Biogeography of telomere dynamics in a vertebrate

Canestrelli, Daniele; Bisconti, Roberta; Liparoto, Anita; Angelier, Frédéric; Ribout, Cécile; Carere, Claudio

doi:10.1111/ecog.05286

Cited by 15 publications

(13 citation statements)

References 14 publications

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“…Instead, they might reflect more local environmental conditions and/or genetical differences. These marked population differences in telomere length dispute the common practice of using 'species' as unit in meta-and comparative analyses, as recently suggested by Canestrelli et al (2020) and highlight the need to study telomeres at between-population level (Burraco et al, 2021). Future studies would benefit from closer examination of potential factors driving the observed between-population differences, and from assessing whether these differences in telomere length translate into between-population differences in lifespan, survival, and/or fitness proxies.…”

Section: Discussionmentioning

confidence: 96%

Population differences in the length and early-life dynamics of telomeres among European pied flycatchers

Kärkkäinen

Laaksonen

Burgess

et al. 2021

Preprint

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Telomere length and shortening rate are increasingly used as biomarkers for long-term costs in ecological and evolutionary studies because of their relationships with survival and fitness. Telomere length can be heritable, but both early-life conditions and later-life stressors can create variation in telomere shortening rate. Studies on between-population telomere length and dynamics are mostly lacking, despite the expectation that populations exposed to varying environmental constraints would present divergent telomere length patterns. Pied flycatcher (Ficedula hypoleuca) is a passerine bird spending the non-breeding period in sub-Saharan Africa but breeding across Eurasia (from Spain to western Siberia). Populations show marked differences in migration distance, genetics, breeding parameters, and egg components. We studied the large-scale variation of telomere length, early-life dynamics and heritability in the pied flycatcher by comparing six European populations across a north-south gradient (Finland, Estonia, England and Spain). There were clear population differences in telomere length, with English birds having the longest telomeres, followed by Spanish and lastly by Estonian and Finnish birds. Early-life telomere shortening rate tended to vary between populations, and faster nestling growth affected telomeres more negatively in northern than southern populations. The heritability of telomere length was moderate (h2 = 0.34 - 0.40), with stronger heritability to paternal than maternal telomere length. There was also evidence indicating that the level of paternal heritability could differ between populations. While the sources of between-population differences in telomere-related biology remain to be identified (i.e. genetics, environmental factors), our study illustrates the need to expand telomere studies at the between-population level.

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Section: Discussionmentioning

confidence: 96%

Population differences in the length and early-life dynamics of telomeres among European pied flycatchers

Kärkkäinen

Laaksonen

Burgess

et al. 2021

Preprint

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“…In another amphibian, the natterjack toad Epidalea calamita , a study across a continental case of dwarfism in Southern Spain found telomere differences between populations, but these did not match population variation in body size or habitat type and occurred in the absence of genetic isolation (Hyeun‐Ji et al 2020). Finally, a one‐year longitudinal common‐garden experiment investigated whether telomere dynamics, in the Sardinian tree frog Hyla sarda , differ in populations with contrasting biogeographic history (Canestrelli et al 2021). At the beginning of the study, telomere length was similar between populations.…”

Section: Telomere Dynamics Across Spatial Scalesmentioning

confidence: 99%

“…As previously mentioned in this review, telomere length seems to have an important heritable component; thus, studies comparing multiple populations need to be aware of the importance of disentangling environmental from genetic effects sensu lato. This might be a difficult aspect in natural populations, but conducting common garden or translocation experiments, together with the study of environmental variation, could be a useful approach (Salmón et al 2016, Fitzpatrick et al 2019, Canestrelli et al 2021). The use of experiments may also help to understand whether acclimation or local adaptation is governing the telomere dynamics, although this is a virtually unexplored aspect yet.…”

Section: Measuring Telomeres Across Spatial Patterns – Theoretical An...mentioning

confidence: 99%

Telomeres in a spatial context: a tool for understanding ageing pattern variation in wild populations

2021

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Ageing refers to the loss of organismal functionality with age, a process that is characterised by decreased reproduction and survival probability. In natural populations, it is expected that environmental conditions influence an individual's ageing trajectory. Understanding the role of environmental heterogeneity on ageing variation could provide critical insights into population resilience and species distribution but remains overlooked. Telomeres, the end cap of chromosomes, are a promising integrative physiological marker of an individual's health and a possible proxy to aid the understanding of variation in ageing trajectories. Here, we review the existing information on telomere length and its dynamics in wild populations distributed across spatial scales. Despite a relative scarcity of information, there is evidence for divergence in telomere length between populations facing contrasting environments. Nonetheless, a higher spatial resolution and temporal replication are needed to fully understand the role that environmental conditions play on telomere length variation. Since most of the existing studies are correlational, future field and laboratory experiments are required. For the first time, we demonstrate the use of population telomere data to predict species habitat suitability through species distribution models (SDMs). This represents a promising new research area in the study of ageing pattern variation in wild populations. Furthermore, the inclusion of telomere data in future physiological SDMs may improve our understanding of species distribution and population resilience. However, the use of telomeres within this context could be limited if no previous knowledge on the relevance of telomeres as markers of health and survival at the species level is available. Finally, we suggest some key practical and theoretical considerations that, ideally, future studies combining biogeographic and telomere data should pay attention.

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“…Reconstructing the evolutionary history of TL changes within recent radiations of closely related species that represent independent replicated branching events, may elucidate adaptations underlying shifts in TL during speciation (Baird, 2018). As species progress through series of changes in species ecology and life-history (Pepke, Irestedt, Fjeldså, Rahbek, & Jønsson, 2019), associated changes in telomere biology may be observed within taxonomically more densely sampled clades (Canestrelli et al, 2020; Dupoué et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Early-life telomere length covaries with life-history traits and scales with chromosome length in birds

Pepke

Ringsby

Eisenberg

2021

Preprint

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Telomeres, the short DNA sequences that protect chromosome ends, are an ancient molecular structure, which is highly conserved across most eukaryotes. Species differ in their telomere lengths, but the causes of this variation are not well understood. Here, we demonstrate that mean early-life telomere length is an evolutionary labile trait across 58 bird species (representing 35 families in 12 orders) with the greatest trait diversity found among passerines. Among these species, telomere length is significantly negatively associated with the fast-slow axis of life-history variation, suggesting that telomere length may have evolved to mediate trade-offs between physiological requirements underlying the diversity of pace-of-life strategies in birds. Curiously, within some species, larger individual chromosome size predicts longer telomere lengths on that chromosome, leading to the suggestion that telomere length also covaries with chromosome length across species. We show that longer mean chromosome length or genome size tends to be associated with longer mean early-life telomere length (measured across all chromosomes) within a phylogenetic framework constituting up to 32 bird species. Combined, our analyses generalize patterns previously found within a few species and provide potential adaptive explanations for the 10-fold variation in telomere lengths observed among birds.

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Biogeography of telomere dynamics in a vertebrate

Cited by 15 publications

References 14 publications

Population differences in the length and early-life dynamics of telomeres among European pied flycatchers

Population differences in the length and early-life dynamics of telomeres among European pied flycatchers

Telomeres in a spatial context: a tool for understanding ageing pattern variation in wild populations

Early-life telomere length covaries with life-history traits and scales with chromosome length in birds

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