Longitudinal dynamics and behavioural correlates of telomeres in male wire‐tailed manakins

Abstract

Building on the predictions of state‐dependent life‐history theory, telomeres are hypothesized to either correlate with or function as an adaptive, proximate mediator of an individual's behaviour and life‐history strategy. To further understand the relationship between telomeres, behaviour and life‐history strategies, we measured male behaviour, telomere lengths and telomere dynamics in a free‐living population of known‐age, male wire‐tailed manakins Pipra filicauda. Male wire‐tailed manakins perform coordinated displays with other males at leks and these displays form the basis of long‐term coalition partnerships. Males exhibit consistent individual differences in the number of social partners within their social network and the frequency of social interactions. Male sociality is also positively correlated with both social rise and reproductive success. We measured male behaviour using a telemetry‐based, proximity datalogging system and blood telomere lengths were quantified using qPCR. We examined the relationships between telomere length, telomere dynamics, social status, and male behaviour. We also quantified the repeatability of telomere lengths, examined age‐related changes in telomere length, and tested for instances of telomere elongation that exceed residual error in telomere length. Telomere length was found to be highly repeatable. More social males exhibited shorter telomeres and higher rates of telomere attrition. Telomeres did not significantly vary with age within or between individuals in either of the male social classes. Two out of 25 individuals exhibited patterns telomere elongation that exceeded residual error in telomere measurements. Here we show that telomeres consistently vary between male wire‐tailed manakins and these differences are related to variation in male social behaviour. In this relatively long‐lived species, telomeres appear to be flexible traits that can increase or decrease in length. Overall, this study provides observational support for the hypothesis that telomeres act as a molecular marker that relates to behaviour in a state‐dependent manner. We also provide insight into the molecular consequences of individual variation in male social behaviour. A free Plain Language Summary can be found within the Supporting Information of this article.

Neurogenomic landscape associated with status-dependent cooperative behavior

“…2021), suggesting that the brain region-specific patterns may be more important in modulating male wire-tailed manakin behavior. However, the broader associations of social status with metabolic, immune, and telomere gene ontology categories suggests differences in allostatic load among status classes in male-male cooperative systems (Goymann and Wingfield 2004; Vernasco et al . 2021; Jones and DuVal 2021).…”

“…2021; Jones and DuVal 2021). Further, differential global regulation of telomeres may explain the relative stability of telomere length in territorial wire-tailed manakin males (Vernasco et al . 2021), and collectively these results may represent metabolic adaptations for territoriality.…”

“…suggesting that the brain region-specific patterns may be more important in modulating male wire-tailed manakin behavior. However, the broader associations of social status with metabolic, immune, and telomere gene ontology categories suggests differences in allostatic load among status classes in male-male cooperative systems (Goymann and Wingfield 2004;Vernasco et al 2021;Jones and DuVal 2021). Further, differential global regulation of telomeres may explain the relative stability of telomere length in territorial wire-tailed manakin males (Vernasco et al 2021), and collectively these results may represent metabolic adaptations for territoriality.…”

Telomere length predicts timing and intensity of migratory behaviour in a nomadic songbird

“…(c) Relative telomere length measurement DNA from whole blood samples was extracted using a Gentra Puregene Blood Kit (Qiagen) and the modified extraction protocol described in [23]. This extraction method as well as our approach for storing samples result in high molecular weight DNA suitable for telomere measurement by qPCR [23,48]. Relative telomere lengths (rTL) were quantified using real-time quantitative PCR (qPCR) following the methodologies of [48,49].…”

“…Telomeres are therefore considered a biomarker of biological state [8,17,20]. A number of studies also report correlations between telomere lengths and behaviour [6,[20][21][22][23]. These relationships could arise due to specific behaviour causing changes in telomere lengths (i.e.…”