Plasticity and cross‐tolerance to heterogeneous environments: divergent stress responses co‐evolved in an African fruit fly

Abstract

Plastic adjustments of physiological tolerance to a particular stressor can result in fitness benefits for resistance that might manifest not only in that same environment but also be advantageous when faced with alternative environmental stressors, a phenomenon termed 'cross-tolerance'. The nature and magnitude of cross-tolerance responses can provide important insights into the underlying genetic architecture, potential constraints on or versatility of an organism's stress responses. In this study, we tested for cross-tolerance to a suite of abiotic factors that likely contribute to setting insect population dynamics and geographic range limits: heat, cold, desiccation and starvation resistance in adult Ceratitis rosa following acclimation to all these isolated individual conditions prior to stress assays. Traits of stress resistance scored included critical thermal (activity) limits, chill coma recovery time (CCRT), heat knockdown time (HKDT), desiccation and starvation resistance. In agreement with other studies, we found that acclimation to one stress typically increased resistance for that same stress experienced later in life. A more novel outcome, however, is that here we also found substantial evidence for cross-tolerance. For example, we found an improvement in heat tolerance (critical thermal maxima, CT max ) following starvation or desiccation hardening and improved desiccation resistance following cold acclimation, indicating pronounced cross-tolerance to these environmental stressors for the traits examined. We also found that two different traits of the same stress resistance differed in their responsiveness to the same stress conditions (e.g. HKDT was less cross-resistant than CT max ). The results of this study have two major implications that are of broader importance: (i) that these traits likely co-evolved to cope with diverse or simultaneous stressors, and (ii) that a set of common underlying physiological mechanisms might exist between apparently divergent stress responses in this species. This species may prove to be a valuable model for future work on the evolutionary and mechanistic basis of cross-tolerance.

City limits: Heat tolerance is influenced by body size and hydration state in an urban ant community

“…Therefore, water limitation in our study did not facilitate cross‐tolerance, which is when exposure to one stressor better equips an animal to tolerate a subsequent and different stressor (reviewed in Harrison, Woods, & Roberts, 2012). However, other work has shown a link between mechanisms underlying responses to desiccation and heat stress (Benoit et al, 2010; Gotcha et al, 2018). Continued work is required to better understand factors influencing contradictory results, such as those due to variation in taxon and/or methodology (e.g., life stage of desiccation exposure, or the duration of desiccation or recovery from desiccation).…”

“…The availability of water constrains terrestrial life, and hydration state plays a critical role in CT max , body temperature, and homeostasis (Da Lage, Capy, & David, 1989; Manenti, Cunha, Sørensen, & Loeschcke, 2018; Nguyen et al, 2017; Smit et al, 2018). Desiccation can enhance the physiological heat shock response in some species (flies: Benoit et al, 2010; Gotcha, Terblanche, & Nyamukondiwa, 2018); yet, in other species, it reduces CT max and does not increase the upregulation of inducible Hsps during a heat shock (ants: Nguyen et al, 2017). Thus, a comparative examination of the effects of body size, thermal life history, and water availability on CT max in terrestrial animals is required, and such a comprehensive approach may also provide insight into community dynamics associated with invasion biology.…”

Evidence of rapid spread and establishment of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in semi-arid Botswana

“…Improved environmental tolerance and thermal plasticity are the key contributing factors towards invasion success of invasive alien species into a novel environment [30,39,71]. Lower and upper lethal temperatures (LLT and ULTs) for T. absoluta adults ranged from − 1 to − 12 °C and 37 to 43 °C respectively for 2 h treatments.…”

“…Insects have been reported to experience multiple overlapping abiotic and biotic stressors such as temperature, starvation and desiccation in the wild [3,38,39]. Hence, an understanding of bioecology of invasive species is of paramount importance in enlightening mechanisms underlying the successful spread and establishment of invasive alien species [1,40].…”

Thermal plasticity potentially mediates the interaction between host Chilo partellus Swinhoe (Lepidoptera: Crambidae) and endoparasitoid Cotesia flavipes Cameron (Hymenoptera: Braconidae) in rapidly changing environments

“…22 In addition, acclimation to high temperature improved CT min for both species, suggesting significant cross-tolerance, consistent with previous studies on Linepithema humile 63 and D. melanogaster. 64 This cross-tolerance suggests the presence of overlapping thermal stress resistance mechanisms 64,65 or signal pathways ('cross-talk'). [see 52] Species comparisons of CT min between the two trophic levels (Fig.…”