Climate change and ageing in ectotherms

Human activity is changing climatic conditions at an unprecedented rate. The impact of these changes may be especially acute on ectotherms since they have limited capacities to use metabolic heat to maintain their body temperature. An increase in temperature is likely to increase the growth rate of ectothermic animals, and may also induce thermal stress via increased exposure to heat waves. Fast growth and thermal stress are metabolically demanding, and both factors can increase oxidative damage to essential biomolecules, accelerating the rate of ageing. Here, we explore the potential impact of global warming on ectotherm ageing through its effects on reactive oxygen species production, oxidative damage, and telomere shortening, at the individual and intergenerational levels. Most evidence derives primarily from vertebrates, although the concepts are broadly applicable to invertebrates. We also discuss candidate mechanisms that could buffer ectotherms from the potentially negative consequences of climate change on ageing. Finally, we suggest some potential applications of the study of ageing mechanisms for the implementation of conservation actions. We find a clear need for more ecological, biogeographical, and evolutionary studies on the impact of global climate change on patterns of ageing rates in wild populations of ectotherms facing warming conditions. Understanding the impact of warming on animal life histories, and on ageing in particular, needs to be incorporated into the design of measures to preserve biodiversity to improve their effectiveness.

environmental conditions, rising temperatures can put ectotherms outside their physiological optima and closer, or even above, their thermal tolerance limits (Kingsolver et al., 2013;Sunday et al., 2014).
A mismatch between the rate of change in environmental conditions and the capacity of ectotherms to cope with these changes may severely affect their physiology and lead to decreases in fitness.
While the effects of global warming on several components of ectothermic physiology are well understood (Abram, Boivin, Moiroux, & Brodeur, 2017;Gunderson, Dillon, & Stillman, 2017;Gunderson & Stillman, 2015), one particular aspect that has hitherto received little attention is its effect on the dynamics of ageing. Ageing can broadly be defined as the time-dependent functional decline that affects most living organisms (López-Otín, Blasco, Partridge, Serrano, & Kroemer, 2013). Here, we highlight three routes by which climate change might alter the rate of ageing in ectotherms: (a) warmer average temperatures causing an acceleration of growth rates; (b) more frequent heat waves inducing thermal stress; and (c) changes in the pace-of-life of parents affecting the ageing rate of their offspring. As we show below, all three scenarios can induce the loss of organismal homeostasis and accelerate senescence in ectotherms.
Here, in using the term 'ectotherm', we are primarily referring to vertebrates, since this is where most relevant existing data on ageing mechanisms occur, but the processes are likely to be also relevant to invertebrates. At present, it is unclear whether organisms have the capacity to compensate for these potential changes in lifespan, or the demographic consequences for populations. Further research is clearly needed to fully evaluate the effects of climate change on rates of ageing of wild organisms, and to incorporate these issues into biodiversity conservation actions.
Thermally induced alterations in growth can be particularly costly for ectotherms at early ontogenetic stages, since at this point resources are prioritized towards the development of new structures and away from somatic maintenance (Dmitriew, 2011;Metcalfe & Monaghan, 2001). Many ectotherms develop complex life cycles and are especially sensitive to warming impacts on growth if these occur in early life stages, that is, before metamorphosis (Huey et al., 2012).
Environmentally induced acceleration of growth is known to impact on lifespan. The costs of rapid growth were first demonstrated in fish showing a negative relationship between growth rate and longevity (Comfort, 1963). A negative relationship between faster growth in early life and later survival has been found in other fish species, and also in insects (e.g. Lee & Roh, 2010), amphibians (e.g. Altwegg & Reyer, 2003), and reptiles (e.g. Olsson & Shine, 2002).
While most of these studies have been correlational, a trade-off between growth rate and lifespan has been demonstrated experimentally in sticklebacks (Lee, Monaghan, & Metcalfe, 2013). In this study, temperature-induced faster growth was associated with reduced longevity, while experimental slowing of growth was associated with increased longevity, confirming the role of thermally induced growth in shaping the pattern and pace of ageing in ectotherms.
