The evolution of vocal learning

Highlights

• Comparative evidence supports two explanations for the origin of vocal learning.

• In one, vocal learning is favored by sexual selection for complex vocalizations.

• In the second, vocal learning is favored by kin selection for information sharing.

• Environmental adaptation for transmission may play a role under either hypothesis.

Vocal learning, in which animals modify their vocalizations to imitate those of others, has evolved independently in scattered lineages of birds and mammals. Comparative evidence supports two hypotheses for the selective advantages leading to the origin of vocal learning. The sexual selection hypothesis proposes that vocal learning evolves to allow expansion of vocal repertoires in response to mating preferences for more complex vocalizations. The information-sharing hypothesis also proposes that vocal learning evolves to allow expansion of vocal repertoires, but in this case in response to kin selection favoring sharing of information among relatives.

Introduction

Although vocal learning has evolved multiple times in vertebrates, relatively few lineages possess this ability [1, 2]. Vocal learning is especially rare among mammals, and among primates is well developed only in humans [3]. The rarity of vocal learning may be explained in part by the complexity of the neurological underpinnings that this ability seems to require [2]. Given the complexity of vocal learning as an adaptation, and its centrality to the life histories of some species, it is not surprising that attention has been given to explaining its evolution. Because the evolution of vocal learning in any one lineage, including our own, is typically a one-off affair, progress in testing ideas on the evolution of vocal learning requires a comparative approach. This approach is challenging because the lineages that have evolved vocal learning are few and diverse, hampering the application of formal comparative methods, which require a much larger number of taxa for statistical comparison. Nonetheless, progress is only possible by synthesizing patterns across multiple lineages, as we attempt here in a qualitative fashion.

When we speak of vocal learning, we are referring specifically to vocal production learning, in which signalers alter the form of their vocalizations by imitating the vocalizations of others [4]. Additional types of vocal learning occur, such as usage learning, in which signalers learn the context in which to produce specific vocalizations, and comprehension learning, in which receivers learn to modify their response to vocalizations produced by others [4]. These additional forms of vocal learning have a wider taxonomic occurrence [1] and perhaps can be accomplished without the considerable neural apparatus that undergirds vocal production learning [2], and consequently their evolution seems less puzzling.

Because vocal production learning requires complex neural adaptations that are presumably costly, this type of learning is not expected to evolve except in response to some compensating fitness advantage. Some of the hypothesized advantages of vocal learning are experienced by an individual only when most or all of the other signalers in its population are vocal learners and receiver response has evolved to adjust to this circumstance. Advantages such as these are not relevant to the evolutionary origin of vocal learning because they only would accrue when the trait has already evolved, although they may be important to its evolutionary maintenance. Our focus here is principally on the origins of vocal production learning, and thus on the benefits that accrue to the first individuals that begin to modify their vocalizations based on the sounds they hear from others.