Integrating telomere biology into the ecology and evolution of natural populations: Progress and prospects

Telomeres are fascinating stretches of protective DNA that cap the chromosome ends of eukaryotes. Without telomeres, during cell division and DNA replication, DNA repair proteins would misread the ends of chromosomes and attempt to repair or remove this region of the genome, leading to instability. Furthermore, the loss of DNA that inevitably occurs during cell replication due to the “end replication problem” and oxidative damage would erode the coding sequences of chromosomes, eventually causing genome malfunction. Thus functional telomeres protect genome integrity. In the absence of telomere restoration, some reduction in telomere length will occur with each cell division, eventually giving rise to cell replicative senescence often followed by cell death. Short and/or dysfunctional telomeres underly many disease states and are associated with ageing. Consequently, telomere biology is a vibrant area of biomedical research. However, until relatively recently, most of the research on telomeres has been focused on humans or animal models. The basic pattern of progressive telomere loss and little restoration in most somatic tissues, as found in humans, might not apply to all eukaryotes and has received relatively little attention. In fact, any variation in the expected pattern of decline in chromosomal telomere length with progressive rounds of cell replication, as observed in most human tissues, was initially attributed to methodological issues. Importantly, the science of studying telomeres has now expanded to encompass nonmodel organisms. Variation in the pattern of telomere loss and restoration across a range of species promises to reveal great insights into the drivers of life-history trade-offs and evolution, population ecology and consequences of exposure to environmental stress in natural populations. The burgeoning interest in telomere dynamics in nonmodel organisms and increased communication between biomedical researchers and evolutionary ecologists is now enriching our understanding of the diversity of telomere dynamics. While the basics of telomere biology do indeed appear to be conserved across almost all eukaryotes, and the range of species studied is still phylogenetically restricted, differences in detail are increasingly being revealed (Monaghan & Ozanne, 2018). We now have information on how the pattern of telomere change can vary among species and include lengthening as well as shortening across the life course (Brown et al., 2021; Remot et al., 2021). Our understanding of how these patterns relate to environmental factors, species, individual histories and population process is increasing. Furthermore, telomere biology has the potential to be used in conservation biology, providing information about individual and population health (e.g., Eastwood et al., 2022). The molecular ecology of telomeres in nonmodel organisms will have greater impact as new discoveries increase our understanding of the genomics, ecology and evolution underlying telomere diversity. This Special Issue brings together a collection of papers that illustrate the breadth of taxa now being investigated and ways in which emerging hypotheses, formed from the perspectives of ecology, evolution and conservation, are being tested. In this introduction, we highlight how this body of work, including new information and insights, points the way to many research questions that remain to be investigated in this emerging, cross-disciplinary area of biology. Many hypotheses have been put forward about how telomeres function, and how they relate to whole organism outcomes. These hypotheses have their roots in different disciplines and biological levels, and some appear contradictory. The study by Tobler et al. (2021) provides a broad perspective on the literature to date. They spell out the hypotheses most likely to be of interest to ecologists and provide a framework that can be used to clarify and guide further research questions. They group the hypotheses in terms of the biological issues addressed, mainly telomere length and loss in the context of ageing, individual quality and health, life history trade-offs and physiological processes, identifying underlying assumptions and inter-relationships. Exposure to stressful environments can have long lasting effects on health and longevity, and some of these effects are linked to changes in telomere dynamics. In addition to furthering our understanding of the mechanism underlying these adverse effects, the study of telomere dynamics in relation to environmental conditions offers the potential to measure the scale and extent of their impact at individual and population levels (Burraco et al., 2022; Kärkkäinen et al., 2022), evaluate environmental quality and examine the effect of conservation measures, such as habitat restoration. In this Special Issue, Brown et al. (2021) report apparent telomere lengthening in both sexes associated with increased survival in a small passerine bird, the Seychelles warbler Acrocephalus sechellensis. However, sex-specific effects of stressors influenced the patterns of telomere change. In females, stress induced by low food