Functionally referential signals: a promising paradigm whose time has passed

Finding the evolutionary origins of human language in the communication systems of our closest living relatives has, for the last several decades, been a major goal of many in the field of animal communication generally and primate communication specifically.1–4 The so-called “functionally referential” signals have long been considered promising in this regard, with apparent parallels with the semantic communication that characterizes language. The once-prominent idea that functionally referential signals are word-like, in that they are arbitrary sounds that refer to phenomena external to the caller, has largely been abandoned.5 However, the idea that these signals may offer the strongest link between primate communication and human language remains widespread, primarily due to the fact the behavior of receivers indicates that such signals enable them to make very specific inferences about their physical or social environment. Here we review the concept of functional reference and discuss modern perspectives that indicate that, although the sophistication of receivers provides some continuity between nonhuman primate and human cognition, this continuity is not unique to functionally referential signals. In fact, because functionally referential signals are, by definition, produced only in specific contexts, receivers are less dependent on the integration of contextual cues with signal features to determine an appropriate response. The processing of functionally referential signals is therefore likely to entail simpler cognitive operations than does that of less context-specific signals. While studies of functional reference have been important in highlighting the relatively sophisticated processes that underlie receiver behavior, we believe that the continued focus on context-specific calls detracts from the potentially more complex processes underlying responses to more unspecific calls. In this sense, we argue that the concept of functional reference, while historically important for the field, has outlived its usefulness and become a red herring in the pursuit of the links between primate communication and human language

Prenatal Androgen Effects as a Proximate Mechanism Underpinning Variation in Social Behavior Among Female Nonhuman Primates

While the role of ecological factors in shaping primate social systems has been a central focus for decades, less attention has been given to phylogenetic relationships and the potential role of underlying proximate mechanisms. This study aimed to investigate the relationship between one such proximate mechanism, prenatal androgen effects (PAEs), and aspects of social behavior in female nonhuman primates using the 2D:4D ratio as a proxy for PAEs and phylogenetically controlled methods. In general, female 2D:4D ratios were highest in monogamous species (low inferred PAEs) and lowest in polygynandrous and polygynous species (high inferred PAEs). 2D:4D ratios also varied with the form of polygyny/polygynandry, potentially with regard to the need for competitive over cooperative behaviors and the intensity of female reproductive competition. Species characterized by female dominance had lower 2D:4D ratios than species characterized by male dominance or codominance. There were no significant relationships between 2D:4D ratio and either degree of frugivory or group size. Relationships between 2D:4D ratios and the directional consistency index and 2D:4D ratios and rates of female–female agonism were also nonsignificant although sample sizes for both of these variables were small. Female social relationships are a manifestation of complex competitive and cooperative behaviors and the results suggest thatPAEs may act as a proximate mechanism underlying the expression of certain aspects of behavior in female primates in ways that are adaptive to their social system

Is there any evidence for vocal learning in chimpanzee food calls?

In their study “Vocal Learning in the Functionally Referential Food Grunts of Chimpanzees”, Watson et al. [1] claimed that they “provide the first evidence for vocal learning in a referential call in non-humans”. We challenge this conclusion, on two counts. For one, we are not convinced that the authors controlled for arousal (or at least they did not report such data); furthermore, the vocal characteristics of the two groups largely overlapped already at the beginning of the study. Accordingly, we also question the authors’ claim that their finding “sheds new light on the evolutionary history of human referential words”

Experimental Evidence for Heterospecific Alarm Signal Recognition via Associative Learning in Wild Capuchin Monkeys

Many vertebrate taxa respond to heterospecific alarm calls with anti-predator behaviours. While it is unclear how apparent recognition is achieved, learned associations between the occurrence of the call and the presence of a predator are considered the most likely explanation. Conclusive evidence that this behaviour is indeed underpinned by learning, however, is scarce. This study tested whether wild black capuchin monkeys (Sapajus nigritus) learn to associate novel sounds with predators through a two-phase field experiment. During an initial training phase, three study groups were each presented with a playback of one of the three novel sounds together with a simulated felid predator on four occasions over an 8- to 12-week period. This was followed by a test phase, wherein each of the three sounds was played back to individuals in all three groups, allowing each sound to serve as both a test stimulus for individuals trained with that sound, and a control stimulus for individuals trained with another sound. Antipredator responses were significantly stronger in response to test sounds than to controls. Limited observations suggest that antipredator responses persisted for at least 2 years without reinforcement of the predator–sound link. Additionally, responses to noisier sounds were typically stronger than were those to more tonal sounds, although the effect of sound type cannot be disentangled from potential effects of group. This study provides the strongest evidence to date that learning affects the responses of primates to sounds such as heterospecific alarm calls, and supports the contention that signals provide receivers with information

Competition-induced stress does not explain deceptive alarm calling in tufted capuchin monkeys

