Costs of cold acclimation on survival and reproductive behavior in Drosophila melanogaster

Everman, Elizabeth R.; Delzeit, Jennifer; Hunter, F. Kate; Gleason, Jennifer M.; Morgan, Theodore J.

doi:10.1371/journal.pone.0197822

Cited by 20 publications

(18 citation statements)

References 66 publications

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“…Thus, whether the correlation structure of our dataset would hold true for winteracclimated flies is uncertain. Plastic changes in cold tolerance are well documented in insects (e.g., Rinehart et al 2000;Shreve et al 2004;Jakobs et al 2015;Sinclair et al 2015), and in D. melanogaster, gradual and/or rapid acclimation improves CCR and CT min (Garcia and Teets 2019), cold stress survival (Colinet and Hoffmann 2012;Everman et al 2018;Gerken et al 2018), fecundity (Emerson et al 2009), and behavior (Shreve et al 2004;Garcia and Teet 2019). Recent work has indicated that correlations between CT min and measures of thermal plasticity within the DGRP depend on developmental temperature (Ørsted et al 2019).…”

Section: Discussionmentioning

confidence: 99%

Distinct cold tolerance traits independently vary across genotypes inDrosophila melanogaster

et al. 2020

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Cold tolerance, the ability to cope with low temperature stress, is a critical adaptation in thermally variable environments. An individual's cold tolerance comprises several traits including minimum temperatures for growth and activity, ability to survive severe cold, and ability to resume normal function after cold subsides. Across species, these traits are correlated, suggesting they were shaped by shared evolutionary processes or possibly share physiological mechanisms. However, the extent to which cold tolerance traits and their associated mechanisms covary within populations has not been assessed. We measured five cold tolerance traits—critical thermal minimum, chill coma recovery, short‐ and long‐term cold tolerance, and cold‐induced changes in locomotor behavior—along with cold‐induced expression of two genes with possible roles in cold tolerance (heat shock protein 70 and frost)—across 12 lines of Drosophila melanogaster derived from a single population. We observed significant genetic variation in all traits, but few were correlated across genotypes, and these correlations were sex‐specific. Further, cold‐induced gene expression varied by genotype, but there was no evidence supporting our hypothesis that cold‐hardy lines would have either higher baseline expression or induction of stress genes. These results suggest cold tolerance traits possess unique mechanisms and have the capacity to evolve independently.

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Section: Discussionmentioning

confidence: 99%

Distinct cold tolerance traits independently vary across genotypes inDrosophila melanogaster

et al. 2020

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“…Collectively, these responses permit maintenance of neuronal homeostasis under cold stress (Armstrong, Rodríguez, & Robertson, ) and reduce apoptosis following cold injury (Yi, Moore, & Lee, ). However, cold hardening also carries costs in terms of future reproductive output (Everman, Delzeit, Hunter, Gleason, & Morgan, ; Overgaard et al, ), suggesting that avoiding cold hardening could be beneficial if temperatures never drop to lethally cold. Individual D. melanogaster genotypes vary in their cold hardening response (Gerken, Eller, Hahn, & Morgan, ; Gerken, Eller‐Smith, & Morgan, ); therefore, different cold hardening abilities may be advantageous under different conditions.…”

Section: Introductionmentioning

confidence: 99%

Phenotypic plasticity, but not adaptive tracking, underlies seasonal variation in post‐cold hardening freeze tolerance of Drosophila melanogaster

