Adult Cold Tolerance Research Articles

Transcriptomic and functional genetic evidence for distinct ecophysiological responses across complex life cycle stages.

Organisms with complex life cycles demonstrate a remarkable ability to change their phenotypes across development, presumably as an evolutionary adaptation to developmentally variable environments. Developmental variation in environmentally sensitive performance, and thermal sensitivity in particular, has been well documented in holometabolous insects. For example, thermal performance in adults and juvenile stages exhibit little genetic correlation (genetic decoupling) and can evolve independently, resulting in divergent thermal responses. Yet, we understand very little about how this genetic decoupling occurs. We tested the hypothesis that genetic decoupling of thermal physiology is driven by fundamental differences in physiology between life stages, despite a potentially conserved cellular stress response. We used RNAseq to compare transcript expression in response to a cold stressor in Drosophila melanogaster larvae and adults and used RNA interference (RNAi) to test whether knocking down nine target genes differentially affected larval and adult cold tolerance. Transcriptomic responses of whole larvae and adults during and following exposure to -5°C were largely unique both in identity of responding transcripts and in temporal dynamics. Further, we analyzed the tissue-specificity of differentially expressed transcripts from FlyAtlas 2 data, and concluded that stage-specific differences in transcription were not simply driven by differences in tissue composition. In addition, RNAi of target genes resulted in largely stage-specific and sometimes sex-specific effects on cold tolerance. The combined evidence suggests that thermal physiology is largely stage-specific at the level of gene expression, and thus natural selection may be acting on different loci during the independent thermal adaptation of different life stages.

Effects of developmental stage, cold acclimation and diet on the cold tolerance of three species of Cryptolestes (Coleoptera: Laemophloeidae)

Flat grain beetles (Coleoptera: Laemophloeidae) are common stored-product insect pests in Canada, infesting cereals in grain bins, equipment and end products in flour mills. We studied the cold tolerance of the three most common flat grain beetles: Cryptolestes ferrugineus, Cryptolestes turcicus and Cryptolestes pusillus, by measuring the survival at −10 °C and supercooling point (SCP) for different life stages (egg, young larva, old larva, pupa and adult) reared on flour mixed with brewer’s yeast. Probit analysis was used to estimate the lethal time for 50 and 95% mortality. This was done with non-acclimated individuals (only held at 30 °C) or cold-acclimated individuals (held at 18, 10 and 5 °C, for 1 week/temperature). In general, adults were the most cold-hardy stage for each of the species. Acclimated insects were anywhere from no increase in cold tolerance to 14-fold more cold-tolerant than the corresponding non-acclimated stage and species. Cryptolestes ferrugineus was most cold-tolerant species (58 d at −10 °C to reach 95% mortality for acclimated adult), C. turcicus was the next most cold-tolerant, (39 d) and C. pusillus was the least cold-tolerant (11 d). The cold tolerance of adults reared on three diets was measured both for acclimated and non-acclimated insects. The adults reared on grain diet (whole wheat kernels, cracked wheat kernels and wheat germ (90:5:5 mass ratio) were the most cold-tolerant, adults reared on white-wheat flour and brewer’s yeast diet (95:5 mass ratio) had the next highest cold tolerance followed by the adults reared on 100% white-wheat flour. Supercooling point (SCP) of insects ranged from −20.6 to −26.7 °C. In general, acclimated insects had slightly lower SCP than non-acclimated insects.

Larval foraging decisions in competitive heterogeneous environments accommodate diets that support egg-to-adult development in a polyphagous fly.

In holometabolous insects, larval nutrition is a key factor underpinning development and fitness. Heterogeneity in the nutritional environment and larval competition can force larvae to forage in suboptimal diets, with potential downstream fitness effects. Little is known about how larvae respond to competitive heterogeneous environments, and whether variation in these responses affects current and next generations. Here, we designed nutritionally heterogeneous foraging arenas by modifying nutrient concentration, where groups of the polyphagous fruit fly Bactrocera tryoni could forage freely at various levels of larval competition. Larval foraging preferences were highly consistent and independent of larval competition, with greatest foraging propensity for high (100%) followed by intermediate (80% and 60%) nutrient concentration diets, and avoidance of lower concentration diets (less than 60%). We then used these larval preferences (i.e. 100%, 80% and 60% diets) in fitness assays in which larvae competition was maintained constant, and showed that nutrient concentrations selected by the larvae in the foraging trials had no effect on fitness-related traits such as egg hatching and pupation success, adult flight ability, sex ratio, percentage of emergence, nor on adult cold tolerance, fecundity and next-generation pupal weight. These results support the idea that polyphagous species can exploit diverse hosts and nutritional conditions with minimal fitness costs to thrive in new environments.

