Phenotypic plasticity is an important avenue by which organisms may persist in the face of rapid environmental change. Environmental cues experienced by the mother can also influence the phenotype of offspring, a form of plasticity called maternal effects. Maternal effects can adaptively prepare offspring for the environmental conditions they will likely experience; however, their ability to buffer offspring against environmental stressors as embryos is understudied. Using captive zebra finches, we performed a maternal‐offspring environmental match‐mismatch experiment utilizing a 2 × 2 × 2 factorial design. Mothers were exposed to a mild heat conditioning (38°C) or control (22°C) treatment as juveniles, an acute high heat (42°C) or control (22°C) treatment as adults, then paired for breeding. The eggs produced by those females were incubated at a hyperthermic (38.5°C) or optimal temperature (37.2°C). We found that when mothers were exposed to a mild heat conditioning as juveniles, their embryos exhibited reduced water loss, longer development times, and produced hatchlings with heavier pectoralis muscles when incubated at high incubation temperatures, compared to embryos from control mothers. Mothers exposed to both the mild heat conditioning as juveniles and a high heat stressor as adults produced eggs with a higher density of shell pores and embryos with lower heart rates during development. However, there was a cost when there was a mismatch between maternal and embryo environment. Embryos from these conditioned and heat‐stressed mothers had reduced survival at control incubation temperatures, indicating the importance of offspring environment when interpreting potential adaptive effects.
The environment in which animals develop can have important consequences for their phenotype. In reptiles, incubation temperature is a critical aspect of the early developmental environment. Incubation temperature influences morphology, physiology, and behavior of non‐avian reptiles, however, little is known about how incubation temperature influences offspring phenotype and behaviors important to avian survival. To investigate whether incubation temperature influences avian behaviors, we collected wood duck (
- NSF-PAR ID:
- 10067068
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Journal of Experimental Zoology Part A: Ecological and Integrative Physiology
- Volume:
- 329
- Issue:
- 4-5
- ISSN:
- 2471-5638
- Page Range / eLocation ID:
- p. 191-202
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract -
more » « less
Abstract Aspects of global change create stressful thermal environments that threaten biodiversity. Oviparous, non‐avian reptiles have received considerable attention because eggs are left to develop under prevailing conditions, leaving developing embryos vulnerable to increases in temperature. Though many studies assess embryo responses to long‐term (i.e., chronic), constant incubation temperatures, few assess responses to acute exposures which are more relevant for many species. We subjected brown anole (
Anolis sagrei ) eggs to heat shocks, thermal ramps, and extreme diurnal fluctuations to determine the lethal temperature of embryos, measure the thermal sensitivity of embryo heart rate and metabolism, and quantify the effects of sublethal but stressful temperatures on development and hatchling phenotypes and survival. Most embryos died at heat shocks of 45°C or 46°C, which is ~12°C warmer than the highest constant temperatures suitable for successful development. Heart rate and O2consumption increased with temperature; however, as embryos approached the lethal temperature, heart rate and CO2production continued rising while O2consumption plateaued. These data indicate a mismatch between oxygen supply and demand at high temperatures. Exposure to extreme, diurnal fluctuations depressed embryo developmental rates and heart rates, and resulted in hatchlings with smaller body size, reduced growth rates, and lower survival in the laboratory. Thus, even brief exposure to extreme temperatures can have important effects on embryo development, and our study highlights the role of both immediate and cumulative effects of high temperatures on egg survival. Such effects must be considered to predict how populations will respond to global change. -
more » « less
Abstract Many ectotherms rely on temperature cues experienced during development to determine offspring sex. The first descriptions of temperature‐dependent sex determination (TSD) were made over 50 years ago, yet an understanding of its adaptive significance remains elusive, especially in long‐lived taxa.
One novel hypothesis predicts that TSD should be evolutionarily favoured when two criteria are met—(a) incubation temperature influences annual juvenile survival and (b) sexes mature at different ages. Under these conditions, a sex‐dependent effect of incubation temperature on offspring fitness arises through differences in age at sexual maturity, with the sex that matures later benefiting disproportionately from temperatures that promote juvenile survival.
