Introduction
Understanding how an organism’s fitness is influenced by its traits is a central tenet in evolutionary biology. While most measurable traits are manifested at the organismal level, for example in reproduction, survival, and behaviour, it is equally important to examine traits at deeper levels of biological organization, including cell and body physiology, as they underlie organismal performance. One of such traits is telomere dynamics, which could reflect the cellular and body state of the organism, bridging together physiology and fitness.
Telomeres are nucleoprotein complexes at the ends of chromosome consisting of repeating DNA sequences (TTAGGGn in vertebrates; Blackburn, 1991). Telomeres are vulnerable to erosion due to 1) the end-replication problem, where linear DNA is not fully replicated during cell proliferation (Levy et al., 1992; Olovnikov, 1973); and 2) chemical damage from oxidative stress (Blackburn et al., 2015; von Zglinicki, 2002). They therefore shorten over time. Shortened telomeres can be restored, e.g. by telomerase, but telomerase activity varies across life stages and species (Haussmann et al., 2007), and is generally thought to be suppressed in adult somatic cells in humans and mammals (Blackburn et al., 2015; Young, 2018). This creates a decline of telomere length throughout lifespan, typically rapidly during early life due to prominent cell proliferation, and more slowly in adulthood (Heidinger et al., 2012; Spurgin et al., 2018; Stier et al., 2020), though patterns vary across taxa (Remot et al., 2022). When telomeres are critically short, cells enter a senescent state, and can undergo apoptosis, leading to a decline in tissue function (Blackburn et al., 2015; Campisi, 2005). Because of this, telomere length, and the rate of telomere shortening, have gained attention in evolutionary biology and epidemiology, as a biomarker of body state or individual quality (e.g. Angelier et al., 2019; Bauch et al., 2013; Monaghan, 2010), a measurement of physiological costs in life-history trade-offs (e.g. Bauch et al., 2013), and a hallmark of ageing (e.g. López-Otín et al., 2013).
Because telomeres link to cellular senescence, thereby tissue function, and thus perhaps ultimately ageing, one would expect telomere dynamics to be under selection, and therefore to be correlated with fitness. However, studies examining the relationship between telomere dynamics and survival and/or lifespan have provided mixed results. On average, shorter telomeres are associated with higher mortality, but variation exists (Wilbourn et al., 2018). Some studies found positive relationships between early-life telomere length and survival or lifespan (e.g. Eastwood et al., 2019; Fairlie et al., 2016; Heidinger et al., 2012; Sheldon et al., 2022; van Lieshout et al., 2019); while others found such a relationship also in adults (e.g. Bakaysa et al., 2007; Bichet et al., 2020; Froy et al., 2021; Vedder et al., 2022), even at a genetic level (Vedder et al., 2022). There has also been some evidence that telomere shortening predicts survival and/or lifespan (e.g. Boonekamp et al., 2014; Brown et al., 2022; Tricola et al., 2018; Whittemore et al., 2019; Wood & Young, 2019). To date, it remains unclear whether, and how, telomere biology causally contribute to organismal senescence (Simons, 2015; Young, 2018) and fitness variation. This is particularly true for adult telomere dynamics, as most studies focused on early-life telomere lengths.
The link between telomere dynamics and reproductive success, another essential component of fitness, also demands attention (Sudyka, 2019). Two main hypotheses link telomere dynamics with variation in reproductive output: (1) the ‘individual quality hypothesis’ suggests that individuals with longer telomeres and/or slower telomere shortening are of higher quality, either due to genetic differences (e.g. Pepke et al., 2023), or environmental variation, e.g. better habitat that offers more resources and less stress, such that these individuals both live longer and have higher lifetime and annual reproductive output, generating a positive relationship between telomere dynamics and reproduction (e.g. Angelier et al., 2019; Heidinger et al., 2021). (2) The ‘pace-of-life hypothesis’ suggests that individuals differ in their relative energetic investment in self maintenance versus reproductive effort, such that individuals with a slower pace-of-life would exhibit a longer lifespan, have longer telomeres and slower shortening, but decreased annual reproductive success, resulting in a negative relationship between telomere dynamics and reproduction (Bauch et al., 2020; Bichet et al., 2020; Eastwood et al., 2019; Heidinger et al., 2021; Ravindran et al., 2022). So far, research has largely focused on early-life telomere length and its association with reproductive output, and has provided mixed results: Support for the ‘individual quality hypothesis’ was found by e.g. Angelier et al., (2019); Eastwood et al., (2019) and Heidinger et al., (2021), whereas support for the ‘pace-of-life hypothesis’ was found by e.g. Bauch et al., (2013) and Pepke et al., (2022). Additionally, it is still unclear how telomere shortening relates to reproductive output. For example, Heidinger et al. (2021) did not find an association between telomere shortening and reproductive success, while Sudyka et al. (2019) found a negative association. Further testing for fitness associations with telomere length and shortening, especially in longitudinal, natural systems, can thus enable us to better understand the evolutionary mechanism that drives variation in telomere dynamics.
Here, we examined the links between telomere dynamics and fitness in a free-living, insular population of house sparrows (Passer domesticus ), using longitudinal telomere measurements that span 16 years, and for which we have precise survival and lifetime reproductive data. As there has been a relative lack of focus on telomere dynamics beyond early life, we selected samples and quantified telomere lengths from birds after they have fledged, and tested: 1) whether adult telomere length predicts immediate survival up to 1 year post-measurement; 2) whether average individual telomere length and rate of telomere shortening across adulthood are associated with lifespan; 3) whether adult telomere length is associated with annual reproductive output; and 4) whether average telomere length and telomere shortening are associated with lifetime reproductive output.