Across-species comparisons indicate that larger endotherms live longer than smaller ones (r 2 = .46 and .39 in birds and mammals, respectively; Speakman, 2005). In contrast, body size explains only a small portion of the variance in longevity in vertebrate ectotherms, as observed in amphibians (r 2 = .07-.14;  or reptiles (r 2 = .04-.23; Stark, Tamar, Itescu, Feldman, & Meiri, 2018). The weaker correlation between body size and maximum lifespan in vertebrate ectotherms than in endotherms probably indicates that the traits have evolved at least partially independently in species with indeterminate growth. Ectotherms can potentially show some degree of thermal independence via a reduced heat exchange rate with the environment. The ability to be thermally independent mainly benefits larger-bodied ectotherms under cold environments rather than warming conditions. However, reductions in body size due to induced fast growth caused by warming may facilitate heat loss in large species. Among-species differences in the rate of growth from birth to maturation, and the variation in this rate caused by rising temperatures, may be even more relevant than differences in body size to understand the impact of warming on ageing in ectotherms.
Another unexplored topic is how among-species differences in life expectancy at birth can affect responses to warming. The likelihood of being exposed to warming and thermal stress during a single lifetime is, obviously, higher in long-lived species, but these species have often evolved protective mechanisms to slow the ageing process (Tian, Seluanov, & Gorbunova, 2017). Further comparative research will help to disentangle the relative importance of growth, body size, and lifespan on ectotherms ageing under a global warming scenario.

| Fast growth and oxidative damage
The reduction in lifespan of ectotherms experiencing faster growth could be due to greater mitochondrial activity ( Figure 1a). Rapid growth requires the formation in the mitochondria of increased amounts of ATP, and this can lead to the generation of reactive oxygen species (ROS) as a by-product. While ROS have many beneficial physiological functions such as maintenance of homeostasis and cell signalling, they can also cause oxidative damage to essential biomolecules like membrane lipids, proteins, and DNA when their concentration exceeds the antioxidant capacity of cells to detoxify them (Halliwell & Gutteridge, 2015). This damage can lead to accelerated ageing of the cells and ultimately the whole organism (Halliwell & Gutteridge, 2015). A meta-analysis across all animal groups has shown that faster growth is associated with greater oxidative damage (Smith, Nager, & Costantini, 2016). In ectotherms, fast growth can alter the redox status in insects (e.g. De Block & Stoks, 2008 F I G U R E 1 Mechanisms whereby environmental warming could increase the rates of ageing in ectotherms. (a) Left side: differences in individual growth trajectories and body size at maturation in response to normal (yellow thermometer) or warm (red thermometer) thermal conditions; right side: fast growth may include cellular damage and a consequent increase in the rate of shortening of the telomeres (the red caps on the ends of the chromosomes). (b) Left side: ectotherms have evolved to cope with normal temperature regimes without incurring in thermal stress; right side: heat waves induce thermal stress, leading to cellular damage and consequent faster erosion of telomeres. Such responses would not necessarily include significant changes in growth since they often take place during a brief period of time. (c) Possible intergenerational effects of climate warming on telomere length. Left side: normal thermal regimes result in normal telomere lengths in offspring; right side: higher mean temperatures and heat waves in parental generation have deleterious effects on offspring. Such effects, evident at very early offspring life stages, could be caused by faster erosion of germline telomeres, by poor parental condition and/or impaired parental care during post-natal stages during post-natal stages Noguera, . Amphibians can also experience redox imbalances at metamorphosis as a negative consequence of growing at high rates earlier in life, when compensating for delayed hatching (Burraco et al., 2020).

