Altricial brains and the evolution of infant vocal learning.

Unlabelled: Human infant vocal development is strongly influenced by interactions with caregivers who reinforce more speech-like sounds. This trajectory of vocal development in humans is radically different from those of our close phylogenetic relatives, Old World monkeys and apes. In these primates most closely related to humans on the evolutionary tree, social feedback plays no significant role in their vocal development. Oddly, infant marmoset monkeys, a more distantly related New World primate, do exhibit socially guided vocal learning. To explore what developmental mechanism could have evolved to account for these behavioral differences, we hypothesized that the evolution of human and marmoset vocal learning in early infancy in both species is because they are born neurally altricial relative to other primate and in a cooperative breeding social environment. Our analysis found that, indeed, human and marmoset brain are growing faster at birth when compared with chimpanzees and rhesus macaques, making them altricial relative to these primates. We formalized our hypothesis using a logistic growth model showing that the maturation of a system dependent on the rate of brain growth and the amount of social stimuli benefits from an altricial brain and a cooperative breeding environment. Our data suggest that in primates, the evolution of socially guided vocal learning during early infancy in humans and marmosets was afforded by infants with a relatively altricial brain and behavior, sustained and stimulated by cooperative breeding environments.

Significance Statement: Humans rely on social feedback from caregivers to learn how to produce species-typical sounds, whereas other primates like macaque monkeys or chimpanzees do not. What accounts for this difference in developmental strategies? We tested the hypothesis that being born with a more immature (thus more plastic) brain may be the reason by using marmoset monkeys. This species is more distantly related to humans but exhibit the same type of vocal learning and who have a similar socially rich infant care environment. We found that, indeed, human and marmoset brain are growing faster at birth when compared with chimpanzees and rhesus macaques, making them altricial relative to these primates and this explains their similar vocal developmental strategies.