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(definition) restoration, some reduction in telomere length will occur with each cell division, eventually giving rise to cell replicative senescence(definition) 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 sin