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.