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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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).
The authors declare no competing interests.
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Noguera, J.C., Velando, A. Bird embryos perceive vibratory cues of predation risk from clutch mates. Nat Ecol Evol 3, 1225–1232 (2019). https://doi.org/10.1038/s41559-019-0929-8
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