availability and malarial infection was associated with the expected telomere shortening, but there were no such effects in males. Moreover, less exposure to such stresses appeared to lead to telomere lengthening (Brown et al., 2021). Reichard et al. (2021) also report intraspecific variation in the outcome of stress exposure using African killifish. This involves strains derived from wild populations of Nothobranchius furzeri and its sister species, N. kadleci, from sites along a strong gradient of aridity, which ultimately determines maximum natural lifespan in these species. Interestingly, they demonstrate that individual condition and environmentally-driven selection can modulate the relationship between telomere length and lifespan in opposite directions, validating the existence of inverse trends within a single taxon and again highlighting the importance of sex-specific effects. Altogether, the apparent association between telomere lengthening and stress exposure (see below for further examples) and among individual differences in telomere dynamics, for example in relation to age, sex or individual history, require further investigation. Such studies need to use accurate and repeatable within-individual measurements where possible and bear in mind the need to take measurement error into account (Steenstrup et al., 2013). Intrinsic and extrinsic stress exposures in early life are known to have substantial and long-lasting effects on phenotypic development. Conditions experienced inside the cell or from the external environment during growth can influence telomere dynamics, as shown in this Special Issue. In European badgers Meles meles, van Lieshout et al. (2021) report that cubs born in warmer, wetter springs have longer telomere lengths, which is in turn linked to survival. In purple-crowned fairy wrens (Malurus coronatus) the rate of telomere shortening in the first year of life predicted lifespan (Sheldon, Ton, et al., 2021). More broadly, it has been hypothesized that measuring the effects of adverse environmental conditions induced by anthropogenic stressors (such as chemical pollutants, noise and inappropriate light) on telomere dynamics could assist in the monitoring and conservation of wildlife. In this context telomere measurements have the potential advantage over many other biomarkers of representing a potential fitness proxy, allowing effects to be studied over a time scale that could be much shorter than required to measure actual fitness consequences. In line with this, Salmón and Burraco (2022) evaluated the use of changes in telomere dynamics as a way of assessing such anthropogenic impacts, providing an exhaustive literature review and meta-analysis. Oxidative stress induced by internal and external factors can be a major cause of DNA damage which could increase telomere attrition. Metcalfe and Olsson (2021) provide a compelling case that endogenous reactive oxygen species produced in the mitochondria create links between mitochondrial function, DNA integrity and telomere dynamics. They argue that telomere dynamics are best understood when considering the optimal solution to the trade-off between energetic efficiency and chromosomal protection that will differ among individuals and change over time, depending on resource availability, energetic demands and life history strategy. Such inferences may cumulatively help explain why the effects of stressors on telomere dynamics are evident (but apparently also stressor, taxon, and sometimes sex-specific). Clearly the research directions proposed in this Special Issue will contribute to a better understanding of these mechanisms that link environment, lifestyle and telomere dynamics. At present, telomere research on nonmodel organisms has been primarily focused on the endothermic vertebrates - birds and mammals. Amongst the mammals, one group that has been relatively little studied in this context but is of great interest given their much longer than expected longevity for their body size, is the bats. Power et al. (2022) provide an overview of what we know about this group so far, and how variation in their telomere dynamics relates to their ecology and life history traits. They also discuss and illustrate how future genomic approaches might provide important new insights. In telomere studies, especially where the sampling is longitudinal, DNA from nucleated red blood cells is primarily used in bird studies while DNA from white blood cells is most often used in mammals, particularly humans. Thus, it is important to bear in mind that tissue specificity in telomere dynamics associated with these cell types might itself underlie some of the differences reported. We should also bear in mind that the majority of animals are ectotherms and often differ from many endotherms by having telomerase production in somatic tissues. Furthermore, many aspects of ectotherm development and performance are linked to environmental temperature and are, therefore, potentially significantly affected by climate disruption. Friesen et al. (2021) suggest that developing thermal performance curves for the processes affecting telomere dynamics could assist in monitoring climate impacts, highlighting the pressing need for more experimental work in