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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West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, 2003).
Uller, T. Developmental plasticity and the evolution of parental effects. Trends Ecol. Evol. 23, 432–438 (2008).
Nettle, D. & Bateson, M. Adaptive developmental plasticity: what is it, how can we recognize it and when can it evolve? Proc. R. Soc. B 282, 20151005 (2015).
Jablonka, E. & Raz, G. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q. Rev. Biol. 84, 131–176 (2009).
Laubach, Z. M. et al. Epigenetics and the maintenance of developmental plasticity: extending the signalling theory framework. Biol. Rev. 93, 1323–1338 (2018).
Champagne, F. A. Epigenetic influence of social experiences across the lifespan. Dev. Psychobiol. 52, 299–311 (2010).
Harris, K. D., Bartlett, N. J. & Lloyd, V. K. Daphnia as an emerging epigenetic model organism. Genet. Res. Int. 2012, 147892 (2012).
Groothuis, T. G. G., Müller, W., von Engelhardt, N., Carere, C. & Eising, C. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev. 29, 329–352 (2005).
Marshall, D. & Uller, T. When is a maternal effect adaptive? Oikos 116, 1957–1963 (2007).
Mousseau, T. A., Uller, T., Wapstra, E. & Badyaev, A. V. Evolution of maternal effects: past and present. Philos. Trans. R. Soc. B 364, 1035–1038 (2009).
Mariette, M. M. & Buchanan, K. L. Prenatal acoustic communication programs offspring for high posthatching temperatures in a songbird. Science 353, 812–814 (2016).
Aubret, F., Blanvillain, G., Bignon, F. & Kok, P. J. Heartbeat, embryo communication and hatching synchrony in snake eggs. Sci. Rep. 6, 23519 (2016).
Doody, J. S., Stewart, B., Camacho, C. & Christian, K. Good vibrations? Sibling embryos expedite hatching in a turtle. Anim. Behav. 83, 645–651 (2012).
McGlashan, J. K., Spencer, R.-J. & Old, J. M. Embryonic communication in the nest: metabolic responses of reptilian embryos to developmental rates of siblings. Proc. R. Soc. B 279, 1709–1715 (2012).
Vince, M. in Bird Vocalizations (ed. Hinde, R. A.) 88–89 (Cambridge Univ. Press, 1969).
Warkentin, K. M. How do embryos assess risk? Vibrational cues in predator-induced hatching of red-eyed treefrogs. Anim. Behav. 70, 59–71 (2005).
Middlemis Maher, J., Werner, E. E. & Denver, R. J. Stress hormones mediate predator-induced phenotypic plasticity in amphibian tadpoles. Proc. R. Soc. B 280, 20123075 (2013).
Warkentin, K. M. Wasp predation and wasp-induced hatching of red-eyed treefrog eggs. Anim. Behav. 60, 503–510 (2000).
Benard, M. F. Predator-induced phenotypic plasticity in organisms with complex life histories. Annu. Rev. Ecol. Evol. Syst. 35, 651–673 (2004).
Noguera, J. C., Kim, S.-Y. & Velando, A. Family-transmitted stress in a wild bird. Proc. Natl Acad. Sci. USA 114, 6794–6799 (2017).
Harvell, C. D. The ecology and evolution of inducible defenses. Q. Rev. Biol. 65, 323–340 (1990).
McNamara, J. M., Dall, S. R., Hammerstein, P. & Leimar, O. Detection vs. selection: integration of genetic, epigenetic and environmental cues in fluctuating environments. Ecol. Lett. 19, 1267–1276 (2016).
Munoz, N. E. & Blumstein, D. T. Multisensory perception in uncertain environments. Behav. Ecol. 23, 457–462 (2012).
Stamps, J. A. & Frankenhuis, W. E. Bayesian models of development. Trends Ecol. Evol. 31, 260–268 (2016).
Freeman, B. M. & Vince, M. A. Development of the Avian Embryo: A Behavioural and Physiological Study (Chapman and Hall, 1974).
Persson, I. & Andersson, G. Intraclutch hatch synchronization in pheasants and mallard ducks. Ethology 105, 1087–1096 (1999).