Environmental and genetic control of cold tolerance in the Glanville fritillary butterfly.

Thermal tolerance has a major effect on individual fitness and species distributions and can be determined by genetic variation and phenotypic plasticity. We investigate the effects of developmental and adult thermal conditions on cold tolerance, measured as chill coma recovery (CCR) time, during the early and late adult stage in the Glanville fritillary butterfly. We also investigate the genetic basis of cold tolerance by associating CCR variation with polymorphisms in candidate genes that have a known role in insect physiology. Our results demonstrate that a cooler developmental temperature leads to reduced cold tolerance in the early adult stage, whereas cooler conditions during the adult stage lead to increased cold tolerance. This suggests that adult acclimation, but not developmental plasticity, of adult cold tolerance is adaptive. This could be explained by the ecological conditions the Glanville fritillary experiences in the field, where temperature during early summer, but not spring, is predictive of thermal conditions during the butterfly's flight season. In addition, an amino acid polymorphism (Ala‐Glu) in the gene flightin, which has a known function in insect flight and locomotion, was associated with CCR. These amino acids have distinct biochemical properties and may thus affect protein function and/or structure. To our knowledge, our study is the first to link genetic variation in flightin to cold tolerance, or thermal adaptation in general.

Sex‐dependent thermal history influences cold tolerance, longevity and fecundity in false codling moth Thaumatotibia leucotreta (Lepidoptera: Tortricidae)

Abstract Environmental temperature plays a critical role in the field performance of mass‐reared insects. For sterile insect technique programmes, the influence of larval (developmental) temperature variation on subsequent adult field performance is generally poorly understood but may be a significant avenue for increasing efficacy. In the present study, we investigated the influence of larval thermal acclimation on several traits of adult performance in the false codling moth Thaumatotibia leucotreta (Meyrick). After larvae were reared at 15, 20 or 25 °C for their full larval developmental period, we determined the effect of different acute (2 h) temperature treatments (10, 15 or 20 °C) during the adult stage on traits of (i) cold tolerance; (ii) fecundity; and (iii) longevity. Cold tolerance of adults was not influenced by larval acclimation temperature but was affected by sex and adult treatment temperature. Adult fecundity and longevity were affected by larval acclimation temperature, adult treatment temperature and the interaction of these factors with sex. These results suggest a complex, sex‐dependent interplay of short‐ and longer‐ term temperature history across developmental stages for these traits. Exploring the field impacts of this trait variation is essential, coupled with information on how these traits might respond to artificial manipulation.

Diapause and winter survival of two Orius species from southern Africa

The cold hardiness and overwintering potential of the southern African pirate bugs, Orius thripoborus (Hesse) and Orius naivashae (Poppius) (Hemiptera: Anthocoridae), were assessed in the laboratory. Diapause traits were studied by observing nymphal development and reproductive performance of adults at 18 °C and three photoperiods (10:14, 12:12 and 14:10 (L:D) h). A 12 h light regime was also tested at 23 °C. A 12 h photoperiod and 18 °C induced reproductive diapause in 84 and 42 % of O. naivashae and O. thripoborus females, respectively. Cold tolerance of adults was measured by determining the supercooling point (SCP, the temperature at which the insect’s body fluids freeze) and lethal time (LT50, the time required to kill 50 % of the population) at 0 and 5 °C. All observed SCPs ranged from −21 to −17 °C. Significantly lower SCP values were observed for acclimated (seven days at 10 °C) O. naivashae females. LT50-values averaged 6.4 and 4.4 days at 0 °C and 11.6 and 7.8 days at 5 °C, for adults of O. thripoborus and O. naivashae, respectively. The findings indicate that O. naivashae is less cold tolerant and has a higher diapause incidence compared with O. thripoborus. Therefore, the latter species may have better potential for use in biological control programmes in the cooler regions of southern Africa or elsewhere.

