Bird embryos perceive vibratory cues of predation risk from clutch mates

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Abstract

During development in fluctuating environments, phenotypes can be adjusted to the conditions that individuals will probably encounter later in life. As developing embryos have a limited capacity to fully capture environmental information, theory predicts that they should integrate relevant information from all reliable sources, including the social environment. In many oviparous species, embryos are able to perceive cues of predator presence in some circumstances, but whether this information is socially transmitted among clutch mates—promoting phenotypic adjustments in the whole clutch—is unknown. Here, using an experimental design for which we modified the exposure to some, but not all, embryos of the same clutch to cues of predator presence (that is, alarm calls), we show that exposed embryos of the yellow-legged gull (Larus michahellis) and their unexposed clutch mates showed similar developmental changes that were absent in embryos from control clutches. Compared with the control broods, both embryos that were exposed to alarm calls and their unexposed clutch mates showed altered prenatal and postnatal behaviours, higher levels of DNA methylation and stress hormones, and reduced growth and numbers of mitochondria (which may be indicative of the capacity for energy production of cells). These results strongly suggest that gull embryos are able to acquire relevant environmental information from their siblings. Together, our results highlight the importance of socially acquired information during the prenatal stage as a non-genetic mechanism promoting developmental plasticity.

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Fig. 1: Schematic of prenatal and postnatal exposure of gull embryos to social cues that indicate the presence of predators
Fig. 2: Prenatal exposure to adult alarm calls delayed hatching, increased the rate of egg vibration, promoted a higher level of global DNA methylation and basal corticosterone, and enhanced prenatal and postnatal antipredator responses.
Fig. 3: Prenatal exposure to adult alarm calls reduced mitochondrial content and the growth of the chicks

Data availability

All of the data needed to evaluate the conclusions in the paper are presented in the paper and/or the Supplementary Information. The raw data can also be found in the Figshare digital repository: https://doi.org/10.6084/m9.figshare.6510092.

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Acknowledgements

We thank the staff at the Atlantic Islands of Galicia National Park, especially to P. Mallo, R. Castiñeira and J. Arcas; A. da Silva for their help with the laboratory analyses; B. Otero and H. Martinez for their support during the fieldwork; P. Monaghan, N. B. Metcalfe, S.-Y. Kim for their comments on an earlier version of the manuscript. J.C.N. was supported by the Juan de la Cierva Research Program (IJI-2014-20246) and the project was supported by MINECO and MICINN (CGL2015-69338-C2-1-P and PGC2018-095412-B-I00).

Author information

J.C.N. and A.V. conceived the study and designed the experiment. J.C.N. collected the field data, performed the laboratory analyses and analysed the data. J.C.N. and A.V. discussed the results and wrote the paper.

Correspondence to Jose C. Noguera.

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Supplementary Information

Supplementary Methods, Supplementary Figs. 1–5, Supplementary Tables 1–8, Supplementary references

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Supplementary Video 1

An example of experimental eggs vibrating inside the incubator

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