Suboptimal is good enough: Aligning thermal sensitivity to habitat temperature across season

Predicting the thermal performance of organisms is crucial for understanding the effects of climate warming. In ectotherms, organismal performance depends on how well aligned the thermal sensitivities of fitness components are to body temperatures in the natural habitat. It is frequently assumed that T_opt (temperatures that maximize performance) for important fitness components has evolved to align with habitat temperatures. However, most organisms at temperate latitudes experience significant seasonal temperature variation, and therefore frequently operate at suboptimal temperatures. Importantly, seasonal performance patterns may differ among fitness components if those components have different thermal sensitivities. The extent to which habitat temperature can deviate from T_opt before an organism can no longer persist in its environment, and the role of seasonality in driving this deviation, is infrequently explored. Here, we assess how well aligned the thermal sensitivity (thermal performance curves, or TPCs) of development, growth and survival is to local habitat temperatures across two seasons using embryos of the marine gastropod Haminoea vesicula. We develop a mechanistic model by integrating thermal sensitivity for development, growth and survival with habitat temperatures to predict embryo performance across seasons. Our results demonstrate that habitat temperatures mostly fall far below T_opt for development and growth. Accordingly, model predictions show that in the cool spring, developmental periods are 20% longer and hatchling sizes are slightly (~1%) smaller on average than in the summer. Survival risk intensifies in the summer due to an acute high-temperature event, indicating that seasonal temperature variation affects performance differently between fitness components. We horizontally shift TPC functions to assess how well aligned the thermal sensitivity of each fitness component is to habitat temperatures. Simulations indicate that thermal sensitivity for survival is well aligned to habitat temperature, but T_opt for development and growth would need to cold shift by 11°C and 16°C, respectively, to achieve maximal performance. However, cold shifting TPCs to maximize development and growth results in sharp survival reductions due to summer heat spikes. Overall, T_opt greatly exceeds the most frequent habitat temperatures, leading to suboptimal performance most of the time. However, high T_opt allows embryos to survive seasonally driven heat spikes. Sometimes 'suboptimal' is good enough.