Review
Acoustic developmental programming: a mechanistic and evolutionary framework

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Highlights

  • Prenatal sounds and vibrations from parents, siblings, or the environment are used by embryos across taxonomic groups to obtain information on the external world and respond to risks and opportunities.

  • Acoustic signals are used at transitions between life stages to optimize that transition (e.g., hatching time) or the postnatal phenotype.

  • Prenatal sounds can directly alter developmental trajectories and provide accurate anticipatory cues to program offspring for particular postnatal environments.

  • Acoustic developmental programming affects individual physiology and cognition through changes in brain connectivity, endocrinology, and gene expression.

  • Acoustic signals differ from maternal nutritional and endocrine cues in multiple ways, and this has implications for conflict and coadaptation within the family, as well as for adaptation to rapidly changing environments.

Conditions experienced prenatally, by modulating developmental processes, have lifelong effects on individual phenotypes and fitness, ultimately influencing population dynamics. In addition to maternal biochemical cues, prenatal sound is emerging as a potent alternative source of information to direct embryonic development. Recent evidence suggests that prenatal acoustic signals can program individual phenotypes for predicted postnatal environmental conditions, which improves fitness. Across taxonomic groups, embryos have now been shown to have immediate adaptive responses to external sounds and vibrations, and direct developmental effects of sound and noise are increasingly found. Establishing the full developmental, ecological, and evolutionary impact of early soundscapes will reveal how embryos interact with the external world, and potentially transform our understanding of developmental plasticity and adaptation to changing environments.

Section snippets

Prenatal sounds: a novel avenue for developmental programming

Sound presents unrivalled potential for information transfer. From noise betraying the presence of an approaching predator, to simple stereotyped vocalizations such as begging and alarm calls, to incredibly complex language and song – sound provides invaluable information to whomever listens. Inside the egg or womb, the embryos of many species listen to the external world (Box 1). From human newborns recognizing their mother’s voice to ducklings imprinting on a familiar prenatal call, it is

Sound provides immediate and anticipatory information at the transition between life-stages

There is evidence across a broad taxonomic range that embryos perceive and discriminate biologically relevant sounds and vibrations, including in taxa where neurological evidence for embryonic auditory sensitivity is lacking (Box 1). Partly because of the timing of sensory development in late prenatal life [26., 27., 28.], vibro-acoustic cues appear to be used typically at around the time of transition between the embryonic and postnatal stages, or during other transitions between life-stages

Programming of physiological functions by prenatal sounds

Repeated exposure to particular sounds in prenatal life may program physiological development through epigenetic changes that influence gene expression, as well as by reshaping brain connectivity. For example, in crickets and birds, the advance in hatching date brought on by chronic vibro-acoustic exposure [30,41] implies that sound directly accelerates the many physiological processes underlying the transition from embryonic to postnatal life [50], with accompanying changes in gene expression [

Evolutionary origin of acoustic developmental programming

Although the downstream mechanistic pathways of programming by sound resemble other developmental programming processes (Box 3), the evolutionary origin of developmental sensitivity to sound requires investigation. The broad range of vertebrate, invertebrate, and even plant [71] taxa where sounds and vibrations trigger embryonic developmental responses (Table 1) suggests an ancestral origin, but a systematic comparative study is needed. Vibration sensing through tactile and vestibular

Concluding remarks

The developmental impact of prenatal sounds is likely to be considerably more profound and widespread than is currently appreciated. Beyond recognized cognitive effects, the neural and physiological pathways exist for sound to trigger broad developmental plasticity (Box 3), thereby allowing input from the environment, the parents, and siblings to shape individual phenotypes. Integrating acoustic developmental plasticity with the fundamental and well-documented process of programming by the

Acknowledgments

We are grateful to John Endler, members of the Centre for Integrative Ecology, and anonymous reviewers for helpful comments on the manuscript. This work was supported by Australian Research Council (ARC) grants DE170100824 to M.M.M.; DP180101207 to K.L.B. and M.M.M; FT14010013 to K.L.B; and BB/S003223/1 to D.F.C., K.L.B., and M.M.M.

Declaration of interests

The authors declare no conflicts of interest.

Glossary

Anticipatory cues
cues from the parental environment that predict the offspring environment, or, from the point of view of the embryo, prenatal cues that predict the postnatal environment.
Developmental plasticity
the capacity of a given genotype to produce alternative phenotypes through early life exposure to maternal or environmental conditions, which causes (adaptive or non-adaptive) changes to individual behavior, physiology, and/or morphology.
Developmental programming
developmental plasticity

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    Current address: Department of Genetics and Biochemistry, Clemson University, Clemson, SC 29 632, USA

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