Effects of early-life competition and maternal nutrition on telomere lengths in wild meerkats

Abstract

Effects of early-life competition and maternal nutrition on telomere lengths in wild meerkats. Proceedings of the Royal Society of London Series B: Biological Sciences, 284(1861), 20171383. (doi:10.1098/rspb.2017.1383 This is the author's final accepted version.There may be differences between this version and the published version. You are advised to consult the publisher's version if you wish to cite from it.http://eprints.gla.ac.uk/147697/ Here, we investigate the link between early-life competition and telomere length in wild 23 meerkats. Our results show that, when multiple females breed concurrently, increases in the 24 number of pups in the group are associated with shorter telomeres in pups. Given that pups 25 from different litters compete for access to milk, we tested whether this effect is due to 26 nutritional constraints on maternal milk production, by experimentally supplementing 27 females' diets during gestation and lactation. While control pups facing high competition had 28 shorter telomeres, the negative effects of pup number on telomere lengths were absent when 29 maternal nutrition was experimentally improved. Shortened pup telomeres were associated 30 with reduced survival to adulthood, suggesting that early-life competition for nutrition has 31 detrimental fitness consequences that are reflected in telomere lengths. Dominant females 32 commonly kill pups born to subordinates, thereby reducing competition and increasing 33 growth rates of their own pups. Our work suggests an additional benefit of infanticide may be 34 that it also reduces telomere shortening caused by competition for resources, with associated 35 benefits for offspring ageing profiles and longevity. 36 37 KEY WORDS 38telomeres, early-life adversity, early-life stress, Suricata suricatta, meerkats, infanticide 39 40 41Introduction 42

Early‐life telomere length predicts lifespan and lifetime reproductive success in a wild bird

“…A meta‐analysis of 27 studies which measured TL at variable stages suggests that longer telomeres are associated with better survival (Wilbourn et al, ). Similarly, studies which investigate early‐life TL and survival have also demonstrated positive TL effects on short‐term survival (post growth period or fledging in birds (Geiger et al, ; Stier et al, ; Watson, Bolton, & Monaghan, )) or first year survival (Cram, Monaghan, Gillespie, & Clutton‐Brock, ; Salmón, Nilsson, Watson, Bensch, & Isaksson, ) but not always (Boonekamp, Mulder, Salomons, Dijkstra, & Verhulst, ; Cerchiara et al, ; McLennan et al, ; Stier et al, ; Ujvari & Madsen, ; Vedder et al, ). However, because extrinsic factors are always likely to be a major cause of mortality and TL‐associated mortality is likely to diminish with age (Boonekamp, Simons, Hemerik, & Verhulst, ), the predictive effect of early‐life TL on survival may be age‐dependent under natural conditions, a plausible yet untested hypothesis in the wild (Supporting Information Table ).…”

“…Positive associations between early‐life TL and early‐life survival are likely to extend to fitness (e.g., Cram et al, ; Watson et al, ), while this is likely to be true in many cases, life‐history trade‐offs, behaviour, and environmental conditions may obscure this association (Ricklefs & Wikelski, ). If individuals pursue different pace‐of‐life strategies (Ricklefs & Wikelski, ), those with a slower pace‐of‐life may favour self‐maintenance (associated with longer early‐life TL and longer lifespan) over investment in reproductive bouts, resulting in no, or even a negative, association between early‐life TL and fitness.…”

Individual variation in early‐life telomere length and survival in a wild mammal

“…Telomere length has been linked positively to survival to adulthood and/or annual adult survival probability in both captive (Heidinger et al, ) and wild populations (Asghar, Hasselquist, et al, ; Barrett, Burke, Hammers, Komdeur, & Richardson, ; Cram, Monaghan, Gillespie, & Clutton‐Brock, ; Fairlie et al, ; Haussmann, Winkler, & Vleck, ). Even though other studies have tested for, but not found such associations (Beaulieu, Reichert, Le Maho, Ancel, & Criscuolo, ; Sudyka et al, ), a meta‐analysis in nonhuman vertebrates reported an overall association between short telomeres and higher mortality risk (Wilbourn et al, ).…”

“…Compelling evidence exists that early‐life conditions such as maternal effects, developmental stress and competition for resources (e.g., Asghar, Bensch, Tarka, Hansson, & Hasselquist, ; Cram et al, ; Haussmann, Longenecker, Marchetto, Juliano, & Bowden, ) can be particularly influential in shaping telomere length. The greater strength of early‐life than late‐life effects could be due to stronger forces of selection, since natural selection acts on the proportion of a cohort that is alive, which is greatest in early‐life (Hamilton, ).…”

“…Nevertheless, early‐life telomere length might be an important predictor of life histories (Monaghan, ; Wilbourn et al, ; Young, ). While studies into the effects of the environment on telomeres are emerging in wild mammals (Cram et al, ; Izzo, Hamer, Bertozzi, Donnellan, & Gillanders, ; Lewin, Treidel, Holekamp, Place, & Haussmann, ), longitudinal studies in wild mammals remain relatively rare (Beirne, Delahay, Hares, & Young, ; Fairlie et al, ). Gaining a better understanding of telomere dynamics, its relationship with survival, and early‐life effects requires more comprehensive longitudinal studies in wild populations.…”