Abstract
The capacity to learn and reproduce vocal sounds has evolved in phylogenetically distant tetrapod lineages. Vocal learners in all these lineages express similar neural circuitry and genetic factors when perceiving, processing, and reproducing vocalization, suggesting that brain pathways for vocal learning evolved within strong constraints from a common ancestor, potentially fish. We hypothesize that the auditory-motor circuits and genes involved in entrainment have their origins in fish schooling behavior and respiratory-motor coupling. In this acoustic advantages hypothesis, aural costs and benefits played a key role in shaping a wide variety of traits, which could readily be exapted for entrainment and vocal learning, including social grouping, group movement, and respiratory-motor coupling. Specifically, incidental sounds of locomotion and respiration (ISLR) may have reinforced synchronization by communicating important spatial and temporal information between school-members and extending windows of silence to improve situational awareness. This process would be mutually reinforcing. Neurons in the telencephalon, which were initially involved in linking ISLR with forelimbs, could have switched functions to serve vocal machinery (e.g. mouth, beak, tongue, larynx, syrinx). While previous vocal learning hypotheses invoke transmission of neurons from visual tasks (gestures) to the auditory channel, this hypothesis involves the auditory channel from the onset. Acoustic benefits of locomotor-respiratory coordination in fish may have selected for genetic factors and brain circuitry capable of synchronizing respiratory and limb movements, predisposing tetrapod lines to synchronized movement, vocalization, and vocal learning. We discuss how the capacity to entrain is manifest in fish, amphibians, birds, and mammals, and propose predictions to test our acoustic advantages hypothesis.
Highlights
Entrainment appears to be linked with the capacity for vocal learning, the mechanisms behind this relationship are hotly debated (Schachner et al 2009; Patel et al 2009; Patel 2014; Soma and Mori 2015; Merker et al 2015)
We hypothesized that the neural circuitry, genetic factors, and anatomy originally used in fish synchronization provided constraints on the evolution of entrainment and vocal learning in tetrapods, and that locomotor-respiratory coupling in fish is linked with forelimb motor processing and vocalization in tetrapod descendants
Acoustic benefits of locomotor-respiratory coordination in fish may have selected for genetic factors and brain circuitry capable of synchronizing respiratory and limb movements, predisposing tetrapod lines to synchronized movement, vocalization, and vocal learning
Summary
Synchronized movement at organismal and group levels is ubiquitous in vertebrates, for example, schooling fish, swarming starlings, and ballet dancers. Evolutionary Biology (2018) 45:359–373 tetrapods, including humans, share similar genetic factors (See: “FoxP2 in Vocalization”) and neuroanatomical structures for vocalization (Bass et al 2008; Scharff and Petri 2011). Multiple gene factors and neural circuits shared by all vocal learners suggest strong genetic or epigenetic constraints on the evolution of this trait, potentially stemming from neuroanatomical structures inherited from a common ancestor (Jarvis 2004; Scharff and Petri 2011), either reptiles or fish. The vocal learning and rhythmic synchronization hypothesis proposes that the ability to entrain to rhythmic auditory cues evolved as a by-product of vocal learning (Patel 2006; Schachner et al 2009). We present an alternative hypothesis, that the ability to entrain movement to external sounds is prerequisite to the development of vocal learning and that some of the auditory-motor circuits and genes for entrainment and vocal learning have their origins in schooling behavior in fish. While no species basal to both teleost and tetrapod lineages still exist, we compare genetic, neural, and behavioral characteristics of vertebrates across these groups to assess likelihood of deep homology
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