Sound is an essential source of information in many taxa and can notably be used by embryos to program their phenotypes for postnatal environments. While underlying mechanisms are mostly unknown, there is growing evidence for the implication of mitochondria – main source of cellular energy (i.e. ATP) – in developmental programming processes. Here, we tested whether prenatal sound programs mitochondrial metabolism. In the arid-adapted zebra finch, prenatal exposure to “heat-calls” – produced by parents incubating at high temperatures – adaptively alters nestling growth in the heat. We measured red blood cell mitochondrial function, in nestlings exposed prenatally to heat- or control-calls, and reared in contrasting thermal environments. Exposure to high temperatures always reduced mitochondrial ATP production efficiency. However, as expected to reduce heat production, prenatal exposure to heat-calls improved mitochondrial efficiency under mild heat conditions. In addition, when exposed to an acute heat-challenge, LEAK respiration was higher in heat-call nestlings, and mitochondrial efficiency low across temperatures. Consistent with its role in reducing oxidative damage, LEAK under extreme heat was also higher in fast-growing nestlings. Our study, therefore, provides the first demonstration of mitochondrial acoustic sensitivity, and brings us closer to understanding the underpinning of acoustic developmental programming and avian strategies for heat adaptation.

Variable names ch: chick identity date / dateJD: sampling and mitochondrial measurement date / date in Julian days idclutch / idnest / idnest_num: nest of origin (genetic) / foster nest / simpler label for foster nest tray: prenatal playback (A= heat-calls, B= control-calls) from: experimental conditions (nest= in-nest, chamber= heat-challenge) mNT / NT3hsamp: average nest temperature from hatching to D12 during daytime (=12D-Tnest) / nest temperature 3h before sampling (= AM-Tnest) chamber_maxTemp: max temperature experienced in the heat-challenge (2 birds stopped at 42, all others at 44°C) mNT_dev / NT3h_dev: for heat-challenged birds only, temperature deviations experienced from the nest (chamber_maxTemp - mNT / chamber_maxTemp - NT3hsamp) broodSize: brood size (number of chicks in the rearing nest) routineTP to fcr_retsTP: mitochondrial respiration rates and FCRs. Rates are corrected by total protein (TP) content. FCRs do not need normalisation (they are ratios). growth: mass gained (g) between D7 and D12 massD12: mass (g) at D12