Introduction
Senescence affects most living organisms
(Gaillard, Lemaître, & Fox, 2020). With
advancing age, individual performance in reproduction, physical
activities, or cognition diminish, while concomitantly the rate of
actuarial senescence (i.e. mortality rate with age) increases
(Nussey, Froy, Lemaitre, Gaillard, &
Austad, 2013). The age at which senescence occurs varies among species
and individuals (Gaillard et al., 2020),
while energy gathered from the environment may be differently allocated
to promote self-maintenance, and thus delay ageing
(Bouwhuis, Charmantier, Verhulst, &
Sheldon, 2010; Jones et al., 2008;
Ricklefs, 2008). The view of senescence
as an outcome of energy trade-offs that underlie life history
trajectories has shaped our understanding of the evolution of animal
longevities. Fast living species, with rapid growth, early sexual
maturity, and high reproduction rates experience senescence earlier
(Jones et al., 2008). However, whether
trade-offs are the only determinants of the rate of senescence has been
debated, and environmental and biological constraints may also be
influential, particularly in comparisons among species
(Cohen et al., 2019). In addition,
senescence might differently affect phenotypic traits in relation to
their impact on fitness (Hayward et al.,
2015), with senescence in reproduction beginning at different points in
the lifecycles of different species, compared to senescence in other
traits that are directly linked to survival
(Gaillard & Lemaître, 2017). Studying
ageing among species will reveal how longevities co-vary with other
organismal traits, and under which trade-offs among patterns of growth,
reproduction, and lifespan (Boonekamp,
Bauch, & Verhulst, 2020; Cohen et al.,
2019). Further, studies among species may also reveal underlying
cellular and physiological mechanisms of interest that sustained the
diversity of animal longevities.
When comparing species, there is a strongly supported pattern of larger
body size associated with longer life expectancy
(Lindstedt & Calder, 1976;
LIndstedt & Calder, 1981). This
association should reflect physiological traits of large species, like
lower mass-specific metabolic rates, which have not been fully
characterized (Speakman, 2005a).
Metabolism produces damages, like radical oxygen species (ROS) that are
by-products of aerobic respiration. Radical oxygen species were proposed
as the main underlying mechanism of ageing, thus linking together the
co-evolution of body size and lifespan via the higher ROS
production of fast-living, and generally small-sized species, with
higher rates of oxygen consumption (Beckman
& Ames, 1998; Buttemer, Abele, &
Costantini, 2010; Delhaye et al., 2016).
However, there are caveats to the so-called free-radical damage theory
of ageing (e.g. lower ROS production at high metabolism due to
uncoupling of mitochondrial respiration;
(Speakman et al., 2015). Cohen et al.
(2019) called for additional study of age-related mechanistic processes
that may be integral to the important trade-offs in play. Thereby, such
research might yield a more complete explanation of inter-specific
variation in lifespan (Hulbert, Pamplona,
Buffenstein, & Buttemer, 2007).
Shortening of telomere length is well known for its role in cell
senescence in vitro (Harley,
Futcher, & Greider, 1990). Within species, an increasing number of
studies have examined the link between telomere length or its rate of
erosion (i.e. telomere rate of change, TROC, expressed asbp lost per year, a mostly negative variable) with ageing and
lifespan (e.g. a seminal paper by
(Haussmann et al., 2003)). For instance,
in recent comparative analyses, short telomeres have been associated
with higher risks of mortality in non-model and wild animals
(Wilbourn et al., 2018) and TROC was
found inversely related to maximum lifespan in birds and mammals
(Sudyka, Arct, Drobniak, Gustafsson, &
Cichoń, 2015; Tricola et al., 2018;
Whittemore, Vera, Martínez-Nevado,
Sanpera, & Blasco, 2019). However, the sample size in the latter study
was small, and a negative relationship between TROC and lifespan was
lacking in intraspecific studies (Beaulieu,
Reichert, Le Maho, Ancel, & Criscuolo, 2011;
Sudyka et al., 2014). In addition,
experimental evidence is lacking for a causal link between telomere
length or TROC and lifespan ((Simons,
2015; Young, 2018); but see
(Varela, Muñoz-Lorente, Tejera, Ortega, &
Blasco, 2016)). Telomere length and TROC need not be highly correlated
(Tricola et al., 2018), since telomere
length an individual starts in life with may have a strong heritable
basis ((Vedder et al., 2021), but see
(Becker et al., 2015;
Viblanc et al., 2020)), and both
variables may be differently regulated by up-stream cell mechanisms
(i.e. oxidative stress or telomerase activity,
Grasman, Salomons, & Verhulst, 2011). As
a consequence, they may not display similar associations with lifespan
when comparing species.
