High developmental temperature leads to low reproduction despite adult temperature

Phenotypic plasticity can be an important tool in helping organisms to cope with changing thermal conditions and it may show an interdependency between life-stages. For instance, exposure to stressful temperatures during development can trigger a positive plastic response in adults. In this study, we analyse the thermal plastic response of laboratory populations of Drosophila subobscura, derived from two contrasting latitudes of the European cline. We measured fecundity characters in the experimental populations after exposure to five thermal treatments, with different combinations of developmental and adult temperatures (14°C, 18°C or 26°C). We ask whether (1) adult performance is enhanced (or reduced) by exposing flies to higher (or lower) temperatures during development only; (2) flies raised at lower temperatures outperform those developed at higher ones, supporting the “colder is better” hypothesis; (3) there is a cumulative effect on adult performance of exposing both juveniles and adults to higher (or lower) temperatures; (4) there is any evidence for historical effects on adult performance. Our main findings show that (1) higher developmental temperatures led to low reproductive performance regardless of adult temperature, while at lower temperatures reduced performance only occurred when cold conditions were persistent across juvenile and adult stage; (2) flies raised at lower temperatures did not always outperform those developed at other temperatures; (3) there was no (negative) cumulative effect of exposing both juveniles and adults to higher temperatures; (4) both latitudinal populations showed similar thermal plasticity patterns. The negative effect of high developmental temperature on reproductive performance, regardless of adult temperature, highlights the developmental stage as a critical and most vulnerable stage to climate change and associated heat waves.

[1]  M. Matos,et al.  Beneficial developmental acclimation in reproductive performance under cold but not heat stress. , 2020, Journal of thermal biology.

[2]  A. Moehring,et al.  Local thermal adaptation detected during multiple life stages across populations of Drosophila melanogaster , 2019, Journal of evolutionary biology.

[3]  V. Loeschcke,et al.  Evolution and plasticity of thermal performance: an analysis of variation in thermal tolerance and fitness in 22 Drosophila species , 2019, Philosophical Transactions of the Royal Society B.

[4]  T. N. Girish,et al.  Reproductive fitness of Drosophila is maximised by optimal developmental temperature , 2019, Journal of Experimental Biology.

[5]  P. J. Moore,et al.  Impact of heat stress on development and fertility of Drosophila suzukii Matsumura (Diptera: Drosophilidae). , 2019, Journal of insect physiology.

[6]  A. Bretman,et al.  The impact of climate change on fertility , 2019, Trends in ecology & evolution.

[7]  Michael J. Angilletta,et al.  Thermal acclimation of flies from three populations of Drosophila melanogaster fails to support the seasonality hypothesis. , 2019, Journal of thermal biology.

[8]  Kun Xing,et al.  Effects of developmental acclimation on fitness costs differ between two aphid species. , 2018, Journal of thermal biology.

[9]  C. Sgrò,et al.  Evidence for lower plasticity in CTMAX at warmer developmental temperatures , 2018, Journal of evolutionary biology.

[10]  F. Bozinovic,et al.  Colder is better: The differential effects of thermal acclimation on life history parameters in a parasitoid fly. , 2017, Journal of thermal biology.

[11]  K. Fischer,et al.  Carried over: Heat stress in the egg stage reduces subsequent performance in a butterfly , 2017, PloS one.

[12]  Mauro Santos,et al.  Predictable phenotypic, but not karyotypic, evolution of populations with contrasting initial history , 2017, Scientific Reports.

[13]  V. Loeschcke,et al.  Linear reaction norms of thermal limits in Drosophila: predictable plasticity in cold but not in heat tolerance , 2017 .

[14]  V. Loeschcke,et al.  Environmental heterogeneity does not affect levels of phenotypic plasticity in natural populations of three Drosophila species , 2017, Ecology and evolution.

[15]  K. Gaston,et al.  Local adaptation of reproductive performance during thermal stress , 2017, Journal of evolutionary biology.

[16]  J. G. Sørensen,et al.  Evolutionary and ecological patterns of thermal acclimation capacity in Drosophila: is it important for keeping up with climate change? , 2016, Current opinion in insect science.

[17]  A. Hoffmann,et al.  What Can Plasticity Contribute to Insect Responses to Climate Change? , 2016, Annual review of entomology.

[18]  F. Seebacher,et al.  Evolution of Plasticity: Mechanistic Link between Development and Reversible Acclimation. , 2016, Trends in ecology & evolution.

[19]  Mauro Santos,et al.  Keeping your options open: Maintenance of thermal plasticity during adaptation to a stable environment , 2016, Evolution; international journal of organic evolution.

[20]  A. Hoffmann,et al.  Impact of hot events at different developmental stages of a moth: the closer to adult stage, the less reproductive output , 2015, Scientific Reports.

[21]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[22]  Mauro Santos,et al.  Laboratory Selection Quickly Erases Historical Differentiation , 2014, PloS one.

[23]  Mauro Santos,et al.  Genome-wide evolutionary response to a heat wave in Drosophila , 2013, Biology Letters.

[24]  V. Loeschcke,et al.  Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically , 2012, Proceedings of the National Academy of Sciences.

[25]  A. Malmendal,et al.  Inconsistent effects of developmental temperature acclimation on low-temperature performance and metabolism in Drosophila melanogaster , 2012 .

[26]  J. Kingsolver,et al.  Complex life cycles and the responses of insects to climate change. , 2011, Integrative and comparative biology.

[27]  Sanford Weisberg,et al.  An R Companion to Applied Regression , 2010 .

[28]  Mauro Santos,et al.  Climate change and chromosomal inversions in Drosophila subobscura , 2010 .

[29]  M. Angilletta Thermal Adaptation: A Theoretical and Empirical Synthesis , 2009 .

[30]  K. Brodersen,et al.  Are altitudinal limits of equatorial stream insects reflected in their respiratory performance , 2008 .

[31]  Yulia R. Gel,et al.  lawstat: An R Package for Law, Public Policy and Biostatistics , 2008 .

[32]  R. Huey,et al.  Size, temperature, and fitness: Three rules , 2008 .

[33]  R. Huey,et al.  Global Genetic Change Tracks Global Climate Warming in Drosophila subobscura , 2006, Science.

[34]  B. Lemos,et al.  Male sterility at extreme temperatures: a significant but neglected phenomenon for understanding Drosophila climatic adaptations , 2005, Journal of evolutionary biology.

[35]  A. Clarke,et al.  Why does metabolism scale with temperature , 2004 .

[36]  R. Huey,et al.  Testing the Adaptive Significance of Acclimation: A Strong Inference Approach , 1999 .

[37]  J. David,et al.  Evolutionary changes of nonlinear reaction norms according to thermal adaptation: a comparison of two Drosophila species. , 1997, Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie.

[38]  L. Nunney,et al.  THE EFFECT OF TEMPERATURE ON BODY SIZE AND FECUNDITY IN FEMALE DROSOPHILA MELANOGASTER: EVIDENCE FOR ADAPTIVE PLASTICITY , 1997, Evolution; international journal of organic evolution.

[39]  R. Huey,et al.  Within- and between-generation effects of temperature on early fecundity of Drosophila melanogaster , 1995, Heredity.

[40]  M. Aguadé,et al.  Colonization of America by Drosophila subobscura: Experiment in natural populations that supports the adaptive role of chromosomal-inversion polymorphism. , 1988, Proceedings of the National Academy of Sciences of the United States of America.