| Warmer temperature and telomeres
Oxidative stress can also induce faster ageing through its impact on telomeres. Telomeres are specialized sections of non-coding DNA that mark and protect the ends of chromosomes. Telomere regions are essential for maintaining genome stability by preventing end-toend fusion of chromosomes, and also protect the coding sequences from loss at the ends of the lagging DNA strands that occurs during DNA replication (Richter & von Zglinicki, 2007). The length of the telomeres becomes shorter at each cell division. Cells enter a state of replicative senescence once their telomeres reach a critically short length; this is followed by either cell death or a change in cell secretory profile to a more pro-inflammatory state (Aubert & Lansdorp, 2008). Such changes can provide a link between the rate of telomere shortening and tissue (and hence organismal) senescence. The causal relationship between oxidative stress and the rate of telomere shortening has been evidenced via the administration of antioxidants, which slow the rate of telomere erosion (Badás et al., 2015;Pineda-Pampliega et al., 2020), and confirmed through field and laboratory studies (reviewed in Barnes, Fouquerel, & Opresko, 2018;Monaghan & Ozanne, 2018;Reichert & Stier, 2017).
A recent meta-analysis (Chatelain, Drobniak, & Szulkin, 2020) supports the idea that oxidative stress mediates telomere shortening, although this relationship is mainly linked to differences in the levels of the antioxidant machinery. Differences in telomere length or loss rate can predict life expectancy, but the telomere-fitness relationship is highly variable in ectotherms and still need further research (Olsson, Wapstra, & Friesen, 2018a, 2018b. Telomere loss can also indicate the degree of stress exposure of an individual across the life course, although as yet most of the evidence of this comes from endotherms (Bateson & Poirier, 2019;Tricola et al., 2018;Wilbourn et al., 2018). The variation in telomere length among populations of brown trout correlates negatively with the river temperatures they experienced in the previous summer, and thus telomere length has been suggested as a marker of past thermal stress in fish (Debes, Visse, Panda, Ilmonen, & Vasemägi, 2016). In ectotherms, fast growth can lead to accelerated telomere shortening, as found in juvenile fish (McLennan et al., 2016;Pauliny, Devlin, Johnsson, & Blomqvist, 2015) or amphibian larvae (Burraco, Díaz-Paniagua, & Gomez-Mestre, 2017). Since differences in length-at-age and rate of loss of telomeres can be considered as ageing biomarkers, a detailed understanding of telomere dynamics over a species' lifetime, and across taxa, will improve our predictions of the impact of warming on ectotherm ageing. To this end, knowing the age of individuals is helpful in studies in the wild. In temperate vertebrate ectotherms, growth shows seasonal variation and age can be determined through skeletochronology, for example, by counting lines of arrested growth in reptiles and amphibians, growth rings in fish scales or bands in fish otoliths (Zhao, Klaassen, Lisovski, & Klaassen, 2019).
However, when faster growth is induced by higher temperatures, the relationship with telomere attrition is not always straightforward since adult ectotherms can undergo partial telomere restoration as a result of expressing the enzyme telomerase. Telomerase restores telomere length and is more often active in somatic tissue after birth in ectotherms than in endotherms (Olsson, Wapstra, & Friesen, 2018a). Telomerase expression is predicted to be higher in warmer environments, so potentially compensating for damage to telomeres in those organisms experiencing temperature-induced fast growth (Olsson et al., 2018a). This hypothesis is supported by recent research showing that lizards held in hot basking conditions for 3 months experienced increases in telomere length, unlike those held in cooler conditions (Fitzpatrick et al., 2019). Further empirical studies will clarify the possible interaction between temperature, growth, and telomerase expression.