Proteomic data reveal a physiological basis for costs and benefits associated with thermal acclimation.

Physiological adaptation through acclimation is one way to cope with temperature changes. Biochemical studies on acclimation responses in ectotherms have so far mainly investigated consequences of short-term acclimation at the adult stage and focussed on adaptive responses. Here, we assessed the consequences of rearing Drosophila melanogasterat low (12°C), benign (25°C) and high (31°C) temperatures. We assessed cold and heat tolerance and obtained detailed proteomic profiles of flies from the three temperatures. The proteomic profiles provided a holistic understanding of the underlying biology associated with both adaptive and non-adaptive temperature responses. Results show strong benefits and costs across tolerances: rearing at low temperature increased adult cold tolerance and decreased adult heat tolerance and vice versa with development at high temperatures. In the proteomic analysis, we were able to identify and quantify a large number of proteins compared with previous studies on ectotherms (1440 proteins across all replicates and rearing regimes), enabling us to extend the proteomic approach using enrichment analyses. This gave us detailed information on individual proteins, as well as pathways affected by rearing temperature, pinpointing potential mechanisms responsible for the strong costs and benefits of rearing temperature on functional phenotypes. Several well-known heat shock proteins, as well as proteins not previously associated with thermal stress, were among the differentially expressed proteins. Upregulation of proteasome proteins was found to be an important adaptive process at high-stress rearing temperatures, and occurs at the expense of downregulation of basal metabolic functions.

Cold hardiness of the biological control agent, Agasicles hygrophila, and implications for its potential distribution

The physiological adaptations of biological control agents may determine where and when they will be successful. Agasicles hygrophila Selman & Vogt, has been introduced into China for biological control of an invasive weed, Alternanthera philoxeroides (Mart.) Griseb. The extent to which A. hygrophila can withstand low temperatures was tested to determine whether this physiological trait can be used to predict its potential distribution and effectiveness as a biological control agent. Our results showed that A. hygrophila eggs, larvae, pupae and adults had similar super cooling point temperatures (SCPs) which were not affected by acclimatization. Mortality increased with decreasing temperatures and with length of exposure to low temperatures. SCP was the limiting survival temperature, and chilling injury was one of the main causes of death. The upper limit of chill injury zone (ULCIZ) was 6.7°C and the sum of injurious temperature (SIT) was about 15.0degree days. Based on adult cold tolerance, the distribution of A. hygrophila in China is unlikely to extend beyond areas that experience temperatures at or below −8°C, and the flea beetles will probably overwinter successfully only in areas where the annual minimum air temperature remains above 6.7°C. These predictions were compared with known distribution data and seem to be a reliable and economical method to predict effectiveness of potential of biological control agents in regions with extreme climates.

Sensitivity to thermal extremes in AustralianDrosophilaimplies similar impacts of climate change on the distribution of widespread and tropical species

Climatic factors influence the distribution of ectotherms, raising the possibility that distributions of many species will shift rapidly under climate change and/or that species will become locally extinct. Recent studies have compared performance curves of species from different climate zones and suggested that tropical species may be more susceptible to climate change than those from temperate environments. However, in other comparisons involving responses to thermal extremes it has been suggested that mid-latitude populations are more susceptible. Using a group of 10 closely related Drosophila species with known tropical or widespread distribution, we undertake a detailed investigation of their growth performance curves and their tolerance to thermal extremes. Thermal sensitivity of life history traits (fecundity, developmental success, and developmental time) and adult heat resistance were similar in tropical and widespread species groups, while widespread species had higher adult cold tolerance under all acclimation regimes. Laboratory measurements of either population growth capacity or acute tolerance to heat and cold extremes were compared to daily air temperature under current (2002-2007) and future (2100) conditions to investigate if these traits could explain current distributions and, therefore, also forecast future effects of climate change. Life history traits examining the thermal sensitivity of population growth proved to be a poor predictor of current species distributions. In contrast, we validate that adult tolerance to thermal extremes provides a good correlate of current distributions. Thus, in their current distribution range, most of the examined species experience heat exposure close to, but rarely above, the functional heat resistance limit. Similarly, adult functional cold resistance proved a good predictor of species distribution in cooler climates. When using the species' functional tolerance limits under a global warming scenario, we find that both tropical and widespread Drosophila species will face a similar proportional reduction in distribution range under future warming.

