Dalton C. Leibold

The ability to detect prey is crucial for survival in many animals. However, prey detection is a cognitive process that can be influenced by early life conditions such as prenatal stress or temperature. Mitochondrial function is likely to underlie these effects because cognitive abilities are energetically demanding (i.e. dependent on efficient metabolic function) and because metabolic‐derived oxidative stress and oxidative damage can impair cognitive function. Yet, whether prenatal stress and thermal environments affect prey detection, and whether mitochondrial function mediates such effects, remains poorly understood. Here, we investigated the links between prenatal environments, mitochondrial function and prey detection in the delicate skink ( Lampropholis delicata ). We manipulated egg corticosterone (CORT) levels—a key stress hormone in reptiles—and incubation temperature and assessed the ability of lizards to detect chemical and visual prey stimuli. Then, using flow cytometry, we measured metabolic function, oxidative stress and oxidative damage in the olfactory bulbs and optic tecta, two brain regions involved in sensory processing. While metabolic function and oxidative stress remained robust to early life conditions, CORT and temperature interacted to influence oxidative damage. Particularly, CORT decreased DNA damage in the olfactory bulbs of cold‐incubated lizards but had no effect on hot‐incubated lizards. In both brain regions, lipid peroxidation was lower in CORT‐treated lizards incubated at high temperatures compared to CORT‐treated cold‐incubated lizards, but no other between‐treatment differences were detected. Additionally, CORT‐treated lizards responded faster when presented with chemical cues but not visual stimuli. We did not find any relationship between mitochondrial function and prey detection. Our findings suggest that prenatal conditions have lasting effects on DNA damage and prey detection, but prey detection appears decoupled from mitochondrial function in L. delicata . Read the free Plain Language Summary for this article on the Journal blog.

Quantity discrimination affects a range of behaviours essential for fitness, including social interactions, navigation, and foraging and is widespread across animal taxa. However, in reptiles, evidence for this ability — particularly for small number contrasts — remains limited and mixed. Early-life conditions, such as hormonal exposure and temperature, can also shape brain development and cognitive performance, potentially affecting numerical abilities. Here, we tested the ability of the common garden skink ( Lampropholis guichenoti ) to discriminate between quantities and the effects of elevated prenatal glucocorticoids and incubation temperature on quantity discrimination and decision-making. We assessed quantity discrimination using a spontaneous choice test with food as a stimulus. We subjected lizards to five two-choice tests differing in the number of items (1 VS 4, 1 VS 3, 2 VS 4, 2 VS 3, 3 VS 4) while controlling for total length and area. Contrary to our predictions, lizards did not show clear preferences toward the larger items, providing no evidence of spontaneous quantity discrimination in L. guichenoti . Furthermore, prenatal conditions did not influence latency to make a choice, also a proxy for decision-making. Despite these results, further investigation of quantity discrimination in live-prey-feeding reptiles and the impact of early conditions on other taxa remains an important area of research.

The environmental conditions organisms experience during early development can have powerful and sustained effects on morphology, physiology, behaviour, and performance. Such developmental effects can influence reproductive success, survival, and life‐history strategies and can be transmitted across generations (i.e. trans and intergenerational effects). In this way, developmental effects can be powerful drivers of evolutionary change. Given the developmental environment affects a range of phenotypic traits, it has been proposed that physiological responses to developmental conditions are modulated through cellular mechanisms that are shared across cell and tissue types, such as mitochondrial function. Mitochondrial respiratory function is highly sensitive to environmental conditions and exposure to adverse conditions during development can have sustained effects on different aspects of aerobic respiration in mitochondria. However, it is currently unknown if these effects are widespread across taxonomic groups and which components of mitochondrial respiratory function are most likely to be affected by the environment during development. We compiled data from 86 studies to examine the effects of developmental stressors (nutritional imbalance, glucocorticoid hormone exposure, parental care deprivation, and psychological disturbance) on mitochondrial respiratory function using meta‐analysis. We sought to uncover whether there are general effects of developmental stressors on different aspects of mitochondrial respiratory function (antioxidants, metabolic capacity, oxidative damage, oxidative stress, and aerobic respiration). We tested how the type of developmental stressor, together with timing of exposure (prenatal versus postnatal), and sex and taxon of the test subjects influenced the magnitude, direction, and duration of effects on mitochondrial respiratory function. Finally, we tested which aspects of mitochondrial respiratory function were most impacted by developmental stressors. We found that exposure to glucocorticoids, parental care deprivation, and psychological disturbances during development generally decreased mitochondrial respiratory function. Generally, these developmental stressors increased the production of reactive oxygen species and oxidative damage and reduced aerobic respiration, metabolic capacity, and antioxidant levels. Nutritional imbalances during development (including both restricted and excessive nutrition) had a slight negative effect on mitochondrial respiratory function, but this effect may be influenced by publication bias. Overall, our results show that exposure to stressors during development negatively affects mitochondrial respiratory function, suggesting that changes in cellular metabolism may link developmental stressors to variation in whole animal traits and individual fitness.

