Developmental plasticity in thermal tolerance: Ontogenetic variation, persistence, and future directions

Abstract

Understanding the factors affecting thermal tolerance is crucial for predicting the impact climate change will have on ectotherms. However, the role developmental plasticity plays in allowing populations to cope with thermal extremes is poorly understood. Here, we meta‐analyse how thermal tolerance is initially and persistently impacted by early (embryonic and juvenile) thermal environments by using data from 150 experimental studies on 138 ectothermic species. Thermal tolerance only increased by 0.13°C per 1°C change in developmental temperature and substantial variation in plasticity (~36%) was the result of shared evolutionary history and species ecology. Aquatic ectotherms were more than three times as plastic as terrestrial ectotherms. Notably, embryos expressed weaker but more heterogenous plasticity than older life stages, with numerous responses appearing as non‐adaptive. While developmental temperatures did not have persistent effects on thermal tolerance overall, persistent effects were vastly under‐studied, and their direction and magnitude varied with ontogeny. Embryonic stages may represent a critical window of vulnerability to changing environments and we urge researchers to consider early life stages when assessing the climate vulnerability of ectotherms. Overall, our synthesis suggests that developmental changes in thermal tolerance rarely reach levels of perfect compensation and may provide limited benefit in changing environments.

Adaptive variation in avian eggshell structure and gas conductance across elevational gradients?

“…Given the narrow elevational distribution of species in the tropics and their presumably narrow physiological tolerances (Janzen, 1967), montane species may be especially susceptible to changes in environmental conditions (Pearson & Dawson, 2003; Colwell et al, 2008). Even minor environmental changes may affect microclimates where birds breed and may have deleterious effects on the embryo development (Lourens et al, 2005; Pottier et al 2022) and species persistence if populations cannot evolve fast enough (or adjust via phenotypic plasticity in structures or behaviors) to cope with changes. This would be especially important in highland areas, where gas conductance through the eggshell shows limited variation.…”

orchaRd 2.0: An R package for visualizing meta-analyses with orchard plots

“…Yet, differences in variances can be as biologically insightful as differences in means among groups. For example, Pottier et al ( 2022) found that not only were aquatic ectotherms more thermally plastic than their terrestrial counterparts, but their plastic responses were much more variable than those of terrestrial ectotherms (even after taking into account the sample size difference). Our orchard_plot now allows for visualization of modelled heteroscedasticity by depicting different prediction intervals (PIs) for different groups (Fig 1).…”

“…Orchard plots (using orchard_plot function) and model result tables (using mod_result function) for terrestrial and aquatic ectotherm developmental acclimation response ratios (dARR). A) Model assuming the variance in terrestrial and aquatic ectothermic species is the same (i.e., homogeneity of variance); B) Model assuming the variance in terrestrial and aquatic ectothermic species is not the same (i.e., heterogeneity of variance), with the lower and upper confidence intervals (CIs) and prediction intervals (PIs) adjusted accordingly for each level of the habitat type moderator (data from Pottier et al 2022).…”

Divergence in rates of phenotypic plasticity among ectotherms

“…Lande, 2014) and empirical interest (e.g. Seebacher et al, 2015;Pottier et al 2022) from ecologists and evolutionary biologists, empirical support for certain predictions regarding the evolution of this plasticity parameter remain equivocal. For example, while it has been proposed that organisms inhabiting more variable environments should evolve greatercapacity for plasticity , this is rarely supported by empirical data (Gunderson & Stillman, 2015;Kelly et al, 2012;MacLean et al, 2019;Pereira et al, 2017;Phillips et al, 2016;Sgro et al, 2010;van Heerwaarden et al, 2016;van Heerwaarden et al, 2014).…”