DISCUSSION
Parasitic infection by the carnid fly and sibling competition interacted
to negatively affect telomere dynamics in developing individuals.
Telomere shortening was accelerated in parasitized nestling jackdaws
reared in enlarged broods but not in parasitized nestlings reared in
reduced broods, indicating a synergistic effect of these stressors.
Furthermore, ectoparasitic infections by Carnus hemapterus did
not affect nestling growth but nestlings reared in enlarged broods
gained less weight, in accordance with previous findings in the same
population .
Telomeres shortened on average 264 bp over the 25-day development
period, but when nestlings in enlarged broods suffered from infections
by the parasitic carnid fly this was increased to 415 bp, a 57%
increase relative to the overall mean. This increase could be a direct
effect of enhanced cell proliferation to replenish the red blood cells
(RBCs) depleted by the hematophagous fly, as reported for species
parasitized by blow fly larvae . Alternatively, but not mutually
exclusive, increased telomere loss could be an indirect effect of the
parasitic infection, for example through an increase in oxidative stress
. The latter possibility is supported by studies reporting increased
oxidative stress in birds infected by hematophagous ectoparasites .
However, an effect of parasitic infections on telomere dynamics via
oxidative stress remains speculative at this stage. Future studies
combining brood size manipulation with anti-parasite medication would
further confirm a direct effect of parasitic infections on telomere
dynamics (i.e. when infected nestlings shorten their telomeres more than
non-infected siblings reared in reduced broods). Additionally, measuring
physiological parameters such as haemoglobin and markers of oxidative
damage could shed light on the mechanism through which blood-sucking
parasites increase telomere loss.
The effect of parasitic infection on telomere shortening was contingent
on brood size, with Carnus presence accelerating telomere
shortening in enlarged broods, but not in reduced broods. This result is
in line with findings in other studies showing that the negative effects
of adversity on telomere dynamics are more evident under ecological
hardship (e.g. in the American alligator, . The finding that nestlings
in enlarged broods were more susceptible to effects of Carnusinfestation is an example of a reverse Matthew effect, i.e. individuals
that are in a poorer state suffer more from additional adversity than
individuals in a better state. This appears to be a widespread
phenomenon (e.g. . Occurrence of the reverse Matthew effect during early
life may contribute to the fitness consequences of adverse developmental
conditions, in a sense that offspring that are in a poorer state because
of a particular adverse aspect of their environment may end up more
disadvantaged relative to individuals in a better state due to
additional challenges.
Environmental adversity generally decreases growth rate, and adverse
conditions accelerate telomere shortening. One could therefore expect
fast growth to be associated with long telomeres . However, reality is
more complex, because studies find contrasting relationships between
growth and telomere length . We found TL to decrease with increasing
body mass (scaled – see methods), and this association was independent
of age, brood size manipulation and Carnus infestation. The fact
that the mass effect on TL did not change with age, despite the
approximately four-fold increase in body mass, could be taken to mean
that the mass effect at fledging age was in fact the day 5 mass effect
that was carried over to fledging age. This underlines our earlier
finding that individual variation in telomere length is largely
determined very early in life (Boonekamp et al 2014). Telomere dynamics
during development is the outcome of resource allocation between growth
and somatic maintenance, and depending on variation in resource
allocation and availability positive and negative associations between
growth and TL can arise . Apparently, jackdaw nestlings canalized
resources to early growth at the expense of telomere maintenance,
possibly because day 5 mass has strong fitness consequences, with
survival up to fledging increasing strongly with increasing day 5 mass .
Had we restricted our study of the effects of Carnus infection to
growth, we would have concluded that Carnus infection does not
noticeably affect jackdaw nestlings, and it is only with the extension
of our study to telomere dynamics that effects of Carnusinfection were revealed. Given the earlier finding that telomere
shortening predicts post-fledging survival to recruitment in this
population (Boonekamp et al 2014), we assume that Carnusinfection thereby affects offspring fitness prospects, but we
acknowledge that this remains to be established. Here, we indicate that
the effects of early life adversity depend on environmental conditions
(i.e. parasite presence), complicating predictions of early-life effects
on fitness. Thus, the implications of parasitic infections in
combination with brood competition in the longer term remain to be
explored under different scenarios. Telomere length and dynamics are
proving a useful tool for this purpose (e.g. ; DNA methylation is
another promising candidate in this context . For example, it might be
that extrinsic stressors have an additive effect on survival, further
confirming the impact that early-life adversity can have on fitness
prospects . Alternatively, when the negative effects of parasitic
infections are more canalised , one might expect no direct effect ofCarnus parasites on survival. Furthermore, cryptic sub-lethal
effects of developmental conditions that are expressed beyond the time
frame of the study highlight the need to evaluate the effects of
developmental conditions beyond morphological parameters.