Mitochondria as the powerhouses of sexual selection: testing mechanistic links between development, cellular respiration, and bird song

Although the influence of developmental conditions on the expression of sexually selected traits is established, the physiological mechanisms that modulate such effects remain a matter of intense debate. Here, we test the role of the developmental environment in shaping adult mitochondrial function and link mitochondrial function to expression of a sexually selected trait in males (bird song). We exposed male zebra finches (Taeniopygia guttata) to corticosterone (CORT) treatment during development. After males reached adulthood, we quantified mitochondrial function from whole red blood cells and measured baseline CORT and testosterone levels, body condition/composition, and song structure. CORT-treated males had less efficient mitochondrial function (FCRL/R), lower mitochondrial ‘working pace’ (FCRR/ETS), and higher baseline levels of CORT as adults compared to control males. Using structural equation modelling, we found that the effects of CORT treatment during development on adult mitochondrial function were indirect and modulated by baseline CORT levels, which are programmed by CORT treatment during development. Developmental treatment had an indirect effect on song peak frequency. Males treated with CORT during development sang songs with higher peak frequency than control males, but this effect was modulated through increased CORT levels and decreased mitochondrial efficiency (FCRL/R). CORT-treated males had smaller tarsi compared to control males; however, there were no associations between body size and measures of song frequency. Here, we provide the first evidence supporting links between the developmental environment, mitochondrial function, and the expression of a sexually selected display (bird song).

Urban Noise Restricts Song Frequency Bandwidth and Syllable Diversity in Bananaquits: Increasing Audibility at the Expense of Signal Quality

Anthropogenic noise can interfere with animal behavior through masking of acoustic communication. In response to masking, animals may change their acoustic signals as an apparent adjustment strategy, but this may have a drawback on signal quality. Songs and calls may show noise-dependent changes in frequency and duration, which may yield some masking avoidance, but may also constrain other acoustic parameters that might carry information about the sender. In the present study, we investigated whether noise-dependent reduction in frequency bandwidth or song duration restricted syllable diversity or song elaboration in a Neotropical songbird, the bananaquit (Coereba flaveola). We show that bananaquits sing higher frequency songs, of narrower bandwidth, in noisier territories, independent of variation in territory density, without significant variation in song duration. We also show that songs with higher minimum frequencies, narrower bandwidths, and shorter durations have on average a lower number of syllable types and higher syllable rates. This finding is in line with an acoustic restriction and may reflect a functional trade-off between audibility and signal value: higher frequencies may be more audible but less elaborate songs may weaken the message of sender quality. Consequently, noise pollution may not only alter avian communities, but also shape acoustic diversity and processes of sexual selection in urban environments.

Noise-Related Song Variation Affects Communication: Bananaquits Adjust Vocally to Playback of Elaborate or Simple Songs

Birds communicate through acoustic variation in their songs for territorial defense and mate attraction. Noisy urban conditions often induce vocal changes that can alleviate masking problems, but that may also affect signal value. We investigated this potential for a functional compromise in a neotropical songbird: the bananaquit (Coereba flaveola). This species occurs in urban environments with variable traffic noise levels and was previously found to reduce song elaboration in concert with a noise-dependent reduction in song frequency bandwidth. Singing higher and in a narrower bandwidth may make their songs more audible in noisy conditions of low-frequency traffic. However, it was unknown whether the associated decrease in syllable diversity affected their communication. Here we show that bananaquits responded differently to experimental playback of elaborate vs. simple songs. The variation in syllable diversity did not affect general response strength, but the tested birds gave acoustically distinct song replies. Songs had fewer syllables and were lower in frequency and of wider bandwidth when individuals responded to elaborate songs compared to simple songs. This result suggests that noise-dependent vocal restrictions may change the signal value of songs and compromise their communicative function. It remains to be investigated whether there are consequences for individual fitness and how such effects may alter the diversity and density of the avian community in noisy cities.