A prenatal acoustic signal of heat afects thermoregulation capacities at adulthood in an arid‑adapted bird

Understanding animal physiological adaptations for tolerating heat, and the causes of interindividual variation, is key for predicting climate change impacts on biodiversity. Recently, a novel mechanism for transgenerational heat adaptation was identified in a desert-adapted bird, where parents acoustically signal hot conditions to embryos. Prenatal exposure to “heat-calls” adaptively alters zebra finch development and their thermal preferences in adulthood, suggesting a long-term shift towards a heat-adapted phenotype. However, whether such acoustic experience improves long-term thermoregulatory capacities is unknown. We measured metabolic rate (MR), evaporative water loss (EWL) and body temperature in adults exposed to a stepped profile of progressively higher air temperatures (Ta) between 27 and 44 °C. Remarkably, prenatal acoustic experience affected heat tolerance at adulthood, with heat-call exposed individuals more likely to reach the highest Ta in morning trials. This was despite MR and EWL reaching higher levels at the highest Ta in heat-call individuals, partly driven by a stronger metabolic effect of moderate activity. At lower Ta, however, heat-call exposed individuals had greater relative water economy, as expected. They also better recovered mass lost during morning trials. We therefore provide the first evidence that prenatal acoustic signals have long-term consequences for heat tolerance and physiological adaptation to heat.The Australian Research Council, the Holsworth Wildlife Research Endowment and international travel costs by the National Research Foundation of South Africa.https://www.nature.com/srepdm2022Zoology and Entomolog

Using an Electronic Monitoring System to Link Offspring Provisioning and Foraging Behavior of a Wild Passerine

Although the costs of parental care are at the foundations of optimal-parental-investment theory, our understanding of the nature of the underlying costs is limited by the difficulty of measuring variation in foraging effort. We simultaneously measured parental provisioning and foraging behavior in a free-living population of Zebra Finches (Taeniopygia guttata) using an electronic monitoring system. We fitted 145 adults with a passive transponder tag and remotely recorded their visits to nest boxes and feeders continuously over a 2-month period. After validating the accuracy of this monitoring system, we studied how provisioning and foraging activities varied through time (day and breeding cycle) and influenced the benefits (food received by the offspring) and costs (interclutch interval) of parental care. The provisioning rates of wild Zebra Finches were surprisingly low, with an average of only one visit per hour throughout the day. This was significantly lower than those reported for this model species in captivity and for most other passerines in the wild. Nest visitation rate only partially explained the amount of food received by the young, with parental foraging activity, including the minimum distance covered on foraging trips, being better predictors. Parents that sustained higher foraging activity and covered more distance during the first breeding attempt took longer to renest. These results demonstrate that in some species matching foraging activity with offspring provisioning may provide a better estimate of the true investment that individuals commit to a reproductive attempt

The Adaptive significance of provisioning and foraging coordination between breeding partners

Sexual conflict over parental care relies on the fundamental assumption that parents do not share the cost of their partner’s effort on future reproduction. However, this is unlikely to be true whenever partners breed together more than once. In that case, individuals should try to optimize the cost and benefits for the pair, rather than only for themselves. Here we seek to establish whether the synchronization of parents’ provisioning visits to the nest could fulfill this function. We conducted a brood-size manipulation experiment on wild zebra finches to test whether nest visit synchrony was flexible and beneficial for nestlings’ growth, while controlling for the confounding effects of pair “quality” and synchrony away from the nest during foraging. Using a network of readers to track parents at nests and feeding stations, we found that nest visit synchrony responded directly to the brood manipulation and increased with brood size. Synchrony at the nest and while foraging were correlated, but the latter better predicted nestling mass, possibly because it was associated with more regular provisioning patterns. Our findings suggest that parental coordination could indeed play an important role in partners’ investment decisions, underpinning the evolution of the most prominent mating system in birds.11 page(s

Data from: The adaptive significance of provisioning and foraging coordination between breeding partners

Sexual conflict over parental care relies on the fundamental assumption that parents do not share the cost of their partner’s effort on future reproduction. However, this is unlikely to be true whenever partners breed together more than once. In that case, individuals should try to optimize the cost and benefits for the pair, rather than only for themselves. Here we seek to establish whether the synchronization of parents’ provisioning visits to the nest could fulfill this function. We conducted a brood-size manipulation experiment on wild zebra finches to test whether nest visit synchrony was flexible and beneficial for nestlings’ growth, while controlling for the confounding effects of pair “quality” and synchrony away from the nest during foraging. Using a network of readers to track parents at nests and feeding stations, we found that nest visit synchrony responded directly to the brood manipulation and increased with brood size. Synchrony at the nest and while foraging were correlated, but the latter better predicted nestling mass, possibly because it was associated with more regular provisioning patterns. Our findings suggest that parental coordination could indeed play an important role in partners’ investment decisions, underpinning the evolution of the most prominent mating system in birds

