Abstract
There are many costs associated with increased body size and longevity in animals, including the accumulation of genotoxic and cytotoxic damage that comes with having more cells and living longer. Yet, some species have overcome these barriers and have evolved remarkably large body sizes and long lifespans, sometimes within a narrow window of evolutionary time. Here, we demonstrate through phylogenetic comparative analysis that multiple turtle lineages, including Galapagos giant tortoises, concurrently evolved large bodies, long lifespans, and reduced cancer risk. We also show through comparative genomic analysis that Galapagos giant tortoises have gene duplications related to longevity and tumor suppression. To examine the molecular basis underlying increased body size and lifespan in turtles, we treated cell lines from multiple species, including Galapagos giant tortoises, with drugs that induce different types of cytotoxic stress. Our results indicate that turtle cells, in general, are resistant to oxidative stress related to aging, whereas Galapagos giant tortoise cells, specifically, are sensitive to endoplasmic reticulum stress, which may give this species an ability to mitigate the effects of cellular stress associated with increased body size and longevity.
Highlights
Body size and longevity are fundamental life history traits that vary tremendously across vertebrates
Consistent with the evolution of reduced intrinsic cancer risk in this lineage, we found that gene duplications in the Galapagos lineage are enriched in ER stress associated pathways is similar to a previous analysis by Quesada et al (2019), who found that genes under positive selection in Galapagos giant tortoises are enriched for ER function and stress pathways
Numerous studies have found comparative genomic signatures associated with the evolution of body size, longevity, and cancer resistance (Keane et al 2015; Herrera-Alvarez et al 2021; Babarinde and Saitou 2020), there have been few attempts to validate these findings experimentally at the cellular level (Jimenez et al 2018)
Summary
Body size and longevity are fundamental life history traits that vary tremendously across vertebrates. Maximum body mass in vertebrates ranges from 0.5 g in the red-backed salamander (Plethodon cinereus) (Moore et al 2001) to 136,000 kg in the blue whale (Balaenoptera musculus) (Magalh~aes and Costa 2009), whereas maximum lifespan ranges from 8 weeks in the pygmy goby (Eviota sigillata) (Depczynski and Bellwood 2005) to over 400 years in the Greenland shark (Somniosus ß The Author(s) 2021.
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