Trends in Ecology & Evolution
ReviewAcoustic developmental programming: a mechanistic and evolutionary framework
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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Twitter: @MyleneMariette (M.M. Mariette).
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Current address: Department of Genetics and Biochemistry, Clemson University, Clemson, SC 29 632, USA