Among species, TROC seems more strongly and negatively associated with
mean longevity compared to a lack of significant association of mean
telomere length and longevity (Dantzer &
Fletcher, 2015; Haussmann et al., 2003;
Sudyka et al., 2015;
Tricola et al., 2018). Those studies also
showed that TROC is phylogenetically conserved within bird families,
thereby suggesting that mechanisms modulating telomere loss co-evolved
with lifespan similarly among closely-related species
(Tricola et al., 2018). However, Dantzer
and Fletcher (2015) extended analyses to associations of TROC and life
history traits, finding that among the 14 bird species, those with a
more rapid pace of life also had greater TROC
(Dantzer & Fletcher, 2015). The pace of
life was calculated using a principal component analysis (PCA) that
merged 9 variables on a single PCA axis, including adult body mass.
However, body size effects must be removed from pace of life analysis,
because the slow-fast continuum in life histories is statistically
independent of body size (Gaillard et al. 1989; Read and Harvey 1989;
reviewed by Harvey and Purvis 1999; Dobson and Oli 2007). The results of
Dantzer and Fletcher (2015), therefore, could not differentiate
associations of body size and the slow-fast pace of life with TROC. Body
mass was further used as covariate in comparative analysis of
interspecific link between TROC and lifespan among 19 species of birds,
and this analysis likely adjusted for variation among species in body
size (via body mass vs lifespan and TROC;
(Tricola et al., 2018). Body size may
also modulate the inter-specific variation of telomere length through
its interaction with telomere maintenance enzyme, i.e.telomerase, which appears inoperative in larger rodent species;
(Gorbunova & Seluanov, 2009), perhaps
with an associated risk of cell immortalization
(Risques & Promislov, 2018;
Seluanov et al., 2007;
Tian et al., 2018). In addition, body
mass may be a key determinant of survival in animals
(Miller, Harper, Galecki, & Burke,
2002), including bird species
(e.g. (Briga, 2016;
Stier et al., 2014); but see
(Briga, Jimeno, & Verhulst, 2019) and
has a significant association with senescence rate among species
(Jones et al., 2008). Thus, one needs to
statistically account for differences in body mass among species, to
avoid spurious correlative conclusions about relationships between TROC
or telomere length and longevity
(Speakman, 2005b).
Telomere length at the end of growth seems to predict individual
lifespan (Asghar et al., 2015;
Heidinger et al., 2012;
Lieshout et al., 2019). Early growth is
the period when the greatest amount of telomere loss occurs, due either
to rapid cell proliferation or high metabolism during early growth
(Monaghan & Ozanne, 2018).
Alternatively, longer telomeres early in life may inevitably erode
faster (Grasman, Salomons, & Verhulst,
2011). Early growth is also the period during which physiological
maturation of tissues occurs (Cornell,
Gibson, Williams, & Portugal, 2017;
Ricklefs, Shea, & Choi, 1994;
Starck & Ricklefs, 1998), a phenomenon
influenced by both genetic and environmental factors. From such cells
and physiological mechanisms, ontogeny produces the adult phenotype.
