Collaborative Research: Referential alarm calling as a window into the mechanisms and evolution of a complex cognitive phenotype

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In avian brood parasitism, birds lay their eggs into others’ nests, leaving the foster hosts to look after the parasitic young. Some hosts combat such parasitism by actively defending their nests from adult parasites. Yellow Warblers (Setophaga petechia) produce unique "seet" calls to warn about the presence of Brown-headed Cowbirds (Molothrus ater). In response to seet calls, female warblers return to sit tightly on the nest to prevent cowbird parasitism. This means that, much like words in human languages, seet calls symbolize cowbird parasitism for the warblers. The project’s aim is to understand how hosts perceive and process the acoustic and functional meaning of these symbolic signals by studying the behavioral responses (in the field) and neurophysiological patterns (using fMRI) of warblers to the cowbird’s own calls, seet calls, and other sounds typical of the warbler’s habitat. The grant will train a postdoctoral fellow, three PhD students, one Master's student, and at least eight undergraduate researchers, including students from groups underrepresented in STEM fields. The researchers will write and share case studies based on their research as open online educational resources for undergraduate courses in organismal biology. Additional broader impacts will include bird banding workshops for the general public, especially during the vibrant migratory seasons in central Illinois and Michigan. Finally, a short 3D virtual reality film-feature will be produced entitled "A Day in the Life of the Cowbird", featuring characteristic daily activities of parasitic birds and their interactions with hosts, as seen from the parasite's own eyes' perspective.Current and past research on alarm calling in animals has often focused on the detailed discovery and characterization of the meaning of referential communication signals. However, the sensory-perceptual abilities of animals to recognize referential calls and the potentially high-level neural processing that ultimately leads to a specific behavioral response have not yet been fully explored. Through integrating field and laboratory experiments and levels of analyses, this research aims to test the overarching hypothesis that referential signaling requires high-level cognitive abilities. Using Yellow Warblers’ anti-brood parasitic alarm calls to Brown-headed Cowbirds as a study system, four specific predictions will be assessed regarding that referential calling (i) involves perceptual equivalency of alarm calls and their referents, (ii) is socially acquired but may be modified by personal experience with cowbirds, (iii) involves mental imagery, episodic-like memory, and mental time travel, modifying future behavior so as to decrease risks to fitness, and (iv) is a functionally specific response to obligate brood parasitism. The project couples behavioral and population-level predictions of Yellow Warblers' responses to seet calls with probing of developmental trajectories and neural substrates of referential communication in wild birds via in vivo imaging (fMRI) to repeatedly collect data across development. This integrative research will provide new perspectives on the cognitive ecology and mechanisms of referential communication, including potentially transformative understanding of the neural substrates underlying the perception of symbolic calls, the existence of mental time travel in novel contexts, and the functional substrates of referential signaling.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.