Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Species-specific effects of thermal stress on the expression of genetic variation across a diverse group of plant and animal taxa under experimental conditions

Abstract

Assessing the genetic adaptive potential of populations and species is essential for better understanding evolutionary processes. However, the expression of genetic variation may depend on environmental conditions, which may speed up or slow down evolutionary responses. Thus, the same selection pressure may lead to different responses. Against this background, we here investigate the effects of thermal stress on genetic variation, mainly under controlled laboratory conditions. We estimated additive genetic variance (VA), narrow-sense heritability (h2) and the coefficient of genetic variation (CVA) under both benign control and stressful thermal conditions. We included six species spanning a diverse range of plant and animal taxa, and a total of 25 morphological and life-history traits. Our results show that (1) thermal stress reduced fitness components, (2) the majority of traits showed significant genetic variation and that (3) thermal stress affected the expression of genetic variation (VA, h2 or CVA) in only one-third of the cases (25 of 75 analyses, mostly in one clonal species). Moreover, the effects were highly species-specific, with genetic variation increasing in 11 and decreasing in 14 cases under stress. Our results hence indicate that thermal stress does not generally affect the expression of genetic variation under laboratory conditions but, nevertheless, increases or decreases genetic variation in specific cases. Consequently, predicting the rate of genetic adaptation might not be generally complicated by environmental variation, but requires a careful case-by-case consideration.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Estimated heritabilities (h2 ± SE) for control (blue) and stress (red) treatment across species and traits.
Fig. 2: Effects of stress on heritability and the coefficient of genetic variation.

Data availability

All data used in our analyses are deposited in the Dryad Digital Repository (https://doi.org/10.5061/dryad.k0p2ngf60).

References

  1. Ågren J, Schemske DW (2012) Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range. New Phyt 194:1112–1122

    Google Scholar 

  2. Angilletta MJ, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509

    PubMed  Google Scholar 

  3. Appenroth KJ, Teller S, Horn M (1996) Photophysiology of turion formation and germination in Spirodela polyrhiza. Biologia Plantarum 38:95–106.

    Google Scholar 

  4. Atkinson D (1994) Temperature and organism size—a biological law for ectotherms? Adv Ecol Res 25:1–58

    Google Scholar 

  5. Barker JSF, Podger RN (1970) Interspecific competition between Drosophila melanogaster and Drosophila simulans: effects of larval density on viability and adult body size. Ecology 51:170–189

    Google Scholar 

  6. Barnosky A, Matzke N, Tomiya S, Wogan G, Swartz B, Quental T et al. (2011) Has the Earth’s sixth mass extinction already arrived? Nature 471:51–57

    CAS  PubMed  Google Scholar 

  7. Bates DM, Sarkar D (2007) lme4: linear mixed-effects models. R package version 0. 9975-13. http://www.R-project.org

  8. Beaulieu M, Geiger RE, Reim E, Zielke L, Fischer K (2015) Reproduction alters oxidative status when it is traded-off against longevity. Evolution 69:1786–1796

    PubMed  Google Scholar 

  9. Berg MP, Kiers ET, Driessen G, Van der Heijden M, Kooi BW, Kuenen F et al. (2010) Adapt or disperse: understanding species persistence in a changing world. Glob Change Biol 16:587–598

    Google Scholar 

  10. Borenstein M, Hedges LV, Higgins JPT, Rothstein HR (2009) Introduction to meta-analysis. John Wiley & Sons, Chichester

    Google Scholar 

  11. Boyd PW, Collins S, Dupont S, Fabricius K, Gattuso JP, Havenhand J et al. (2018) Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change—a review. Glob Change Biol 24:2239–2261

    Google Scholar 

  12. Ceballos G, Ehrlich PR, Barnosky AD, García A, Pringle RM, Palmer TM (2015) Accelerated modern human-induced species losses: entering the sixth mass extinction. Sci Adv 1:e1400253

    PubMed  PubMed Central  Google Scholar 

  13. Ceballos G, Ehrlich PR, Dirzo R (2017) Population losses and the sixth mass extinction. Proc Natl Acad Sci USA 114:E6089–E6096

    CAS  PubMed  Google Scholar 

  14. Charmantier A, Garant D (2005) Environmental quality and evolutionary potential: lessons from wild populations. Proc R Soc B 272:1415–1425

