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Proc Biol Sci
2023 Feb 08;2901992:20222448. doi: 10.1098/rspb.2022.2448.
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Ageing across the great divide: tissue transformation, organismal growth and temperature shape telomere dynamics through the metamorphic transition.
Burraco P
,
Hernandez-Gonzalez M
,
Metcalfe NB
,
Monaghan P
.
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Telomere attrition is considered a useful indicator of cellular and whole-organism ageing rate. While approximately 80% of animal species undergo metamorphosis that includes extensive tissue transformations (involving cell division, apoptosis, de-differentiation and de novo formation of stem cells), the effect on telomere dynamics is unknown. We measured telomeres in Xenopus laevis developing from larvae to adults under contrasting environmental temperatures. Telomere dynamics were linked to the degree of tissue transformation during development. Average telomere length in guttissue increased dramatically during metamorphosis, when the gut shortens by 75% and epithelial cells de-differentiate into stem cells. In the liver (retained from larva) and hindlimbmuscle (newly formed before metamorphosis), telomeres gradually shortened until adulthood, likely due to extensive cell division. Tailmuscle telomere lengths were constant until tail resorption, and those in heart (retained from larva) showed no change over time. Telomere lengths negatively correlated with larval growth, but for a given growth rate, telomeres were shorter in cooler conditions, suggesting that growing in the cold is more costly. Telomere lengths were not related to post-metamorphic growth rate. Further research is now needed to understand whether telomere dynamics are a good indicator of ageing rate in species undergoing metamorphosis.
Figure 1.
. Relative telomere length (log-transformed) across tissues and developmental stages for Xenopus laevis from larval (tadpole) stage NF54 to 7-month-old frogs. Black dots and lines indicate overall mean and s.e. Blue and red dots and lines indicate estimated marginal means and s.e. in individuals exposed to a cold (19°C) or warm (23°C) temperature regime during the larval period, respectively. Temperature conditions were the same (19°C) for all individuals from NF60 onwards. The brown bands highlight the metamorphosis period. Drawings are non-scale representations of the appearance of individuals at each sampling point.
Figure 2.
. Linear correlations between relative telomere length (log-transformed) and an individual's whole-body growth rate across tissues and stages of development in Xenopus laevis. Growth rate was calculated as the mean gain in mass/day from hatching until the time of sampling. Blue and red dots and lines indicate values and the slope of the regressions in individuals exposed during the larval period to a cool (19°C) or warm (23°C) temperature regime, respectively. Regression lines are shown when an overall (growth rate or temperature) or interaction effect was significant (table 2). Temperature conditions were the same (19°C) for all individuals from NF60 onwards. Drawings are non-scale representations of the appearance of individuals at each sampling point.
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