this area to isolate the causes of environmentally induced changes in telomere dynamics. Rouan et al. (2021) present such an experimental study on the coral, Stylophora pistillata, in which bleaching, the devastating loss of symbionts that can results from climate change, was induced by continuous darkness. This resulted in increased telomere loss. As well as telling us something about the damaging effects, these findings could inform methods for monitoring coral reef health. In a field experiment using young salmon Salmo salar, in freshwater streams, McLennan et al. (2021) found that both a lack of suitable substrate and living at high density were associated with reduced telomere length. However, in streams in which nutrient levels were experimentally restored, these adverse effects on telomere length were greatly reduced, demonstrating the potential utility of changes in telomere length in a conservation context. Further, the experiment presented by Bae et al. (2021) revealed that the effects of temperature can be influenced by interactions with pollutants. This appears to be especially prevalent in species with temperature-dependent sex determination, such as the American alligator Alligator mississippiensis. Here, the effect of experimental exposure to an endocrine disrupting chemical depended on the environmental temperature; at temperatures promoting female development, the effect on telomere length was positive, while at the higher, male promoting temperature, the effect was negative. On the other hand, raising crickets at different temperatures, which strongly affected their growth, did not significantly affect their telomere dynamics Boonekamp et al. (2021). Much may depend on how severely the potential stressor is perceived by the organism in question. In a somewhat different context, but still potentially linked to differences in stress exposure, a nonexperimental study by Wood et al. (2021) used extensive longitudinal assessments of within-individual rates of change in telomere length to investigate the impacts of dominance status on telomere dynamics in the cooperative breeder, the white-browed sparrow-weaver Plocepasser mahali. They found that social dominance and rainfall predicted telomere dynamics. Looking at mechanistic processes in more detail, Wolf et al. (2021) provided novel insight into the telomere dynamics of a natural system of tree swallows Tachycineta bicolor, reporting lower expression of the telomere regulatory gene POT1 in female breeders of higher quality. They also reported that experimentally induced stress exposure in chicks induced lower POT1 expression and telomere lengthening. Collectively, these studies show that variation in stress exposure and individual resilience can contribute to intraspecific differences in telomere dynamics. They highlight the need to consider the biology of the species (including sex differences), the local conditions to which it has been exposed, what different levels of temperature change mean in terms of stress exposure for different species and populations, and the need to examine interacting environmental effects in natural populations. They also highlight that examining telomere dynamics in relation to differential expression of relevant genes associated with ecological and environmental variables could potentially be of great interest. Much of the interest in telomeres from ecologists relates to their potential in mediating life history trade-offs. For example, is increased telomere damage traded off against potential advantages of larger size or greater energy expenditure? The outcome of such trade-offs may be influenced by individual state. Such state-dependent relationships are difficult to measure but variation in telomere length, or loss, might provide a relative measure. Carrying elaborate sexual ornaments is thought to be costly thereby maintaining the honesty of the signal, but there have been few studies done to test the relative cost of ornamentation using telomeres. Kauzálová et al. (2022) found that barn swallows Hirundo rustica, with long tail streamers (a sexually selected ornament (Møller, 1988), have shorter telomeres. This suggests a cost to elaborate ornamentation in this species. Ravindran et al. (2022) used bivariate analysis to decompose correlations between telomere length and reproduction into within- and among individual effects. They conclude that, in wild Soay sheep Ovis aries, females had shorter telomeres in August in years in which they gave birth in spring compared to years without the gestation effort, indicative of a trade-off involving reproduction. However, at the same time in years in which they gave birth, the mother's telomeres were longer when their lambs survived to August, compared with years when they lost their lambs earlier, suggesting complex state dependent effects. Sepp et al. (2021) conducted a cross-fostering experiment in common gulls (Larus canus), to tease apart pre- and post-natal parental age effects on offspring telomere length. Neither the age of the natal- nor the foster parents in this study predicted the length or rate of change of telomeres in chicks. The above results are interesting, but also demonstrate that additional experimental work is needed, particularly