Fountain of youth? – Investigating stress resilience and ageing dynamics in Icelandic threespine stickleback diverging between ambient and geothermally warmed habitats

Abstract

Climate change driven increases in temperature are predicted to enhance oxidative stress as well as to accelerate telomere shortening and thus ageing in ectotherms. Understanding if and how populations can adapt to environmental stressors by altering telomere dynamics and decelerating the ageing process is therefore of major concern. I approached this question by taking advantage of two naturally diverging populations of Icelandic threespine stickleback (Gasterosteus aculetatus) inhabiting geothermally warmed and adjacent ambient areas of a lake (Áshildarholtsvatn). To investigate whether Icelandic stickleback are divergent in ageing dynamics, I performed a 2x2 factorial experiment during which I subjected first generation offspring (F1) derived from both ambient and geothermal ecotypes to elevated rearing temperatures and contrasting food availability. I then analysed oxidative damage (via lipid peroxidation) and telomere length in muscle and liver tissue. Geothermal fish displayed elevated oxidative damage in muscle tissue in response to the high food treatment but did not differ in body condition or telomere length between the groups. Ambient fish, however, reacted to the high food treatment with sex- and tissue-specific changes in body condition, oxidative damage and telomere length. By revealing differences in energy allocation and telomere dynamics between geothermal and ambient ecotypes, I found evidence for adaptive divergence in stress resilience and ageing processes in Icelandic threespine stickleback. My findings suggest that fish might be able to adapt to multiple stressors by mediating oxidative damage and decelerating the ageing process, thus diverging towards increased stress-resilience in a warming world.

Popular Abstract

Forever young? - Icelandic threespine stickleback and the evolution of ageing

Wouldn’t it be cool if we could stay forever young? In numerous fantasy stories, brave heroes start on an adventure to find the fountain of youth, a spring which promises everlasting life to whoever takes a bath in its water. In most cases, these searches ended deadly and eternal youth still seems infinitely far away. However, could it be that a small freshwater fish succeeded at something that so many heroes have failed to do? Did the Icelandic threespine stickleback (Gasterosteus aculeatus) find the fountain of youth and manage to slow ageing? In this project, I tried to answer this question and explored whether sticklebacks can adapt to climate change driven increases in temperatures and slow down the natural ageing process.

Aquatic organisms, such as fish, are extremely sensitive to global warming as their body temperature is directly determined by the surrounding environment. Elevated temperatures lead to an increase in the production of reactive oxygen species (ROS) in the cells. This is problematic because ROS cause oxidative stress and accelerate ageing as they attack and damage telomeres. Telomeres are small fragments of non-coding DNA that protect chromosomes from attrition. They shorten a little bit every day and once a telomere is completely eroded, the cell dies. Therefore, telomeres are suitable markers for ageing: the older the organisms, the shorter the telomeres. Luckily, organisms can mitigate telomere erosion and oxidative stress to a certain extent, for example by producing enzymes that protect the cell from ROS, and repair damaged telomeres. Telomere shortening and elongation are consequently in a complex balance, called telomere dynamics.

Áshildarholtsvatn, a lake in Northwest Iceland, is the ideal system to study the effects of climate change on telomere dynamics. The main area of the lake is only 8 – 12 °C warm, whereas other parts have geothermal hot water inflows and reach temperatures of up to 20 °C all year around. Both ambient and geothermal parts of the lake are inhabited by threespine sticklebacks, small, colourful freshwater fish. I wanted to find out whether sticklebacks in the geothermal part of the lake have adapted to high temperatures and if they found ways to slow down their ageing process. In 2022, my colleagues caught fish from both geothermal and ambient parts of the lake and bred them in the lab. The fish babies were reared under high temperatures (18 °C) and once they were about one year old, I conducted a feeding experiment. I overfed half of the fish for four weeks and even though large amounts of food might initially seem beneficial, high food uptake also increase ROS production and cause oxidative stress. Geothermal sticklebacks are not only used to elevated temperatures but they are also always hungrier and eat more than ambient fish. I therefore predicted that geothermal fish have adapted to high temperatures and increased food availability by a change in their telomere dynamics to slow down the ageing process.

I found that ambient fish had a slightly higher body condition (meaning the ratio of body size to mass) and less oxidative damage as compared to geothermal fish. However, telomere length did not differ between the two ecotypes. As I predicted, ambient fish differed in body condition, oxidative damage and telomere length between the food treatments, showing that high food uptake and fat cell formation seem to be stressful and accelerate ageing. Geothermal fish, however, varied only slightly in oxidative damage but did not differ in body condition or telomere length between high and low food availability. Apparently, geothermal fish were just not stressed by the combination of high temperature and elevated food availability.

I observed very different patterns in muscle and liver tissue and realised again how incredibly complex telomere dynamics actually are. I did not find direct differences in telomere length between the ecotypes but I could clearly see that geothermal sticklebacks were considerably more resistant to stress than ambient fish. Telomere dynamics in geothermal fish did not change in response to multiple stressors, and as stress resilience and ageing are closely linked, it is very likely that they also age slower. Overall, living in a warm environment over several generations had forced geothermal stickleback to adapt to high temperatures and to stay relaxed when stress increases. That is, they have evolved to be more stress resilient!

Can we now consider lake Áshildarholtsvatn now the fountain of youth and do sticklebacks stay forever young? Well, unfortunately there is nothing magical about this lake and these fish have to die sooner or later as well. What we can see in stickleback though, is the evolution of stress resilience and an adaptation to warmer environments. How exactly elevated temperatures and increased stress shape telomere dynamics in this lake still needs more research. Yet, finding evidence for adaptive divergence of stress resilience raises hope that fish might be able to cope with the negative impacts of climate change with the help of evolution.

Master’s Degree Project in Aquatic Ecology, 45 credits, Department of Biology, Lund university

Advisor: Kaj Hulthén, Kevin Parsons
Department of Biology, Lund university, School of Biodiversity, One Health and Veterinary Medicine, University of Glasgow

• author: Hemme, Franka
• supervisor: Kaj Hulthén; Kevin Parsons
• organization: Degree Projects in Biology
• course: BION02 20241
• year: 2024
• type: H2 - Master's Degree (Two Years)
• subject: Biology and Life Sciences
• language: English
• id: 9185164
• date added to LUP: 2025-02-13 14:33:27
• date last changed: 2025-02-13 14:43:45