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      Parent-embryo acoustic communication: a specialised heat vocalisation allowing embryonic eavesdropping

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          Abstract

          Sound is arguably the external cue most accessible to embryos of many species, and as such may constitute an unrivalled source of early information. Recent evidence shows that prenatal sounds, similarly to maternal effects, may shape developmental trajectories. Establishing whether parental vocalisations are signals directed at embryos, or parental cues on which embryos eavesdrop, can elucidate whether parents or embryos control developmental outcomes. Prenatal exposure to a characteristic heat-related parental call was recently shown to alter zebra finch growth and fitness. Here, we test the ecological context of this behaviour in the wild, and assess the information value and specificity of this vocalisation for an embryonic audience. We show that wild zebra finches also produce this characteristic call, only at high temperatures. In addition, in the lab, we demonstrate experimentally that calling is specifically triggered by high air temperatures, can occur without an embryonic audience, and importantly, is predicted by individuals’ body mass. Overall, our findings reveal a specialised heat vocalisation that enables embryonic eavesdropping, by indicating high ambient temperatures, and parents’ capacity to cope with such conditions. This challenges the traditional view of embryos as passive agents of their development, and opens exciting research avenues on avian adaptation to extreme heat.

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          Most cited references32

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          The adaptive significance of maternal effects

          T Mousseau (1998)
          Recently, the adaptive significance of maternal effects has been increasingly recognized. No longer are maternal effects relegated as simple `troublesome sources of environmental resemblance' that confound our ability to estimate accurately the genetic basis of traits of interest. Rather, it has become evident that many maternal effects have been shaped by the action of natural selection to act as a mechanism for adaptive phenotypic response to environmental heterogeneity. Consequently, maternal experience is translated into variation in offspring fitness.
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            Keeping up with a warming world; assessing the rate of adaptation to climate change.

            The pivotal question in the debate on the ecological effects of climate change is whether species will be able to adapt fast enough to keep up with their changing environment. If we establish the maximal rate of adaptation, this will set an upper limit to the rate at which temperatures can increase without loss of biodiversity. The rate of adaptation will primarily be set by the rate of microevolution since (i) phenotypic plasticity alone is not sufficient as reaction norms will no longer be adaptive and hence microevolution on the reaction norm is needed, (ii) learning will be favourable to the individual but cannot be passed on to the next generations, (iii) maternal effects may play a role but, as with other forms of phenotypic plasticity, the response of offspring to the maternal cues will no longer be adaptive in a changing environment, and (iv) adaptation via immigration of individuals with genotypes adapted to warmer environments also involves microevolution as these genotypes are better adapted in terms of temperature, but not in terms of, for instance, photoperiod.Long-term studies on wild populations with individually known animals play an essential role in detecting and understanding the temporal trends in life-history traits, and to estimate the heritability of, and selection pressures on, life-history traits. However, additional measurements on other trophic levels and on the mechanisms underlying phenotypic plasticity are needed to predict the rate of microevolution, especially under changing conditions. Using this knowledge on heritability of, and selection on, life-history traits, in combination with climate scenarios, we will be able to predict the rate of adaptation for different climate scenarios. The final step is to use ecoevolutionary dynamical models to make the link to population viability and from there to biodiversity loss for those scenarios where the rate of adaptation is insufficient.
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              Of human bonding: newborns prefer their mothers' voices

              By sucking on a nonnutritive nipple in different ways, a newborn human could produce either its mother's voice or the voice of another female. Infants learned how to produce the mother's voice and produced it more often than the other voice. The neonate's preference for the maternal voice suggests that the period shortly after birth may be important for initiating infant bonding to the mother.
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                Author and article information

                Contributors
                m.mariette@deakin.edu.au
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                7 December 2018
                7 December 2018
                2018
                : 8
                : 17721
                Affiliations
                [1 ]ISNI 0000 0001 0526 7079, GRID grid.1021.2, Centre for Integrative Ecology, School of Life & Environmental Sciences, , Deakin University Geelong, ; Geelong, Australia
                [2 ]ISNI 0000 0004 0486 528X, GRID grid.1007.6, School of Biological Sciences, , University of Wollongong, ; Wollongong, Australia
                [3 ]ISNI 0000 0001 2107 2298, GRID grid.49697.35, DST-NRF Centre of Excellence at the FitzPatrick Institute, Department of Zoology and Entomology, , University of Pretoria, ; Pretoria, South Africa
                [4 ]ISNI 0000 0001 2166 5237, GRID grid.452736.1, South African Research Chair in Conservation Physiology, National Zoological Garden, , South African National Biodiversity Institute, ; P.O. Box 754, Pretoria, 0001 South Africa
                Author information
                http://orcid.org/0000-0003-0567-4111
                http://orcid.org/0000-0002-1323-1954
                Article
                35853
                10.1038/s41598-018-35853-y
                6286336
                30532029
                c7b1c448-d107-47f3-ba8e-6667ea9439bc
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 22 June 2018
                : 30 October 2018
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100000923, Australian Research Council (ARC);
                Award ID: DE170100824
                Award ID: DP180101207
                Award ID: LP140100691
                Award ID: DP180100250
                Award ID: FT14010013
                Award ID: DP180101207
                Award Recipient :
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