Spencer, R. J., Thompson, M. B. & Banks, P. B. Hatch or wait? A dilemma in reptilian incubation. Oikos 93, 401–406 (2001).
Velando, A., Morán, P., Romero, R., Fernández, J. & Piorno, V. Invasion and eradication of the American mink in the Atlantic Islands National Park (NW Spain): a retrospective analysis. Biol. Invasions 19, 1227–1241 (2017).
Tinbergen, N. The Herring Gull’s World: A Study of the Social Behaviour of Birds (Collins, 1953).
Morales, J., Lucas, A. & Velando, A. Maternal programming of offspring antipredator behavior in a seabird. Behav. Ecol. 29, 479–485 (2018).
Rumpf, M. & Tzschentke, B. Perinatal acoustic communication in birds: why do birds vocalize in the egg? Open Ornithol. J. 3, 141–149 (2010).
Impekoven, M. & Gold, P. S. in Studies on the Development of Behavior and the Nervous System (eds Whitsett, J. M., Vandenbergh, J. G. and Gottlieb, G.) 325–356 (Elsevier, 1973).
Manoli, I. et al. Mitochondria as key components of the stress response. Trends Endrocrinol. Metab. 18, 190–198 (2007).
Herborn, K. A. et al. Stress exposure in early post-natal life reduces telomere length: an experimental demonstration in a long-lived seabird. Proc. R. Soc. B 281, 20133151 (2014).
Tona, K. et al. Effects of storage time on incubating egg gas pressure, thyroid hormones, and corticosterone levels in embryos and on their hatching parameters. Poult. Sci. 82, 840–845 (2003).
Tawa, R., Ono, T., Kurishita, A., Okada, S. & Hirose, S. Changes of DNA methylation level during pre‐and postnatal periods in mice. Differentiation 45, 44–48 (1990).
Reik, W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447, 425–432 (2007).
Yan, X.-p et al. Evidence in duck for supporting alteration of incubation temperature may have influence on methylation of genomic DNA. Poult. Sci. 94, 2537–2545 (2015).
Laine, V. N. et al. Evolutionary signals of selection on cognition from the great tit genome and methylome. Nat. Commun. 7, 10474 (2016).
Derks, M. F. et al. Gene and transposable element methylation in great tit (Parus major) brain and blood. BMC Genom. 17, 332 (2016).
Baker-Andresen, D., Ratnu, V. S. & Bredy, T. W. Dynamic DNA methylation: a prime candidate for genomic metaplasticity and behavioral adaptation. Trends Neurosci. 36, 3–13 (2013).
Paoli-Iseppi, D. et al. Measuring animal age with DNA methylation: from humans to wild animals. Front. Genet. 8, 106 (2017).
Ostlund, B. D. et al. Prenatal stress, fearfulness, and the epigenome: exploratory analysis of sex differences in DNA methylation of the glucocorticoid receptor gene. Front. Behav. Neurosci. 10, 147 (2016).
Morales, J. & Velando, A. Signals in family conflicts. Anim. Behav. 86, 11–16 (2013).
Mariette, M. M. et al. Parent-embryo acoustic communication: a specialised heat vocalisation allowing embryonic eavesdropping. Sci. Rep. 8, 17721 (2018).
Lickliter, R. Prenatal sensory ecology and experience: implications for perceptual and behavioral development in precocial birds. Adv. Study Behav. 35, 235–274 (2005).
Gottlieb, G Behavioral Embryology: Studies on the Development of Behavior and the Nervous System Vol. 1 (Academic Press, 2013).
Schwagmeyer, P., Mock, D., Lamey, T., Lamey, C. & Beecher, M. Effects of sibling contact on hatch timing in an asynchronously hatching bird. Anim. Behav. 41, 887–894 (1991).
Müller, G. B. Embryonic motility: environmental influences and evolutionary innovation. Evol. Dev. 5, 56–60 (2003).
Impekoven, M. Responses of laughing gull chicks (Larus atricilla) to parental attraction- and alarm-calls, and effects of prenatal auditory experience on the responsiveness to such calls. Behaviour 56, 250–277 (1976).
