Nature vs. Nurture: Disentangling the Influence of Inheritance, Incubation Temperature, and Post-Natal Care on Offspring Heart Rate and Metabolism in Zebra Finches

Abstract

A historic debate in biology is the question of nature vs. nurture. Although it is now known that most traits are a product of both heredity (“nature”) and the environment (“nurture”), these two driving forces of trait development are rarely examined together. In birds, one important aspect of the early developmental environment is egg incubation temperature. Small changes (<1°C) in incubation temperature can have large effects on a wide-array of offspring traits. One important trait is metabolism, because it is related to life-history traits and strategies, organismal performance, and energetic and behavioral strategies. Although it has been shown that embryonic and post-hatch metabolism are related to egg incubation temperature, little is known about how this may vary as a function of genetic differences or post-hatching environmental conditions. Here, we investigated this question in zebra finches (Taeniopygia guttata). We experimentally incubated eggs at two different temperatures: 37.5°C (control), which is optimal for this species and 36.3°C (low), which is suboptimal. We first measured embryonic heart rate as a proxy of embryonic metabolic rate. Then, at hatch, we cross-fostered nestlings to differentiate genetic and pre-hatching factors from post-hatching environmental conditions. When offspring were 30 days-old, we measured their resting metabolic rate (RMR; within the thermoneutral zone) and thermoregulatory metabolic rate (TMR; 12°C; birds must actively thermoregulate). We also measured RMR and TMR of all genetic and foster parents. We found that embryonic heart rate was greater in eggs incubated at the control temperature than those at the low temperature. Further, embryonic heart rate was positively related to genetic father RMR, suggesting that it is both heritable and affected by the pre-natal environment. In addition, we found that post-hatch metabolic rates were positively related to genetic parent metabolic rate, and interactively related to incubation temperature and foster mother metabolic rate. Altogether, this suggests that metabolism and the energetic cost of thermoregulation can be influenced by genetics, the pre-natal environment, and the post-natal environment. Our study sheds light on how environmental changes and parental care may affect avian physiology, as well as which traits may be susceptible to natural selection.

How important is hidden phenotypic plasticity arising from alternative but converging developmental trajectories, and what limits it?

“…This is most evident in ectotherms, owing to the pervasive effect of ambient temperature on their physiological processes ( Jonsson and Jonsson, 2019 ; Jonsson et al, 2022 ). However, it is also important for birds, where the temperature at which the eggs are incubated is now known to influence post-hatching traits such as metabolic rate ( Hope et al, 2022 ). This may explain why the basal metabolic rate of wintering wild great tits ( Parus major ) is negatively correlated with the ambient minimum temperature they experienced during incubation: it has been suggested that this is adaptive, with the metabolism of embryos experiencing a cold spring being programmed to cope with colder winters ( Broggi et al, 2022 ).…”

“…Given the difficulty in separating these intergenerational effects and their complex terminology, in this paper I consider transgenerational and early developmental effects together, for the simple reason that in many species it can be hard to determine whether it is the parent or the developing offspring that is responding to an environmental cue. A further reason why transgenerational effects can be hard to unravel in nature is that they can derive from either parent ( Hope et al, 2022 ; Papatheodoulou et al, 2022 ), and their impact on offspring can be sex-dependent: for example, the effects of parental stress can depend on the sex of both the parent and the offspring ( Hellmann et al, 2020a ). These sex×stress×generation interactions become ever more complex by the grandoffspring F2 generation ( Hellmann et al, 2020b ).…”

“…A further reason why transgenerational effects can be hard to unravel in nature is that they can derive from either parent ( Hope et al, 2022 ; Papatheodoulou et al, 2022 ), and their impact on offspring can be sex-dependent: for example, the effects of parental stress can depend on the sex of both the parent and the offspring ( Hellmann et al, 2020a ). These sex×stress×generation interactions become ever more complex by the grandoffspring F2 generation ( Hellmann et al, 2020b ).…”