Shared neural substrates for song discrimination in parental and parasitic songbirds.
In many social animals, early exposure to conspecific stimuli is critical for the development of accurate species recognition. Obligate brood parasitic songbirds, however, forego parental care and young are raised by heterospecific hosts in the absence of conspecific stimuli. Having evolved from non-parasitic, parental ancestors, how brood parasites recognize their own species remains unclear. In parental songbirds (e.g. zebra finch Taeniopygia guttata), the primary and secondary auditory forebrain areas are known to be critical in the differential processing of conspecific vs. heterospecific songs. Here we demonstrate that the same auditory brain regions underlie song discrimination in adult brood parasitic pin-tailed whydahs (Vidua macroura), a close relative of the zebra finch lineage. Similar to zebra finches, whydahs showed stronger behavioral responses during conspecific vs. heterospecific song and tone pips as well as increased neural responses within the auditory forebrain, as measured by both functional magnetic resonance imaging (fMRI) and immediate early gene (IEG) expression. Given parallel behavioral and neuroanatomical patterns of song discrimination, our results suggest that the evolutionary transition to brood parasitism from parental songbirds likely involved an "evolutionary tinkering" of existing proximate mechanisms, rather than the wholesale reworking of the neural substrates of species recognition.
Department of Biology, East Carolina University, Greenville, NC 27858, USA; Department of Psychology, Hunter College and the Graduate Center, City University of New York, NY, NY 10065, USA. Electronic address: mckimlouder@gmail.com.
Matthew I M
MI
Louder
Department of Radiology, Weill Cornell Medical College, NY, NY 10065, USA.
Henning U
HU
Voss
Department of Psychology, Hunter College and the Graduate Center, City University of New York, NY, NY 10065, USA.
Thomas J
TJ
Manna
Department of Psychology, Hunter College and the Graduate Center, City University of New York, NY, NY 10065, USA; Department of Biological Sciences, Lehman College, City University of New York, Bronx, NY 10468, USA.
Sophia S
SS
Carryl
Department of Psychology, Institute for Mind and Biology, University of Chicago, Chicago, IL 60637, USA.
Sarah E
SE
London
Department of Biology, East Carolina University, Greenville, NC 27858, USA.
Christopher N
CN
Balakrishnan
Department of Psychology, Hunter College and the Graduate Center, City University of New York, NY, NY 10065, USA.
Mark E
ME
Hauber
D000161:Acoustic Stimulation; D000818:Animals; D001303:Auditory Cortex / Q000502:physiology*; D004192:Discrimination, Psychological; D005260:Female; D017781:Genes, Immediate-Early; D008279:Magnetic Resonance Imaging; D008297:Male; D046109:Passeriformes / Q000502:physiology*; D010897:Pitch Discrimination; D020308:Songbirds / Q000502:physiology; D013045:Species Specificity; D014828:Vocalization, Animal / Q000502:physiology*
Auditory cortex; Birdsong; Brood parasite; Oscines; Species recognition; Zebra finch