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

Integrating telomere biology into the ecology and evolution of natural populations: progress and prospectsMonaghan, Pat1; Olsson, Mats2; Richardson, David S.3; Verhulst, Simon4; and Rogers, Sean M.5,6,*1. Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow Glasgow, G12 8QQ, UK.2. Department of BioEnv – Zoologen, University of Gothenburg, Sweden3. School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, Norfolk NR4 7TJ, UK4. Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands.5. Department of Biological Sciences, University of Calgary, Calgary, Canada6. Bamfield Marine Sciences Centre, Bamfield, Canada* corresponding authorOrcid Id:Simon Verhulst: 0000-0002-1143-686Pat Monaghan: 0000-0003-2430-0326Mats Olssen; 0000-0002-4130-1323Sean M Rogers; 0000-0003-0851-8050David S Richardson: 0000-0001-7226-9074Telomeres 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. Telomeres protect the chromosome, but in the absence of 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. That the basic pattern of progressive telomere loss and little restoration in most somatic tissues, as found in humans, might not apply to all eukaryotes had 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 non-model 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 non-model 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 appear to be conserved across the eukaryotes, and the range of species studied is still phylogenetically restricted, differences in detail are increasingly being revealed (Monaghan et al. 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 (Remot et al 202x, Brown et al. 2022). 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 non-model organisms will have greater impact as discoveries will 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.Ecological and environmental stressorsExposure 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 (Kärkkäinen et al 202xa), 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 ofNothobranchius 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 et al 2021b). 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 non-model organisms has been primarily focused on the endothermic vertebrates - birds and mammals. Nucleated red blood cells are primarily used in bird studies while white blood cells are most often in mammals, particularly humans. Thus, tissue specificity in telomere dynamics associated with these cell types may itself underlie some of the differences reported. However, 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 alligatorAlligator 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 at which affected their not significantly their telomere dynamics et al. may on how the potential is by the in a but still potentially linked to differences in stress a study by et al. (2021) used of within-individual of change in telomere length to the of on telomere dynamics in the the . They found that and predicted telomere dynamics. at processes in more et al. (2021) into the telomere dynamics of a natural of , of the telomere in female of They also that experimentally induced stress exposure in induced and telomere these studies that variation in stress exposure and individual can contribute to differences in telomere dynamics. 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