Heat alters diverse thermal tolerance mechanisms: an organismal framework for studying climate change effects in a wild bird
Data files
Oct 25, 2024 version files 129.38 KB
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README.md
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Woodruff_By_Individual.csv
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Woodruff_By_Nest.csv
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Woodruff_iButton_Data.csv
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Abstract
The ability to cope with heat is likely to influence species success amidst climate change. However, heat coping mechanisms are poorly understood in wild endotherms, which are increasingly pushed to their thermoregulatory limits.
We take an organismal approach to this problem, unveiling how behavioral and physiological responses may allow success in the face of sublethal heat. We experimentally elevated nest temperatures for four hours to mimic a future climate scenario (+4.5°C) during a critical period of post-natal development in tree swallows (Tachycineta bicolor).
Heat-exposed nestlings exhibited marked changes in behavior, including movement to cooler microclimates in the nest. They panted more and weighed less than controls at the end of the four-hour heat challenge, suggesting panting-induced water loss. Physiologically, heat induced high levels of heat shock protein (HSP) gene expression in the blood, alongside widespread transcriptional differences related to antioxidant defenses, inflammation, and apoptosis.
Critically, all nestlings survived the heat challenge, and those exposed to milder heat were more likely to recruit into the breeding population. Early-life but sub-lethal heat may therefore act as a selective event, with the potential to shape population trajectories.
Within the population, individuals varied in their physiological response to heat, namely in HSP gene expression, which exhibited higher mean and higher variance in heat-exposed nestlings than in controls. Heat-induced HSP levels were unrelated to individual body mass, or among-nest differences in brood size, temperature, and behavioral thermoregulation. Nest identity explained a significant amount of HSP variation, yet siblings in the same nest differed by an average of ~4-fold, and individuals in the population differed by as much as ~100-fold in their HSP response. This massive variation extends previous laboratory work in model organisms showing that heat shock proteins may harbor cryptic phenotypic variation.
These results shed light on oft-ignored elements of thermotolerance in wild birds at a critical stage of post-natal development. By highlighting the scope of heat-induced HSP gene expression and coupling it with a suite of organismal traits, we provide a framework for future testing of the mechanisms that shape species success in the face of change.
Mary J. Woodruff1,2, Susanna N. Tsueda1,2, Tiernan S. Cutrell1,2, Ethan A. Guardado1,2,3, Douglas B. Rusch4, Aaron Buechlein4, Kimberly A. Rosvall1,2
1Biology, Indiana University, Bloomington, IN, USA; 2Center for Integrative Study of Animal Behavior, Indiana University, Bloomington, IN, USA; 3Biology, Purdue University, West Lafayette, IN, USA; 4Center for Genomics and Bioinformatics, Indiana University, Bloomington, IN, USA
File: By_Individual.csv
Nestling data quantified at the individual level. Missing values are indicated by “NA.”
Column Name | Description |
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Nest_ID | ID of nest box |
Nestling_ID | Individual ID from USGS band number, or for terminally collected individuals the nest ID and “EUTH” to indicate “euthanized” |
Brood_Size | Number of nestlings in the nest |
Nesting_Sex | Sex of terminally collected nestlings. All others unknown sex |
Treatment | Experimental treatment |
Date | Date the experiment occurred (12 days post-hatch) |
Time_Start | Time experiment began (packs in nest) |
Time_End | Time experiment ended (nestlings out of nest for sampling) |
D12_Mass | 12 days-post-hatch nestling body mass in grams |
D12_Wing_Length | 12 days-post-hatch nestling wing length in millimeters |
Euth (Y/N) | Yes (Y) or no (N) indicating if an individual was euthanized for tissue collection |
Fledge (Y/N) | Yes (Y) or no (N) indicating if an individual successfully fledged. NAs indicate individuals that were terminally collected or predated before fledging (NA (predated on D13)). |
Recruit (Y/N) | Yes (Y) or no (N) indicating if an individual recruited into the breeding population in the subsequent two years. NAs indicate individuals that were terminally collected, predated before fledging, or did not fledge. |
Rq_BL_HSP90AA1 | Blood relative gene expression of HSP90AA1 (2-∆ct) |
Rq_HPC_HSP90AA1 | Hippocampus relative gene expression of HSP90AA1 (2-∆ct) |
Rq_PM_HSP90AA1 | Pectoral Muscle relative gene expression of HSP90AA1 (2-∆ct) |
Log2_Rq_BL_HSP90AA1 | Log2 transformed blood relative gene expression of HSP90AA1 (2-∆ct) |
Log2_Rq_HPC_HSP90AA1 | Log2 transformed hippocampus relative gene expression of HSP90AA1 (2-∆ct) |
Log2_Rq_PM_HSP90AA1 | Log2 transformed pectoral Muscle relative gene expression of HSP90AA1 (2-∆ct) |
File: Woodruff_By_Nest.csv
Nestling behavior, parental behavior, and environmental measures quantified at the nest level. Missing values are indicated by “NA.”
Column Name | Description |
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Nest_ID | ID of nest box |
Treatment | Experimental treatment |
Date | Date the experiment occurred (12 days post-hatch) |
Brood_Size | Number of nestlings in the nest |
Mean_#_nestlings_visible | Mean number of nestlings visible to the camera |
Total_time_bins_panting | Total number of 5-second time bins with nestling panting |
Panting_min | Total number of 5-second time bins panting converted into minutes |
Total_time_bins_head-out-box-hole | Total number of 5-second time bins with nestling head-out-box-hole |
Head-out-box-hole_min | Total number of 5-second time bins head-out-box-hole converted into minutes |
Total_parental_feeds | Total number of parental feeds during the 1hr observation |
Mean_Begging_Intensity | Mean begging intensity, averaged across feeds (0-4 scale; see manuscript supplemental information for details) |
Mean_Prop_Beg | Mean proportion of nestlings begging, averaged across feeds |
Mean_Rq_HSP90AA1_BL | D12 blood relative telomere length (2-∆ct) |
Mean_nest_temp_C | Mean nest temperature during the experiment (iButton data). degrees Celsius. |
Mean_ambient_temp_C | Mean ambient temperature during the experiment (NOAA data). degrees Celsius. |
File: Woodruff_iButton_Data.csv
Nest and ambient temperature and relative humidity measures. Each row represents one nest temperature/relative humidity measure. Missing values are indicated by “NA.”
Column Name | Description |
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Nest_ID | ID of nest box |
Treatment | Experimental treatment group |
Brood_Size | Number of nestlings in the nest |
Date/Time | Date and time (24-hour clock) nest environment was measured |
#10min_recordings_since_exp_start | Number of 10-minute ibutton recordings since the start of the experiment. Negative numbers represent measures that occurred before the start of the experiment |
Pre-exp/Exp | PRE = pre-experiment, EXP = during the experiment |
Nest_%RH | Percent relative humidity inside the nest box |
Nest_Temp_C | Temperature (degrees Celsius) inside the nest box |
Ambient_Hrly_Temp_C | Air temperature (dry bulb, degrees Celsius) from a nearby NOAA weather station. Temperature was measured hourly, so values are repeated for each row that occurred within a given hour |
Ambient_Hrly_%RH | Percent relative humidity from a nearby NOAA weather station. Relative humidity was measured hourly, so values are repeated for each row that occurred within an hour |