Does coloniality improve foraging efficiency and nestling provisioning? A field experiment in the wild Zebra Finch

The foraging benefits of coloniality, whereby colony members exchange information about food location, have been suggested as a primary factor influencing the evolution of coloniality. However, despite its longstanding popularity, this hypothesis has rarely been tested experimentally. Here, we conducted a field experiment in the wild Zebra Finch Taeniopygia guttata to test whether colonial birds are better at finding food than solitary individuals. We manipulated food patch location and directly measured foraging activity of many colonial and solitary parents at those patches using an electronic monitoring system. We provided nesting sites in excess to alleviate nest site competition and manipulated brood size to eliminate the possible correlation between brood size, nesting density, and individual quality (including foraging activity). We found that solitary birds found experimental food patches first, closely followed by colonial birds. Moreover, solitary parents adjusted the amount of food per nestling to experimental brood size, whereas colonial parents did not, although overall, nestlings were fed more per capita in colonial than in solitary nests. In addition, brood size and, to a lesser extent, nesting density negatively affected nestling growth. Therefore, with the effect of provisioning rate, sibling competition, and cost of coloniality combined, nestling mass was not affected by the brood manipulation in solitary nests, whereas nestlings were lighter in enlarged than in reduced broods in colonies. Our results therefore suggest that individuals settling in solitary nests were intrinsically better foragers and more optimal parents. While they do not invalidate the possibility of information transfer at colonies, our findings highlight the importance of considering settlement bias in future studies and add to the existing evidence that the effects of nesting density on fitness are both complex and multiple.11 page(s

Data from: Prenatal acoustic communication programs offspring for high post-hatching temperatures in a songbird

In many species, embryos can perceive and learn external sounds. Yet, the possibility that parents may use these embryonic capacities to alter their offspring’s developmental trajectories has not been considered. Here, we demonstrate that zebra finch parents acoustically signal high ambient temperatures (above 26°C) to their embryos. We show that exposure of embryos to these acoustic cues alone adaptively alters subsequent nestling begging and growth in response to nest temperature and influences individuals’ reproductive success and thermal preferences as adults. These findings have implications for our understanding of maternal effects, phenotypic plasticity, developmental programming, and the adaptation of endothermic species to a warming world

A prenatal acoustic signal of heat affects thermoregulation capacities at adulthood in an arid‑adapted bird

Understanding animal physiological adaptations for tolerating heat, and the causes of interindividual variation, is key for predicting climate change impacts on biodiversity. Recently, a novel mechanism for transgenerational heat adaptation was identified in a desert-adapted bird, where parents acoustically signal hot conditions to embryos. Prenatal exposure to “heat-calls” adaptively alters zebra finch development and their thermal preferences in adulthood, suggesting a long-term shift towards a heat-adapted phenotype. However, whether such acoustic experience improves long-term thermoregulatory capacities is unknown. We measured metabolic rate (MR), evaporative water loss (EWL) and body temperature in adults exposed to a stepped profile of progressively higher air temperatures (Ta) between 27 and 44 °C. Remarkably, prenatal acoustic experience affected heat tolerance at adulthood, with heat-call exposed individuals more likely to reach the highest Ta in morning trials. This was despite MR and EWL reaching higher levels at the highest Ta in heat-call individuals, partly driven by a stronger metabolic effect of moderate activity. At lower Ta, however, heat-call exposed individuals had greater relative water economy, as expected. They also better recovered mass lost during morning trials. We therefore provide the first evidence that prenatal acoustic signals have long-term consequences for heat tolerance and physiological adaptation to heat.This work was supported by the Australian Research Council (DE170100824 and DP180101207 to MMM) and the Holsworth Wildlife Research Endowment. International travel costs for A.E.M. were provided by the National Research Foundation of South Africa (Grant no. 119754)Peer reviewe

Appendix A. Figure of settlement patterns and nest box availability at different densities throughout the breeding season.

Figure of settlement patterns and nest box availability at different densities throughout the breeding season

dataset for five-minute mating test

The dataset was created in excel. All variables included in this dataset are described in details in the associated manuscript. For binary variables, 0 indicates absence and 1 presence. "Decr" and "cont" refer to decreased and control broods respectively. missing values are indicated by "na"