Immediate and delayed effects of growth conditions on ageing parameters in nestling zebra finches

Abstract

Conditions experienced during development and growth are of crucial importance as they can have a significant influence on the optimisation of life histories. Indeed, the ability of an organism to grow fast and achieve a large body size often confers short-and long-term fitness benefits. However, there is good evidence that organisms do not grow at their maximal rates as growth rates seem to have potential costs on subsequent lifespan. There are several potential proximate causes of such a reduced lifespan. Among them, one emerging hypothesis is that growth impacts adult survival and/or longevity through a shared, end point, ageing mechanism: telomere erosion. In this study, we manipulated brood size in order to investigate whether rapid growth (chicks in reduced broods) is effectively done at the cost of a short-(end of growth) and long-term (at adulthood) increase of oxidative damage and telomere loss. Contrary to what we expected, chicks from the enlarged broods displayed more oxidative damage and had shorter telomeres at the end of the growth period and at adulthood. Our study extends the understanding of the proximate mechanisms involved in the trade-off between growth and ageing. It highlights that adverse environmental conditions during growth can come at a cost via transient increased oxidative stress and pervasive eroded telomeres. Indeed, it suggests that telomeres are not only controlled by intrinsic growth rates per se but also may be under the control of some extrinsic environmental factors, which could complicate our understanding of the growthageing interaction. KEY WORDS: Birds, Flight performance, Growth conditions, Oxidative stress, Telomeres INTRODUCTIONConditions experienced during growth are of crucial importance as they can have a significant influence on the optimisation of life histories (Ricklefs, 1979;Lindström, 1999). Indeed, early life conditions are known to directly impact growth patterns (De Kogel, 1997), metabolism (Desai and Hales, 1997), immune function (Saino et al., 1997) and sexual attractiveness (Gustafsson et al., 1995). Moreover, the ability of an organism to grow fast and achieve a large body size often correlates with short-and long-term fitness benefits (Richner, 1992;Reeve, 2000;Bonduriansky, 2001). Growth is a vulnerable stage for individuals, and organisms would therefore be expected to grow as quickly as they could in order to escape this risky (Arendt, 1997). Because growing fast is often associated with a large 'final' body size, especially in species with determinate growth, fast growth is also thought to greatly influence fitness at adulthood. Indeed, adult body size is frequently under strong natural and sexual selection, and larger individuals are often better 'equipped' to defend their food resources, territories or mates against conspecifics. In addition, larger individuals are often the favourites when it comes to choosing a mate (Shine, 1988; Arendt, 1997). However, the accumulation of counterintuitive data underlines that individuals presenting a...

Brood size moderates associations between relative size, telomere length, and immune development in European starling nestlings

“…Our telomere data showed very similar patterns to our own previous studies in starlings (Nettle et al., 2013, 2015), and those observed in nestlings of other passerines (Boonekamp et al., 2014; Reichert et al., 2014; Stier et al., 2015). Erythrocyte telomere lengths at the two time points were strongly correlated with one another, indicating repeatable individual differences (this study, r  = .74; Nettle et al., 2013; r  = .72; Nettle et al., 2015; r  = .90).…”

“…The present study was purely observational, whereas much of the previous evidence concerning effects of nestling conditions on telomere or immune dynamics in birds has been based on experimental manipulation of brood size, position in the size hierarchy, or food supply (Birkhead et al., 1999; Boonekamp et al., 2014; Killpack et al., 2015; Nettle et al., 2013, 2015; Reichert et al., 2014). We see the two approaches as complementary.…”

“…For example, the positive correlations between growth and immune function in the six broods could be due to variation among nestlings in genetic quality rather than the impact of competition. However, we can set the patterns observed here in the context of the evidence from the experimental studies, which clearly shows that factors such as relative size have a causal, not just correlative, significance for individual development (Nettle et al., 2015; Reichert et al., 2014). Experimental approaches alone are also incomplete, as it is necessary to show that the causal factors they expose are actually operative and significant in the range of natural, un‐manipulated broods.…”

“…To repair damage to telomeres is assumed to carry some cost. Thus, other things being equal, there should be a trade‐off between body size at the end of the fledgling period and telomere length (Reichert et al., 2014). In accordance with this possibility, several recent avian studies have observed associations between larger body size or faster growth and shorter telomere length at the end of development (Herborn et al., 2014; Noguera, Metcalfe, Boner, & Monaghan, 2015; Ringsby et al., 2015).…”

Traffic noise exposure affects telomere length in nestling house sparrows

“…[7]). Environmental conditions experienced during development are thus likely to be a particularly important driver of telomere shortening [8,9], and consequently, might entail important costs (e.g. reduced longevity [3]).…”