Prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird.

Eve Udino,Mylene M Mariette,Julia M George,Katherine L Buchanan,Matthew Mckenzie,Ondi L Crino,Anaïs Pessato

doi:10.1098/rspb.2021.1893

Eve Udino, Mylene M Mariette + Show 5 more

Open Access

https://doi.org/10.1098/rspb.2021.1893

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Abstract

Sound is an essential source of information in many taxa and can notably be used by embryos to programme their phenotypes for postnatal environments. While underlying mechanisms are mostly unknown, there is growing evidence for the involvement of mitochondria—main source of cellular energy (i.e. ATP)—in developmental programming processes. Here, we tested whether prenatal sound programmes 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.

Highlights

Developmental programming occurs across taxa, as early life environments alter developmental processes and thereby shape individual phenotype [1,2]
We found that an acoustic signal experienced prenatally shaped individual mitochondrial function in postnatal life
While short-term hot conditions consistently reduced nestling mitochondrial efficiency, prenatal exposure to heat-call altered this response, in the directions predicted by each of our hypotheses relating to the adaptive function of mitochondrial programming

Summary

Introduction

Developmental programming occurs across taxa, as early life environments alter developmental processes and thereby shape individual phenotype [1,2]. We predicted that (iii) if high temperatures, in the nest or the heated-chamber, represent a stressor for the individual, this would decrease mitochondrial efficiency, either because of mitochondrial function impairment or because LEAK increases to reduce the oxidative impact of stress. In both experiments, including clutch as random factor (to account for genetic similarities) instead of brood, did not affect results (electronic supplementary material, table S1) For both experiments, to test how mitochondrial parameters relate to nestling growth while accounting for brood size, we ran separate LMMs including growth rate as the response variable and one of the mitochondrial parameters as a fixed effect, together with brood size, prenatal playback, 12D-Tnest and the playback by 12D-Tnest interaction, and including brood identity as a random factor. Full models and AICcs comparisons with reduced models are presented in electronic supplementary material, tables S2–S6

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