Does selection on increased cold tolerance in the adult stage confer resistance throughout development?

Artificial selection is a powerful approach to unravel constraints on genetic adaptation. Although it has been frequently used to reveal genetic trade-offs among different fitness-related traits, only a few studies have targeted genetic correlations across developmental stages. Here, we test whether selection on increased cold tolerance in the adult stage increases cold resistance throughout ontogeny in the butterfly Bicyclus anynana. We used lines selected for decreased chill-coma recovery time and corresponding controls, which had originally been set up from three levels of inbreeding (outbred control, one or two full-sib matings). Four generations after having terminated selection, a response to selection was found in 1-day-old butterflies (the age at which selection took place). Older adults showed a very similar although weaker response. Nevertheless, cold resistance did not increase in either egg, larval or pupal stage in the selection lines but was even lower compared to control lines for eggs and young larvae. These findings suggest a cost of increased adult cold tolerance, presumably reducing resource availability for offspring provisioning and thereby stress tolerance during development, which may substantially affect evolutionary trajectories.

Low temperature survival of post-eclosion stages of the potato rot nematode <i>Ditylenchus destructor</i> Thorne (Tylenchida: Anguinidae)

AbstractThe potato rot nematode, Ditylenchus destructor, may experience extreme environmental stress caused by freezing temperatures when overwintering in the field. A series of laboratory experiments were conducted in order to clarify overwintering strategies of the nematode. The current study aimed to examine the cold tolerance of this species in various aqueous environments as well as in plant tissues in order to determine its ability to survive 24 h exposure to subzero temperatures. Cold tolerance of adults and fourth-stage juveniles was significantly lower than that of younger juveniles. The lower lethal temperature of adults was –15°C. Although external ice formation affects all life stages, a few second-stage juveniles were able to survive temperatures as low as –30°C. The results expand the current understanding of freezing survival in the potato rot nematode and will lead to better comprehension of its ability to withstand subzero temperature conditions.

Effects of methoprene on extreme temperature tolerance and reproduction of Tribolium castaneum (Coleoptera: Tenebrionidae)

The juvenile hormone analogue methoprene is a reduced-risk insecticide. It disrupts insect development of immature stages preventing the emergence of adults. Several studies have shown that lower concentrations that permit the emergence of adults also have sub-lethal effects. Exposure to methoprene (Diacon II) at 3.33 ppm reduced the heat tolerance of Tribolium castaneum (Herbst) adults. However, it did not affect the heat tolerance of larvae at 0.07 ppm. Higher concentrations of methoprene were lethal to larvae without heat treatment. Methoprene (67 ppm) had no effect on the cold tolerance of adults. Furthermore, methoprene (0.03 ppm) did not alter cold tolerance of larvae. Exposure to 15°C for 2 weeks increased the cold tolerance of adults from 4 d to 7 d, and larvae 3 d to 5 d; however, methoprene concentrations had no effect on cold tolerance. Tribolium castaneum larvae exposed to methoprene (0.001 ppm) had lower fecundity as adults. Males were more affected than females in reducing the offspring when paired with untreated mates. These results show the potential of methoprene as an emerging insecticide and a viable alternative to currently used synthetic insecticides. The data on the effect of methoprene on extreme temperature tolerance of T. castaneum have been submitted to the Journal of Stored Products Research. Keywords : Methoprene, Extreme temperature tolerance, Reproduction, Larvae, Adults

Effect of methoprene on the heat tolerance and cold tolerance of Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae)

