Species interactions such as mutualism, parasitism, and predation underpin much of life’s diversity. We aimed to understand the role of learnt traits in the origin and maintenance of mutually beneficial interactions between species (mutualisms), and to test their evolutionary and ecological consequences. To do so, we studied a remarkable mutualism: the foraging partnership between an African bird species, the greater honeyguide, and the human honey-hunters whom it guides to bees’ nests. Honeyguides know where bees’ nests are located and like to eat beeswax; humans have the ability to subdue the bees and open the nest, thus exposing beeswax for the honeyguides and honey for the humans. This rare example of cooperation between humans and wild animals gives us a wonderful opportunity to study mutualisms, because local human and honeyguide populations vary strikingly in whether and how they interact, and because we can readily manipulate these interactions experimentally. We carried out research in close cooperation with rural honey-hunting communities, particularly in northern Mozambique. Here, and at other locations in south-eastern Africa, we asked how learning is involved in maintaining a geographical mosaic of honeyguide adaptation to different human cultures. We asked how reciprocal communication between humans and honeyguides mediates their interactions, and in so doing tested for the first time the hypothesis that reciprocal learning can give rise to matching cultural traits between interacting species. We asked how the mutualism both maintains, and is maintained by, other species in the ecosystem, and investigated how it helps to shape ecosystem processes (such as wildfires) in its wider environment . Understanding the role of such behavioural adaptations is crucial to explaining how and why the outcome of species interactions varies in space and time, and to predict how they will respond to a rapidly changing world.