The environmental and genetic determinants of chick telomere length in Tree Swallows (Tachycineta bicolor)

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.

Estimation of environmental, genetic and parental age at conception effects on telomere length in a wild mammal

“…Studies in vertebrates have provided evidence for positive (e.g. Eisenberg et al., 2017; Kimura et al., 2008; Njajou et al., 2007), negative (summarized in table 1 in Belmaker et al., 2019; Eisenberg, 2019) or no (summarized in table 1 in Eisenberg, 2019) PAC effect, and positive (Asghar et al., 2015) or no (Bauch et al., 2019; Belmaker et al., 2019; Bouwhuis et al., 2018; Froy et al., 2017; Heidinger et al., 2016; McLennan et al., 2018) MAC effect on offspring telomere length. In cross‐sectional mammalian studies, positive PAC effects have been reported in humans, a negative PAC effect was found in a captive population of short‐lived house mice ( Mus musculus ; de Frutos et al., 2016), and in a wild population of longer‐lived Soay sheep there was no relationship between offspring RLTL (either measured across all ages or only as lambs) and PAC or MAC (Froy et al., 2017).…”

“…Studies from different taxa, with a variety of mating systems, have shown a negative PAC effect (Bouwhuis et al., 2018; Criscuolo et al., 2017; Olsson et al., 2011), including a longitudinal (Bauch et al., 2019) and an experimental study (Noguera et al., 2018). However, other studies have reported no PAC or MAC effect on offspring telomere length (Belmaker et al., 2019; Froy et al., 2017; Heidinger et al., 2016; McLennan et al., 2018), a positive MAC effect (Asghar et al., 2015) or a positive mean parental age effect (Dupont et al., 2018). The variation in PAC and MAC effects on offspring telomere length among species requires more studies to disentangle potential causes and mechanisms underlying such variation in transgenerational effects.…”

Estimation of environmental and genetic contributions to telomere length variation in a wild mammal

“…Studies from different taxa, with a variety of mating systems, have shown a negative PAC effect (Bouwhuis et al, 2018;Criscuolo, Zahn, & Bize, 2017;Olsson et al, 2011), including a longitudinal (Bauch, Boonekamp, Korsten, Mulder, & Verhulst, 2019) and an experimental manipulation (Noguera, Metcalfe, & Monaghan, 2018) study. However, other studies have reported no PAC or MAC effect on offspring telomere length (Heidinger et al, 2016;McLennan et al, 2018;Froy et al, 2017;Belmaker, Hallinger, Glynn, Winkler, & Haussmann, 2019) or a positive MAC effect (Asghar et al, 2015). The variation in PAC and MAC effects on offspring telomere length among species requires more studies to disentangle potential causes and mechanisms underlying such variation in transgenerational effects.…”

Foster rather than biological parental telomere length predicts offspring survival and telomere length in king penguins

“…For species with parental care, an extrapolation of this “telomere – individual quality hypothesis” is that parental telomere length may reflect parental quality, parents with longer telomeres being better at raising a large number of high‐quality offspring with high survival rates (i.e., “telomere – parental quality hypothesis”). Remarkably, because telomeres are genetic material passed on from parents to offspring, one topical question is the extent to which parent–offspring resemblance in telomere length is explained by genetic additive variance (heritability) and/or by other environmental effects caused by variation in the quality of pre‐ and posthatching parental care (Belmaker, Hallinger, Glynn, Winkler, & Haussmann, 2019).…”

“…Early studies suggested that telomere length is fixed in the zygote (i.e., inherited from the gametes in a sex‐ and age‐dependent way; Eisenberg, 2019), remaining unchanged for life relative to other individuals from the same cohort (Graakjaer et al., 2004). However, estimates of telomere length heritability appear to be largely variable across species (Asghar, Bensch, Tarka, Hansson, & Hasselquist, 2014; Atema et al., 2015; Becker et al., 2015; Belmaker et al., 2019; Stier, Reichert, Criscuolo, & Bize, 2015), suggesting that both genetics and environmental factors (including parental care) may influence offspring telomere length. However, assessing the effects of parental care quality on telomere length is complex, because it requires disentangling the contribution of additive genetic effects (i.e., heritability) from parental care per se on offspring telomeres.…”