Telomere length is highly repeatable and shorter in individuals with more elaborate sexual ornamentation in a short‐lived passerine

Abstract

Quantifying an individual's state as a fitness proxy has proven challenging, but accumulating evidence suggests that telomere length and attrition may indicate individual somatic state and success at self‐maintenance, respectively. Sexual ornamentation is also thought to signal phenotypic quality, but links between telomeres and sexual ornamentation have been little explored. To address this issue, we examined whether telomere length and dynamics are predicted by the expression of a sexually selected ornament, the length of the outermost tail feathers (streamers), using longitudinal data from a population of European barn swallows (Hirundo rustica). In 139 adult individuals, each measured twice, we further assessed associations of telomere length with age, sex, breeding status and survival. Telomere length showed high individual repeatability (R = .97) across years while shortening with age in both sexes. Telomere length and dynamics were not significantly associated with survival to the next year, remaining lifespan or reproduction status (comparing breeding and nonbreeding yearlings). Tail streamer length, a sexually selected trait in barn swallows, was negatively associated with telomere length, independent of sex. Thus, telomere length may reflect the costs of carrying an elaborated sexual ornament, although ornament size did not significantly predict telomere shortening. In conclusion, telomere length in adult barn swallows is a highly consistent trait that shows a negative relationship with sexual ornamentation, suggesting a trade‐off between sexual ornamentation and telomere length.

Age-related changes in sperm traits and evidence for aging costs of sperm production in a sexually promiscuous passerine

“…Birds that were captured un-ringed were assumed as 1-year old that hatched outside our observed populations. This approach has been used in previous studies (Costanzo et al, 2017;Kauzálová et al, 2022) and is possible because of high breeding philopatry and fidelity of barn swallows. Adult birds that did not return to the breeding locality were presumed dead (Costanzo et al, 2017;Kauzálová et al, 2022).…”

“…This approach has been used in previous studies (Costanzo et al, 2017;Kauzálová et al, 2022) and is possible because of high breeding philopatry and fidelity of barn swallows. Adult birds that did not return to the breeding locality were presumed dead (Costanzo et al, 2017;Kauzálová et al, 2022). Only resident birds (repeatedly occurring on breeding grounds) with a known year of birth and death were included in the analysis.…”

“…To date, most available evidence for age-related changes in sperm traits and sperm production available is based on cross-sectional studies (see above) but longitudinal data are urgently needed to assess withinmale age-related patterns in postcopulatory traits, as well as to reveal hidden survival and aging costs of potentially expensive and energetically demanding sperm production reviewed in Lemaître et al (2020). Here we assess age related changes in sperm morphology traits, velocity, and CP sizes in longitudinally observed European barn swallow (Hirundo rustica rustica) males (Michálková et al, 2019;Kauzálová et al, 2022) using generalized additive mixed models (Wood, 2017;Cooper et al, 2021) to construct aging trajectories of each trait across individual lifespans. The studied population of barn swallows is characterized by moderate to high levels of sperm competition, with older males more successful in gaining extra-pair fertilizations than younger males (Michálková et al, 2019).…”

Integrating telomere biology into the ecology and evolution of natural populations: Progress and prospects

“…Carrying elaborate sexual ornaments is thought to be costly thereby maintaining the honesty of the signal, but there have been few studies done to test the relative cost of ornamentation using telomeres. Kauzálová et al (2022) found that barn swallows Hirundo rustica , with long tail streamers (a sexually selected ornament (Møller, 1988), have shorter telomeres. This suggests a cost to elaborate ornamentation in this species.…”

Editorial 2023

“…Additional studies also emphasize that what qualifies as a stressor depends greatly on the biology of the organism (Friesen et al, 2022; Wood et al, 2022), and demonstrate there is much to be gained by examining telomere dynamics across diverse forms of life (Bae et al, 2022; Boonekamp et al, 2022; McLennan et al, 2022; Power et al, 2022; Rouan et al, 2022). The third suite of articles in this special issue addresses the idea that telomeres may mediate life history trade‐offs, examining correlations between telomere length and reproductive fitness (Heidinger et al, 2022; Kauzálová et al, 2022; Ravindran et al, 2022; Sepp et al, 2022) physical state (e.g., body mass, size: Atema et al, 2022; Le Pepke, Kvalnes, Rønning, et al, 2022), and cancer prevalence (Le Pepke & Eisenberg, 2022; Ujvari et al, 2022) in natural and experimental systems. A final group of manuscripts explores the intriguing nature of heritability of telomere length and rate of shortening (Bauch et al, 2022; Kärkkäinen, Briga, et al 2022; Le Pepke, Kvalnes, Lundregan, et al, 2022; Sparks et al, 2022; Vedder et al, 2022).…”