    PubMed  Google Scholar 

  15. Chevin LM, Lande R, Mace GM (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLOS Biol 8:e1000357

    PubMed  PubMed Central  Google Scholar 

  16. Chown SL, Jumbam KR, Sørensen JG, Terblanche JS (2009) Phenotypic variance, plasticity and heritability estimates of critical thermal limits depend on methodological context. Funct Ecol 23:133–140

    Google Scholar 

  17. Cvjetko P, Tolić S, Šikić S, Balen B, Tkalec M, Vidaković-Cifrek Ž et al. (2010) Effect of copper on the toxicity and genotoxicity of cadmium in duckweed (Lemna minor L.). Arch Indust Hyg Toxicol 61:287–296

    CAS  Google Scholar 

  18. DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81

    CAS  PubMed  Google Scholar 

  19. Falconer DS, Mackay TF (1996) Introduction to quantitative genetics, 4th edn. Benjamin Cummings, Essex

    Google Scholar 

  20. Fischer K, Brakefield PM, Zwaan BJ (2003) Plasticity in butterfly egg size: why larger offspring at lower temperatures? Ecology 84:3138–3147

    Google Scholar 

  21. Fischer K, Bot ANM, Zwaan BJ, Brakefield PM (2004) Genetic and environmental sources of egg size variation in the butterfly Bicyclus anynana. Heredity 92:163–169

    CAS  PubMed  Google Scholar 

  22. Fischer K, Dierks A, Franke K, Geister TL, Liszka M, Winter S et al. (2010) Environmental effects on temperature stress resistance in the tropical butterfly Bicyclus anynana. PLoS One 5:e15284

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Fischer K, Klockmann M, Reim E (2014) Strong negative effects of simulated heat waves in a tropical butterfly. J Exp Biol 217:2892–2898

    PubMed  Google Scholar 

  24. Fischer K, Kölzow N, Höltje H, Karl I (2011) Assay conditions in laboratory experiments: is the use of constant rather than fluctuating temperatures justified when investigating temperature-induced plasticity? Oecologia 166:23–33

    PubMed  Google Scholar 

  25. Geber MA, Griffen LR (2003) Inheritance and natural selection on functional traits. Int J Plant Sci 164:S21–S42.

    Google Scholar 

  26. Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407

    Google Scholar 

  27. Gienapp P, Reed TE, Visser ME (2014) Why climate change invariably leads to selection on phenology. Proc R Soc B 281:20141611

    PubMed  Google Scholar 

  28. Gienapp P, Lof M, Reed TE, McNamara J, Verhulst S, Visser ME (2013) Predicting demographically sustainable rates of adaptation: can great tit breeding time keep pace with climate change? Phil Trans R Soc B 368:20120289

    PubMed  Google Scholar 

  29. Gienapp P, Teplitsky C, Alho JS, Mills JA, Merilä J (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178

    CAS  PubMed  Google Scholar 

  30. Gurevitch J, Hedges LV (2001) Meta-analysis: combining the results of independent experiments. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press, New York, p 347–369

  31. Hacket-Pain AJ, Cavin L, Friend AD, Jump AS (2016) Consistent limitation of growth by high temperature and low precipitation from range core to southern edge of European beech indicates widespread vulnerability to changing climate. Eur J Forest Res 135:897–909

    Google Scholar 

  32. Hangartner S, Hoffmann AA (2016) Evolutionary potential of multiple measures of upper thermal tolerance in Drosophila melanogaster. Funct Ecol 30:442–452

    Google Scholar 

  33. Helle W (1967) Fertilization in 2-spotted spider mite (Tetranychus urticae - Acari). Ent Exp Appl 10:103–110

    Google Scholar 

  34. Henke R, Eberius M, Appenroth KJ (2011) Induction of frond abscission by metals and other toxic compounds in Lemna minor. Aquatic Toxicol 101:261–265

    CAS  Google Scholar 

  35. Hoffmann AA, Chown SL, Clusella‐Trullas S (2013) Upper thermal limits in terrestrial ectotherms: how constrained are they? Funct Ecol 27:934–949

    Google Scholar 

  36. Hoffmann AA, Merila J (1999) Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol Evol 14:96–101

    CAS  PubMed  Google Scholar 

  37. Hoffmann AA, Parsons PA (1991) Evolutionary genetics and environmental stress. University Press, Oxford

    Google Scholar 

  38. Hoffmann AA, Sgro CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485

    CAS  Google Scholar 

  39. Hoffmann AA, Sgrò CM, Kristensen TN (2017) Revisiting adaptive potential, population size, and conservation. Trends Ecol Evol 32:505–517.