Maternal stress and the developmental environment jointly affect offspring fitness and phenotype during early life. Mothers transmit stress to offspring through the deposition of hormones and energy into developing embryos, who are themselves subject to environmental stressors. A species’ life-history strategy (e.g. size and number of eggs) may further buffer or exacerbate the effects of developmental stress on offspring. We experimentally tested the joint effects of stress hormones (exogenous corticosterone applied directly to eggs) and the developmental environment (incubation temperature) on the hatching success and size of two lizards (Lampropholis delicata and Lampropholis guichenoti) that differ in maternal investment strategy. Hatching success was reduced by corticosterone exposure, but only in L. delicata, which produces clutches of more numerous but smaller eggs than L. guichenoti. Hatchling size in both species, however, was reduced by corticosterone exposure, incubation at high temperatures or both. In both species, maternal investment (egg size) was the best predictor of hatching success and hatchling size, regardless of treatment. Our findings suggest that, both within species and between species, greater maternal investment buffers offspring from maternal and developmental stress effects on early-life fitness (survival) but does not prevent their effects on fitness-associated phenotypes (hatchling size).

Early environmental factors such as heat or stress hormones can impair learning through brain metabolic function, which is crucial for neural development and synaptic plasticity. However, whether early environments always result in cognitive impairment through changes in neural physiology is not well established outside of a few model systems. Here, we investigated the effects of prenatal temperature and corticosterone (CORT) on brain mitochondrial activity and spatial learning in the delicate skink (Lampropholis delicata). We treated eggs with either CORT or a control vehicle and incubated at cold (23±3°C) or hot (28±3°C) temperatures. Juveniles were tested in a spatial learning task over 40 days after which mitochondrial function in the medial cortex was assessed. Despite among-individual variation in learning ability, mitochondrial physiology and spatial learning in L. delicata remained robust to prenatal temperature and CORT exposure. No significant relationship was found between mitochondrial function and cognitive performance, contrary to predictions. Increased metabolic capacity correlated with higher production of reactive oxygen species but did not affect oxidative damage, possibly as a result of protective mechanisms. These findings highlight the physiological and cognitive resilience of L. delicata to early-life challenges. Future research should explore whether this robustness extends to other brain regions, cognitive domains and life stages.

Animals must acquire new information through learning to adjust their behavior adaptively. However, learning ability can be constrained by conditions experienced during early development, when the brain is especially susceptible to environmental conditions. For example, temperature can result in phenotypically plastic adjustments to growth, metabolism, and learning in ectotherms. In vertebrates, thermal conditions can increase the production of glucocorticoid (GCs) - ‘stress’ hormones. Maternal GCs can be transmitted to offspring during development, potentially impacting their learning abilities. GCs and thermal environments are, therefore, predicted to have interactive effects on the development of learning in ectotherms. Here, we investigated the combined effects of prenatal corticosterone (CORT) - the main GC in reptiles—and incubation temperature on associative learning using two species of lizards, Lampropholis delicata and L. guichenoti. We manipulated CORT levels and temperature in a 2 × 2 factorial design, and then subjected juveniles to a color-associative learning task. We predicted that elevated CORT and low temperatures would impair associative learning. However, both species showed similar learning rates independently of treatment. Our results suggest that these two species may have evolved mechanisms to maintain learning performance despite prenatal challenges. We also found that color affected decision-making in both species. Overall, we observed a non-learned preference towards blue, underscoring the need to carefully select the color used in cognitive tests involving visual stimuli.

Developing animals are increasingly exposed to elevated temperatures as global temperatures rise as a result of climate change. Vertebrates can be affected by elevated temperatures during development directly, and indirectly through maternal effects (e.g. exposure to prenatal glucocorticoid hormones). Past studies have examined how elevated temperatures and glucocorticoid exposure during development independently affect vertebrates. However, exposure to elevated temperatures and prenatal corticosterone could have interactive effects on developing animals that affect physiology and life-history traits across life. We tested interactions between incubation temperature and prenatal corticosterone exposure in the delicate skink (Lampropholis delicata). We treated eggs with high or low doses of corticosterone and incubated eggs at 23°C (cool) or 28°C (warm). We measured the effects of these treatments on development time, body size and survival from hatching to adulthood and on adult hormone levels and mitochondrial respiration. We found no evidence for interactive effects of incubation temperature and prenatal corticosterone exposure on phenotype. However, incubation temperature and corticosterone treatment each independently decreased body size at hatching and these effects were sustained into the juvenile period and adulthood. Lizards exposed to low doses of corticosterone during development had elevated levels of baseline corticosterone as adults. Additionally, lizards incubated at cool temperatures had higher levels of baseline corticosterone and more efficient mitochondria as adults compared with lizards incubated at warm temperatures. Our results show that developmental conditions can have sustained effects on morphological and physiological traits in oviparous lizards but suggest that incubation temperature and prenatal corticosterone do not have interactive effects.

The climate crisis necessitates predicting how organisms respond to changing environments, but this requires understanding the mechanisms underlying thermal tolerance. The Hierarchical Mechanisms of Thermal Limitation (HMTL) hypothesis proposes that respiratory capacity and marginal stability of proteins and membranes interact hierarchically to determine thermal performance and limits. An untested prediction of the HMTL hypothesis is that behavioral anapyrexia (i.e., reduced body temperature in hypoxia) is exacerbated when metabolic demand is high. We tested this prediction by manipulating western fence lizards' (Sceloporus occidentalis) metabolic demand and oxygen environment, then measuring selected body temperatures. Lizards with elevated metabolic demand selected lower body temperatures at higher oxygen concentrations than resting lizards, but this occurred only at oxygen concentrations 2, suggesting thermal limits are unaffected by naturally‐occurring oxygen variation. Given our results and the ubiquity of behavioral anapyrexia, the HMTL hypothesis may generally explain how oxygen and temperature interactively affect reptile performance.