Final Report Summary - ECOTELO (The ecological significance of telomere dynamics: environments, individuals and inheritance)
Telomeres are specialised DNA sequences that occur at the ends of chromosomes, and their structure is highly conserved across the eukaryote taxa. Because some of the chromosome end is lost during cell division, telomeres protect the coding sequences from this erosion; they also serve to identify chromosome ends to the cellular DNA repair processes and help maintain genome stability. Conditions within the cell influence the amount of telomere loss per round of cell division. When a critical telomere length is reached, cells cease to function and often die. The pattern of telomere and resulting cell changes and loss has therefore been linked to organism health and longevity. This project is concerned with environmental effects on telomere dynamics in mothers and in their offspring, and grand offspring. This has been examined in zebra finches in the laboratory, living from adulthood in either benign (ad libitum food) or mildly stressful (unpredictable food availability, but abundant when available) environments, with the same mothers being studied when they were young, middle aged and old. It is the first time that such an ambitious, long term project has been undertaken. This laboratory work has been supplemented by related work in the field.
The long term experiment on zebra finches has only recently been completed and the large amount of data collected are still being analysed. Key findings so far are as follows. Based on looking at within individual changes in telomere length across their lifetimes, telomere length at the end of growth was found to be a highly significant predictor of longevity (P<0.001) and better than telomere length measured later in life. Living with unpredictable food was found to temporarily increase corticosterone levels while food was not available. There was no evidence of habituation, and the hormonal response to the temporary unavailability of food persisted throughout life. The birds experiencing this were found to show improved resilience to oxidative stress, reduced telomere loss and increased survival during middle age; this reduced aging rate appears to be traded-off against reproductive performance early in life, which was reduced. However, the survival benefit of mild stress exposure disappeared when the birds were old, when survival decreased and telomere loss increased. These data support an emerging paradigm which posits that stress exposure needs to be optimised rather than minimised; stress exposure is not always a bad thing. However, that the effects vary at different life stages has not previously been considered. Overall, we found a relatively low heritability of telomere length between mothers and offspring, but the environment in which the mother was living had effects on the telomere length of the offspring; sons, but not daughters, of mothers living in the more stressful environments had reduced telomere length at the end of growth; we also have evidence that the strength of these effects vary with maternal age. We have also shown for the first time that the later laid eggs within a clutch result in embryos with reduced telomere length after only 48 hours of development, and that this reduced telomere length persists into adulthood. Our data suggest that this is due to reduced antioxidants in the later-laid eggs. For the first time, we examined telomere length changes from hatching through to completion of growth; surprisingly, we found no telomere loss over the period of most rapid growth (days 1-15) but substantial loss between days 15-30. More results will emerge as data analyses progresses.
Our complementary experiments in the field in wild birds and other taxa have shown that experimental manipulation of corticosterone levels increased telomere loss during growth, and that being a subordinate chick in brood results in increased telomere loss, and more impulsive decision making later in life. Older mothers produce offspring with reduced telomere length, due to the quality of the rearing environment. We have also shown that larger body size is associated with reduced telomere length. Experiments with Atlantic salmon (in which eggs from the same females were fertilised by sperm from males with different life history strategies using in vitro fertilisation, and placed in different environments) have shown that growing under harsher stream conditions is associated with more telomere loss than growing to the same size in benign conditions. We also found that the more years that fathers had spent growing at sea, the longer the telomere length of their offspring; this surprising effect must be transmitted via the father’s sperm.
We have established a specialised research laboratory during the project, and developed new methods for use in non-model species. We have shared the expertise that we have built up during the project with other researchers by publishing two methodological papers, and by hosting other researchers in our lab. The work has also stimulated other research projects. We have established an International Telomere Network, bringing together researchers from a wide range of disciplines, including biomedicine, physiology, ecology and evolution, which has increased cross disciplinary connections and brought new perspectives. A special edition of Philosophical Transactions of the Royal Society scheduled for 2017 will bring this to the wider scientific community.
The long term experiment on zebra finches has only recently been completed and the large amount of data collected are still being analysed. Key findings so far are as follows. Based on looking at within individual changes in telomere length across their lifetimes, telomere length at the end of growth was found to be a highly significant predictor of longevity (P<0.001) and better than telomere length measured later in life. Living with unpredictable food was found to temporarily increase corticosterone levels while food was not available. There was no evidence of habituation, and the hormonal response to the temporary unavailability of food persisted throughout life. The birds experiencing this were found to show improved resilience to oxidative stress, reduced telomere loss and increased survival during middle age; this reduced aging rate appears to be traded-off against reproductive performance early in life, which was reduced. However, the survival benefit of mild stress exposure disappeared when the birds were old, when survival decreased and telomere loss increased. These data support an emerging paradigm which posits that stress exposure needs to be optimised rather than minimised; stress exposure is not always a bad thing. However, that the effects vary at different life stages has not previously been considered. Overall, we found a relatively low heritability of telomere length between mothers and offspring, but the environment in which the mother was living had effects on the telomere length of the offspring; sons, but not daughters, of mothers living in the more stressful environments had reduced telomere length at the end of growth; we also have evidence that the strength of these effects vary with maternal age. We have also shown for the first time that the later laid eggs within a clutch result in embryos with reduced telomere length after only 48 hours of development, and that this reduced telomere length persists into adulthood. Our data suggest that this is due to reduced antioxidants in the later-laid eggs. For the first time, we examined telomere length changes from hatching through to completion of growth; surprisingly, we found no telomere loss over the period of most rapid growth (days 1-15) but substantial loss between days 15-30. More results will emerge as data analyses progresses.
Our complementary experiments in the field in wild birds and other taxa have shown that experimental manipulation of corticosterone levels increased telomere loss during growth, and that being a subordinate chick in brood results in increased telomere loss, and more impulsive decision making later in life. Older mothers produce offspring with reduced telomere length, due to the quality of the rearing environment. We have also shown that larger body size is associated with reduced telomere length. Experiments with Atlantic salmon (in which eggs from the same females were fertilised by sperm from males with different life history strategies using in vitro fertilisation, and placed in different environments) have shown that growing under harsher stream conditions is associated with more telomere loss than growing to the same size in benign conditions. We also found that the more years that fathers had spent growing at sea, the longer the telomere length of their offspring; this surprising effect must be transmitted via the father’s sperm.
We have established a specialised research laboratory during the project, and developed new methods for use in non-model species. We have shared the expertise that we have built up during the project with other researchers by publishing two methodological papers, and by hosting other researchers in our lab. The work has also stimulated other research projects. We have established an International Telomere Network, bringing together researchers from a wide range of disciplines, including biomedicine, physiology, ecology and evolution, which has increased cross disciplinary connections and brought new perspectives. A special edition of Philosophical Transactions of the Royal Society scheduled for 2017 will bring this to the wider scientific community.