Individual telomere dynamics and their links to life history in a viviparous lizard

Abstract

Emerging patterns suggest telomere dynamics and life history are fundamentally linked in endotherms through life-history traits that mediate the processes underlying telomere attrition. Unlike endotherms, ectotherms maintain the ability to lengthen somatic telomeres throughout life and the link between life-history strategies and ectotherm telomere dynamics is unknown. In a well-characterized model system ( Niveoscincus ocellatus ), we used long-term longitudinal data to study telomere dynamics across climatically divergent populations. We found longer telomeres in individuals from the cool highlands than those from the warm lowlands at birth and as adults. The key determinant of adult telomere length across populations was telomere length at birth, with population-specific effects of age and growth on adult telomere length. The reproductive effort had no proximate effect on telomere length in either population. Maternal factors influenced telomere length at birth in the warm lowlands but not the cool highlands. Our results demonstrate that life-history traits can have pervasive and context-dependent effects on telomere dynamics in ectotherms both within and between populations. We argue that these telomere dynamics may reflect the populations' different life histories, with the slow-growing cool highland population investing more into telomere lengthening compared to the earlier-maturing warm lowland population.

Of telomeres and temperature: Measuring thermal effects on telomeres in ectothermic animals

“…Since environmental temperature affects development, growth and metabolism, telomere dynamics may capture the effects of assimilation, allocation and somatic maintenance through life (Figure 1; Olsson, Wapstra, et al, 2018). The effects of environmental temperature on telomeres may be transgenerational (Dugdale & Richardson, 2018), which is supported by the evidence of thermal effects on TL and dynamics we review below, parental epigenetic effects on offspring TL and the correspondence between individual blood and sperm TL in squamate reptiles (Fitzpatrick et al, 2021;Friesen et al, 2020;Olsson et al, 2011a;Rollings et al, 2020). On the other hand, behavioural thermoregulation and thermal plasticity can shield ectotherms from selection by thermal extremes, facilitating adaptation or potentially constraining evolutionary responses in thermal tolerances (Bodensteiner et al, 2021;Kelly, 2019;Oostra et al, 2018).…”

“…A promising-but underexplored-research approach is to leverage standing geographical variation in thermally adapted or plastic life-history traits in common-garden experiments. With this design, maternal and temperature effects on growth and development can be manipulated and their flow-on effects monitored on oxidative stress, telomere dynamics and relative fitness after release into the wild (Fitzpatrick et al, 2019(Fitzpatrick et al, , 2021.…”

Lizards from warm and declining populations are born with extremely short telomeres

“…This implies that the proportion of developmental time spent within the natural habitat did not explain why offspring displayed shorter TL at birth. Instead, we propose that offspring TL variation falls along a continuum from early to late phenology indicated by differences in female quality, given the recurrent finding that reproduction follows a "sooner is better" pattern in lizards living in seasonal environments (29). These observations coupled with relatively high heritability estimations from the full-sib analysis and a strong mother-offspring correlation for TL imply that the shorter telomeres in offspring were more likely inherited at conception through parental gametes instead of being reset after fecundation and shortened during early embryonic life.…”

“…Multiple biotic and abiotic factors may alter gamete TL ( 26 ), which may condition environmental influences on TL heritability ( 27 ). The TL is normally reset by telomerase activity in germ cells, zygotes, and early life ( 18 ), but deleterious parental effects such as abnormally high and stressful developmental temperatures may either directly favor telomere shortening and/or indirectly affect telomerase repair functions in early life ( 28 , 29 ). However, impacts of external temperature on telomere dynamics during embryonic life in juvenile ectotherms are not that straightforward, as shown by lacking effect of incubation temperature in Atlantic salmon ( 30 ) or thermal effects conditioned by pollutant exposure in American alligators ( 31 ).…”

Longitudinal telomere dynamics within natural lifespans of a wild bird

“…However, further studies on multiple populations are required to disentangle the speci c (environmental) effects shaping such population differences [87]. Contrasting intraspeci c TL dynamics have also been found in different populations of European roe deer (Capreolus capreolus) whose habitats differ in food availability [88], in great tits (Parus major) living in urban or rural environments where diet composition differs [89], in American redstarts (Setophaga ruticilla) over-wintering in different non-breeding habitat types that also vary in food availability [90], in pied ycatchers (Ficedula hypoleuca) breeding in different habitats across Europe [91], and in populations of spotted snow skinks (Niveoscincus ocellatus [92]), common lizards (Zootoca vivipara [93]) and moose (Alces alces [94]) experiencing different thermal environments.…”