Methoprene, a Juvenile Hormone analogue, was evaluated for its ability to alter heat tolerance or cold tolerance of Tribolium castaneum, the red flour beetle. Young adults and late instar larvae were exposed to a series of methoprene concentrations. They were held either at 46 °C or 0 °C for different durations, and survival of adults or the adult emergence from larvae was recorded to determine their tolerance to extreme temperatures. At 46 °C, the lethal time to kill 50% of the population (confidence intervals) for untreated adults was 10.8 (9.6–11.8) h compared to 9.3 (8.3–10.0) h for adults exposed to 3.33 ppm of methoprene for 48 h. Higher concentrations of methoprene also caused adults to be less heat tolerant. In contrast, there was no evidence that methoprene reduced the heat tolerance of larvae. At 0 °C, both unacclimated and cold-acclimated insects were tested. Methoprene did not affect the cold tolerance of adults or larvae, regardless of cold acclimation. As seen in other studies, methoprene was not toxic to adults even at 66.6 ppm, but it was highly toxic to larvae (LD 50 0.015 to 0.020 ppm). Cold tolerance was slightly greater in both adults and larvae, after being held at 15 °C for two weeks. This is the first study to report that a Juvenile Hormone analogue has an impact on insect heat tolerance.

Genetic and physiological variation among sexual and parthenogenetic populations of Asobara japonica (Hymenoptera: Braconidae), a larval parasitoid of drosophilid flies

We studied variations in genetic, physiological, and ecological traits, and the phylogenetic relationship among sexual and parthenogenetic populations of Asobara japonica, a larval parasitoid of drosophilid flies, in order to understand how they adapt to local environments and have differentiated. The strain from Iriomote-jima (IR) differed from other Japanese strains in the nucleotide sequences of its cytochrome oxidase subunit I (COI) and in not undergoing diapause and having a shorter preimaginal period and a higher adult tolerance of cold. The strains other than IR showed a low level of nucleotide variation in COI but varied in their mode of reproduction; the strains from the Ryukyu Islands were sexual, whereas those from the main islands of Japan and Ogasawara were parthenogenetic. In addition, strains from higher latitudes generally showed a high incidence of diapause, although there were some exceptions. On the other hand, preimaginal period and adult cold tolerance varied little among the strains excluding IR, and pupal cold tolerance, oviposition preference and incidence of parasitism varied little among the strains including IR. Evolution and environmental adaptations in this species are discussed, particularly focusing on parthenogenetic populations.

EVOLUTION OF THERMOTOLERANCE IN SEASONAL ENVIRONMENTS: THE EFFECTS OF ANNUAL TEMPERATURE VARIATION AND LIFE-HISTORY TIMING IN WYEOMYIA SMITHII

In organisms with complex life cycles, the adaptive value of thermotolerance depends on life-history timing and seasonal temperature profiles. We illustrate this concept by examining variation in annual thermal environments and thermal acclimation among four geographic populations of the pitcher plant mosquito. Only diapausing larvae experience winter, whereas both postdiapause and nondiapause adults occur only during the growing season. Thus, adults experience transient cold stress primarily during the spring. We show that adult cold tolerance (chill coma recovery) is enhanced in spring-like conditions via thermal acclimation but is unaffected by diapause state. Moreover, adult mosquitoes from northern populations were more cold tolerant than those from southern populations largely because acclimation responses were steeper in the north. In contrast to cold tolerance, there was no significant acclimation of heat tolerance (heat knockdown), and no significant differences in heat tolerance between northern and southern populations. Field temperature data show that because of evolved differences in diapause timing, adult exposure to cold stress is remarkably consistent across geography. This suggests that geographic variation in cold tolerance may not be the result of direct selection on adults. Our results illustrate the importance of the interplay between phenological and thermal adaptation for understanding variation along climatic gradients.

