The ontogeny of vocal communication in host-parasite systems

A project undertaken at the School of Biological Sciences, Flinders University, and supervised by Sonia Kleindorfer

We made the extraordinary discovery that female Superb Fairy-wrens (Malurus cyaneus) call to their unhatched eggs, and upon hatching the nestlings develop begging calls that closely match key elements in their mother’s incubation call. We suspect we have uncovered the vocal cue that females use to recognise their own nestlings and thus detect the presence of an intruding cuckoo nestling. Yet many questions remain. Is the call matching innate, with nestlings matching their mother’s calls because of shared genes; or are the key elements learnt with the mother fine-tuning the begging calls of her offspring?

This international research project will generate novel methodologies to address key questions about the mechanism of parasite detection. While we have a well-developed framework to understand the adaptive value of brood parasite recognition by hosts, very little is understood about the mechanism of such recognition including neural organisation, sensory development, imprinting, or vocal recognition. Understanding the mechanism of individual recognition following stimulus communication between mothers and their embryos could have significant impact for related disciplines including psychology and medicine.

Ever since the ancient Greeks, we have been intrigued by the evolutionary arms race between cuckoos and their hosts, in which a successful cuckoo offspring deceives its hosts so they rear it to independence. There is thus an arms race between brood parasites and their hosts, in which hosts evolve strategies to counter parasitism, while parasites develop more refined means to deceive hosts into rearing their offspring.

Theoretical models predict a strong selection against hosts using visual cues to detect nestlings, because any recognition error that results in mistakenly rejecting one’s own young is extremely expensive in terms of fitness. Nestlings grow and change their visual appearance, so a big chick could just be an older or stronger chick, and not necessarily a different species. Surprisingly, female Superb Fairy-wrens have been shown to detect cuckoo nestlings and abandon them to starve. This remarkable finding leads to many questions – why are these fairy-wrens an exception to what seems a global rule, what is the cue with which they detect cuckoos, and how do their nestlings avoid being mistakenly rejected?

In this study, we build on previous findings that show that wrens use acoustical cues to identify and abandon cuckoo nestlings, and test the mechanism for this discrimination. The main research aims are:

  1. To discover the processes that drive an Australian coevolutionary system whereby Superb Fairy-wrens successfully detect young cuckoo nestlings.
  2. To determine the role of acoustic cues in the detection of cuckoo nestlings, and the means by which host nestlings avoid being mistakenly rejected.
  3. To use cross fostering and playback experiments in wild populations to experimentally test whether the similarity of nestling begging calls and maternal incubation calls is innate or a learnt response.
  4. To measure the development of the auditory processing system by applying fMRI methodology and technique to both fairy-wren and cuckoo embryos in the egg exposed to a range of acoustic stimuli at different incubation phases.
Figure 1. Singing female Superb Fairy-wren (Photo: J. Robertson).

Figure 2. Male Superb Fairy-wren (Photo: J. Robertson).

Figure 3. Begging Superb Fairy-wren nestling (Photo: K. Mahr).

Figure 4. Horsfield’s Bronze-cuckoo nestling (Photo K. Mahr).

Figure 5. Pair of male and female Superb Fairy-wrens responding to playback of cuckoo song in their territory (Photo: K. Mahr).