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In the light of this we used consistent storage and extraction protocols, and if small changes were made, we were able to validate that, within this sample set, it did not influence telomere measurement. For specific methodology on the in-gel TRF assay used in this study see Haussmann et al.

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  5. The rate of telomere loss is related to maximum lifespan in birds.

The amount of radioactive signal optical density, OD in each lane corresponds with the amount of telomere at that position on the gel i , and was quantified by densitometry in ImageJ v. Background signal from nonspecific binding of the radioactive probe was subtracted from all OD measures. However, regardless of the molecular marker used, the distance each band of the molecular marker migrated i was plotted against the molecular weight in kilobases and converted into molecular weights L using a three-parameter log-linear function.

Thus, we made a heuristic assumption of a linear rate of telomere loss across all ages as it allowed for unbiased TROC estimates due to differences in the range of the species lifespan sampled. Differences among species' mean telomere length and TROC were assessed in a linear model. The relationships between telomere length or TROC with maximum lifespan among species were assessed using comparative analysis.

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In comparative analysis, shared ancestry violates the assumption of independence among data points, and including phylogenetic information statistically accounts for such dependence. To this end, phylogenetically corrected regressions were analysed using generalized least squares assuming a Brownian correlation structure in package ape in R [ 53 ]. The phylogeny we used was extracted from a bird supertree [ 54 ]. Our models therefore do not incorporate phylogenetic uncertainty [ 56 ].

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  • The phylogenetic signal—the amount of variation among species explained by shared ancestry [ 57 ]—in both TROC and mean TL was analysed in phytools [ 58 ]. Trait evolution was plotted on the phylogeny in phytools [ 58 ] in R. Our main hypothesis centred on if and how TROC is associated with maximum lifespan across species hypothesis i.

    However, we also explored whether mean telomere length is associated with maximum lifespan across species, as is the case in mammals hypothesis ii [ 11 ].

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    To this end, we fitted several models around these predictors, and also included body mass as a covariate [ 60 ]. Body mass log 10 -transformed was included because of the clear associations between body mass and longevity [ 61 ]. Mean telomere length and TROC were log 10 -transformed prior to analysis. Telomere length increased with age in two species H. Including or removing these covariates allowed us to investigate any sensitivity of our results to mean telomere length and body mass, but the results were similar in all models.

    We prefer the presentation of full models rather than performing model selection, since full models show the full range of the predictors investigated both significant and nonsignificant and are not as likely to inflate type I error [ 62 ].

    In addition, our comparative dataset allowed us test two other specific hypothesis presented in the literature. First, we considered the telomeric brink hypothesis hypothesis iii [ 42 ] , which suggests that telomere shortening is causal in the ageing process, and when telomeres become too short they cause death. Here, the prediction is that species with both short average telomere length and faster telomere shortening rates would also have shorter maximum lifespans.

    If such a relationship is present in the data this should result in an interaction between mean TL and TROC against maximum lifespan of a species.

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    Second, we tested the prediction that species with longer telomeres may exhibit faster telomere shortening, which was suggested previously within-species hypothesis iv [ 63 ]. We performed a phylogenetic regression of mean TL against TROC, where a positive relationship would suggest that those species with longer telomeres also show more rapid telomere loss. Some species show very sharp declines in telomere length with age, while others even increase with age. Maximum observed lifespan as a function of a telomere rate of change TROC and b mean telomere length in 19 bird species. The dashed lines represent the regressions from the phylogenetic regressions without any other covariates included.

    Models were tested with and without body mass log 10 -transformed as a covariate, and with and without mean telomere length as a covariate. Telomere rate of change TROC is the only significant and strong predictor of maximum lifespan variation among species, with greater telomere loss rates associating with shorter maximum lifespan hypothesis i.

    TROC was not related to mean telomere length of a species hypothesis ii. Note that when K is larger than 1 it indicates that phylogenetically related species are more similar than expected under Brownian motion [ 59 ]. Trait evolution of telomere rate of change TROC mapped to the phylogeny in 19 bird species. Colours indicate different levels of the trait value transformed values were used for mapping, but linear values are depicted for illustrative purposes in the legend.

    TROC shows a strong phylogenetic signal and the major families or clades of species which were included in this analysis show similar rates of telomere loss with age. Our study confirms previous reports that species with greater TROC have shorter maximum lifespans hypothesis i [ 35 — 37 ]. By contrast, among the species sampled here, mean telomere length was not associated with longevity hypothesis ii. In support of this suggestion, TROC shows a strong phylogenetic signal, whereas absolute telomere length does not, although it does vary widely among species.

    TROC, in contrast to absolute telomere length, therefore, appears evolutionarily conserved and selected within bird families. We acknowledge that this inference is less firm when phylogenies are small, but the difference in phylogenetic signal is striking when considering the potential biological significance of telomere length loss compared to absolute telomere length. The pattern reported here between TROC and lifespan may be caused in part by selective disappearance, in which certain phenotypes are preferentially removed from a population [ 41 ].

