A Modular Approach to Vocal Learning: Disentangling the Diversity of a Complex Behavioral Trait

Abstract

Vocal learning is a behavioral trait in which the social and acoustic environment shapes the vocal repertoire of individuals. Over the past century, the study of vocal learning has progressed at the intersection of ecology, physiology, neuroscience, molecular biology, genomics, and evolution. Yet, despite the complexity of this trait, vocal learning is frequently described as a binary trait, with species being classified as either vocal learners or vocal non-learners. As a result, studies have largely focused on a handful of species for which strong evidence for vocal learning exists. Recent studies, however, suggest a continuum in vocal learning capacity across taxa. Here, we further suggest that vocal learning is a multi-component behavioral phenotype comprised of distinct yet interconnected modules. Discretizing the vocal learning phenotype into its constituent modules would facilitate integration of findings across a wider diversity of species, taking advantage of the ways in which each excels in a particular module, or in a specific combination of features. Such comparative studies can improve understanding of the mechanisms and evolutionary origins of vocal learning. We propose an initial set of vocal learning modules supported by behavioral and neurobiological data and highlight the need for diversifying the field in order to disentangle the complexity of the vocal learning phenotype.

Figure 1.. A phylogeny of vocal learners.

As vocalizations are thought to be innate in vocalizing fish, amphibians, and reptiles, most studies of vocal learning focus on birds and mammals. The canonical set of taxa widely cited as being vocal production learners [–4] is fairly restricted (in blue). However, some limited evidence has led to claims that a much broader range of taxa may possess some capacity for vocal learning (in red) [–9, 135, 136]. In many cases these examples rely on highly anecdotal examples, in others the evidence has been contested [137]. The remaining taxa are largely assumed to be vocal non-learners, although this has been conclusively demonstrated (classically, through deafening, hand-rearing, or cross-fostering experiments) in remarkably few taxa.

Figure 2.. Vocal learning as the intersection of several component sub-traits.

Vocal production learning has traditionally been viewed, explicitly or implicitly, as a binary trait that is either present or absent. More recently it has been proposed to be a continuum, with species increasing linearly in ability from ‘low’ to ‘high’ vocal learners [16]. An alternate view, presented here, suggests that vocal learning may be a multidimensional trait, in which species exhibit varying capacities for learning across a set of interrelated behavioral trait modules, which do not necessarily vary co-linearly. This view enables a neuroethological approach, in which species that excel in a particular module could represent ideal model to disentangle particular aspects of the vocal learning phenotype in isolation. As a starting point, we present three example modules, listed here with (in black) related concepts from the broader vocal learning literature. Species discussed in relation to each module in this review include, for vocal production variability, common marmoset (Callithrix jacchus); for vocal coordination, warbling antbirds (Hypocnemis sp.); and for vocal versatility, Egyptian fruit bat (Rousettus aegypticus).

Figure 3.. Vocal coordination.

As with any social signal, vocal communication signals must be appropriately timed and coordinated in order to produce their intended effect on their recipient(s). (A) In marmoset antiphonal calling (adapted from [138]), adults engage in ongoing bouts of rhythmically coordinated calling, a phenomenon known as turn-taking that is also exhibited in human speech. (B) Bats use the acoustic reflections of echolocation calls to navigate and detect prey. While flying and foraging in a group context, the echolocation of conspecifics then threatens to “jam” the signal of a caller, a possibility that much be avoided. One of several solutions to this problem, exhibited by the European free-tailed bat (Tadarida teniotis), is for individuals to dynamically shift the acoustic frequency of their calls to avoid overlap (blue and red dots indicate the minimum frequency of echolocation calls of two bats, adapted from [28]). (C) During vocal duetting, conspecifics tightly coordinate their vocal production as means of defending territories or maintain social bonds, among other possibilities. In some cases, as in the Rufous hornero (Furnarius rufus), these duets are refined over time between partners to match a highly-structured pattern with subsecond temporal precision (adapted from [46]).

Figure 4.. Vocal production variability & feedback.

During the plastic period of vocal development, diverse sources contribute to variability in vocal output, and the neural motor signal that underlies it. This exploratory variability is dynamically regulated to facilitate motor learning. (A) Juvenile Japanese quail exhibit an initial period of vocal variability that wanes over the course of the development of their adult crow [20]. (B) Juvenile zebra finches similarly experience an initial period of high vocal variability (subsong), which gradually (via plastic song) crystallizes into the adult song type. Uniquely in the finch relative to the quail, this decrease in vocal variability coincides with increasing similarity to the song of a tutor it was exposed to during this critical period [139]. Vocal learning is then in some respects the process by which internally guided developmental processes (as in the quail) are exposed to external influences (as in the finch).

Figure 5.. Vocal versatility.

A fundamental concept in the study of animal vocalizations is the complexity of its vocal repertoire. In some cases, as in vocalizing fish and crocodilians crocodilians (A, adapted from [140]), a species may present a very small set of calls used under a limited set of circumstances. Other species may present a more diverse acoustic repertoire with a range of categorically discrete call types, as in the case of the macaque monkey (B, adapted from [141]. Expanding the complexity of the vocal repertoire can be accomplished through various means, including increasing the dynamic motility of the vocal apparatus and taking advantage of nonlinear vocal phenomena. Vocal repertoires may also be made more versatile through the influence of learning. At its most basic, this may involve small modifications to pre-existing vocal signals to match a template, as in the case of a harbor seal trained to imitate a sequence of human vowel formants (C, adapted from [113]). In its most advanced instantiation, species may present the ability to mimic other species, novel sounds, and complex series of syllables, motifs, and phrases, as in the common starling (D, adapted from [142]).