The untapped potential of reptile biodiversity for understanding how and why animals age

Abstract

1. The field of comparative ageing biology has greatly expanded in the past 20 years.Longitudinal studies of populations of reptiles with a range of maximum lifespans have accumulated and been analysed for evidence of mortality senescence and reproductive decline. While not as well represented in studies of amniote senescence, reptiles have been the subjects of many recent demographic and mechanistic studies of the biology of ageing.2. We review recent literature on reptile demographic senescence, mechanisms of senescence, and identify unanswered questions. Given the ecophysiological and demographic diversity of reptiles, what is the expected range of reptile senescence rates? Are known mechanisms of ageing in reptiles consistent with canonical hallmarks of ageing in model systems? What are the knowledge gaps in our understanding of reptile ageing? 3. We find ample evidence of increasing mortality with advancing age in many reptiles. Testudines stand out as slower ageing than other orders, but data on crocodilians and tuatara are sparse. Sex-specific analyses are generally not available.Studies of female reproduction suggest that reptiles are less likely to have reproductive decline with advancing age than mammals. 4. Reptiles share many physiological and molecular pathways of ageing with mammals, birds and laboratory model organisms. Adaptations related to stress physiology coupled with reptilian ectothermy suggest novel comparisons and contrasts that can be made with canonical ageing phenotypes in mammals. These include stem cell and regeneration biology, homeostatic mechanisms, IIS/TOR signalling, and DNA repair. 5. To overcome challenges to the study of reptile ageing, we recommend extending and expanding long-term monitoring of reptile populations, developing reptile cell lines to aid cellular biology, conducting more comparative studies of reptile morphology and physiology sampled along relevant life-history axes and sequencing more reptile genomes for comparative genomics. Given the diversity of reptile life histories and adaptations, achieving these directives will likely greatly benefit all ageing biology.

A unifying, eco‐physiological framework for animal dormancy

“…Animals expressing dormancy also share broader aspects of their life history. Dormancy leads to a slowing of biological time and enhanced maintenance of cellular homeostasis, including increased resistance to some types of stress (Carey et al., 2003; Hoekstra et al., 2020; Schmidt et al., 2005). Dormancy decreases mortality rates and slows senescence, leading to life span extension in both insects and mammals (Tatar et al., 2001; Tatar & Yin, 2001; Turbill et al., 2011, 2013; Turbill & Prior, 2016).…”

“…Animals expressing dormancy also share broader aspects of their life history. Dormancy leads to a slowing of biological time and enhanced maintenance of cellular homeostasis, including increased resistance to some types of stress (Carey et al, 2003;Hoekstra et al, 2020;Schmidt et al, 2005).…”

Population position along the fast–slow life‐history continuum predicts intraspecific variation in actuarial senescence

“…Most of the studies on senescence in vertebrates focus on endothermic organisms, such as birds and mammals, and largely neglect ectotherms (Bronikowski et al, 2002;Hoekstra, Schwartz, Sparkman, Miller, & Bronikowski, 2019;Jones et al, 2014;Lemaître et al, 2015; but see Cayuela, Akani, et al, 2019;Cayuela, Olgun, et al, 2019;Massot et al, 2011;Sparkman, Arnold, & Bronikowski, 2007;Warner, Miller, Bronikowski, & Janzen, 2016). Both actuarial and reproductive senescence are understudied in ectotherms, mainly due to the scarcity of demographic data and methodological limitations (juveniles cannot be marked easily and information about the age of individuals is often partial and uncertain).…”

An integrative view of senescence in nature

“…These authors provide a clear roadmap to overcoming the methodological challenges inherent in any longitudinal monitoring of wild insects, which should thus stimulate new field investigations (Zajitschek et al, 2020). As with insects, Hoekstra et al (2020) emphasize that our understanding of senescence in reptiles is still in its infancy. However, the diversity of demographic senescence patterns is likely to be particularly pronounced among reptiles, which range from species with unambiguous senescence to species showing negligible senescence (Hoekstra et al, 2020).…”

“…Zajitschek, Zajitschek, and Bonduriansky (2020) fill this knowledge gap by reviewing our current knowledge on senescence in insects and by setting the scene for future research. Lastly, Hoekstra, Schwartz, Sparkman, Miller, and Bronikowski (2020) review our current knowledge of senescence in ectotherms and emphasize that the current framework used to understand the biological basis of ageing in humans can be successfully applied to these species.…”