The study of telomere dynamics in populations inhabiting divergent temperature conditions might allow us to evaluate the effects of human-induced thermal stress on ageing rates. This would be particularly relevant for populations of ectotherms living in regions of rapid thermal change, especially if they have long generation times that slow the potential rate of adaptation to changing environments (Morley, Peck, Sunday, Heiser, & Bates, 2019). Species with shorter generation time and larger populations are predicted to evolve quickly while maintaining genetic variation (Hoffmann & Sgrò, 2011). Artificial selection experiments comparing the genetic responses to warming conditions will help to evaluate the relative importance of generation time, population size, and plasticity, in evolutionary adaptation processes. Unfortunately, there is a lack of studies combining biogeographical and gerontological approaches which would allow us to appropriately predict the impact that global warming will have on the comparative rates of ageing of ectotherms along climatic gradients.

| HE AT WAVE S AND AG EING IN EC TOTHERM S
Forecasts for the next 50 years predict a dramatic increase in the likelihood of heat waves (IPCC, 2014), characterized by sudden rises in air or water temperature that could reach the upper thermal limits for many ectotherms (Gunderson & Stillman, 2015). Heat waves are one of the most powerful environmental forces affecting the welfare and physiology of ectotherms (Kingsolver et al., 2013), and may cause the acceleration of senescence by inducing thermal stress.
Similar to the alterations caused by other stressful conditions, thermal stress can disrupt individual's homeostasis and compromise organismal health. In vertebrates, the response to stressful conditions is mainly regulated by neuroendocrine pathways. These pathways mediate biological processes such as growth or reproduction (Crespi, Williams, Jessop, & Delehanty, 2013) but also accelerate the rate of ageing, as determined, for example, by a higher rate of telomere attrition (Angelier, Costantini, Blevin, & Chastel, 2018;Haussmann & Heidinger, 2015). Stress often leads to a higher secretion of hormones that enhances cellular catabolism and exacerbates the generation of ROS, with putative impacts on antioxidant defences and the rate of telomere shortening (Haussmann & Heidinger, 2015;Haussmann & Marchetto, 2010;Monaghan, 2014). The antioxidant machinery of ectotherms seems to be particularly sensitive to extreme thermal events, as indicated by strong redox responses to high temperatures observed in arthropods (e.g. Yang, Huang, & Wang, 2010) and fish (e.g. Banh, Wiens, Sotiri, & Treberg, 2016). On the other hand, the redox machinery of some reptiles seems relatively insensitive to thermal stress (e.g. Stahlschmidt, French, Ahn, Webb, & Butler, 2017), which may be a consequence of the downregulation of particular genes in response to warming (Bentley, Haas, Tedeschi, & Berry, 2017). show increased juvenile mortality (Kappenman, Fraser, Toner, Dean, & Webb, 2009). Desert lizards, which do not show signs of telomere shortening or reductions in survival when exposed to gradual warming, experience telomere shortening and lower overwinter survival after a week of simulated heat wave conditions (Zhang et al., 2018). This is perhaps surprising, given the lack of oxidative stress induced by high temperatures in other reptiles, and highlights the need for more comprehensive studies investigating the impact of temperature on physiological indicators of ageing in ectotherms.