Life history adaptations and stress tolerance of four domestic species of Drosophila

AbstractLife history traits and stress tolerance were studied in four domestic species of Drosophila–D. melanogaster, D. simulans, D. auraria and D. immigrans– to understand how they adapt to their environments. In all species, larval weight approximately doubled in 1 day. The relative egg weight (egg weight : pupal weight) was smaller and the larval period was longer in D. immigrans than in the other three species. The pupal period was the longest in D. auraria. However, the adaptive significance of these differences in larval and pupal periods was not clear. The pupal case was generally thicker in the larger species, probably to support the larger pupal body. The start of oviposition was earliest and reproductive effort was greatest in female D. simulans, followed by female D. melanogaster. In contrast, starvation tolerance and the increase in bodyweight after eclosion was greater in D. immigrans and D. auraria than in the other two species. Pupal desiccation tolerance was greatest in D. melanogaster and lowest in D. auraria, and the less tolerant species seemed to select more humid sites for pupation. Adult tolerance to desiccation was greatest in D. melanogaster and lowest in D. simulans. In contrast, adult cold tolerance was greater in D. auraria and adult heat tolerance was lower in D. immigrans than in the other species. These differences in life history traits and stress tolerance represent the Drosophila species differential adaptations, and are assumed to allow coexistence of the species.

Role of Cold Tolerance in the Seasonal Life History ofBathyplectes curculionis(Hymenoptera: Ichneumonidae) in the Southern Great Plains

Emergence patterns and cold tolerance of adult Bathyplectes curculionis (Thomson) were studied in relation to weather conditions that are typical during fall and winter in the Southern Great Plains. Laboratory studies were conducted to confirm that daylength and environmental temperatures prevailing during fall and winter are conducive to termination of diapause, pupal development, and emergence of B. curculionis adults. Mean Julian dates for first detection of the parasite in larvae of Hypera postica (Gyllenhal) were 69 and 72 for two field research sites in Oklahoma. These dates indicate that adults of B. curculionis emerge during winter and are frequently subjected to freezing temperatures as they begin parasitizing the first larvae of H. postica to infest alfalfa, Medicago sativa L., each year. Both laboratory and field studies demonstrate that >80% of adult parasites can survive repeated exposures to daily low temperatures ranging from 0 to −9°C. This level of cold tolerance indicates that the adults can survive during February and March when mean low temperatures are −1 and 3°C, respectively, in central Oklahoma. Although some adults of B. curculionis do emerge during fall and winter in the Southern Great Plains when there are no hosts available, this potential disadvantage to effective biological control is offset somewhat by the cold tolerance of adults, which allows survival during late winter and spring when they parasitize the first larvae of H. postica to infest alfalfa annually.

The Effect of Exercise Training on Cold Tolerance in Adult and Old C57BL/6J Mice

In order to ascertain the effect of aging on cross-adaptation between exercise training and cold tolerance, we studied cold tolerance in adult and old C57BL/6J male mice before and after 6 weeks of an exercise regimen of moderate intensity. There were two age groups of 32 mice each, including 12-month-old (adult) and 24-month-old (aged) mice equally divided into control and exercise groups. The exercise consisted of daily runs on a treadmill (1 hr/day, 5 days/week) for 6 weeks, while the control mice spent the same time on a stationary treadmill. All mice were subjected to a cold stress test (3-hr partial restraint at 6 degrees C) prior to and following the designated regimen. The results revealed a statistically significant interaction between age and exercise training. In adult mice, exercise resulted in a reduction of cold-induced heat production and weakening of cold tolerance, while in aged mice, the opposite effect was observed; i.e., an increase in cold-induced heat production accompanied by greater cold tolerance. However, only the attenuating effect on cold tolerance of adults was statistically significant. The results of our experiments do not support the existence of cross-adaptation between exercise training and cold tolerance. They indicate, however, that exercise training affects the cold tolerance in adult and old mice through different physiological mechanisms.

Cold Tolerance of Adults and Pupae of the Face Fly1

Journal Article Cold Tolerance of Adults and Pupae of the Face Fly Get access N. O. Morgan, N. O. Morgan Entomology Research Division, Agr. Res. Serv., USDA, Beltsville, Maryland Search for other works by this author on: Oxford Academic PubMed Google Scholar L. G. Pickens L. G. Pickens Entomology Research Division, Agr. Res. Serv., USDA, Beltsville, Maryland Search for other works by this author on: Oxford Academic PubMed Google Scholar Journal of Economic Entomology, Volume 60, Issue 5, 1 October 1967, Pages 1464–1466, https://doi.org/10.1093/jee/60.5.1464 Published: 01 October 1967 Article history Accepted: 07 June 1967 Published: 01 October 1967