Lasting benefits of embryonic eavesdropping on parent-parent communication

Francisco Ruiz-Raya; Alberto Velando

doi:10.1126/sciadv.adn8542

journal article Aug 30, 2024

Lasting benefits of embryonic eavesdropping on parent-parent communication

Francisco Ruiz-Raya

Alberto Velando

Science Advances Vol. 10 No. 35 · American Association for the Advancement of Science (AAAS)

View at Publisher Save 10.1126/sciadv.adn8542

Abstract

Developing embryos have traditionally been viewed as passive agents in the evolution of family conflicts, with maternal substances within the uterus or eggs as main factors modulating later expression of offspring solicitation behaviors. Yet, parent-offspring conflict theory predicts that offspring might also rely on alternative cues to adjust demand in response to prenatal cues of parental capacity for resource provisioning. Here, we show how embryonic experience with vocalizations carried out by parents during nest-relief displays at incubation adaptively shapes avian offspring development, providing lasting benefits to offspring. Genetic siblings prenatally exposed to different levels of parent-parent communication showed differences in epigenetic patterns, adrenocortical responsiveness, development, and food solicitation behavior. The correspondence between prenatal acoustic experience and parental context positively influenced the nutritional status and growth rate of offspring reared by communicative parents. Offspring can thus retain strong control over their own development by gathering prenatal acoustic information about parental generosity.

Topics

No keywords indexed for this article. Browse by subject →

References

84

[1]

10.1016/s0065-3454(08)00006-5

[2]

R. L. Trivers “Parental investment and sexual selection” in Sexual Selection and the Descent of Man Cambell B Ed. (London: Heinemann 1972) pp. 136–207. 10.4324/9781315129266-7

[3]

N. J. Royle P. T. Smiseth Mathias. Kölliker Eds. The Evolution of Parental Care (Oxford Univ. Press 2012).

[4]

10.1093/icb/14.1.249

[5]

10.1038/376133a0

[6]

10.1086/491687

[7]

C. A. Hinde, K. L. Buchanan, R. M. Kilner, Prenatal environmental effects match offspring begging to parental provisioning. Proc. R. Soc. 276, 2787–2794 (2009).

[8]

P. T. Smiseth, J. Wright, M. Kölliker, Parent–offspring conflict and co-adaptation: Behavioural ecology meets quantitative genetics. Proc. R. Soc. 275, 1823–1830 (2008).

[9]

10.1126/science.1186056

[10]

10.1111/brv.12733

[11]

10.1086/511962

[12]

10.1016/j.tree.2021.04.007

[13]

10.1073/pnas.1302159110

[14]

10.1126/sciadv.adj3524

[15]

10.1016/0163-6383(94)90051-5

[16]

D. Colombelli-Négrel, M. E. Hauber, S. Kleindorfer, Prenatal learning in an Australian songbird: Habituation and individual discrimination in superb fairy-wren embryos. Proc. R. Soc. 281, 20141154 (2014).

[17]

10.1086/728105

[18]

10.1186/s40850-018-0038-1

[19]

10.1016/j.cub.2012.09.025

[20]

10.1126/science.ade5868

[21]

10.1038/s41598-018-33301-5

[22]

10.1126/science.aaf7049

[23]

10.1038/s41559-019-0929-8

[24]

10.1016/j.neulet.2021.135917

[25]

10.1016/j.yhbeh.2023.105316

[26]

10.1152/jn.00599.2005

[27]

10.1006/anbe.2001.1684

[28]

M. R. Servedio, T. D. Price, R. Lande, Evolution of displays within the pair bond. Proc. R. Soc. 280, 20123020 (2013).

[29]

10.1073/pnas.1904138116

[30]

10.1006/anbe.2001.1684

[31]

10.1093/beheco/arz049

[32]

10.1111/bij.12705

[33]

10.1098/rspb.2003.2496

[34]

10.1098/rspb.2008.1942

[35]

R. Pierotti, Male and female parental roles in the western gull under different environmental conditions. Auk 98, 532–549 (1981).

[36]

N. Tinbergen Social Behaviour in Animals: With Special Reference to Vertebrates (Methuen 1953).

[37]

10.1016/s0003-3472(83)80225-5

[38]

Evolution and molecular mechanisms of adaptive developmental plasticity

PATRÍCIA BELDADE, ANA RITA A. MATEUS, ROBERTO A. KELLER

Molecular Ecology 10.1111/j.1365-294x.2011.05016.x

[39]

10.1016/j.coemr.2020.07.010

[40]

10.2307/5424

[41]

10.1186/1742-9994-8-24

[42]

Evolution and molecular mechanisms of adaptive developmental plasticity

PATRÍCIA BELDADE, ANA RITA A. MATEUS, ROBERTO A. KELLER

Molecular Ecology 10.1111/j.1365-294x.2011.05016.x

[43]

10.1163/156853951x00197

[44]

10.1098/rspb.2020.0242

[45]

10.3354/meps13601

[46]

10.1098/rspb.2005.3351

[47]

10.1093/icesjms/fsp210

[48]

10.3382/ps/peu006

[49]

10.1098/rstb.2007.0011

[50]

10.1242/jeb.246024

Showing 50 of 84 references

Metrics

6

Citations

84

References

Details

Published: Aug 30, 2024
Vol/Issue: 10(35)

Authors

F

Francisco Ruiz-Raya

Centro de Investigación Mariña, Universidade de Vigo, Grupo de Ecoloxía Animal, Vigo 36310, Spain.

A

Alberto Velando

Centro de Investigación Mariña, Universidade de Vigo, Grupo de Ecoloxía Animal, Vigo 36310, Spain.

Cite This Article

Francisco Ruiz-Raya, Alberto Velando (2024). Lasting benefits of embryonic eavesdropping on parent-parent communication. Science Advances, 10(35). https://doi.org/10.1126/sciadv.adn8542

Lasting benefits of embryonic eavesdropping on parent-parent communication

You May Also Like