| INTERG ENER ATI ONAL EFFEC TS OF CLIMATE CHANG E ON AG EING R ATE S IN EC TOTHERM S
Stress experienced by parents can influence the physiology of their offspring. To establish whether the environmental conditions experienced by parents can influence the rates of ageing of their offspring, we need to understand the mechanisms whereby rates of ageing could be transmitted between generations. In the absence of detailed information on life expectancy (not normally available over multiple generations), the usual approach is to use a biomarker of the rate of ageing, such as telomere length. Telomere length at a given developmental stage is a function of their initial length (i.e. at zygote), minus the accumulated shortening, plus the amount of restoration experienced until that point (Dugdale & Richardson, 2018). If climate warming causes a reduction in the physiological condition of ectotherms at the time of breeding, this could lead to shorter telomeres in their offspring through two different routes. First, stressors could affect germline telomere lengths, causing offspring to inherit shorter telomeres from parents that were exposed to more stressful environments. Second, indirect parental effects can cause faster ageing in offspring, either during the embryonic stages (e.g. through maternally derived stress hormones or suboptimal temperatures during development), or in the early post-natal stages (e.g. through changes in parental behaviour or care; Haussmann & Heidinger, 2015). Both routes may be particularly important for ectotherms in a warming world because higher temperatures can induce maturation earlier in life and at a smaller size (Angilletta, Steury, & Sears, 2004). Smaller size at breeding is often associated with the production of lower-quality offspring and poor parental care, which can negatively affect offspring performance at embryonic and postbirth stages (Angilletta et al., 2004), and cause accelerated ageing (Haussmann & Heidinger, 2015; Figure 1c). Detrimental thermal conditions experienced by parents can lead to poor offspring condition as a consequence of a reduction in the energy invested by the parents in each offspring. However, although rare, compensatory responses by parents or changes in breeding strategies could mitigate this effect, for example by reducing clutch size to allocate a larger amount of energy to each offspring (Charnov & Ernest, 2006).
There are several other factors that ideally should be considered when studying the intergenerational effects of warming on ageing dynamics in ectotherms. Many ectotherms show sexual dimorphism, with females typically larger than males, and temperature-dependent sex determination during embryogenesis can also occur. The negative consequences on ageing caused by warming may be exacerbated in species producing females at higher incubation temperatures. Embryos developing as females, and hatching at smaller sizes due to warming, could then show compensatory growth responses, which may result in a lifespan penalty (Metcalfe and Monaghan, 2003). Sex differences in lifespan and ageing can also be driven by the reproductive strategy of species. For example, in polygynous species, survival declines with age faster in males than in females (Clutton-Brock & Isvaran, 2007); warming could exacerbate such sex differences in lifespan by uncoupling the time at which each sex reaches sexual maturation, a process that may be particularly important in semelparous species.

| C AND IDATE MECHANIS MS TO BUFFER THE EFFEC TS OF WARMING ON AG EING IN EC TOTHERM S
Different mechanisms could allow ectotherms to counteract the negative effects of climate change on their ageing rate (Figure 2). Temperature-induced plasticity is a ubiquitous feature of ectothermic animals (Gunderson et al., 2017). Adaptive behavioural plasticity can be essential for thermoregulation in mobile ectotherms and may play an important role both under gradual warming and during thermal stress events. At low and medium latitudes, where exposure to the sun can otherwise cause body temperatures to increase above an organism's thermal limits, many ectotherms have developed behavioural strategies to avoid overheating (Abram et al., 2017). This is mainly explained by the fact that metabolic responses do not follow a linear pattern, and at those latitudes small increases in temperature may induce significant changes in metabolism. However, species at higher latitudes, including polar environments, may be as vulnerable to global warming as those in the tropics because they may have very narrow thermal tolerances (Johansson, Orizaola, & Nilsson-Örtman, 2020;Somero, 2010).
The ability to plastically modify the onset of some life strategies can reduce the negative impact of warming on ectotherm ageing. Dormancy, diapause and resting egg stages, processes very common in ectotherms living in highly seasonal environments, involve a significant decrease in development and physical activity. In an endotherm, the edible dormouse, a reduction in telomere attrition has been observed during hibernation (Turbill, Ruf, Smith, & Bieber, 2013), although intermittent arousal also carries costs in terms of increased telomere loss (Hoelzl, Cornils, Smith, Moodley, & Ruf, 2016). Under a global warming scenario, dormant ectotherms will probably experience a reduction in the duration and number of dormancy events. Therefore, individuals may need to adjust their use of dormancy in response to environmental temperatures, to reduce the negative effects on ageing. The possible role of this process F I G U R E 2 Putative impacts of warming conditions on ageing in ectotherms. Higher temperatures are predicted to cause faster growth or thermal stress in ectotherms, which can involve changes in body size, physiological homeostasis, age at maturation, and/or offspring quality. Both faster growth and thermal stress can cause a detrimental impact on ageing-related mechanisms, as for example inducing telomere attrition or oxidative stress. From an eco-evolutionary point of view, a species' biology and buffering mechanisms will likely define the extent to which warming will impact on ageing both at the individual or intergenerational levels Rate of ageing in regulating ageing dynamics has not been tested yet in ectotherms, but a recent study shows that higher winter and summer temperatures impact positively and negatively, respectively, on telomere lengths in a hibernating lizard (Axelsson, Wapstra, Miller, Rollings, & Olsson, 2020).
