American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

“Antagonistic responses of exposure to sublethal temperatures: Adaptive phenotypic plasticity coincides with a reduction in organismal performance”

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Anthony L. Gilbert and Donald B. Miles (Sep 2019)

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Exposure to stressful temperatures induces adaptive plasticity but constrains ecological and organismal performance

When adaptive phenotypic plasticity is expressed, the original stimuli can elicit other unforeseen physiological and behavioral consequences

Tree lizards (<i>Urosaurus ornatus</i>).<br />(Credit: Kyle Brooks)
Tree lizards (Urosaurus ornatus).
(Credit: Kyle Brooks)

Anthropogenic climate change is exposing populations to new environmental pressures that can lead to a variety of physiological, genetic, or behavioral responses. When novel environmental conditions cause phenotypic shifts in the absence of genetic change (i.e. phenotypic plasticity), oftentimes researchers only consider quantifying how traits-of-interest shift, without considering that particularly stressful stimuli might lead to other unforeseen phenotypic outcomes. Because many species are now predisposed to higher incidences of heat waves within their environment, exposure to sublethal temperatures is considered to be a trigger of adaptive phenotypic plasticity, otherwise called ‘heat hardening’. Heat hardening occurs when an individual is exposed to sublethal temperatures, and as a result they can temporarily tolerate higher temperatures than they could prior to heat shock. However, because the trigger of heat hardening is a stressful increase in body temperatures close to upper thermal tolerance limits, organisms might exhibit unforeseen physiological consequences. In this study, Gilbert and Miles show that for tree lizards in the Sonoran Desert, when heat hardening is expressed, lizards prefer cooler temperatures when they thermoregulate, and exhibit reductions in locomotor performance (maximal speed) throughout the response. They also find that because of these physiological costs, tree lizards are not fully able to exploit the adaptive nature of a higher heat tolerance, thus weakening their reliance on phenotypic plasticity as a buffer from temperature extremes. This study demonstrates that even though plasticity can be adaptive and beneficial, when organisms are exposed to extreme environmental stimuli, these stimuli might induce maladaptive responses in other traits leading to antagonistic interactions between the phenotypic shifts triggered by new environments.


Abstract

A fitness benefit of phenotypic plasticity is the ability of an organism to survive short-term, deleterious environmental fluctuations. Yet, the influence of selection on plasticity in modulating shifts in phenotypic traits remains unclear. Short-term phenotypic plasticity in thermal tolerance traits is attained by exposure to sublethal hot or cold temperatures (i.e. the hardening response). Heat hardening is expected to buffer organisms from the unpredictability of extreme thermal fluctuations in the environment so as to minimize interruptions in activity and enhance survival. However, exposure to sublethal temperatures might entail other phenotypic costs that constrain or inhibit the prolonged use of hardening responses across longer timescales. Here, we estimated the onset of the heat hardening response, physiological and behavioral shifts during heat hardening, and geographic variation in heat hardening using tree lizards (Urosaurus ornatus). Peak heat hardening occurred 6h after exposure to sublethal temperatures. We found that both preferred body temperatures and locomotor performance diminished following exposure to sublethal temperatures, and performance levels did not approach pre-exposure levels until after the peak hardening response. We also found support for intraspecific variation in the hardening response along an environmental gradient, where populations in more thermally variable environments exhibited stronger plastic responses and populations with higher baseline heat tolerances exhibited weaker plastic responses. Sublethal temperature exposure might induce adaptive plasticity in thermal tolerance, however we find that these responses entail other phenotypic shifts that might curtail chronic reliance on plasticity in thermal traits as a mechanism of responding to changes in thermal environments induced by climate warming.