Among-population variation in telomere regulatory proteins and their potential role as hidden drivers of intraspecific variation in life history

Abstract

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 the 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.

Keywords: POT1; TPP1; TRF2; bird; latitude; life history; shelterin proteins; telomere.

FIGURE 1

Schematic of the shelterin protein complex. (a) The six‐subunit shelterin protein complex binds to double‐stranded and single‐stranded telomeric DNA (TTAGGG repeats). (b) Shelterin complexes bind repeatedly along the telomere's length. Co‐factors are not shown.

FIGURE 2

Latitudinal variation in telomere biology in the blood of nestling tree swallows (a) across a latitudinal gradient in the eastern US. (b) Model outputs for shelterin protein gene expression (condensed into PC1). One unit of PC1 equates to increases in gene expression of 50% for POT1 and 100% (or doubling) for TPP1, TRF2 and TRF2IP. (c) Model outputs for relative telomere length (T/S ratio). Points and grey circles represent average ± SE values per population and individual points, respectively. Shaded areas show 95% confidence intervals.

FIGURE 3

Morphological variation in age‐matched nestlings across a latitudinal gradient in the eastern US: (a) body mass and (b) wing length. Points represent model outputs for average ± SE values per population, and grey circles are individual data points. Shaded areas show 95% confidence intervals.

FIGURE 4

The relationship between body mass and (a) shelterin protein gene expression (PC1) or (b) relative telomere length (T/S ratio) among nestlings at 12 days old. One unit of PC1 equates to increases in gene expression of 50% for POT1 and 100% (or doubling) for TPP1, TRF2 and TRF2IP. Points represent individual nestlings. Shaded areas show 95% confidence intervals. Note that different Indiana nestlings were used for telomere and shelterin protein analyses, and so they could not be included here.