    Google Scholar 

  40. Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics 130:195–204

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Janero DR (1990) Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radical Biol Med 9:515–540

    CAS  Google Scholar 

  42. Jump AS, Hunt JM, Penuelas J (2006) Rapid climate change-related growth decline at the southern range edge of Fagus sylvatica. Glob Change Biol 12:2163–2174

    Google Scholar 

  43. Kellermann V, van Heerwaarden B, Sgrò CM, Hoffmann AA (2009) Fundamental evolutionary limits in ecological traits drive Drosophila species distributions. Science 325:1244–1246

    CAS  PubMed  Google Scholar 

  44. Klockmann K, Günter F, Fischer K (2016) Heat resistance throughout ontogeny: body size constrains thermal tolerance. Glob Change Biol 23:686–696

    Google Scholar 

  45. Körner C (2006) Significance of temperature in plant life. In: Morison JIL, Morecroft MD (eds) Plant growth and climate change. Blackwell Publishing, Oxford, p 48–69

  46. Kruuk LEB (2004) Estimating genetic parameters in natural populations using the ‘animal model’. Phil Trans R Soc B 359:873–890

    PubMed  Google Scholar 

  47. Landolt E (1986) The family of Lemnaceae—a monographic study. Stiftung Ruebel, Zürich

    Google Scholar 

  48. Larsen TB (1991) The butterflies of Kenya and their natural history. University Press, Oxford

    Google Scholar 

  49. Lenoir J, Svenning J‐C (2014) Climate‐related range shifts—a global multidimensional synthesis and new research directions. Ecography 38:15–28

    Google Scholar 

  50. Leuschner C, Meier IC, Hertel D (2006) On the niche breadth of Fagus sylvatica: soil nutrient status in 50 Central European beech stands on a broad range of bedrock types. Ann For Sci 63:355–368

    CAS  Google Scholar 

  51. Loveys BR, Scheurwater I, Pons TL, Fitter AH, Atkin OK (2002) Growth temperature influences the underlying components of relative growth rate: an investigation using inherently fast- and slow-growing plant species. Plant Cell Environ 25:975–988

    Google Scholar 

  52. Magri D, Vendramin GG, Comps B, Dupanloup I, Geburek T, Gomory D et al. (2006) A new scenario for the quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol 171:199–221

    CAS  PubMed  Google Scholar 

  53. Mahroof R, Subramanyam B, Eustace D (2003) Temperature and relative humidity profiles during heat treatment of mills and its efficacy against Tribolium castaneum (Herbst) life stages. J Stored Prod Res 39:555–569

    Google Scholar 

  54. Merilä J, Kruuk LEB, Sheldon BC (2001) Cryptic evolution in a wild bird population. Nature 412:76–79

    PubMed  Google Scholar 

  55. Mitchell-Olds T, Schmitt J (2006) Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441:947–952

    CAS  PubMed  Google Scholar 

  56. Moritz C, Agudo R (2013) The future of species under climate change: resilience or decline? Science 341:504–508

    CAS  PubMed  Google Scholar 

  57. Müller C, Zwaan BJ, de Vos H, Brakefield PM (2003) Chemical defence in a sawfly: genetic components of variation in relevant life-history traits. Heredity 90:468–475

    PubMed  Google Scholar 

  58. Naumann B, Eberius M, Appenroth KJ (2007) Growth rate based dose-response relationships and EC-values of ten heavy metals using the duckweed growth inhibition test (ISO 20079) with Lemna minor L. clone St. J Plant Physiol 164:1656–1664

    CAS  PubMed  Google Scholar 

  59. Niemelä PT, Vainikka A, Hedrick AV, Kortet R (2012) Integrating behaviour with life history: boldness of the field cricket, Gryllus integer, during ontogeny. Funct Ecol 26:450–456

    Google Scholar 

  60. Ørsted M, Hoffmann AA, Sverrisdóttir E, Lehmann Nielsen K, Kristensen TN (2019) Genomic variation predicts adaptive evolutionary responses better than population bottleneck history. PLoS Genetics 15:e1008205

    PubMed  PubMed Central  Google Scholar 

  61. Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588

    PubMed  Google Scholar 

  62. Ramakers JJC, Culina A, Visser ME, Gienapp P (2018) Environmental coupling of heritability and selection is rare and of minor evolutionary significance in wild populations. Nature Ecol Evol 2:1093–1103