Adaptive physiological plasticity can also help ectotherms acclimate to warmer conditions (Gunderson et al., 2017;Norin & Metcalfe, 2019;Seebacher et al., 2015). However, both behavioural and physiological plasticity may prove insufficient to fully compensate for the effects of warming (Gunderson et al., 2017;Gunderson & Stillman, 2015). This is exemplified by the fact that physiological (e.g. locomotor, metabolic, heart, enzymatic activity) rates in ectotherms have increased up to 20% over the last 20 years as result of climate change, and chronic exposure to higher temperatures has resulted in reductions in their thermal sensitivity (Norin & Metcalfe, 2019;Seebacher et al., 2015). Metabolic rates of terrestrial, freshwater, and marine ectothermic species are predicted to keep increasing in the coming decades (Seebacher et al., 2015). Plasticity is, on average, higher in aquatic than terrestrial ectotherms (Gunderson & Stillman, 2015;Huey et al., 2012;Morley et al., 2019), and it may buffer the negative impact of warming on ectotherm physiology.
However, plasticity alone cannot fully protect aquatic ectotherms from overheating (Gunderson et al., 2017). Among ectotherms, crustacea and fish are expected to have smaller decreases in thermal safety margins when environmental temperatures rise than insects, reptiles, and amphibians (Gunderson & Stillman, 2015). Measured impacts of past and current global warming on ectothermic metabolism would suggest that there will be a global acceleration in the rate of senescence of ectotherms as warming continues.
There are also potential molecular mechanisms that could buffer warming impact on ageing. These mechanisms might either prevent damage in cells by reducing the generation of ROS, or repair the damage already caused. Both metabolic rate, usually measured in terms of whole-body oxygen consumption, and mitochondrial efficiency, defined as the amount of ATP generated per molecule of oxygen consumed, show great within-and among-individual variation, and can change in response to environmental conditions (Salin, Auer, Rey, Selman, & Metcalfe, 2015;Salin et al., 2019). Metabolic plasticity at the organelle and tissue/organ level may allow organisms to adjust ROS production to increase their resilience to climate change (Norin & Metcalfe, 2019;Seebacher et al., 2015). Greater mitochondrial uncoupling, which reduces the rate of ROS production at the expense of ATP production efficiency, has been proposed as a mechanism to reduce the rate of senescence (the 'uncoupling to survive' hypothesis, Mookerjee, Divakaruni, Jastroch, & Brand, 2010). This mitigation measure comes at a cost of reduced ATP availability and also increased body heat, since the uncoupling process involves a thermogenic reaction; there is thus an interesting trade-off between ROS production and body temperature in organisms facing warming.
Animals may respond by increasing their production of ROS scavenger molecules so as to prevent excessive oxidative damage caused by responses to warming. As an example, one of the first cellular lines of defence against pro-oxidants is the reduced form of glutathione, the production of which can increase in response to stress events (Angelier et al., 2018). An increased availability of ROS scavengers can allow greater metabolic activity, as demonstrated in endotherms through enhanced growth (Velando, Noguera, da Silva, & Kim, 2019).
However, there is little knowledge about the costs of increased ROS scavenger production-note that ROS are known to play an essential role in signalling pathways (Costantini, 2019).
