Thermal preference and performance in a sub-Antarctic caterpillar: A test of the coadaptation hypothesis and its alternatives

Abstract

Physiological ecologists have long assumed that thermoregulatory behaviour will evolve to optimise physiological performance. The coadaptation hypothesis predicts that an animal's preferred body temperature will correspond to the temperature at which its performance is optimal. Here we use a strong inference approach to examine the relationship between thermal preference and locomotor performance in the caterpillars of a wingless sub-Antarctic moth, Pringleophaga marioni Viette (Tineidae). The coadaptation hypothesis and its alternatives (suboptimal is optimal, thermodynamic effect, trait variation) are tested. Compared to the optimal movement temperature (22.5°C for field-fresh caterpillars and 25, 20, 22.5, 25 and 20°C following seven day acclimations to 0, 5, 10, 15 and 5-15°C respectively), caterpillar thermal preference was significantly lower (9.2°C for field-fresh individuals and 9.4, 8.8, 8.1, 5.2 and 4.6°C following acclimation to 0, 5, 10, 15 and 5-15°C, respectively). Together with the low degree of asymmetry observed in the performance curves, and the finding that acclimation to high temperatures did not result in maximal performance, all, but one of the above hypotheses (i.e. 'trait variation') was rejected. The thermal preference of P. marioni caterpillars more closely resembles temperatures at which survival is high (5-10°C), or where feeding is optimal (10°C), than where locomotion speed is maximal, suggesting that thermal preference may be optimised for overall fitness rather than for a given trait.

Phenotypic plasticity in locomotor performance of a monophyletic group of weevils accords with the warmer is better hypothesis

“…The climate on Marion Island is considered one of the least variable globally, although more importantly this variability in temperature is unpredictable given that within 24 h temperatures can show temporal autocorrelation that is no different from random (compared with continental sites where thermal predictability may endure for weeks) . Thus, many traits do not show acclimation responses, such as supercooling points (SCPs) and locomotion speed in a flightless moth (Klok and Chown, 1998;Haupt et al, 2017), SCPs and lower lethal temperatures and locomotion performance traits in mites, and upper and lower lethal limits in kelp fly larvae and adults (Marais et al, 2009). However, other traits do show acclimation responses, such as SCPs and critical thermal minima in a different species of flightless moth (Klok and Chown, 1997), critical thermal minima in weevils , SCPs of a psocopteran (Slabber and Chown, 2004), several thermal tolerance traits and desiccation resistance in springtails, chill coma recovery in kelp flies (although the form of the response differs between adults and larvae) (Marais and Chown, 2008) and critical thermal minima and maxima in spiders (although responses are decoupled) (Jumbam et al, 2008).…”

“…A temperature-controlled walking stage (following Haupt et al, 2017) was attached to a Grant LTC 12 water bath set to regulate stage temperature. Stage temperature was monitored at each end using Type T 20-gauge thermocouples connected to CHY 507 Digital Thermometers (CHY Firemate Co, Taiwan).…”

“…Despite a sound theoretical basis for the prediction, only a few studies have sought to determine whether this is the case, with contrasting outcomes (e.g. Niehaus et al, 2012;Manenti et al, 2015;Sinclair et al, 2016;Haupt et al, 2017). Hence, further empirical assessments of the idea are essential.…”

“…Based on understanding of the island's marine and terrestrial climates Faulkner et al, 2014) and on information on the acclimation responses of other arthropod species from these major habitats Haupt et al, 2017), we predict that the terrestrial weevils should show no plasticity, or perhaps some measure of compensation (Klok and Chown, 2005), whereas the marine weevil should show beneficial acclimation. Moreover, we also examine the slope of the rate-temperature relationship for all of the populations examined, comparing it with the typically expected value resulting in an activation energy approximation of 0.6-0.7 eV (Gillooly et al, 2001) and the somewhat lower value empirically found for body velocity [0.46±0.03 (s.e.m.)]…”

Behavioral thermoregulation is highly repeatable and unaffected by digestive status in Agama atra

“…These mismatches could reflect multiple mechanisms: compensatory behavior, a heat stress avoidance strategy (Martin & Huey 2008), compromise to incorporate multiple and differing thermal optima or prioritization of particular functions over others (e.g. growth rate rather than nutrient assimilation; Miller et al 2009;Haupt et al 2017), a response to laboratory-induced stress (Christian & Weavers 1996;Dohm 2002) or a combination of these. Recently, the existence of a thermal behavior syndrome has also been proposed, with "hot" and "cold" type individuals presenting particular and consistent associations between behavior and thermal performance (Goulet et al 2016(Goulet et al , 2017.…”