    Google Scholar 

  63. Roff DA (2002) Life history evolution. Sinauer Associates, Oxford

    Google Scholar 

  64. Rolandi C, Lighton JRB, de la Vega GJ, Schilman PE, Mensch J (2018) Genetic variation for tolerance to high temperatures in a population of Drosophila melanogaster. Ecol Evol 8:10374–10383

    PubMed  PubMed Central  Google Scholar 

  65. Rowinski PK, Rogell B (2017) Environmental stress correlates with increases in both genetic and residual variances: a meta-analysis of animal studies. Evolution 71:1339–1351

    CAS  PubMed  Google Scholar 

  66. Saastamoinen M (2008) Heritability of dispersal rate and other life history traits in the Glanville fritillary butterfly. Heredity 100:39–46

    CAS  PubMed  Google Scholar 

  67. Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R et al. (2000) Biodiversity—global biodiversity scenarios for the year 2100. Science 287:1770–1774

    CAS  Google Scholar 

  68. Santos M, Castañeda LE, Rezende EL (2011) Making sense of heat tolerance estimates in ectotherms: lessons from Drosophila. Funct Ecol 25:1169–1180

    Google Scholar 

  69. Sgro CM, Terblanche JS, Hoffmann AA (2016) What can plasticity contribute to insect responses to climate change? Annu Rev Entomol 61:433–451

    CAS  PubMed  Google Scholar 

  70. Sims DA, Gamon JA (2002) Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Remote Sensing Environ 81:337–354

    Google Scholar 

  71. Sørensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037

    Google Scholar 

  72. Stewart JJ, Demmig-Adams B, Cohu CM, Wenzl CA, Muller O, Adams WW (2016) Growth temperature impact on leaf form and function in Arabidopsis thaliana ecotypes from northern and southern Europe. Plant Cell Environ 39:1549–1558

    CAS  PubMed  Google Scholar 

  73. Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC et al. (2004) Extinction risk from climate change. Nature 427:145–148

    CAS  PubMed  Google Scholar 

  74. Torchiano M (2017) effsize: efficient effect size computation, R package version 0.7.1. https://CRAN.R-project.org/package=effsize

  75. Tsuda T, Shiga K, Ohshima K, Kawakishi S, Osawa T (1996) Inhibition of lipid peroxidation and the active oxygen radical scavenging effect of anthocyanin pigments isolated from Phaseolus vulgaris L. Bioch Pharm 52:1033–1039

    CAS  Google Scholar 

  76. Van Leeuwen T, Vanholme B, Van Pottelberge S, Van Nieuwenhuyse P, Nauen R, Tirry L et al. (2008) Mitochondrial heteroplasmy and the evolution of insecticide resistance: non-Mendelian inheritance in action. Proc Natl Acad Sci USA 105:5980–5985

    PubMed  Google Scholar 

  77. Vile D, Pervent M, Belluau M, Vasseur F, Bresson J, Muller B et al. (2012) Arabidopsis growth under prolonged high temperature and water deficit: independent or interactive effects? Plant Cell Environ 35:702–718

    PubMed  Google Scholar 

  78. Wilson AJ, Réale D, Clements MN, Morrissey MM, Postma E, Walling CA et al. (2010) An ecologist’s guide to the animal model. J Anim Ecol 79:13–26

    PubMed  Google Scholar 

  79. Wood CW, Brodie ED (2016) Evolutionary response when selection and genetic variation covary across environments. Ecol Lett 19:1189–1200

    PubMed  Google Scholar 

  80. Wood JL, Yates MC, Fraser DJ (2016) Are heritability and selection related to population size in nature? Meta-analysis and conservation implications. Evol Appl 9:640–657

    PubMed  PubMed Central  Google Scholar 

  81. Ziegler P, Adelmann K, Zimmer S, Schmidt C, Appenroth KJ (2015) Relative in vitro growth rates of duckweeds (Lemnaceae)—the most rapidly growing higher plants. Plant Biol 17:33–41

    PubMed  Google Scholar 

Download references

Funding

This research was funded by the DFG research training group RESPONSE (DFG GRK 2010).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Klaus Fischer.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Associate editor: Sara Knott

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Fischer, K., Kreyling, J., Beaulieu, M. et al. Species-specific effects of thermal stress on the expression of genetic variation across a diverse group of plant and animal taxa under experimental conditions. Heredity 126, 23–37 (2021). https://doi.org/10.1038/s41437-020-0338-4

Download citation

Further reading

Search

Quick links