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

Predicting organismal performance in changing environments is a global
challenge. In ectotherms, organismal performance depends on how
well-aligned the thermal sensitivities of fitness components are to body
temperatures in natural habitat. It is frequently assumed that Topt
(temperatures that maximize performance) for important fitness components
have 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 Topt before an organism can no longer persist in its
environment, and the role of seasonality in driving this deviation, are
infrequently explored. Here, we assess how well-aligned the thermal
sensitivity (thermal performance curves, or TPCs) of development, growth,
and survival are 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 Topt for development and growth.
Accordingly, in the cool spring, developmental periods are 20% longer and
hatchling sizes are slightly (about 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 Topt for survival is well-aligned to habitat
temperature, but Topt for development and growth would need to cold-shift
by 11° and 16° C, respectively, to achieve optimal performance. However,
cold-shifting TPCs to maximize development and growth results in sharp
survival reductions due to summer heat spikes. Overall, Topt greatly
exceed the most frequent habitat temperatures, leading to suboptimal
performance most of the time. However, high Topt allow embryos to survive
seasonally driven heat spikes. Sometimes “suboptimal” is good enough.