A prenatal acoustic signal of heat reduces a biomarker of chronic stress at adulthood across seasons

Front Physiol. 2024 Mar 29:15:1348993. doi: 10.3389/fphys.2024.1348993. eCollection 2024.

Abstract

During development, phenotype can be adaptively modulated by environmental conditions, sometimes in the long-term. However, with weather variability increasing under climate change, the potential for maladaptive long-term responses to environmental variations may increase. In the arid-adapted zebra finch, parents emit "heat-calls" when experiencing heat during incubation, which adaptively affects offspring growth in the heat, and adult heat tolerance. This suggests that heat-call exposure may adjust individual phenotype to hot conditions, potentially compromising individual sensitivity to cool weather conditions. To test this hypothesis, we manipulated individual prenatal acoustic and postnatal thermal experiences during development, and sought to assess subsequent chronic responses to thermal fluctuations at adulthood. We thus measured heterophil to lymphocyte (H/L) ratios in adults, when held in outdoor aviaries during two summers and two winters. We found that birds exposed to heat-calls as embryos, had consistently lower H/L ratios than controls at adulthood, indicative of lower chronic stress, irrespective of the season. Nonetheless, in all birds, the H/L ratio did vary with short-term weather fluctuations (2, 5 or 7 days), increasing at more extreme (low and high) air temperatures. In addition, the H/L ratio was higher in males than females. Overall, while H/L ratio may reflect how individuals were being impacted by temperature, heat-call exposed individuals did not show a stronger chronic response in winter, and instead appeared more resilient to thermal variability than control individuals. Our findings therefore suggest that heat-call exposure did not compromise individual sensitivity to low temperatures at adulthood. Our study also reveals that prenatal sound can lead to long-term differences in individual physiology or quality/condition, as reflected by H/L ratios, which are consistent with previously-demonstrated reproductive fitness differences.

Keywords: Taeniopygia guttata castanotis; environmental matching hypothesis; heterophil:lymphocyte ratio; leucocyte profile; phenotypic plasticity; thermal adaptation.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the Australian Research Council (DE170100824 to MM and DP210101238 to KB and MM), and the Spanish Ministry of Science and Innovation grant (RYC 2019-028066-I and PID 2021-128494NA-100 to MM).