Inspiring song: The role of respiratory circuitry in the evolution of vertebrate vocal behavior

Abstract

Vocalization is a common means of communication across vertebrates, but the evolutionary origins of the neural circuits controlling these behaviors are not clear. Peripheral mechanisms of sound production vary widely: fish produce sounds with a swimbladder or pectoral fins; amphibians, reptiles, and mammalians vocalize using a larynx; birds vocalize with a syrinx. Despite the diversity of vocal effectors across taxa, there are many similarities in the neural circuits underlying the control of these organs. Do similarities in vocal circuit structure and function indicate that vocal behaviors first arose in a single common ancestor, or have similar neural circuits arisen independently multiple times during evolution? In this review, we describe the hindbrain circuits that are involved in vocal production across vertebrates. Given that vocalization depends on respiration in most tetrapods, it is not surprising that vocal and respiratory hindbrain circuits across distantly related species are anatomically intermingled and functionally linked. Such vocal-respiratory circuit integration supports the hypothesis that vocal evolution involved the expansion and functional diversification of breathing circuits. Recent phylogenetic analyses, however, suggest vocal behaviors arose independently in all major tetrapod clades, indicating that similarities in vocal control circuits are the result of repeated co-options of respiratory circuits in each lineage. It is currently unknown whether vocal circuits across taxa are made up of homologous neurons, or whether vocal neurons in each lineage arose from developmentally and evolutionarily distinct progenitors. Integrative comparative studies of vocal neurons across brain regions and taxa will be required to distinguish between these two scenarios.

Keywords: CPG; central pattern generator; evolution; hindbrain; parabrachial; vocal.

FIGURE 1

Evolution and diversity of vocal mechanisms in vertebrates. (a) Vertebrate phylogenetic tree depicting relationships between mammals, birds, non-avian reptiles, amphibians and bony fish (from top to bottom). Phylogenetic evidence suggests that vocal behaviors evolved independently at least once in each of these clades (indicated by asterisks). (b-e) Proposed homologous vocal nuclei in mammals (b), birds (c), amphibians (d) and fish (e). Sagittal view brain diagrams (anterior is left, dorsal is up) illustrating motor and premotor brain regions involved in vocal pattern generation. Gray ovals in (d) and (e) represent vocal regions in frogs (inferior reticular formation, Ri) and fish (pacemaker and prepacemaker nuclei) with uncertain relations to bird and mammalian nuclei. Abbreviations: n.XII, hypoglossal nucleus; NA, nucleus ambiguus; n.IX-X, cranial motor nucleus IX-X; nRA, nucleus retroambiguus; RAm, nucleus retroambigualis; PBC, pre-Bötzinger complex; PAm, nucleus parambigualis; PB, parabrachial complex; PAG, periaqueductal gray

FIGURE 2

Hypothetical respiratory circuits co-opted for vocal production. The evolution of vocal circuits may have resulted from the expansion and functional diversification of respiratory circuitry present in a non-vocal common ancestor of all extant tetrapods; diagram illustrates two hypothetical respiratory nuclei (ovals), each containing two developmentally distinct neuronal subtypes identifiable via expression of distinct genetic markers (indicated by light and dark shaded circles). Vocal neurons may have arisen in the same nuclei independently in two species, albeit via elaboration and functional divergence of developmentally distinct cell types (e.g., vocal species 1 and 2 in (a) and (b); newly evolved vocal neurons with diagonal stripes). Alternatively, two species might independently co-opt the same neuronal populations (e.g., vocal species 2 and 3 in b and c). Finally, different species may co-opt neurons in distinct respiratory nuclei (vocal species 1–3 in a-c, versus vocal species 4 in d)