in relation to evaluating parental state-induced telomere dynamics. A good example is provided by Atema et al. (2021) who manipulated individual state by equipping male great tits Parus major with a “backpack” adding 5% to their body mass for a year. Surprisingly telomere dynamics were not affected by this extra burden, despite the duration of the experiment and large sample size. However, the absence of an effect was consistent with there being little evidence of a fitness costs of carrying this extra mass (Atema et al., 2021), information which is often lacking but critical for the interpretation of any result. In the dark-eyed junco Junco hyemalis, where experimentally elevated testosterone reduces male survival (Reed et al., 2006), elevated testosterone was also linked to accelerated telomere attrition Heidinger et al. (2022). This suggests that telomere dynamics may be part of the mechanism causing the testosterone effect on survival in this species, and that variation in state is an important issue. Trade-offs involving telomeres may also occur very early in life, for example, when resources are allocated to growth at the expense of somatic maintenance, potentially being reflected in early life telomere dynamics (Monaghan & Ozanne, 2018; Vedder et al., 2018). Growth is difficult to manipulate directly and is often done through dietary manipulations, which might have confounding systemic effects that can be difficult to fully take into account. Pepke, Michael, et al. (2022) examined the effect of nestling body size on telomere length within an artificial selection experiment on body size (tarsus length) in free-living house sparrows Passer domesticus. They studied two island populations, with selection for large body size on one island, and selection for small body size on the other. The experiment was successful in creating a difference in tarsus length between the - of almost in the selection year. They found a in telomere length on the island with selection for large body size, but no change on the island with selection for small body size. The of Pepke, Michael, et al. (2022) will be followed by potentially using selection on growth and body size. to fully the results it may be important to also know more about cell division rates and growth patterns in the individuals different body While the pattern from human studies is that telomeres with age, findings in other species, including in this Special Issue in relation to stress exposure, suggest that this is not the case by Remot et al., in this For example, there is evidence of telomere in some and et al., 2018). This questions about the underlying mechanisms in telomere maintenance, with variation in telomerase as a likely et al. (2021) review what is known about telomerase in ecological studies and discuss the in measuring telomerase They that studies have not the expected link between telomere and telomerase for which there can be different telomeres are studied in it is mainly the telomerase in the cells in the that will affect the telomeres, but studying this within individuals is very et al. evaluated the effect of on telomerase in gulls (e.g., or as their to offspring is a potential cost associated with adverse or stressful conditions experienced by They found that can telomerase and longer telomeres during development, suggesting mechanistic links by which may offspring life-history and In et al. (2021) levels of DNA across early life in nestling that was with telomere length providing possible links between and telomeres. Altogether, the ecology of gene expression and in telomere across natural populations should be an important for the et al. (2022) discuss what is known about and telomeres in the a of interest telomeres have been studied in the context of with somatic of telomerase as a protection mechanism in large species. has been as critical that are associated with et al. (2022) that dynamics a complex and a in part in humans both long and telomeres can be associated with an increased effects can be observed in natural populations of other species to be length survival within species et al., raising the as to species have relatively long telomeres. this not appear to be the case et al., at when using the of maximum In et al. reported an inverse relationship between telomere length and maximum lifespan in mammals. Pepke, Michael, and (2021) and the of et al. and this inverse A possible for this pattern is that telomeres protect against cells with telomeres have less for replication telomeres cell replicative In line with this Pepke, Michael, and (2021) show a association between telomere length and the development of tissue growth that can into They further show that species have longer telomeres than wild species with This may be of artificial selection of or of selection in for example, animals will often be the natural of their selection protection against the development of of the most aspects of telomere biology is the range for the of telomere length the parental affecting the telomere length in the its on telomere biology report the range in of any phenotypic from to more than one due to sampling Olsson et al., 2018). This telomere evolution difficult to with evolutionary from the more complex when