Heritable variation in thermal profiles is associated with reproductive success in the world’s largest bird
Data files
Oct 04, 2023 version files 382.45 KB
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README.md
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Thermal-Plasticity-Evolution.csv
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Abstract
Organisms inhabiting extreme thermal environments, such as desert birds, have evolved spectacular adaptations to thermoregulate during hot and cold conditions. However, our knowledge of selection for thermoregulation and the potential for evolutionary responses is limited, particularly for large organisms experiencing extreme temperature fluctuations. Here we use thermal imaging to quantify selection and genetic variation in thermoregulation in ostriches (Struthio camelus), the world’s largest bird species that is experiencing increasingly volatile temperatures. We found that females that are better at regulating their head temperatures (‘thermoregulatory capacity’) had higher egg-laying rates under hotter conditions. Thermoregulatory capacity was both heritable and showed signatures of local adaptation: females originating from more unpredictable climates were better at regulating their head temperatures in response to temperature fluctuations. Together these results reveal that past and present evolutionary processes have shaped genetic variation in thermoregulatory capacity, which appears to protect critical organs, such as the brain, from extreme temperatures during reproduction.
https://doi.org/10.5061/dryad.2ngf1vhw1
Data on head and neck surface temperatures of ostriches using thermal image cameras. For several years, we took repeated thermal images of individually marked ostriches in a pedigreed population at a research farm in the Western Cape Province in South Africa. We also recorded ambient temperatures at the time of each picture, allowing us to relate surface temperatures to ambient air temperatures.
From 2012 to 2017 during October to December, we took 2744 pictures of 423 females between 5 am and 6 pm (average number of images per female = 6.5). This dataset was designed to maximize the number of individuals with repeated measures across years, in order to characterize individual thermal profiles across different thermal environments. Consequently, there was little repeated sampling within days (8 % of the pictures).
Images of the ostriches in the enclosures were taken using an infrared thermography camera (H2640, NEC Avio Infrared Technologies; purchased from the company Senso-Test in Sweden). Pictures were taken in the field, usually from distances between 2 m and 25 m. We regularly calibrated the thermal camera against a black body during our field sessions, following the instructions from the camera supplier, which also provided regular recalibration services of our equipment.
Images that were out of focus were discarded prior to analysis, and we used the software InfRec Analyzer to draw separate polygons within the head and neck regions of the ostrich in each image. The average temperature of these polygons was extracted as individual head and neck surface temperatures, respectively. We used the same procedures and default software settings as in our previous work (Svensson & Waller, 2013; Svensson et al., 2020), which assumes an emissivity of 1.
Biological structures, such as bird skin and feathers, typically have emissivity values ranging between 0.94 -1.0 (Gerken et al., 2006; Yahav & Giloh, 2012). However, the exact emissivity value used does not change our results as we focused on relative temperature measures that are independent of emissivity values. Hourly air temperatures were measured at a weather station positioned 600 m from the study populations. We fitted a cubic spline to the hourly temperature estimates of each day using the R-package mgcv v.1.8 (Wood, 2004), from which we extracted the predicted air temperature at the time-points when thermal images were taken.
References
Gerken, M., Afnan, R. & Dörl, J. (2006) Adaptive behaviour in chickens in relation to thermoregulation. Poultry Science, 70, 199–207.
Svensson, E.I. & Waller, J.T. (2013) Ecology and sexual selection: evolution of wing pigmentation in calopterygid damselflies in relation to latitude, sexual dimorphism and speciation. American Naturalist, 182, E174–E195.
Svensson, E.I., Gomez-Llano, M.A. & Waller, J.T. (2020) Selection on phenotypic plasticity favors thermal canalization. Proceedings of the National Academy of Sciences of the United States of America, 117, 29767–29774.
Yahav, S. & Giloh, M. (2012) Infrared Thermography - Applications in Poultry Biological Research. In Infrared Thermography (ed. by Prakash, R.V.). InTech.
Wood, S.N. (2004) Stable and efficient multiple smoothing parameter estimation for generalized additive models. Journal of the American Statistical Association, 99, 673–686.
Description of the data and file structure
The dataset is a CSV file with individual ostrich records (thermal image information on a given date), with the following columns and variables:
- ID: a variable denoting individual ID (unique)
- animal: a variable denoting individual ID for the link to the pedigree (unique; identical to ID)
- sex: a categorical variable denoting if the individual was male or female (F) or male (M))
- date: date when the individual was photographed (format: DD/MM/YY)
- year: year when the individual was photographed (2012-2017; format 1Year)
- Pop: a categorical variable denoting which population the individual belongs to (ZB, SAB, Hybrid, KR)
- NeckTemp: neck temperature of the individual (measured in °C)
- HeadTemp: head temperature of the individual (measured in °C)
- Temp: ambient air temperature at the local weather station when the individual was photographed (measured in °C)
- Daytime: day-time when the picture was taken (continuous in hours)
- enclosure: a categorical variable denoting the enclosure where the individual was photographed
- TempCat: air temperature category used for character state models (factorial: Benign, Cold or Hot)
- TempDir: direction of air temperature change from optimum temperature (factorial: increasing or decreasing)
- TempCon: absolute air temperature change from optimum temperature. Values are standardized to be between 0 and 1.
- Direction: identical to TempDir but with different naming, increasing = hot and decreasing = cold
- Image: the thermal image from which the data was extracted
Detailed explanations for all these variables and how they are analyzed are given in our article and in our Supporting Material. ID and animal are identical and are unique to each individual; sex refers to if the animal was a male or female and year (2012-2017) is the year of measurement. Pop refers to population (3 categories), also called subspecies, from different parts of Africa. NeckTemp and HeadTemp refer to neck and head temperatures, respectively, whereas Temp refers to ambient (air) temperature at a nearby weather station, and enclosure refers to the specific fenced area where a given individual was when its thermal profile was recorded by us on a given day.
The remaining pedigree data used to support the findings of this study are available from the Western Cape Department of Agriculture in South Africa (WCDA). Restrictions apply to the use of some of these data, which are thus not publicly available. These data are however available from the WCDA upon reasonable request.
Sharing/Access information
Links to other publicly accessible locations of the data: https://osf.io/p94ce
Code/Software
We used the software InfRec Analyzer to draw separate polygons within the head and neck regions of the ostrich in each image and to obtain estimates of surface temperatures of the head and the neck.
For the analyses of individual thermal image data, we combined these individual thermal profiles with pedigree information, constructed and ran generalized linear mixed models (GLMMs) in R v.3.6.0 (R Core Team, 2020) using the Bayesian framework implemented in the R-package MCMCglmm v.2.29 (Hadfield, 2010). Code for analyses is available on Github: www.github.com/abumadsen/thermal-images-ostrich/tree/main
References
Hadfield, J.D. (2010) MCMC Methods for Multi-Response Generalized Linear Mixed Models: The MCMCglmm R Package. Journal of Statistical Software, 33, 1–22.
R Core Team. (2020) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria.
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General information and field setting
- Data on head and neck surface temperatures of ostriches. For several years, we took repeated thermal images of individually marked ostriches in a pedigreed population at a research farm in the Western Cape Province in South Africa. We also recorded ambient temperatures at the time of each picture, allowing us to relate surface temperatures to ambient air temperatures.
- Each year, from 2012 to 2017 and during October to December, we took 2744 pictures of 423 females between 5 am and 6 pm (average number of images per female = 6.5). This dataset was designed to maximize the number of individuals with repeated measures across years, in order to characterize individual thermal profiles across different thermal environments. Consequently, there was little repeated sampling within days (8 % of the pictures).