Coevolution in communication senders and receivers: vocal behavior and auditory processing in multiple songbird species

Abstract

Communication is a strong selective pressure on brain evolution because the exchange of information between individuals is crucial for fitness-related behaviors, such as mating. Given the importance of communication, the brains of signal senders and receivers are likely to be functionally coordinated. We study vocal behavior and auditory processing in multiple species of estrildid finches with the goal of understanding how species identity and early experience interact to shape the neural systems that subserve communication. Male finches learn to produce species-specific songs, and both sexes learn to recognize songs. Our studies indicate that closely related species exhibit different auditory coding properties in the midbrain and forebrain and that early life experience of vocalizations contributes to these differences. Moreover, birds that naturally sing tonal songs can learn broadband songs from heterospecific tutors, providing an opportunity to examine the interplay between species identity and early experience in the development of vocal behavior and auditory tuning.

Figure 1

Cladogram and spectrograms of the songs of five estrildid finch species show the the phylogenetic relationships and spectrotemporal diversity of song among species. The species are owl finch (Taeniopygia bichenovii), zebra finch, blackheart finch, Bengalese finch, and strawberry finch (Amandava amandava).

Figure 2

Sagittal view of the primary auditory (black) and vocal motor (gray) pathways in the male songbird brain. NM, nucleus magnocellularis; NL, nucleus laminaris; SON, superior olivary nucleus; LL, lateral lemniscal nuclei; MLd, mesencephalicus lateralis dorsalis; Ov, nucleus ovoidalis; L, field L; CM, caudal mesopallium; NCM, caudomedial nidopallium; HVC is a proper name; RA, robust nucleus of the arcopallium.

Figure 3

The spiking responses of one single zebra finch (ZF) auditory midbrain neuron (upper) and one single blackheart finch (BhF) auditory midbrain neuron (lower) to Bengalese (BgF) (top), blackheart (middle) and zebra (bottom) finch songs. Recordings were made from awake males. Spectrograms of the songs that were presented to birds are shown above raster plots showing the responses of each neuron during the song presentation (row) and across multiple presentations of the same song (columns). Neurons from each species produce robust and reliable responses to the songs of all three species, but each neuron responds to different spectrotemporal features of the songs.

Figure 4

The songs of a Bengalese finch (BgF) tutor, blackheart finch (BhF) and zebra finch (ZF) tutees and the biological fathers of the tutees show that juvenile estrildids will copy heterospecific songs even when the spectrotemporal acoustics of their natural songs differ dramatically from heterospecific tutors' songs. A. First, a song motif recorded from a Bengalese finch tutor, with syllables that were copied by tutees labeled by black boxes and numbers. Second, a song motif recorded from an adult blackheart finch that was tutored by the Bengalese finch, with the syllables that it copied from the tutor labeled by boxes and numbers. Third, a motif recorded from the blackheart finch tutee's father. Fourth, a song motif recorded from an adult zebra finch that was tutored by the Bengalese finch, with the syllables that it copied from the tutor labeled by boxes and numbers. Fifth, a song bout consisting of several motifs recorded from the zebra finch tutee's father. B. Bengalese finch tutor, blackheart finch tutee and zebra finch tutee syllables that are highly similar show that both blackheart and zebra finch tutees copied song from the Bengalese finch tutor. The syllables shown are the same as those labeled by boxes and numbers in A. The blackheart finch tutee copied two syllables and the zebra finch tutee copied three syllables from the Bengalese finch tutor. Similarity scores between syllables in tutors' songs and copied syllables in tutees' songs measured using Sound Analysis Pro were 58.8 ± 5.9 (mean ± SD, unitless measure). Similarity scores between tutee syllables and syllables from the songs of their genetic fathers were 11.7 ± 1.8.