Stone

Erickson

Bergland

2019

Ecology and Evolution

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In temperate regions, an organism's ability to rapidly adapt to seasonally varying environments is essential for its survival. In response to seasonal changes in selection pressure caused by variation in temperature, humidity, and food availability, some organisms exhibit plastic changes in phenotype. In other cases, seasonal variation in selection pressure can rapidly increase the frequency of genotypes that offer survival or reproductive advantages under the current conditions. Little is known about the relative influences of plastic and genetic changes in short-lived organisms experiencing seasonal environmental fluctuations. Cold hardening is a seasonally relevant plastic response in which exposure to cool, but nonlethal, temperatures significantly increases the organism's ability to later survive at freezing temperatures. In the present study, we demonstrate seasonal variation in cold hardening in Drosophila melanogaster and test the extent to which plasticity and adaptive tracking underlie that seasonal variation. We measured the post-cold hardening freeze tolerance of flies from outdoor mesocosms over the summer, fall, and winter. We bred outdoor mesocosm-caught flies for two generations in the laboratory and matched each outdoor cohort to an indoor control cohort of similar genetic background. We cold hardened all flies under controlled laboratory conditions and then measured their post-cold hardening freeze tolerance. Comparing indoor and field-caught flies and their laboratory-reared G1 and G2 progeny allowed us to determine the roles of seasonal environmental plasticity, parental effects, and genetic changes on cold hardening.We also tested the relationship between cold hardening and other factors, including age, developmental density, food substrate, presence of antimicrobials, and supplementation with live yeast. We found strong plastic responses to a variety of fieldand laboratory-based environmental effects, but no evidence of seasonally varying parental or genetic effects on cold hardening. We therefore conclude that seasonal variation in post-cold hardening freeze tolerance results from environmental influences and not genetic changes.How to cite this article: Stone HM, Erickson PA, Bergland AO. Phenotypic plasticity, but not adaptive tracking, underlies seasonal variation in post-cold hardening freeze tolerance of Drosophila melanogaster.

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“…constant temperature, fast ramp and slow ramp) is correlated, suggesting that all three types of RCH share similar underlying mechanisms (Gerken et al, 2018). Yet, the sublethal costs of hardening on courtship and reproduction are similar across genotypes and unrelated to hardening capacity (Everman et al, 2018), indicating that behavioral responses to hardening are independent of thermal tolerance. Furthermore, the persistence of RCH after rewarming is not genetically variable, and in most genotypes the protection afforded by RCH lasts for 2 h after returning flies to 25°C (Everman et al, 2017).…”

Section: Evolutionary Genetics Of Rchmentioning

confidence: 98%

“…In D. melanogaster, adults coldhardened by slow cooling experience a slight but significant increase in mortality, as well as reduced fecundity during the 8 h period after the treatment, compared with those maintained at the rearing temperature (Overgaard et al, 2007). Chilling at 4°C for 2 h also decreases mating effectiveness in males, indicated by the increased duration of courtship and decreased rates of copulation (Everman et al, 2018). Finally, in the Mediterranean fruit fly Ceratitis capitata, repeated daily inductions of RCH by slow cooling increase mortality after 5 days (Basson et al, 2012).…”

Section: Potential Costs Associated With Rchmentioning

confidence: 99%

Rapid cold hardening: ecological relevance, physiological mechanisms and new perspectives

Teets

Gantz

Kawarasaki

2020

Journal of Experimental Biology

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Rapid cold hardening (RCH) is a type of phenotypic plasticity that allows ectotherms to quickly enhance cold tolerance in response to brief chilling (lasting minutes to hours). In this Review, we summarize the current state of knowledge of this important phenotype and provide new directions for research. As one of the fastest adaptive responses to temperature known, RCH allows ectotherms to cope with sudden cold snaps and to optimize their performance during diurnal cooling cycles. RCH and similar phenotypes have been observed across a diversity of ectotherms, including crustaceans, terrestrial arthropods, amphibians, reptiles, and fish. In addition to its well-defined role in enhancing survival to extreme cold, RCH also protects against nonlethal cold injury by preserving essential functions following cold stress, such as locomotion, reproduction, and energy balance. The capacity for RCH varies across species and across genotypes of the same species, indicating that RCH can be shaped by selection and is likely favored in thermally variable environments. Mechanistically, RCH is distinct from other rapid stress responses in that it typically does not involve synthesis of new gene products; rather, the existing cellular machinery regulates RCH through post-translational signaling mechanisms. However, the protective mechanisms that enhance cold hardiness are largely unknown. We provide evidence that RCH can be induced by multiple triggers in addition to low temperature, and that rapidly induced tolerance and cross-tolerance to a variety of environmental stressors may be a general feature of stress responses that requires further investigation.

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Costs of cold acclimation on survival and reproductive behavior in Drosophila melanogaster

Cited by 20 publications

References 66 publications

Distinct cold tolerance traits independently vary across genotypes inDrosophila melanogaster

Distinct cold tolerance traits independently vary across genotypes inDrosophila melanogaster

Phenotypic plasticity, but not adaptive tracking, underlies seasonal variation in post‐cold hardening freeze tolerance of Drosophila melanogaster

Rapid cold hardening: ecological relevance, physiological mechanisms and new perspectives

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