Mind the cell: Seasonal variation in telomere length mirrors changes in leucocyte profile

Abstract

Leucocytes are typically considered as a whole in studies examining telomere dynamics in mammals. Such an approach may be precarious, as leucocytes represent the only nucleated blood cells in mammals, their composition varies temporally, and telomere length differs between leucocyte types. To highlight this limitation, we examined here whether seasonal variation in leucocyte composition was related to variation in telomere length in free-ranging mandrills (Mandrilllus sphinx). We found that the leucocyte profile of mandrills varied seasonally, with lower lymphocyte proportion being observed during the long dry season presumably because of the combined effects of high nematode infection and stress at that time of the year. Interestingly, this low lymphocyte proportion during the long dry season was associated with shorter telomeres. Accordingly, based on longitudinal data, we found that seasonal changes in lymphocyte proportion were reflected by corresponding seasonal variation in telomere length. Overall, these results suggest that variation in lymphocyte proportion in blood can significantly affect telomere measurements in mammals. However, lymphocyte proportion did not entirely explain variation in telomere length. For instance, a lower lymphocyte proportion with age could not fully explain shorter telomeres in older individuals. Overall, our results show that telomere length and leucocyte profile are strongly although imperfectly intertwined, which may obscure the relationship between telomere dynamics and ageing processes in mammals.

Telomere length is repeatable, shortens with age and reproductive success, and predicts remaining lifespan in a long‐lived seabird

“…As such, we believe that other explanations for the discrepancy in results among long‐term studies on wild populations deserve further investigation. Studies on birds, for example, measure erythrocyte telomere length, while studies on mammals measure leucocyte telomere length, and it cannot be excluded that these tissues differ in their telomere dynamics (Beaulieu, Benoit, Abaga, Kappeler, & Charpentier, ). Moreover, little is known about the dynamics of interstitial telomeric DNA, which is included in qPCR measures of telomere length.…”

Determinants of Variations in Fecal Neopterin in Free-Ranging Mandrills

“…Second, individuals exhibited higher nematode richness during the long dry season, especially the juveniles (Poirotte et al, 2016)-although our analyses show that gut parasites do not explain fecal neopterin levels. Third, the oxidative damages of females, including juvenile females, were found to be higher during the long dry season (Beaulieu et al, 2014), whereas their leucocyte profiles also varied seasonally, with lower lymphocyte proportion being observed during the long dry season, presumably because of the stress at that time of the year (Beaulieu et al, 2017) which is also characterized by increases in cortisol production compared to the long rainy season-although the highest cortisol concentrations are in fact observed during the short dry season (Charpentier et al, 2018). It is therefore likely that the long dry season poses a particular challenge on the immune system of juvenile mandrills, due to combined effects of nutritional stress and higher disease risk, which is reflected by the effect of the mating season (or proportion of cycling females) on neopterin levels.…”

Telomere shortening as a mechanism of long-term cost of infectious diseases in natural animal populations

“…Recent studies in humans have shown that the rate of telomere attrition and telomerase activity are significantly different between cell types, suggesting cell-specific susceptibility and telomere length regulation mechanisms [23,24]. Even more, it has been recently shown in a wild mammal (mandrill, Mandrillus sphinx) that leucocyte composition varies temporally and that these variations are mirrored by change in blood telomere length [25]. Thus, any conclusion based on whole blood or total white blood cells is likely to be biased, especially in the case of infections that affect white blood cell count and composition [26].…”