Tactical deception has long attracted interest because it is often assumed to entail complex cognitive mechanisms. However, systematic evidence of tactical deception is rare and no study has attempted to determine whether such behaviours may be underpinned by relatively simple mechanisms. This study examined whether deceptive alarm calling among wild tufted capuchin monkeys, Cebus apella nigritus, feeding on contestable food resources can be potentially explained by a physiological mechanism, namely increased activation in the adrenocortex and the resulting production of glucocorticoids (GCs; ‘stress hormones’). This was tested experimentally in Iguazu? National Park, Argentina, by manipulating the potential for contest competition over food and noninvasively monitoring GC production through analysis of faecal hormone metabolites. If deceptive false alarms are indeed associated with adreno- cortical activity, it was predicted that the patterns of production of these calls would match the patterns of GC output, generally being higher in callers than noncallers in cases in which food is most contestable, and specifically being higher in callers on those occasions when a deceptive false alarm was produced. This hypothesis was not supported, as (1) GC output was significantly lower in association with the experimental introduction of contestable resources than in natural contexts wherein the potential for contest is lower, (2) within experimental contexts, there was a nonsignificant tendency for noncallers to show higher GC output than callers when food was most contestable, and (3) individuals did not show higher GC levels in cases in which they produced deceptive alarms relative to cases in which they did not. A learned association between the production of alarms and increased access to food may be the most likely cognitive explanation for this case of tactical deception, although unexplored physiological mechanisms also remain possible

Male resource defense mating system in primates? An experimental test in wild capuchin monkeys

Ecological models of mating systems provide a theoretical framework to predict the effect of the defendability of both breeding resources and mating partners on mating patterns. In resource-based mating systems, male control over breeding resources is tightly linked to female mating preference. To date, few field studies have experimentally investigated the relationship between male resource control and female mating preference in mammals due to difficulties in manipulating ecological factors (e.g., food contestability). We tested the within-group male resource defense hypothesis experimentally in a wild population of black capuchin monkeys (Sapajus nigritus) in Iguazú National Park, Argentina. Sapajus spp. represent an ideal study model as, in contrast to most primates, they have been previously argued to be characterized by female mate choice and a resource-based mating system in which within-group resource monopolization by high-ranking males drives female mating preference for those males. Here, we examined whether females (N = 12) showed a weaker preference for alpha males during mating seasons in which food distribution was experimentally manipulated to be less defendable relative to those in which it was highly defendable. Results did not support the within-group male resource defense hypothesis, as female sexual preferences for alpha males did not vary based on food defendability. We discuss possible reasons for our results, including the possibility of other direct and indirect benefits females receive in exercising mate choice, the potential lack of tolerance over food directed towards females by alpha males, and phylogenetic constraints

Uncoupling of Genomic and Epigenetic Signals in the Maintenance and Inheritance of Heterochromatin Domains in Fission Yeast

Many essential aspects of genome function, including gene expression and chromosome segregation, are mediated throughout development and differentiation by changes in the chromatin state. Along with genomic signals encoded in the DNA, epigenetic processes regulate heritable gene expression patterns. Genomic signals such as enhancers, silencers, and repetitive DNA, while required for the establishment of alternative chromatin states, have an unclear role in epigenetic processes that underlie the persistence of chromatin states throughout development. Here, we demonstrate in fission yeast that the maintenance and inheritance of ectopic heterochromatin domains are independent of the genomic sequences necessary for their de novo establishment. We find that both structural heterochromatin and gene silencing can be stably maintained over an ∼10-kb domain for up to hundreds of cell divisions in the absence of genomic sequences required for heterochromatin establishment, demonstrating the long-term persistence and stability of this chromatin state. The de novo heterochromatin, despite the absence of nucleation sequences, is also stably inherited through meiosis. Together, these studies provide evidence for chromatin-dependent, epigenetic control of gene silencing that is heritable, stable, and self-sustaining, even in the absence of the originating genomic signals

Variation in grouping patterns, mating systems and social structure: what socio-ecological models attempt to explain

Socio-ecological models aim to predict the variation in social systems based on a limited number of ecological parameters. Since the 1960s, the original model has taken two paths: one relating to grouping patterns and mating systems and one relating to grouping patterns and female social structure. Here, we review the basic ideas specifically with regard to non-human primates, present new results and point to open questions. While most primates live in permanent groups and exhibit female defence polygyny, recent studies indicate more flexibility with cooperative male resource defence occurring repeatedly in all radiations. In contrast to other animals, the potential link between ecology and these mating systems remains, however, largely unexplored. The model of the ecology of female social structure has often been deemed successful, but has recently been criticized. We show that the predicted association of agonistic rates and despotism (directional consistency of relationships) was not supported in a comparative test. The overall variation in despotism is probably due to phylogenetic grade shifts. At the same time, it varies within clades more or less in the direction predicted by the model. This suggests that the model's utility may lie in predicting social variation within but not across clades

Predictors of orbital convergence in primates: A test of the snake detection hypothesis of primate evolution

Traditional explanations for the evolution of high orbital convergence and stereoscopic vision in primates have focused on how stereopsis might have aided early primates in foraging or locomoting in an arboreal environment. It has recently been suggested that predation risk by constricting snakes was the selective force that favored the evolution of orbital convergence in early primates, and that later exposure to venomous snakes favored further degrees of convergence in anthropoid primates. Our study tests this snake detection hypothesis (SDH) by examining whether orbital convergence among extant primates is indeed associated with the shared evolutionary history with snakes or the risk that snakes pose for a given species. We predicted that orbital convergence would be higher in species that: 1) have a longer history of sympatry with venomous snakes, 2) are likely to encounter snakes more frequently, 3) are less able to detect or deter snakes due to group size effects, and 4) are more likely to be preyed upon by snakes. Results based on phylogenetically independent contrasts do not support the SDH. Orbital convergence shows no relationship to the shared history with venomous snakes, likelihood of encountering snakes, or group size. Moreover, those species less likely to be targeted as prey by snakes show significantly higher values of orbital convergence. Although an improved ability to detect camouflaged snakes, along with other cryptic stimuli, is likely a consequence of increased orbital convergence, this was unlikely to have been the primary selective force favoring the evolution of stereoscopic vision in primates