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Keywords:

  • conservation suboscine;
  • cotinga;
  • cultural evolution;
  • gene flow;
  • population genetics;
  • song learning

Abstract

Vocal learning is thought to have evolved in three clades of birds (parrots, hummingbirds, and oscine passerines), and three clades of mammals (whales, bats, and primates). Behavioural data indicate that, unlike other suboscine passerines, the three-wattled bellbird Procnias tricarunculata (Cotingidae) is capable of vocal learning. Procnias tricarunculata shows conspicuous vocal ontogeny, striking geographical variation in song, and rapid temporal change in song within a population. Deprivation studies of vocal development in P. tricarunculata are impractical. Here, we report evidence from mitochondrial DNA sequences and nuclear microsatellite loci that genetic variation within and among the four allopatric breeding populations of P. tricarunculata is not congruent with variation in vocal behaviour. Sequences of the mitochondrial DNA control region document extensive haplotype sharing among localities and song types, and no phylogenetic resolution of geographical populations or behavioural groups. The vocally differentiated, allopatric breeding populations of P. tricarunculata are only weakly genetically differentiated populations, and are not distinct taxa. Mitochondrial DNA and microsatellite variation show small (2.9% and 13.5%, respectively) but significant correlation with geographical distance, but no significant residual variation by song type. Estimates of the strength of selection that would be needed to maintain the observed geographical pattern in vocal differentiation if songs were genetically based are unreasonably high, further discrediting the hypothesis of a genetic origin of vocal variation. These data support a fourth, phylogenetically independent origin of avian vocal learning in Procnias. Geographical variations in P. tricarunculata vocal behaviour are likely culturally evolved dialects.