The enhancement of repair mechanisms might also slow down ageing in ectotherms. The enzyme telomerase restores telomere length and may play a key role in the extensive regenerative capacity in organisms with indeterminate growth (Gomes, Shay, & Wright, 2010). If selection favours higher levels of telomerase expression in response to warming, it may mitigate the potential damage to telomeres caused by growth acceleration or by thermal stress (Olsson et al., 2018a). However, the prolonged action of telomerase can induce 'immortal cells' and tumorigenesis (Blasco, 2007), which may expose adult ectotherms to a higher risk of cancer (Olsson et al., 2018a;Young, 2018), although our knowledge of the prevalence of cancer in wild animals is very limited.
Field and laboratory studies, ideally including cross-fostering and transgenerational approaches, will help us to understand whether the action of buffering mechanisms is driven either by plasticity or local adaptation across populations. A higher degree of complexity can be added by considering the possibility that the dynamics of ageing-related mechanisms may be tissue-specific. Although telomere lengths seem to correlate among tissues (e.g. in reptiles: Rollings et al., 2019Rollings et al., , 2020, differences in cell division and turnover rate, together with the possible tissue-specific expression of buffering mechanisms, may imply divergent responses in ageing-related mechanisms at the tissue level. Evidence from mammals suggests that telomere attrition rates are similar across tissues in adults, but not necessarily so in early life (Daniali et al., 2013;Sabharwal et al., 2018), so the life stage at which the temperature effects occur could be important. Conducting longitudinal studies on the variation of ageing mechanisms at the tissue level is challenging, since terminal sampling is often required, but cross-sectional studies should help to disentangle this topic. It is clear that much more research is needed to fully understand the role that behavioural, physiological, and molecular mechanisms can play in buffering the effects of climate change on the ageing of ectotherms.

| HOW MI G HT THE S E CON CEP TS HELP IN THE CON S ERVATI ON OF EC TOTHERMS -AND WHAT DO WE S TILL NEED TO FIND OUT ?
There are issues that need to be taken into account in the context of ectotherm conservation in the face of environmental warm-  (Shoo et al., 2011).
Several research questions are still unresolved regarding the impact of warming on the ageing of ectotherms. We need to know the relative importance of high average temperature versus heat waves in affecting rates of ageing, and which ectothermic taxa are most vulnerable to changes in ageing. This is particularly important for invertebrates, where there is currently virtually no information on ageing mechanisms in wild populations. An understanding of these differences will allow managers to develop effective conservation measures that will protect not only declining populations but also others that are apparently healthy. Furthermore, it will allow more accurate modelling of the impact of future warming scenarios on ageing rates in ectotherms that can feed into population models used to set conservation priorities.

| CON CLUS IONS
Temperature increases associated with climate change may alter ageing-related processes in ectotherms, as a consequence of changes in their growth trajectories or an increased risk of thermal stress, and both processes may include intergenerational effects ( Figure 2).
However, there is a need for more ecological, biogeographical, and evolutionary studies on the impact of global climate change on patterns of senescence in wild populations of ectotherms (even more in invertebrates) facing warming conditions. This research should also investigate the possible role of candidate behavioural, cellular, and physiological mechanisms for buffering the predicted negative consequences of warming on the rate of ageing. We also need to understand the putative population consequences of changes in ageing rate, and to link these to location-specific predictions of climate change, to determine which populations and/or species are most vulnerable. Ideally, this information needs to be combined with species-specific knowledge on plasticity or evolutionary adaptability in response to thermal changes (Morley et al., 2019). Understanding the basic effects of climate warming on the ageing rates of ectothermic species will help in developing global and local scientific-based policies aiming at reducing the negative consequences of climatic change on biodiversity.

ACK N OWLED G EM ENTS
We thank three anonymous referees for helpful comments on the manuscript. P.B. was supported by a Marie-Skłodowska-Curie indi-

CO N FLI C T O F I NTE R E S T
We declare no conflict of interest.