Dall, S. R., Giraldeau, L.-A., Olsson, O., McNamara, J. M. & Stephens, D. W. Information and its use by animals in evolutionary ecology. Trends Ecol. Evol. 20, 187–193 (2005).
Ward, A. J. & Mehner, T. Multimodal mixed messages: the use of multiple cues allows greater accuracy in social recognition and predator detection decisions in the mosquitofish, Gambusia holbrooki. Behav. Ecol. 21, 1315–1320 (2010).
Haff, T. M. & Magrath, R. D. Calling at a cost: elevated nestling calling attracts predators to active nests. Biol. Lett. 7, 493–495 (2011).
Caro, T. Antipredator Defenses in Birds and Mammals (Univ. Chicago Press, 2005).
Krause, J. & Ruxton, G. D. Living in Groups (Oxford Univ. Press, 2002).
Schoech, S. J., Rensel, M. A. & Heiss, R. S. Short- and long-term effects of developmental corticosterone exposure on avian physiology, behavioral phenotype, cognition, and fitness: a review. Curr. Zool. 57, 514–530 (2011).
Scanes, C. G. Perspectives on the endocrinology of poultry growth and metabolism. Gen. Comp. Endocrinol. 163, 24–32 (2009).
Jeng, J. Y. et al. Maintenance of mitochondrial DNA copy number and expression are essential for preservation of mitochondrial function and cell growth. J. Cell. Biochem. 103, 347–357 (2008).
Velando, A., Noguera, J. C., da Silva, A. & Kim, S.-Y. Redox-regulation and life-history trade-offs: scavenging mitochondrial ROS improves growth in a wild bird. Sci. Rep. 9, 2203 (2019).
Schwagmeyer, P. & Mock, D. W. Parental provisioning and offspring fitness: size matters. Anim. Behav. 75, 291–298 (2008).
Monaghan, P. & Metcalfe, N. On being the right size: natural selection and body size in the herring gull. Evolution 40, 1096–1099 (1986).
Reiss, M. J. The Allometry of Growth and Reproduction (Cambridge Univ. Press, 1991).
Tong, Q. et al. Effect of species-specific sound stimulation on the development and hatching of broiler chicks. Br. Poult. Sci. 56, 143–148 (2015).
Noguera, J. C., Lores, M., Alonso‐Álvarez, C. & Velando, A. Thrifty development: early‐life diet restriction reduces oxidative damage during later growth. Funct. Ecol. 25, 1144–1153 (2011).
Noguera, J. C., Morales, J., Perez, C. & Velando, A. On the oxidative cost of begging: antioxidants enhance vocalizations in gull chicks. Behav. Ecol. 21, 479–484 (2010).
Boersma, D. C., Ellenton, J. A. & Yagminas, A. Investigation of the hepatic mixed‐function oxidase system in herring gull embryos in relation to environmental contaminants. Environ. Toxicol. Chem. 5, 309–318 (1986).
Jones, T. A., Jones, S. M. & Paggett, K. C. Emergence of hearing in the chicken embryo. J. Neurophysiol. 96, 128–141 (2006).
Sviderskaya, G. Possible pathways for the effect of vibration on motor activity of chick embryos. Bull. Exp. Biol. Med. 66, 1301–1303 (1968).
Burger, J. & Gochfeld, M. Discrimination of the threat of direct versus tangential approach to the nest by incubating herring and great black-backed gulls. J. Comp. Physiol. Psychol. 95, 676–684 (1981).
Kim, S. Y., Noguera, J., Tato, A. & Velando, A. Vitamins, stress and growth: the availability of antioxidants in early life influences the expression of cryptic genetic variation. J. Evol. Biol. 26, 1341–1352 (2013).
Romero, L. M. & Reed, J. M. Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp. Biochem. Physiol. A 140, 73–79 (2005).
Engqvist, L. The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim. Behav. 70, 967–971 (2005).
Pike, N. Using false discovery rates for multiple comparisons in ecology and evolution. Methods Ecol. Evol. 2, 278–282 (2011).
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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