Rapid growth or stressful early-life conditions may increase telomere
loss and shorten individual lifespan
(Boonekamp, Mulder, Salomons, Dijkstra, &
Verhulst, 2014; Herborn et al., 2014;
Metcalfe & Monaghan, 2003;
Tarry-Adkins et al., 2009). One
hypothesis is that growth and longevity are connected via the
processes that shape telomere maintenance during early-life. Still, only
a tenuous and indirect relationship presently relates short telomeres to
reduced long-term survival (Quque et al.,
2021) and more rapid growth to increased telomere shortening
(Vedder, Verhulst, Zuidersma, & Bouwhuis,
2018), both in wild birds. However, in a related study,
inter-individual differences in telomere loss were only moderately
sensitive to early life conditions (i.e. hatching order and
resource acquisition ability), termed “canalization of resource
allocation” towards telomere maintenance
(Vedder, Verhulst, Bauch, & Bouwhuis,
2017). If we hypothesized that this extends to the inter-specific
level, it suggests selection for reduced erosion of telomere length
during growth in long-lived species. Since those species generally
exhibited extended developmental periods, slow growth patterns might
have been associated with reduced shortening of telomere length. This
hypothesis needs to be tested at the phylogenetic level, as well as
within long-lived avian groups of species like procellariforms, were
body size effects can be statistically controlled due to a broad range
in body mass (about 30 g to nearly 10 kg;
(Dobson & Jouventin, 2007). Further, the
relatively small procellariform species Oceanodroma leucorhroaexhibits an intriguing apparent telomere lengthening over life, and
maintains telomerase activity in adult somatic cells
(Haussmann, Winkler, Huntington, Nisbet,
& Vleck, 2004; Haussmann et al., 2003;
Haussmann, Winkler, & Vleck, 2005;
Tricola et al., 2018).
In the present study, we tested the association of telomere length and
TROC with lifespan, reproduction, and growth patterns among 53 bird
species. Our study described the correlative relationships between life
history traits and telomere variables at the interspecific level. We
applied a principal components analysis to typify major elements of life
histories, including body size, the pace of life syndrome, and parental
care (after, e.g. (Bennett & Owens,
2002; Dobson & Jouventin, 2007;
Dobson & Oli, 2007). This approach has
the advantage of separating body size effects from influences of the
pace of life on telomeres, and will nicely complement previous study on
evolution of telomere length and dynamics in birds
(Tricola et al., 2018). We then examined
the association of these life-history indices and telomere variables,
both without and with statistical adjustments for phylogenetic
influence. Because lifespan is more closely associated with TROC than
with telomere length (i.e. TROC being estimated using
between-individual data, (Tricola et al.,
2018), we predicted that after statistically controlling for body size,
species with a fast pace of life should be characterized by higher TROC
(i.e. greater telomere loss per time unit) and little
pattern of change in adult telomere length (Adult TL ). In
addition, we tested the predicted negative association of body mass and
telomere length, previously found in rodents
(Seluanov et al., 2007). We expected thatAdult TL would be negatively associated with body size, and TROC
would be positively associated with body size (TROC is a negative value,
and large-bodied species lose less TL). Predictions for Chick TLare more difficult to make. Since early growth is when telomeres are
shortened the most and long-lived species have slower developmental
rates, other things being equal, fledgling telomere lengths (Chick
TL ), once controlled for body size, might be relatively longer in
species with a slow pace of life because telomere shortening is drawn
out over a longer period (based on low growth rates and reduced telomere
shortening). But Chick TL should also be longer in those with a
rapid pace of life (based on greater TROC, so long Chick TL and
short Adult TL ). Following results of Tricola et al.(Tricola et al., 2018), we did not expect
phylogeny to have a strong influence on Adult TL or Chick
TL , even after controlling for the possible influence of body size (via
body mass). On the other hand, phylogeny was found to explain a
significant part of interspecific variation of TROC
(Tricola et al., 2018). We hypothesized
that extracting the influence of body size from the pace of life would
lead to a comparable result, if closely related species with identical
paces of life have evolved similar TROC independently of their body
masses. This expectation seemed reasonable because some orders, like the
Procellariiformes, have evolved long lifespans along with considerable
variation in body masses among species
(Dobson & Jouventin, 2007), so they
should present different telomere lengths (in relation to body size) but
similar TROC (in relation to lifespan).