Discussion
Our first question concerned the association of lifecycle and telomere variables with the phylogenetic pattern across 30 species of birds. Lifespan and body mass are well known to covary among bird species and exhibit strong phylogenetic constraint (e.g. , Bennett and Owens 2002; Dantzer and Fletcher 2015; Criscuolo et al. 2021). Less is known of phylogenetic influences on telomere dynamics, but Tricola et al. (2018) suggested little phylogenetic influence on telomere length and a significant influence on TROC. We found the expected fairly strong association of phylogenetic pattern and lifespan, body mass, and mass-predicted lifespan, but at best weak associations of the phylogeny with mass-independent lifespan (long or short life at a given body size). Telomere length and the rate of decline in telomere length over time exhibited trivial to weak associations with the phylogeny, contrary to the suggestion of Tricola et al. (2018). Given the fairly strong association of phylogeny with lifespan and body mass, however, it seemed reasonable to account for the phylogenetic pattern statistically when evaluating associations of lifespan, body mass, and telomere dynamics.
Our second question was whether there was a strong association of lifespan and TROC, as suggested by Dantzer and Fletcher (2015) and Tricola et al. (2018). For this, we considered two aspects of longevity. Large animals live longer, as shown by a large number of studies on life-history traits that scale with body size (e.g. , Gaillard et al. 1989; Read and Harvey 1989; Roff 1992; Stearns 1992; Bennett and Owens 2002; Dobson and Jouventin 2007). Larger animals take longer to grow to adult size and must allocate considerable resources and effort to maintaining their large number of cells. As such, the first question about longevity is whether it is associated with the overall size of an organism (Dobson 2007). The second aspect of longevity is associated with the pace of life, along the so-called “slow-fast continuum” (Gaillard et al. 1989; Dobson and Oli 2007). At a given body size, some species have greater maximum lifespan than others, and this may be associated with lower reproductive effort, and vice versa for short-lived species. Thus, alternative life-history tactics may be produced among species, at a given body size.
For the first aspect of lifespan, that associated with the size of the species, mass-predicted lifespan had a small association with TROC, with or without statistical adjustment for the phylogenetic pattern (Figure 2b). However, our lifespan variable that was independent of body size (viz., mass-independent lifespan) had a strong positive association with TROC as judged by effect size, and the association became stronger with statistical adjustment for phylogeny. These results suggest that TROC does not vary strongly with body size per se , but rather has at best a poor association with body size, such that longer-lived species that are somewhat larger exhibited slightly less telomere loss than somewhat smaller species. However, at a given body size, birds exhibit a stronger pattern of association of relative longevity (i.e., a slow pace-of-life) and TROC. Species with the longest lives for their body mass exhibited the slowest rate of loss of telomeres during life. Thus, the division of lifespan into two parts associated with different aspects of life histories reveals biologically meaningful patterns of varying strengths.
The analyses of Dantzer and Fletcher (2015), Tricola et al. (2018), Udroiu (2020), and Le Pepke and Eisenberg (2020) revealed a general pattern of positive association of longevity and TROC, but without testing for different underlying aspects of longevity. Our results reveal nuances to their conclusions: longevity and TROC increase together as body size increases, but a much stronger pattern was the association of longevity and TROC increasing together at a given body size. Together, these two patterns likely underlie the positive associations of longevity and TROC found by previous studies.
Our final question was whether adult telomeres were shorter in the larger and longest-lived species, as suggested by Gomes et al. (2011) and Pepke and Eisenberg (2021) for mammals. This latter study suggested that telomere length coevolved with body size, such that large species have short telomeres, and thus facilitated the evolution of long lifespans, notably via the use of cell replication senescence and the reduction of risks of cell immortalization (Risques and Promislov 2018; Seluanov et al. 2018). On the other hand, Tricola et al. (2018) found a slight but non-significant positive association of telomere length and maximum lifespan among 19 species of birds. While we found that both longevity and body mass followed the phylogenetic pattern fairly closely, telomere dynamics did not. Nonetheless, we found a moderate pattern of larger species having shorter telomeres, with or without statistical adjustment for the influence of the phylogenetic pattern (Figure 2a). In the light of our results, postulating that large birds use replication senescence, as large mammals do, as a mechanism favouring long lifespan is still an unanswered question. This begs the question of whether at least some bird species have evolved specific anti-ageing or anti-cancer mechanisms that are similar to the telomere-related control suggested for long-lived mammalian species that weigh less than a kilogram (Gomes et al. 2011; Tian et al. 2018; but see Seluanov et al. 2018).
Comparative studies like the present one help to point out how aging mechanisms at the cell level may have coevolved with life histories among animal species. So far, as we have seen above, comparative studies have concluded that large body size and long lifespan have evolved with short telomeres and reduced loss of telomeres in mammals, or that longevity and reduced loss of telomeres (but not short telomeres) are matched in birds. This discrepancy might be attributed to the smaller range of sizes in birds, suggesting that if body size and the number of cells is the main constraint to the evolution of long telomeres, this may explain why birds show higher levels of telomere maintenance (e.g. , via an enhanced telomerase expression) than mammals and long up-to Mb telomeres (Delany et al. 2000; Monaghan 2010). Our analysis that controls for the effects of body size suggests that enhanced telomere maintenance has coevolved with longevity in birds independently of body size, and this differently, even in closely related species. This is, in addition to the high glycemia and aerobic metabolism, a paradoxical association with avian longevity (Holmes and Harper 2018), a new aging enigma that requires continued exploration in relation to species’ evolutionary histories.