Phylogenetic patterns in telomere lengths and TROC
In analyses of associations of TL values and life-history axes, strong
phylogenetic values indicate that correlations are not independent over
the history of the species. Species that are closely related may show
similar patterns. A good example was the correlation between TROC and
the body size axis (PC1), for which the “phylogeny-free” correlation
was actually different in sign from the unadjusted correlations (note
the high phylogenetic correlation; Table 2B). Alternatively, different
clades may show different patterns, such the Adult TL and pace of
life (PC2) correlation in the Passeriiformes (positive) and in the
Procellariiformes (negative) (note the high phylogenetic correlation;
Table 2A). After adjustment for phylogeny, residual correlations reveal
ahistorical associations, such as the fairly strong negative association
of TROC and PC2 (see below and Table 2B).
Adult and Chick TL among species were poorly explained by
phylogeny, while TROC showed the strongest phylogenetic signal (Figure
2). Life-history axes, however, were strongly associated with
phylogenetic history. Our result from 53 avian species confirms and
extends previous work done on 19 bird species
(Tricola et al., 2018). These results are
important to our understanding of how life histories and telomere length
on one hand, and the proximate factors that modulate telomere erosion on
the other hand, are inter-related. It suggests that similarity in
telomere lengths between species is not primarily due to
shared-ancestry. Moreover, there may be independent evolutionary
processes that have operated within different avian orders and families,
leading to the present diversity in telomere lengths. If the evolution
of life history traits is strongly constrained by phylogeny, butAdult and Chick TL are not, it may not be surprising that
PC1, 2 and 3 showed only weak associations with telomere lengths
measured at both stages of life. However, even after controlling for
phylogeny, we found that the remaining variance in PC axes andAdult or Chick TL were poorly related (Table 2). This supports
the hypothesis that telomere length evolved short and long forms at both
life stages, even in closely phylogenetically-related species that share
comparable life history traits. Our results seem to accord with a low
phylogenetic pattern of telomere lengths in mammals
(Gomes et al., 2011;
Seluanov et al., 2007). For TROC ,
the apparent high variability in telomerase activity in closely-related
species (Gomes et al., 2011;
Tian et al., 2018) suggests that there
should be little phylogenetic pattern, as we found.
We found no relationship between PC axes and Chick TL . We
expected slow-living species to exhibit more preserved and then longer
telomere lengths at the end of growth, given that rapid growth rate may
enhance telomere shortening (Monaghan &
Ozanne, 2018; Vedder et al., 2018).
However, it is too early for conclusions about the co-evolution of
growth and telomere dynamics at the chick stage. Given that telomere
lengths in early life are a complex mix of inherited traits and
environmental conditions (Dugdale &
Richardson, 2018; Eisenberg, 2019;
Vedder et al., 2017), more data are
needed on embryonic telomere lengths. Further comparative analyses
should include ecological variables that may highlight how specific
local conditions can influence Chick TL .
TROC (calculated over the chick to adult stages) appeared
moderately (our data) or unrelated to mean adult telomere length, such
that most species with long telomere lengths after growth were not
showing high rates of bp loss per year
(Tricola et al., 2018). This result did
not support the hypothesis that long telomeres erode faster because they
are more sensitive to damage, nor that species with short telomeres
should exhibit lower TROC over adulthood (as suggested by intra-specific
research; (Bize, Criscuolo, Metcalfe,
Nasir, & Monaghan, 2009; Grasman et al.,
2011; Salomons et al., 2009)). Whether
this could be the case for TROC calculated from earlier
development remains an open question, and the fact that we found a
negative relationship between TROC and Chick TL suggests
that, during growth, the mechanisms regulating telomere dynamics are
different than those in play during adulthood. As for TROC within
adults and chicks, these may reflect distinct and non-additive processes
defining species and trade-offs of individual growth, short-term chick
survival and adult lifespan (Boonekamp et
al., 2014), through a tightly-regulated balance between energy
investment in telomere maintenance and somatic growth. In addition, our
results suggest a coevolution of low TROC with increasing body
size along the bird phylogenetic tree. This conflict indicates that more
detailed studies are needed on how body size, embryonic development and
reproduction investments may be related to specific telomere dynamics.
However, the strong phylogenetic correlation of TROC and PC1 left
little evidence of a relationship between these variables under current
environmental conditions. In short, the strong phylogenetic pattern
rendered the apparent positive phenotypic correlations of TROC and PC1
non-significant and slightly negative.
Adult TROC was closer to zero in species that produced smaller
clutches and exhibited low embryonic growth rates on the slow-fast
continuum (more negative values on the PC2 axis). Of all the potential
associations of life histories and telomere dynamics, the association of
slow growth and low reproductive rate with less TROC was the only
consistent and significant pattern that we found, whether
phylogenetically adjusted or not, and univariate or multivariate. Little
TROC in slow growing species with low clutch sizes might be maintained
by genetic correlations among these traits. Such negative associations
between life history traits that divert energy from body maintenance and
TROC may reflect two mechanisms of selection. First, the selective
disappearance of individuals that were submitted to rapid telomere loss
early in life, either due to unfavourable growth trajectories or
unbalanced reproductive investments. This has been extensively discussed
previously (Dantzer & Fletcher, 2015;
Tricola et al., 2018): within
individuals, TROC values were significantly higher (i.e. a
greater rate of loss) than between-individuals, suggesting the selective
disappearance of individuals with short telomeres. However, comparisons
of between- and within-individuals TROC relationships with lifespan were
found to be consistent, suggesting that selective disappearance might
have a weak effect at the interspecific level. The second possibility is
that less TROC actually reflects the co-selection of
physiological or cellular mechanisms that protect telomere ends from a
rapid erosion. In our study, the TROC – PC2 relationship was
independent of body size effects, suggesting that it is not specifically
in the largest birds that a co-evolution of slow growth and low
reproductive rates with less TROC has taken place. Because telomerase is
expected to be inactive in somatic cells soon after birth in
large-bodied species (Seluanov et al.,
2007), the underlying mechanisms should be independent of telomerase.