    Since our study is cross-sectional in nature due to the lack of long-term study populations and the long lifespans of some species, the relationship between TROC and lifespan could be a result of selective loss of short-lived individuals from the environment. This selective disappearance of particular individuals [ 41 , 64 ]—those with short telomeres—can cloud the relationship between telomere loss and age in a cross-sectional context [ 65 ].

    For example, the positive relationship between telomere length and age seen in Leach's storm petrels O. It is also possible that selective disappearance is responsible for the positive relationship seen in the Eurasian oystercatcher H. It is difficult to translate a cross-sectional pattern within species to within-individual processes for that species.


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    Future longitudinal studies will allow us to distinguish between population differences that result from the removal of certain phenotypes earlier in life than others. At the moment, longitudinal studies of ageing in free-living populations are rare, but are needed because of their greater power to identify age-related changes compared to cross-sectional studies [ 31 , 66 , 67 ]. However, in a comparative context, cross-sectional studies can still broadly inform us about the biology of ageing and lifespan, though we lose the ability to firmly conclude that these patterns are resulting from processes within individuals.

    The degree to which selective disappearance differs among species can be caused by differences in extrinsic mortality rates and differences in how age-related mortality is influenced by telomere biology. Classical evolutionary theories of ageing predict that extrinsic mortality levels should be inversely correlated with evolved lifespan [ 68 ].

    In other words, short-lived species generally face higher risk of death due to predation, starvation or accident. Given this, one interpretation of our results is that if there is selective disappearance of individuals with short telomeres, this pattern may be partially concealed in populations of species where individuals are removed from the population due to random processes regardless of their condition.

    This is not to say that selective disappearance based on telomere length is not occurring in short-lived species, only that it may be more readily obscured.

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    Conversely, if telomere erosion does in fact increase mortality risks, then one might expect that this would be more evident in long-lived species with lower rates of extrinsic mortality where functional senescence is more easily observed. If extrinsic mortality differences are a major driver of selective disappearance based on telomere length this may explain why the species displaying patterns that most closely resemble selective disappearance are two of the longest-lived species we studied, the storm petrel and oystercatcher.

    However, regardless of species differences in extrinsic mortality, the degree to which telomere biology affects intrinsic ageing processes may also differ across species, thereby affecting selective disappearance. In other words, some species might have a stronger relationship between telomere biology and survival prospects compared to others. Hence, selective disappearance could be stronger in species that are long-lived and for whom telomere biology is more important.

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    Therefore, selective disappearance may be due to both differential association of intrinsic mortality with telomere length and differences in extrinsic mortality that reduce the importance of telomere length in determining mortality at the population level. Regardless of either of these causes, the comparative pattern we find suggests that as the longevity of a species increases, telomere biology becomes increasingly important.

    Moving forward, more longitudinal data are sorely needed to disentangle the possible scenarios outlined above that can result in the cross-sectional relationship we report here. Such efforts will allow us to understand more details of the deteriorative process of senescence in general [ 67 ], and how selective disappearance occurs in species of differing lifespan in particular.

    While selective disappearance may be partially responsible for the pattern we observe between TROC and lifespan, another possibility is that telomere erosion is a potential mechanism underlying the evolution of lifespan in birds, with short-lived birds losing more telomeres each year compared to long-lived birds.

    A recent meta-analysis of 14 avian species reported that the rate of telomere loss is correlated with maximum lifespan estimated from a composite measure of life-history traits [ 36 ]. Another recent study, using existing data from longitudinal studies in bird species, confirmed a negative relationship between the rate of telomere shortening and maximum longevity [ 37 ]. Both of these recent studies provide additional support for the hypothesis that telomere attrition is correlated with interspecific rates of ageing.

    The underlying mechanisms responsible for this relationship are still unknown, and selective disappearance, physiological mechanisms that ameliorate telomere loss, or some combination of the two may be at play. In search for physiological mechanisms that underlie the evolution of lifespan, comparative analyses have revealed that across avian and mammalian species, those species with longer lifespans also have cells that are both more resistant to external stressors [ 69 ] and have lower rates of mitochondrial free radical generation [ 70 ].

    One possible physiological explanation for the different rates of telomere loss in the avian species in our study is that they also had different levels of oxidative stress. Oxidative stress can increase single-stranded breaks in telomeric regions of DNA that can cause telomere shortening during DNA replication due to a proposed pausing of the replication fork [ 13 ], though this work is mainly based on in vitro evidence, and whether it holds in vivo has recently been questioned [ 71 ].

    Nevertheless, species with higher levels of oxidative stress may experience more rapid telomere shortening. Interestingly, this may be due in part to free radicals' preferential damage to the guanine-rich telomeric sequence in comparison to other regions of DNA [ 72 ]. This may allow telomeres to act as a free radical magnet, soaking up damaging free radicals while protecting coding regions of the chromosome.