Biologists aim to explain patterns of growth, reproduction, and ageing that characterize life histories, yet we are just beginning to understand the proximate mechanisms that generate this diversity. Existing research in this area has focused on telomeres but has generally overlooked the telomere’s most direct mediator, the shelterin protein complex. Shelterin proteins physically interact with the telomere to shape its shortening and repair. They also regulate metabolism and immune function, suggesting a potential role in life history variation in the wild. However, research on shelterin proteins is uncommon outside of biomolecular work.
Intraspecific analyses can play an important role in resolving these unknowns because they reveal subtle variation in life history within and among populations. Here, we assessed ecogeographic variation in shelterin protein abundance across eight populations of tree swallow (Tachycineta bicolor) with previously documented variation in environmental and life history traits. Using blood gene expression of four shelterin proteins in 12-day old nestlings, we tested the hypothesis that shelterin protein gene expression varies latitudinally and in relation to both telomere length and life history.
Shelterin protein gene expression differed among populations and tracked non-linear variation in latitude: nestlings from mid-latitudes expressed nearly double the shelterin mRNA on average than those at more northern and southern sites. However, telomere length was not significantly related to latitude.
We next assessed whether telomere length and shelterin protein gene expression correlate with 12-day old body mass and wing length, two proxies of nestling growth linked to future fecundity and survival. We found that body mass and wing length correlated more strongly (and significantly) with shelterin protein gene expression than with telomere length.
These results highlight telomere regulatory shelterin proteins as potential mediators of life history variation among populations. Together with existing research linking shelterin proteins and life history variation within populations, these ecogeographic patterns underscore the need for continued integration of ecology, evolution, and telomere biology, which together will advance understanding of the drivers of life history variation in nature.
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The telomere regulatory gene POT1 responds to stress and predicts performance in nature: Implications for telomeres and life history evolution
Telomeres are emerging as correlates of fitness‐related traits and may be important mediators of ecologically relevant variation in life history strategies. Growing evidence suggests that telomere dynamics can be more predictive of performance than length itself, but very little work considers how telomere regulatory mechanisms respond to environmental challenges or influence performance in nature. Here, we combine observational and experimental data sets from free‐living tree swallows (
- Award ID(s):
- 1656109
- PAR ID:
- 10443054
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 31
- Issue:
- 23
- ISSN:
- 0962-1083
- Format(s):
- Medium: X Size: p. 6155-6171
- Size(s):
- p. 6155-6171
- Sponsoring Org:
- National Science Foundation
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Abstract Telomeres, protective caps at the end of chromosomes, are often positively related to lifespan and are thought to be an important mechanism of organismal aging. To better understand the casual relationships between telomere length and longevity, it is essential to be able to experimentally manipulate telomere dynamics (length and loss rate). Previous studies suggest that exposure to TA‐65, an extract from the Chinese root
Astragalus membranaceus , activates telomerase, lengthens telomeres, increases the growth of keratin‐based structures, and boosts the immune system in adults. However, telomere loss is expected to be greatest during early life but whether TA‐65 has similar effects during this life stage is currently unknown. Here, we experimentally exposed free‐living house sparrow (Passer domesticus ) chicks to TA‐65 during post‐natal development and examined the effects on telomere length and loss, growth of keratin‐based structures, and a measure of cellular immunity. Contrary to expectation, the growth of keratin‐based structures was reduced in TA‐65 chicks and in the second year of the study, chicks exposed to TA‐65 experienced more telomere loss than controls. Thus, the effects of TA‐65 on telomeres and keratin‐based structures differ across life stages and future research will be necessary to determine the mechanisms underlying these age‐specific effects. -
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Abstract Human telomeres are protected by shelterin proteins, but how telomeres maintain a dynamic structure remains elusive. Here, we report an unexpected activity of POT1 in imparting conformational dynamics of the telomere overhang, even at a monomer level. Strikingly, such POT1-induced overhang dynamics is greatly enhanced when TRF2 engages with the telomere duplex. Interestingly, TRF2, but not TRF2ΔB, recruits POT1-bound overhangs to the telomere ds/ss junction and induces a discrete stepwise movement up and down the axis of telomere duplex. The same steps are observed regardless of the length of the POT1-bound overhang, suggesting a tightly regulated conformational dynamic coordinated by TRF2 and POT1. TPP1 and TIN2 which physically connect POT1 and TRF2 act to generate a smooth movement along the axis of the telomere duplex. Our results suggest a plausible mechanism wherein telomeres maintain a dynamic structure orchestrated by shelterin.
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Abstract Conditions during early life can have dramatic effects on adult characteristics and fitness. However, we still know little about the mechanisms that mediate these relationships. Telomere shortening is one possibility. Telomeres are long sequences of DNA that protect the ends of chromosomes. They shorten naturally throughout an individual's life, and individuals with short telomeres tend to have poorer health and reduced survival. Given this connection between telomere length (TL) and fitness, natural selection should favor individuals that are able to retain longer telomeres for a greater portion of their lives. However, the ability of natural selection to act on TL depends on the extent to which genetic and environmental factors influence TL. In this study, we experimentally enlarged broods of Tree Swallows (
Tachycineta bicolor ) to test the effects of demanding early‐life conditions on TL, while simultaneously cross‐fostering chicks to estimate heritable genetic influences on TL. In addition, we estimated the effects of parental age and chick sex on chick TL. We found that TL is highly heritable in Tree Swallow chicks, and that the maternal genetic basis for TL is stronger than is the paternal genetic basis. In contrast, the experimental manipulation of brood size had only a weak effect on chick TL, suggesting that the role of environmental factors in influencing TL early in life is limited. There was no effect of chick sex or parental age on chick TL. While these results are consistent with those reported in some studies, they are in conflict with others. These disparate conclusions might be attributable to the inherent complexity of telomere dynamics playing out differently in different populations or to study‐specific variation in the age at which subjects were measured.
