A lack of repeatability creates the illusion of a trade-off between basal and plastic cold tolerance

Abstract

The thermotolerance–plasticity trade-off hypothesis predicts that ectotherms with greater basal thermal tolerance have a lower acclimation capacity. This hypothesis has been tested at both high and low temperatures but the results often conflict. If basal tolerance constrains plasticity (e.g. through shared mechanisms that create physiological constraints), it should be evident at the level of the individual, provided the trait measured is repeatable. Here, we used chill-coma onset temperature and chill-coma recovery time (CCO and CCRT; non-lethal thermal limits) to quantify cold tolerance of Drosophila melanogaster across two trials (pre- and post-acclimation). Cold acclimation improved cold tolerance, as expected, but individual measurements of CCO and CCRT in non-acclimated flies were not (or only slightly) repeatable. Surprisingly, however, there was still a strong correlation between basal tolerance and plasticity in cold-acclimated flies. We argue that this relationship is a statistical artefact (specifically, a manifestation of regression to the mean; RTM) and does not reflect a true trade-off or physiological constraint. Thermal tolerance trade-off patterns in previous studies that used similar methodology are thus likely to be impacted by RTM. Moving forward, controlling and/or correcting for RTM effects is critical to determining whether such a trade-off or physiological constraint exists.

Trade-offs between baseline thermal tolerance and thermal tolerance plasticity are much less common than it appears

“…Some of the regression to the mean effects demonstrated here are consistent with conclusions drawn by the original authors using different approaches (e.g., Deery et al, 2021; O’Neill et al, 2021; see above). However, most of the initial, unadjusted analyses were interpreted as evidence consistent with the TOH.…”

“…Approaches for identifying, avoiding, and/or correcting for regression to the mean exist, but to date have rarely been applied to tests of the TOH. O’Neill, Davis, & MacMillan (2021) tentatively found support for the TOH among Drosophila melanogaster individuals with respect to cold tolerance, but from the correlation structure within their data, they inferred that the relationship was probably artifactual. Deery et al (2021) found initial support for the TOH at the individual level among Anolis lizards with respect to heat hardening, but subsequently conducted a data resampling analysis (Ghalambor et al, 2015; Jackson & Somers, 1991) and concluded that the relationships were spurious.…”

Trade‐offs between baseline thermal tolerance and thermal tolerance plasticity are much less common than it appears

“…Slopes of the relationship between baseline tolerance and tolerance plasticity for all data sets become less negative when using adjusted versus unadjusted plasticity values (Figure 2). Some of the regression to the mean effects demonstrated here are consistent with conclusions drawn by the original authors using different approaches (e.g., Deery et al, 2021;O'Neill et al, 2021; see above). However, most of the initial, unadjusted analyses were interpreted as evidence consistent with the TOH.…”

“…Approaches for identifying, avoiding, and/or correcting for regression to the mean exist, but to date have rarely been applied to tests of the TOH. O'Neill et al (2021) tentatively found support for the TOH among Drosophila melanogaster individuals with respect to cold tolerance, but from the correlation structure within their TA B L E 1 Summary of the data sets reanalyzed in the present study. "Unadjusted" correlation coefficients were calculated using raw plasticity data as in the original analyses.…”

“…Approaches for identifying, avoiding, and/or correcting for regression to the mean exist, but to date have rarely been applied to tests of the TOH. O'Neill et al (2021) tentatively found support for the TOH among Drosophila melanogaster individuals with respect to cold tolerance, but from the correlation structure within their data, they inferred that the relationship was probably artifactual. Deery et al (2021) found initial support for the TOH at the individual level among Anolis lizards with respect to heat hardening, but subsequently conducted a data resampling analysis (Ghalambor et al, 2015; Jackson & Somers, 1991) and concluded that the relationships were spurious.…”