Telomere shortening and survival in free-living corvids

Abstract

Evidence accumulates that telomere shortening reflects lifestyle and predicts remaining lifespan, but little is known of telomere dynamics and their relation to survival under natural conditions. We present longitudinal telomere data in free-living jackdaws (Corvus monedula) and test hypotheses on telomere shortening and survival. Telomeres in erythrocytes were measured using pulsed-field gel electrophoresis. Telomere shortening rates within individuals were twice as high as the population level slope, demonstrating that individuals with short telomeres are less likely to survive. Further analysis showed that shortening rate in particular predicted survival, because telomere shortening was much accelerated during a bird's last year in the colony. Telomere shortening was also faster early in life, even after growth was completed. It was previously shown that the lengths of the shortest telomeres best predict cellular senescence, suggesting that shorter telomeres should be better protected. We test the latter hypothesis and show that, within individuals, long telomeres shorten faster than short telomeres in adults and nestlings, a result not previously shown in vivo. Moreover, survival selection in adults was most conspicuous on relatively long telomeres. In conclusion, our longitudinal data indicate that the shortening rate of long telomeres may be a measure of 'life stress' and hence holds promise as a biomarker of remaining lifespan.

Figure 1.

Picture of representative pulsed-field gel showing the molecular size ladder and the first seven lanes with smears representing telomeres of individual samples.

Figure 2.

Cross-sectional estimates of (a) age-related telomere shortening rate follow a log-linear function with a decrease in shortening rate with age. Longitudinal analysis of the same data results in estimates of (b) 309 bp per ln(year) between individuals and (c) 664 bp per ln(year) within individuals. The slope within individuals was significantly steeper than the slope between individuals—for comparison, the between-individuals slope was added to the within-individual graph (dashed line).

Figure 3.

Telomere shortening rate (base pairs/ln(year)) (mean ± s.e.) for individuals that did or did not return to the colony the next year.

Figure 4.

(a) The slope (±s.e.) of the relation with age for different estimates of telomere length in adults. The difference between within-individual (black circles) and between-individual (white circles) estimates of telomere shortening in adults shows an accelerated increase. (b) Telomere shortening in the 25 days prior to fledging was much higher compared with adults for all measures used.

Figure 5.

Nestling telomere length at ages 5 and 30 days plotted against each other. Line indicates equal values ( y = x) and hence when telomeres have shortened between ages 5 and 30 days the data points fall below this line.