Somatic growth and telomere dynamics in vertebrates: relationships, mechanisms and consequences

Abstract

Much telomere loss takes place during the period of most rapid growth when cell proliferation and potentially energy expenditure are high. Fast growth is linked to reduced longevity. Therefore, the effects of somatic cell proliferation on telomere loss and cell senescence might play a significant role in driving the growth-lifespan trade-off. While different species will have evolved a growth strategy that maximizes lifetime fitness, environmental conditions encountered during periods of growth will influence individual optima. In this review, we first discuss the routes by which altered cellular conditions could influence telomere loss in vertebrates, with a focus on oxidative stress in both and studies. We discuss the relationship between body growth and telomere length, and evaluate the empirical evidence that this relationship is generally negative. We further discuss the potentially conflicting hypotheses that arise when other factors are taken into account, and the further work that needs to be undertaken to disentangle confounding variables.This article is part of the theme issue 'Understanding diversity in telomere dynamics'.

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

“…Such trade‐offs may account for the plethora of findings that suggest adverse early‐life conditions negatively affect lifespan and lifetime reproductive success (LRS; Kruuk, Clutton‐Brock, Rose, & Guinness, ; Lindström, ; Nussey, Kruuk, Morris, & Clutton‐Brock, ; Tung, Archie, Altmann, & Alberts, ), which can occur when animals invest in growth or competitiveness during development at the expense of their later‐life fitness (Vedder, Verhulst, Bauch, & Bouwhuis, ). The mechanisms behind such patterns are unclear, but recently it has been suggested that telomeres, the nucleoprotein structures at the terminal end of chromosomes, could link early‐life conditions and developmental growth to lifespan and ultimately LRS (Monaghan & Haussmann, ; Monaghan & Ozanne, ).…”

Carry‐over effects of early thermal conditions on somatic and germline oxidative damages are mediated by compensatory growth in sticklebacks

“…However, individuals can compensate poor developmental performance during early life by accelerating growth rate to catch up later when environmental conditions are more favourable, especially in animals that exhibit lifelong somatic growth, such as fish. Mechanisms for the deleterious effects of catch-up growth are often poorly understood but might include elevated levels of oxidative stress (Metcalfe & Alonso-Alvarez, 2010;Monaghan & Ozanne, 2018;Monaghan et al, 2009). Mechanisms for the deleterious effects of catch-up growth are often poorly understood but might include elevated levels of oxidative stress (Metcalfe & Alonso-Alvarez, 2010;Monaghan & Ozanne, 2018;Monaghan et al, 2009).…”

“…However, markers of stress experienced during the life course may accumulate in the telomeres (Herborn et al, 2014;Monaghan, 2014). Each cycle of cell division shortens the noncoding repetitive sequences of the telomeres, and fast somatic growth can accelerate this process (Monaghan & Haussmann, 2006;Monaghan & Ozanne, 2018). Each cycle of cell division shortens the noncoding repetitive sequences of the telomeres, and fast somatic growth can accelerate this process (Monaghan & Haussmann, 2006;Monaghan & Ozanne, 2018).…”

Divergent patterns of telomere shortening in tropical compared to temperate stonechats

“…Furthermore, in tropical species, reproductive workload is reduced as they lay smaller clutches, thereby caring for fewer young and expending less energy than temperate birds (Nilsson, 2002;Tieleman et al, 2006). These slower growth trajectories in combination with increased parental care per offspring may favor lower levels of telomere attrition during early life in tropical birds, which in turn may be important determinants of their longer life spans (Monaghan & Ozanne, 2018). In addition, tropical songbirds seem to have lower post-natal metabolic rates and slower, more sustained growth despite similar nestling times than temperate birds (Martin, 2015;Ton & Martin, 2016).…”