Telomere attrition rates are associated with weather conditions and predict productive lifespan in dairy cattle

Abstract

Telomere length is predictive of adult health and survival across vertebrate species. However, we currently do not know whether such associations result from among-individual differences in telomere length determined genetically or by early-life environmental conditions, or from differences in the rate of telomere attrition over the course of life that might be affected by environmental conditions. Here, we measured relative leukocyte telomere length (RLTL) multiple times across the entire lifespan of dairy cattle in a research population that is closely monitored for health and milk production and where individuals are predominantly culled in response to health issues. Animals varied in their change in RLTL between subsequent measurements and RLTL shortened more during early life and following hotter summers which are known to cause heat stress in dairy cows. The average amount of telomere attrition calculated over multiple repeat samples of individuals predicted a shorter productive lifespan, suggesting a link between telomere loss and health. TL attrition was a better predictor of when an animal was culled than their average TL or the previously for this population reported significant TL at the age of 1 year. Our present results support the hypothesis that TL is a flexible trait that is affected by environmental factors and that telomere attrition is linked to animal health and survival traits. Change in telomere length may represent a useful biomarker in animal welfare studies.

Figure 1

Relative leukocyte telomere length (RLTL) dynamics in dairy cattle. All RLTL measurements were pre-adjusted for qPCR plate and qPCR row to account for known sources of measurement error. (a) Age in years at second RLTL measurement is significantly associated with RLTL change. (b) At all measurement times the present measurement (RLTL at time t) is clearly correlated with the previous measurement (RLTL at time t − 1) (estimate = 0.38, P < 0.001). The red line represents a perfect correlation. (c) RLTL over age in years. (d) RLTL over sample year. (e) Longitudinal RLTL change over age for all animals with at least 7 samples as example for RLTL variation. (f) Early-life change in RLTL over age at sampling and (g) over sampling year.

Figure 2

Association between maximum summer temperature and RLTL attrition.

Figure 3

Relationship between lifetime telomere length dynamics and productive lifespan. RLTL measurements were grouped into tertiles as shown for (a) mean RLTL, (b) mean absolute RLTL change and (c) mean RLTL change. Kaplan–Meier curves show relationship of lifetime RLTL dynamics tertiles with productive lifespan. (d) Greater lifetime mean RLTL (tertile 3) was not significantly differently associated with productive lifespan than moderate or short lifetime mean RLTL (tertiles 2 and 1). (e) Greater mean absolute RLTL change (tertile 3) measured over the lifetime was associated with shorter productive lifespan compared to animals with moderate (tertile 2) or little (tertile 1) mean absolute RLTL change. (f) Greater mean lifetime RLTL attrition was associated with shorter productive lifespan. It can be seen that the mean survival of the group with the most RLTL attrition was about 600 days shorter than the mean survival of the group showing the most stable RLTL with neither dramatic shortening nor elongation (tertile 2).

Figure 4

Early-life change in RLTL and productive lifespan. (a) visualises how continuous RLTL change measurements were grouped into discrete tertiles to allow visualising of survival data. (b) Kaplan–Meier plot that shows the association of early- life RLTL change tertiles with productive lifespan. More RLTL attrition within the first year of life (tertile 1) was associated with a shorter productive lifespan.