the is to the potential of telomere evolution and the of to using for this is to as the expected change a of a These two measures, and have been shown to have due to correlations between the and other of the phenotypic (e.g., and dominance et al., In this Special Issue, aspects of of telomeres and their dynamics are is particularly difficult to from different of species in the a on a study of wild common with blood in study Vedder et al. (2022) found differences in post-natal telomere length and a strongly with The for understanding telomere its and for evolutionary are et al., 2021), and the environmental & 2018). A from is that when environmental is will be very which is what et al., 2021; found in their on field crickets Importantly, are so to what these to telomere selection in the wild to be tested. attempt to do this in a cross-fostering experiment on that for telomere length was high for telomere shortening rate it was lower et al., 2021). This with evolutionary in that telomere shortening in this taxon is more strongly with of fitness than is telomere length et al., and Interestingly, the for telomere length of et al. (2021) was and with in with the review of In in a study with greater sample size and than most studies on telomeres in wild et al. (2021) found low and for telomere length in Seychelles suggesting differences may among species. The collection of studies in this Special Issue the interest in studying telomeres from an evolutionary and ecological and their potential in such as conservation biology. The studies reported highlight that demonstrate the effect of environment on telomere dynamics and the impact on life history trade-offs and consequences. In the studies highlight and where additional studies would the For example, studies on have that telomerase across the are to and eukaryotes, the of a common for telomerase et al., They also provide evidence for the of telomeres for important such as time et al., 2021). However, on telomere in with variation in life body growth patterns and remain More work is on species with complex life high and studies will of hypotheses of telomere evolutionary history, life-history and chromosomal integrity. studies of telomere dynamics have from studies of animal is much to be from the within-individual from such studies and variation in population In for individuals having a environment between the could be by cross-fostering in many species and/or and by offspring at in species without parental et al., or by for environmental in longitudinal studies or experimental and animal The large for telomere work can be by of and by emerging in molecular to be particularly for especially in species with telomeres et al., et al., et al., However, the potential importance of how telomere influence the biology of different taxa has been investigated at all (see et al., for of is important that telomeres measuring are as accurate and as while allowing for large sample to by of is also of these issues are in this Special Issue in major methodological effects on of individual et al., and et al., 2021). A the single telomere offers a for measuring the and of individual telomere et al., & 2021), its to be In the future the use of may higher than telomere analysis et al., and more than Pepke, Michael, et al. (2022) examined and using a of and that new approaches using telomere may higher and of telomeres and their effects on fitness 2021; & many questions to telomere biology in relation to ecology evolution and conservation remain to be For evolutionary and variation is the of and understanding the causes and consequences of such and the of telomeres within that is an important and We still know relatively little about how telomere biology is different selection and to what extent it the of potential life for example in relation to growth, body size, reproduction and In terms of we may what telomere loss or telomere length and loss rate have been found to be of longevity within species and much may depend on the life at which each is it that telomere length would lifespan until relatively age, when cell are and cells show telomere loss might us a better on understanding stress exposure and stress In humans and there is evidence that telomere length variation at the of growth and that telomere length at this time is the best of lifespan et al., et al., Heidinger et al., patterns be revealed in species with we do not have the to this so much more work is in this In a conservation context, can telomere biology help us populations at from environmental due to anthropogenic effects, and species that are likely to be to climate change and stress that the of are now used to the of species in to climate change et al., 2022), it is possible that the of telomere biology may further inform and such in species models. Altogether, this collection of studies the potential for the of ecological and genomic approaches to to our understanding of the consequences of and extrinsic environmental stressors and change on the ecology and evolution of natural populations. This Special Issue how a of the of telomeres and associated of the genome will to the field of molecular is not to this as no new were or in this

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