistic perspective that views the communication and cognition of humans as distinct, but not superior to those of non-human animals. Our position is substantiated by two case studies: the first one focuses on the acquisition and spread of nut-cracking technique among the chimpanzees in the Tai forest, the second one on the communication and cognition of deafblind persons. From an epistemological perspective, our paper is a contribution to contemporary attempts to link biosemiotics and ethology with phenomenological concepts of agency, living bodies, and lifeworld.