The American alligator (
Alligator mississippiensis ) serves as an insightful model in which to test this hypothesis, as males begin reproducing nearly a decade after females. Here, through a combination of artificial incubation experiments and mark‐recapture approaches, we test the specific predictions of the survival‐to‐maturity hypothesis for the adaptive value of TSD by disentangling the effects of incubation temperature and sex on annual survival of alligator hatchlings across two geographically distinct sites.Hatchlings incubated at male‐promoting temperatures (MPTs) consistently exhibited higher survival compared to those incubated at female‐promoting temperatures. This pattern appears independent of hatchling sex, as females produced from hormone manipulation at MPT exhibit similar survival to their male counterparts.
Additional experiments show that incubation temperature may affect early‐life survival primarily by affecting the efficiency with which maternally transferred energy resources are used during development.
Results from this study provide the first explicit empirical support for the adaptive value of TSD in a crocodilian and point to developmental energetics as a potential unifying mechanism underlying persistent survival consequences of incubation temperature.
Read the free
Plain Language Summary for this article on the Journal blog. -
Abstract A major driver of wildlife responses to climate change will include non-genomic effects, like those mediated through parental behavior and physiology (i.e., parental effects). Parental effects can influence lifetime reproductive success and survival, and thus population-level processes. However, the extent to which parental effects will contribute to population persistence or declines in response to climate change is not well understood. These effects may be substantial for species that exhibit extensive parental care behaviors, like birds. Environmental temperature is important in shaping avian incubation behavior, and these factors interact to determine the thermal conditions embryos are exposed to during development, and subsequently avian phenotypes and secondary sex ratios. In this article, we argue that incubation behavior may be an important mediator of avian responses to climate change, we compare incubation strategies of two species adapted to different thermal environments nesting in extreme heat, and we present a simple model that estimates changes in egg temperature based on these incubation patterns and predicted increases in maximum daily air temperature. We demonstrate that the predicted increase in air temperature by 2100 in the central USA will increase temperatures that eggs experience during afternoon off-bouts and the proportion of nests exposed to lethal temperatures. To better understand how species and local adaptations and behavioral-plasticity of incubation behavior will contribute to population responses to climate change comparisons are needed across more avian populations, species, and thermal landscapes.more » « less
-
more » « less
Abstract Phenotypic variation within populations is influenced by the environment via plasticity and natural selection. How phenotypes respond to the environment can vary among traits, populations and life stages in ways that can influence fitness.
Plastic responses during early development are particularly important because they can affect components of fitness throughout an individual's life. Consequently, how natural selection shapes developmental plasticity could be influenced by fitness consequences across different life stages. Moreover, spatial variation in selection pressures could generate differences in plastic responses among populations.
To gain insight into sources of variation in phenotypes and survival, we used a laboratory egg incubation experiment using brown anole lizards
Anolis sagrei from mainland (ancestral) and island (descendent) populations, combined with a mark–release–recapture experiment in the field. Our study was designed to (a) quantify the effects developmental temperature on embryo development and offspring morphology, (b) assess how developmental temperature influences offspring survival across different life stages and (c) quantify how thermal reaction norms vary among ancestral and descendant populations.Developmental temperature influenced offspring morphology, but thermal reaction norms of embryos showed little variation among populations. Developmental temperature influenced offspring survival, but the patterns differed between embryo and hatchling stages; the optimal temperature for embryos was about 5℃ lower than that for hatchlings. High temperatures were thermally stressful to embryos, but they reduced incubation duration and led to early hatching. In turn, earlier hatching increased the probability of survival to adulthood. Moreover, the effect of developmental temperature on hatchling survival was most pronounced for offspring that hatched late in the season.
The difference in optimal developmental temperatures between life stages may be driven by physiological tolerance for embryos and by ecological factors for hatchlings. Moreover, the fitness consequences of the developmental environment depend on the phenology of hatching. Overall, these results highlight how the developmental environment can differentially affect fitness across life stages and show that temporal thermal heterogeneity can influence survival of embryos, but the consequences on post‐hatching stages may vary at different times of the season.
A free
Plain Language Summary can be found within the Supporting Information of this article.
