Interactions between parental traits, environmental harshness and growth rate in determining telomere length in wild juvenile salmon

Abstract

A larger body size confers many benefits, such as increased reproductive success, ability to evade predators and increased competitive ability and social status. However, individuals rarely maximize their growth rates, suggesting that this carries costs. One such cost could be faster attrition of the telomeres that cap the ends of eukaryotic chromosomes and play an important role in chromosome protection. A relatively short telomere length is indicative of poor biological state, including poorer tissue and organ performance, reduced potential longevity and increased disease susceptibility. Telomere loss during growth may also be accelerated by environmental factors, but these have rarely been subjected to experimental manipulation in the natural environment. Using a wild system involving experimental manipulations of juvenile Atlantic salmon Salmo salar in Scottish streams, we found that telomere length in juvenile fish was influenced by parental traits and by direct environmental effects. We found that faster‐growing fish had shorter telomeres and there was a greater cost (in terms of reduced telomere length) if the growth occurred in a harsher environment. We also found a positive association between offspring telomere length and the growth history of their fathers (but not mothers), represented by the number of years fathers had spent at sea. This suggests that there may be long‐term consequences of growth conditions and parental life history for individual longevity.

Evolutionary ecology of telomeres: a review

“…Similar effects can be seen in wild sea birds ( Uria lomvia ), in which the best predictor of among‐year variation in telomere length was environmental quality, with longer telomeres in more food‐rich colonies and years . Effects of environmental harshness were also found in wild salmon, with shorter telomeres in fish growing in colder water . Research on humans has targeted ill effects of overindulgence and obesity and shown (with marginal significance) that telomere length is negatively linked to obesity in women and high glucose levels in men, but with a positive relationship to high‐density lipoprotein (HDL, the “good” cholesterol) in men (using qPCR) …”

Telomere attrition predicts reduced survival in a wild social bird, but short telomeres do not

“…Several potential explanations exist for the unexpected negative association between day 4 telomere length and survival to fledgling (Figure a). Hatchlings investing more heavily in somatic maintenance could consequently have fewer reserves available to weather short‐term resource shortages as nestlings, leaving them differentially vulnerable to starvation (see McLennan et al, for similar logic). However, that this survival association was no longer apparent when predated broods were excluded from the analysis (Figure b) and remained apparent when nestlings that likely starved were excluded (Figure c) suggests that broods of nestlings with longer telomeres may have been differentially vulnerable to in‐nest predation, rather than starvation.…”

Links between parental life histories of wild salmon and the telomere lengths of their offspring

“…DNA was extracted from parent, embryo and fry tissue using the DNeasy Blood and Tissue Kit (Qiagen), as described in McLennan et al. (). For the sperm analysis, sperm was diluted 1/200 with sterile PBS solution.…”

“…Telomere length was measured in all samples using quantitative PCR, and data were analysed using qbase software for windows (Hellemans, Mortier, De Paepe, Speleman, & Vandesompele, ), both as described in McLennan et al. (). Atlantic salmon chromosomes are not thought to have a significant amount of interstitial telomere sites (Perez, Moran, & Garcia‐Vazquez, ), which could potentially add noise to the qPCR measurement.…”

“…In a field study of Atlantic salmon, we recently showed that paternal life history can influence offspring telomere length (at the fry stage), but that there was also a strong influence of environmental conditions experienced by the fry in the wild (McLennan et al., ). A second recent study also found that stream temperature influenced telomere lengths in wild juvenile salmonids, partly because of its influence on growth rates (Debes, Visse, Panda, Ilmonen, & Vasemägi, ).…”