Ageing across the great divide: tissue transformation, organismal growth and temperature shape telomere dynamics through the metamorphic transition

Author:

Burraco Pablo12ORCID,Hernandez-Gonzalez Miguel1,Metcalfe Neil B.1ORCID,Monaghan Pat1ORCID

Affiliation:

1. School of Biodiversity, One Health and Veterinary Medicine, University of Glasgow, Glasgow G12 8QQ, UK

2. Ecology, Evolution and Development Group, Doñana Biological Station (CSIC), 41092, Seville, Spain

Abstract

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 andde novoformation of stem cells), the effect on telomere dynamics is unknown. We measured telomeres inXenopus laevisdeveloping from larvae to adults under contrasting environmental temperatures.Telomere dynamics were linked to the degree of tissue transformation during development. Average telomere length in gut tissue 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 hindlimb muscle (newly formed before metamorphosis), telomeres gradually shortened until adulthood, likely due to extensive cell division. Tail muscle 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.

Funder

ERC

Ministerio de Ciencia e Innovación

Marie-Sklodowska-Curie Individual Fellowship

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Environmental Science,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine

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