Heat resistance throughout ontogeny: body size constrains thermal tolerance

Abstract

Heat tolerance is a trait of paramount ecological importance and may determine a species' ability to cope with ongoing climate change. Although critical thermal limits have consequently received substantial attention in recent years, their potential variation throughout ontogeny remained largely neglected. We investigate whether such neglect may bias conclusions regarding a species' sensitivity to climate change. Using a tropical butterfly, we found that developmental stages clearly differed in heat tolerance. It was highest in pupae followed by larvae, adults and finally eggs and hatchlings. Strikingly, most of the variation found in thermal tolerance was explained by differences in body mass, which may thus impose a severe constraint on adaptive variation in stress tolerance. Furthermore, temperature acclimation was beneficial by increasing heat knock-down time and therefore immediate survival under heat stress, but it affected reproduction negatively. Extreme temperatures strongly reduced survival and subsequent reproductive success even in our highly plastic model organism, exemplifying the potentially dramatic impact of extreme weather events on biodiversity. We argue that predictions regarding a species' fate under changing environmental conditions should consider variation in thermal tolerance throughout ontogeny, variation in body mass and acclimation responses as important predictors of stress tolerance.

Carried over: Heat stress in the egg stage reduces subsequent performance in a butterfly

“…The species inhabits a highly seasonal environment with alternating wet-warm and dry-cool seasons, such that it relies heavily on phenotypic plasticity to master associated challenges [42,43]. Temperature variation induces, for instance, plastic responses in wing coloration, growth and development, reproduction, and survival [14,16,44–47]. Reproduction is confined to the favorable wet season during which oviposition plants are abundantly available [48,49].…”

“…First, thermal tolerance may differ substantially throughout ontogeny, because developmental stages vary in size, morphology, physiology, and behaviour, which may easily affect thermal tolerance [11,15,16]. Second, life stages may not be entirely independent of one another, such that thermal stress experienced in a specific developmental stage may affect later life (“carry-over effects”; [17–21]).…”

“…For instance, heat stress during development may reduce adult body size, which may in turn reduce subsequent heat tolerance [16,32,34–36]. Besides stress tolerance, body size may furthermore affect longevity, reproductive success as well as competitiveness [32,37–39], thereby potentially affecting even subsequent generations.…”

Effects of environmental warming during early life history on libellulid odonates

“…Body size can affect dispersal ability (De Bie et al 2012), range size (Rundle et al 2007), strength of trophic interactions (Rudolf 2012), and fitness (Sokolovska et al 2000;Kingsolver and Huey 2008). However, many of these studies have focused on these effects in later ontogeny, whereas early life-history stages may be equally or even more sensitive to temperature (Klockmann et al 2017). Odonate body size at hatching has been under-reported in the literature and therefore it remains unclear whether faster egg development will lead to smaller hatchling size in this group.…”

“…Additionally, in many studies, survival is only measured at or near maturity. Therefore, it remains unclear at what stage higher temperatures are causing observed increases in mortality (Klockmann et al 2017). In one dragonfly species, higher mortality occurred when larvae were reared in warmer temperatures; however, survival was only measured at metamorphosis (McCauley et al 2015).…”