Temperature and telomeres: thermal treatment influences telomere dynamics through a complex interplay of cellular processes in a cold-climate skink
Telomere dynamics vary fundamentally between endothermic populations and species as a result of differences in life history, yet we know little about these patterns in ectotherms. In ectotherms, the relationships between climate, metabolism and life history suggest that telomere attrition should be higher at relatively high environmental temperatures compared to relatively low environmental temperatures, but these effects may vary between populations due to local adaptation. To address this hypothesis, we sampled reactive oxygen species (ROS) and telomere length of lizards from warm lowland and cool highland populations of a climatically widespread lizard species that we exposed to hot or cold basking treatments. The hot treatment increased relative telomere length compared to the cold treatment independent of climatic origin or ROS levels. Lizards from the cool highland region had lower ROS levels than those from the warm lowland region. Within the highland lizards, ROS increased more in the cold basking treatment than the hot basking treatment. These results are in the opposite direction to those predicted, suggesting that the relationships between temperature, metabolism, ROS and telomere dynamics are not straightforward. Future work incorporating detailed understanding of the thermal reaction norms of these and other linked traits is needed to fully understand these processes.
KeywordsClimate Ectotherm Reactive oxygen species Reptile Telomere
Author contribution statement
LJF, AP, LMP, TLP, GMW, EW and MO conceived the ideas and designed the methodology. LJF, LMP, TP, AP and EW collected the data. LJF, LMP, AP, GMW and EW analysed the data. LJF, GMW and EW led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
EW, MO and GW were supported by ARC Grants and Fellowships. LF was supported by the Holsworth Wildlife Research Endowment (Grant W0024143)—Equity Trustees Charitable Foundation and the Ecological Society of Australia and by the Australian Government’s Australia Awards: Endeavour Research Fellowship.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
Analyses reported in this article can be reproduced using the datasets provided as part of the electronic supplementary material.
All guidelines and procedures for the use of animals were approved by the University of Tasmania Animal Ethics Committee (A0015987). Field collections were carried out under permit number FA 16236 issued by the Department of Primary Industries, Parks, Water and the Environment, Tasmania.
- Atkinson D (1994) Temperature and organism size—a biological law for ectotherms. In: Begon M, Fitter AH (eds) Advances in Ecological Research, vol 25. Academic Press Ltd-Elsevier Science Ltd, London, pp 1–58Google Scholar
- Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. ArXiv14065823 StatGoogle Scholar
- Cliff HB, Wapstra E, Burridge CP (2015) Persistence and dispersal in a Southern Hemisphere glaciated landscape: the phylogeography of the spotted snow skink (Niveoscincus ocellatus) in Tasmania. BMC Evol Biol 15:121. https://doi.org/10.1186/s12862-015-0397-y CrossRefPubMedPubMedCentralGoogle Scholar
- Grabowski TB, Young SP, Libungan LA, Steinarsson A, Marteinsdóttir G (2009) Evidence of phenotypic plasticity and local adaption in metabolic rates between components of the Icelandic cod (Gadus morhua L.) stock. Environ Biol Fishes 86:361–370. https://doi.org/10.1007/s10641-009-9534-z CrossRefGoogle Scholar
- Hill PL, Burridge CP, Ezaz T, Wapstra E (2018) Conservation of sex-linked markers among conspecific populations of a viviparous skink, Niveoscincus ocellatus, exhibiting genetic and temperature-dependent sex determination. Genome Biol Evol 10:1079–1087. https://doi.org/10.1093/gbe/evy042 CrossRefPubMedPubMedCentralGoogle Scholar
- Houben JMJ, Moonen HJJ, van Schooten FJ, Hageman GJ (2008) Telomere length assessment: biomarker of chronic oxidative stress? Free Radic Biol Med 44:235–246. https://doi.org/10.1016/j.freeradbiomed.2007.10.001 CrossRefPubMedGoogle Scholar
- Kawecki TJ (2008) Adaptation to marginal habitats. Annu Rev Ecol Evol Syst 39:321–342. https://doi.org/10.1146/annurev.ecolsys.38.091206.095622 CrossRefGoogle Scholar
- Quirici V, Guerrero CJ, Krause JS, Wingfield JC, Vásquez RA (2016) The relationship of telomere length to baseline corticosterone levels in nestlings of an altricial passerine bird in natural populations. Front Zool 13:1. https://doi.org/10.1186/s12983-016-0133-5 CrossRefPubMedPubMedCentralGoogle Scholar
- R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Wapstra E, Swain R, O’Reilly JM (2001) Geographic variation in age and size at maturity in a small Australian viviparous skink. Copeia 2001:646–655. https://doi.org/10.1643/0045-8511(2001)001%5b0646:gviaas%5d2.0.co;2 CrossRefGoogle Scholar